animal learning

animal learning


      the alternation of behaviour as a result of individual experience. When an organism can perceive and change its behaviour, it is said to learn.

      That animals can learn seems to go without saying. The cat that runs to its food dish when it hears the sound of the cupboard opening; the rat that solves a maze in the laboratory; the bird that acquires the song of its species—these and many other common examples demonstrate that animals can learn. Yet what is meant by saying that animals can learn? What, in other words, is learning? This question proves exceedingly difficult to answer, and, in fact, some theorists propose that no single, all-encompassing definition of learning is at all possible. Moreover, a moment's reflection yields the realization that there exist different kinds of learning. The learning of number concepts, for example, surely seems to be of a different nature than the learning of the association between the sound of a cupboard door and the receipt of food. To explore animal learning, then, this article first considers what learning is and is not and then examines in detail some of the specialized types of learning that occur in animals.

The general nature of learning
      Many animals live out their lives following fixed and apparently unvarying routines. Among numerous species of solitary insects, for example, the life cycle consists of the following unvarying events: the females lay their eggs on a particular plant or captured prey; the newly hatched larvae immediately start eating and then follow a standard sequence of developmental stages; the adults recognize appropriate mates by a set of fixed signs, perform a fixed sequence of mating responses, provision their eggs with suitable nourishment, and finally die before the next generation hatches. The same unchanging sequence is repeated generation after generation. And it is, of course, eminently successful. The same set of responses is invariably elicited by the same set of stimuli, because those responses were, and continue to be, adaptive. Where circumstances do not change, there is little need for an animal's behaviour to change. Even many aspects of the behaviour of mammals show a similar fixity. A dog withdraws its foot if it is pricked and a young child his hand if burned; both people and rabbits blink whenever an object is moved rapidly toward their eyes; the feeding behaviour of young infants of virtually all mammalian species consists of sucking elicited by contact with the lips.

      Whenever the same response is always appropriate in a particular circumstance, there is little reason why an animal should need to learn what to do in that circumstance. But the world is not always so stable a place. The food supply that was plentiful yesterday may be exhausted today, and the foraging animal that always returns to the same spot will starve to death. Moreover, a particular food supply may be temporarily depleted but will be replenished if left long enough; the successful forager needs to remember where the supply was and when it was last visited, so as to time a return to advantage. In other words, circumstances may change, and the same response is not always appropriate to the same stimuli. Knowing what behaviour is appropriate may depend, therefore, on keeping track of past events.

Possible explanations of behavioral changes
      If an animal's behaviour toward a particular stimulus changes, one must look for an explanation of that change. One possible explanation is that the change is due to learning, but there are numerous other possibilities. If a definition of learning is to be provided, that definition must specify when to attribute the change to learning, and when to other causes.

      At least two other major causes of behavioral change have been widely recognized. The first of these is motivation. A laboratory rat may pick up, chew, and swallow a pellet of food at one moment; half an hour later, after having eaten 20 grams of food, the rat will simply ignore any further pellets offered. Similarly, a male rat may mount and copulate with a receptive female introduced into his cage, but he will not repeat this pattern of behaviour endlessly even if offered the opportunity to do so. Some male territorial birds, such as chaffinches, will feed amicably beside other males at certain times of day or certain seasons of the year, but at other times they will launch an attack on any intruding male. In all these cases, it is more reasonable to attribute the change in behaviour not to anything the animal has learned but rather to a change in the creature's motivational state.

      It should not be thought, however, that just because all of these examples can be attributed to a single item—i.e., motivation—that their detailed explanation will always be the same. The analysis of motivation is itself a large field of study, and it has proved to be more profitable to concentrate on the specific explanation of individual cases of changes in behaviour rather than to search for broad explanatory principles that end up being nearly vacuous. Nonetheless, it does seem possible to draw a contrast between motivational explanations for such changes and those that appeal to learning.

      A second broad class of changes in behaviour can be attributed to maturation. We are inclined to ascribe the unfolding pattern of behaviour that emerges over the first few weeks of life to this ill-defined process. Newborn rat pups, for example, are relatively helpless; their eyes do not open for about two weeks, and their main sources of sensory input are probably touch and smell. As their sensory apparatus matures, the pups exhibit changed behavioral responses. The other obvious instance of a maturational change in behaviour is that which comes with sexual maturity: sexually mature adults of most species behave toward one another in ways quite different from those of younger members of the species. It is not only courtship and mating behaviour that change with sexual maturity; for instance, male puppies urinate in the same way as females, by squatting, and it is the onset of sexual maturity that produces the adult pattern of cocking a hind leg.

      The concept of maturation is probably no better defined than that of motivation, and it is equally important to stress that it must cover a number of different processes. And, as with motivation, it is more profitable to analyze each case in detail, in order to uncover the precise mechanisms involved, than it is simply to label a change as an example of maturation. Indeed, at the level of physiological process, it seems probable that both motivational and maturational changes are often due to alterations in the hormonal state of the animal, and the distinction between the two is largely one between the unidirectional nature of the change in the case of maturation contrasted with the cyclical change common to short-term motivational states.

      But how are these changes discerned from those that might be ascribed to learning? In many cases, of course, the answer is because a precise causal explanation has been provided: a great deal is known, at a physiological level, about the changes in brain and body associated with the motivational states of hunger and thirst. Even without any such detailed knowledge of the underlying mechanisms, it is possible to insist that certain changes in behaviour be attributed to motivation rather than to learning if the opportunity to learn anything relevant was lacking and the opportunity for a motivational change was present. If, for example, an animal that has been deprived of food for a long time behaves in one way toward food-related stimuli, but some hours later, after having been given ample opportunity to eat, it behaves differently toward those stimuli, the obvious interpretation is a motivational one. This interpretation would be strengthened if the animal had not come into contact with these stimuli during the intervening period and had been given, as far as one could judge, no other opportunity to learn anything about them. Learning, in other words, depends on certain kinds of opportunity, and a definition of learning may well turn out to be no more than a specification of the particular set of opportunities and experiences that produce it.

Circumstances that produce learning
      A particular change in behaviour is attributed to learning, then, because it is possible to specify the set of circumstances that produced it. What are those circumstances? It is common to claim that learning depends on practice. (An older generation of experimental psychologists would have claimed that it depended on “reinforced” practice.) This definition can be misleading, however, if it causes one to attribute to learning all behavioral changes that follow what appears to be practice. In other words, it is not enough to show that an animal appeared to engage in practice and its behaviour subsequently changed. A temporal correlation of this sort does not establish a causal connection. Young birds, for example, are unable to fly, and their first attempts at flight are clumsy and ill-coordinated. Casual observation suggests that young birds improve with practice, gradually perfecting the set of skills they display as adults, but experimental analysis suggests that this practice may be unnecessary. Young birds have been brought up under restricted conditions that completely prevented their flying. When released at the age at which normally reared birds fly proficiently, the experimental subjects flew—without practice—as successfully as those that had spent their time in trial flight. The development of the skill appears to depend more on the maturation of strength and agility than on specific practice.

      The notion that learning depends on practice also seems unduly restrictive and is, perhaps, an unnecessary legacy of an earlier version of behaviourism. It is not obvious that an animal should actually have to engage in a particular form of behaviour in order that this pattern of behaviour should be affected by learning. In many cases, indeed, no such practice seems necessary. The young of many songbirds must, it is quite clear, learn their species-typical song. There are several aspects to this learning process, one of which may indeed involve practicing the song at the beginning of the young bird's second season. But another critical aspect is simply exposure to the adult song at some point during the autumn of the young bird's first year, at a time when the young bird does not practice singing at all. Deprived of such experience, chaffinches and song sparrows produce an extremely impoverished version of the adult song; some finches may develop a song more characteristic of another species if that is what they heard during this period of their life. There are numerous other examples where learning appears to depend more on the opportunity to observe than on the opportunity for practice.

      This suggests that the definition of learning will have to refer to changes in behaviour that are attributable to particular kinds of experience. The danger now is that, as with motivation and maturation, the definition of learning will be so broad and vague as to be useless. As in those cases, it may be more profitable to concentrate on more detailed analysis of particular instances of learning. Such analysis has, for example, led to widespread agreement on the definition of classical conditioning, a particular type of learning whose study was pioneered by the Russian physiologist Ivan Petrovich Pavlov. In a typical experiment on classical conditioning, an experimenter might arrange a correlation between the ringing of a bell and the delivery of food to an animal. The animal predictably learns to direct food-related activity toward the sound of the bell. Analyses of such experiments have led to the definition of classical conditioning as a type of learning that occurs when there is a correlation between two stimuli and the animal's behaviour toward one of these stimuli changes in a predictable manner determined by the nature of the other. This definition, which will be expanded later in this article, is useful because it specifies both the circumstances responsible for learning (a temporal correlation between two stimuli) and the general way in which experience of those circumstances changes behaviour (the animal starts directing toward one stimulus responses that are related to those normally directed toward the other). Experimental psychologists and ethologists, however, have devised a tremendous range of procedures for studying learning in animals. The range and variety are such that it may be well-nigh impossible to formulate a meaningful definition of the circumstances that produce learning, for the definition either will be so restrictive that it clearly applies to only a fraction of the cases that should be regarded as instances of learning, or it will be so broad that it says nothing.

      Rather than pursue any further the attempt to find an all-embracing, single definition of learning, it seems more useful to provide narrower definitions for particular cases, along the lines suggested above for classical conditioning. One consequence of this approach is that it may encourage the belief that learning consists of a large number of distinct processes that have nothing in common with one another. It is, of course, an open question as to whether this is true: it is certainly possible that, just as with the concept of motivation, the layman's concept of learning encompasses a large number of different cases whose underlying mechanisms are quite distinct. It is important not to prejudge this issue. Insistence on a single, global definition may well tend toward just such prejudgment by encouraging the belief that learning is a single, common process. To start by drawing some distinctions between types of learning does not rule out the possibility of seeing whether the various cases studied do have anything in common.

      In the final analysis, as is true of all scientific definitions, the definition of learning is a matter of theory. It has been said that a good scientific definition is the end product of good theory and experiment, not the starting point. Thus, there is a single process of learning if it turns out to be possible to devise a single theory that adequately accounts for the variety of cases in which learning is assumed to occur. Superficial appearances may be deceptive: just because the circumstances that produce learning in two cases, along with the consequences of that learning, appear quite different, it does not follow that the processes underlying learning are different. For instance, the phenomenon of filial imprinting, first seriously analyzed by the Austrian ethologist Konrad Lorenz (Lorenz, Konrad), appears to be a highly specialized form of learning in which a newborn animal (e.g., a chick, duckling, or gosling) rapidly learns to follow the first salient, moving object it sees. Normally this object will be the mother, but Lorenz discovered that the range of potential imprinting objects is large, extending from Lorenz himself to a bright red ball. There is no question but that some process of learning occurs here, and Lorenz assumed it to be highly specialized. Yet one theory seeks to explain imprinting in terms of simple classical conditioning. Whether or not the account of imprinting provided by this theory is correct, the point is made that how learning is defined and whether it is defined as a single, monolithic process or as many specialized processes are, in the end, questions of theory.

Types of learning

Simple nonassociative learning
      When experimental psychologists speak of nonassociative learning, they are referring to those instances in which an animal's behaviour toward a stimulus changes in the absence of any apparent associated stimulus or event (such as a reward or punishment). Studies have identified two major forms of simple nonassociative learning, which are to some extent mirror images of one another: habituation and sensitization.

      A classic example of habituation is the following observation on the snail Helix albolabris. If the snail is moving along a wooden surface, it will immediately withdraw into its shell if the experimenter taps on the surface. It emerges after a pause, only to withdraw again if the tap is repeated. But continued repetition of the same tapping at regular intervals elicits a briefer and more perfunctory withdrawal response. Eventually, the stimulus, which initially elicited a clear-cut, immediate response, has no detectable effect on the snail's behaviour. Habituation has occurred.

      Habituation can be defined in behavioral terms as a decline in responding to a repeatedly presented stimulus. As such, it is a very widespread phenomenon, one that can be observed in animals ranging from single-celled protozoans to humans. Most animals behave differently to novel and familiar stimuli: the former sometimes elicit startle responses, sometimes investigatory or exploratory responses; the latter often apparently are ignored. The suggestion that habituation is a simple form of learning, however, implies that it can be distinguished from some even simpler potential causes of this sort of change in behaviour. One reason why an animal might stop responding to a stimulus is that it no longer detects the stimulus; i.e., some form of sensory adaptation might have occurred. Another potential cause is fatigue: perhaps some temporary refractory state is produced by repeated elicitation of the same response, making it impossible to perform that response again. Whether or not one would want to call either of these processes a form of learning is doubtful. But both behavioral and physiological evidence establishes that habituation cannot be explained in these terms.

      The critical behavioral evidence is that habituation can be disrupted by almost any change in the experimental conditions. If repeated presentation of one stimulus leads to habituation of a response, the same response can still be elicited by a different stimulus. Even if the experimenter presents a novel stimulus that does not itself elicit the response in question, its presentation may restore the response on the next trial in which the originally habituated stimulus is presented. This latter observation, usually referred to as an instance of dishabituation, seems to rule out any simple sensory adaptation; both observations rule out simple effector fatigue.

      Neurophysiological analysis of habituation in various mollusks (mollusk)—for example, in the sea snail Aplysia—has confirmed that habituation need not depend on changes in the activity of sensory or motor neurons. In the case of Aplysia, researchers have studied the gill withdrawal reflex, a response that rapidly habituates to repeated stimulation of the snail's siphon or mantle shelf. But habituation still occurs even if it is elicited by direct, electrical stimulation of the motor nerve, bypassing the sensory receptors completely; and recording from the sensory nerve during normal habituation reveals no decline in its level of activity. These observations eliminate sensory adaptation as a possible cause of the animal's having ceased to respond to the stimulus. Effector fatigue can be ruled out by showing that direct stimulation of the motor neurons controlling the withdrawal response can still elicit a perfectly normal reaction even after the response has completely habituated. Research shows that habituation in Aplysia depends on changes in the activity of more central neurons. Repeated tactile stimulation of the siphon, leading to habituation of the withdrawal response, causes changes in the activity of the motor neurons innervating the response. Specifically, these motor neurons show a decline in excitatory postsynaptic potential, which is the electrical change that enables the nerve impulse to cross the gap (synaptic cleft) that separates one neuron in the pathway from the next. The decline in excitatory postsynaptic potential short-circuits the response. Moreover, the presentation of a novel stimulus, sufficient to dishabituate the behavioral response, restores the postsynaptic potential.

      Habituation occurs even in animals without a central nervous system—probably in single-celled protozoans; certainly in animals such as the coelenterate Hydra, which have a diffuse nerve net and do not appear to be capable of associative learning. Among mammals, habituation of certain reflex responses can be observed even in “spinal” subjects, that is, those whose spinal cord has been severed from the brain. There can be little doubt, then, that habituation is not only widespread, but that it also can be a relatively simple phenomenon. There is, however, no guarantee that it is the same phenomenon wherever it appears. The waning response to a repeatedly presented stimulus admits of a number of different explanations. In principle, as we have already seen, it might be due to sensory adaptation, effector fatigue, or a more central neural change. These distinctions make rather little sense in the case of a single-celled animal. And one should not necessarily expect the habituation observed in a spinal mammal to involve precisely the same mechanisms as those responsible for comparable behavioral effects in an intact animal. Some psychologists have proposed theories of habituation that appeal to processes of classical conditioning. Such a theory is not likely to apply to the habituation observed in an animal that shows no capacity for classical conditioning.

      Habituation is usually, as here, classified as an instance of simple, nonassociative learning. It is supposedly nonassociative because all that happens in the course of habituation is that a stimulus is repeatedly presented and the animal's behaviour changes; there is, on the face of it, no other event with which the stimulus can be associated. Habituation must therefore, it appears, be understood by reference to some change in the pathway between stimulus and response, and the work with Aplysia and other mollusks shows how this analysis may proceed at the physiological level. But if habituation is not always the same phenomenon, it is possible that different processes may underlie the habituation of the startle response to a loud noise in an intact mammal. And despite appearances to the contrary, those processes may involve some associative learning. One suggestion is that novel stimuli elicit a biphasic response: an initial increase in startle responses, which include components of emotion or anxiety, followed by a rebound in the opposite direction. Habituation occurs when the latter, rebound response becomes conditioned to the stimulus, occurring sooner and sooner with each repetition of the stimulus and thereby damping down and eventually canceling out the initial reaction. An alternative possibility is that long-term habituation depends on associating the repeatedly presented stimulus with the context in which it occurs, a suggestion that would explain why presentation of the stimulus in a different context sometimes leads to dishabituation.

      The generality of habituation implies that this behavioral phenomenon has considerable adaptive significance; if true, it would be quite reasonable to expect that a number of different mechanisms might have evolved to produce the behavioral result. The adaptive value of habituation is not difficult to see. A novel stimulus may signify danger, and an animal should react to this stimulus either by withdrawing or at least by orienting toward it to see what will happen next. But if the same stimulus occurs again with no further consequence, it is probably safe: regular repetition of the same stimulus implies that it is part of the background, such as the waving of a branch in the wind or the shadow caused by a piece of seaweed floating with the waves. If the stimulus is not dangerous, time should not be wasted on it. Withdrawal, especially in the case of a snail into its shell, is a time-consuming effort, incompatible with such vital activities as searching for food. If it is important, therefore, for animals to be wary of novel stimuli, it is equally important that they should discriminate the novel and potentially dangerous from the familiar and probably safe.

      The effect of habituation is to eliminate unnecessary responses, but the main function of learning has usually been thought to be the production of new responses. Traditional psychological theories of learning have assumed that the learning of new patterns of behaviour comes about through the association of a new response with a particular stimulus. Consequently, psychologists usually have either ignored the possibility that nonassociative processes might be sufficient to increase the probability of a new response or regarded it as a nuisance that interferes with the measurement of associative changes. They have rarely treated it as a subject worthy of study in its own right.

      This is unfortunate, for the nonassociative phenomenon of sensitization is probably fairly widespread, and it provides a simple means of acquiring adaptive behaviour. Sensitization is said to occur when the repeated presentation of a particular significant stimulus (such as food or electric shock) lowers the threshold for the elicitation of appropriate behaviour to the point where a second stimulus, not normally capable of calling forth that behaviour, now does so. A typical example is provided by the behaviour of the marine worm Nereis (rag worm). If the worm is kept in a small tube and fed at regular intervals, it becomes progressively more likely to respond to any novel stimulus, such as a change in illumination, by exploratory, food-seeking movements toward the open end of the tube. If, on the other hand, the worm receives mild electric shocks at regular intervals, it becomes progressively more likely to respond to a novel stimulus by withdrawal.

      The first point to note about sensitization is its relationship to habituation. Habituation refers to a decline in the probability of responding to a repeatedly presented stimulus. Sensitization, by contrast, refers to an increase in the probability that behaviour appropriate to a repeatedly presented stimulus will occur, even in response to another stimulus. Although these two outcomes cannot be observed simultaneously, it is quite possible that the same operation—repeated presentation of a stimulus—can simultaneously engage two different processes, one causing a decline in the probability of responding to that stimulus, the other causing an increase. Experimental analysis suggests that both processes are real and may be engaged in the same experiment, so that the observed change in behaviour actually results from a mixture of the two. Typically, the process of habituation wins out, and what is observed is an overall decline in responding. But a common finding in habituation experiments is that responding initially increases before declining; the implication is that the initial presentations of a stimulus result in more sensitization than habituation, while further presentations produce more habituation than sensitization. A second factor influencing the relative importance of the two processes is the intensity or significance of the stimulus. A weak stimulus, or one with little intrinsic biological significance, will show relatively rapid habituation and little or no initial sensitization. A stronger stimulus, especially one, such as food or shock, that has substantial significance to the animal, may show marked sensitization and relatively little habituation.

      The second point about sensitization is that it may mimic the effect of associative learning or conditioning. As has been mentioned, in a classical conditioning experiment a neutral stimulus, such as a change in illumination, is paired with the delivery of a significant stimulus, such as food or shock. Repeated pairing causes the neutral stimulus to elicit responses initially called forth by the significant stimulus; for example, a change in illumination that has been associated with an electric shock would come to elicit retreat or withdrawal. But in the case of the worm Nereis, experiments demonstrate that the light would come to elicit this change in behaviour whether or not it had been paired with shock: all that is needed is sufficient exposure to the shock. To attribute the change in behaviour toward the light to its association with food or shock, one must show that this change is greater than that which would have resulted from sensitization alone.

      The physiological processes underlying sensitization, like those underlying habituation, have been analyzed in experiments on such invertebrate species as Aplysia. Not surprisingly, the mechanisms involved appear to mirror one another. Whereas habituation is correlated with a decline in postsynaptic potentials, sensitization is correlated with an increase in the magnitude of postsynaptic potentials at the same locus.

      Although sensitization has often been treated as a nuisance whose effects must be controlled in studies of habituation or associative learning, it remains a process worthy of study in its own right, for the behavioral changes it produces can have significant adaptive value. Without requiring the presumably more complex neural machinery necessary to subserve associative learning, sensitization enables animals to respond to local variations in the occurrence of significant events. If an animal's sources of food tend to occur together (that is, they are not distributed randomly in time or space), then it pays that animal, having once found food, to continue to behave in a food-gathering manner. Conversely, the animal that is increasingly wary after exposure to danger will have a better chance of evading a lurking predator. Sensitization thus enables an animal to take advantage of statistical regularities in the occurrence of significant events, without requiring it to detect other events that predict the significant ones. No doubt, further advantage accrues to the animal that can perform such calculations, for associative learning provides a powerful means of predicting the future. But there can be equally little doubt that such a process requires a more elaborate nervous system.

Associative learning: (associative learning) conditioning
      The study of animal learning in the laboratory has long been dominated by experiments on conditioning. This domination has been resisted by critics, who complain that conditioning experiments are narrow, artificial, and trivial, and, as such, miss the point of what animals are adapted to learn. From the critics' point of view, one unfortunate effect of their attacks has been the progressive refinement and elaboration of the theory of conditioning to the point where it can often explain the exceptions to which they drew attention. This is not to insist that associative learning is the sole, or even the most important, form of learning in vertebrates, but rather to introduce the idea that the processes underlying conditioning may be more interesting than older theories and an earlier generation of textbooks suggested.

Classical (Pavlovian conditioning) and instrumental conditioning
      Pavlov (Pavlov, Ivan Petrovich) was not the first scientist to study learning in animals, but he was the first to do so in an orderly and systematic way, using a standard series of techniques and a standard terminology to describe his experiments and their results. In the course of his work on the digestive system of the dog, Pavlov had found that salivary secretion was elicited not only by placing food in the dog's mouth but also by the sight and smell of food and even by the sight and sound of the technician who usually provided the food. Anyone who has prepared food for his pet dog will not be surprised by Pavlov's discovery: in a dozen different ways, including excited panting and jumping, as well as profuse salivation, the dog shows that it recognizes the familiar precursors of the daily meal. For Pavlov, at first, these “psychic secretions” merely interfered with the planned study of the digestive system. But he then saw that he had a tool for the objective study of something even more interesting: how animals learn. From about 1898 until 1930, Pavlov occupied himself with the study of this subject.

      Pavlov's experiments on conditioning employed a standard, simple procedure. A hungry dog was restrained on a stand and every few minutes was given some dry meat powder, an event signaled by an arbitrary stimulus, such as the ticking of a metronome. The food itself elicited copious salivation, but, after a few trials, the ticking of the metronome, which regularly preceded the delivery of food, also elicited salivation. In Pavlov's terminology, the food is an unconditional stimulus, because it invariably (unconditionally) elicits salivation, which is termed an unconditional response. The ticking of the metronome is a conditional stimulus, because its ability to elicit salivation (now a conditional response when it occurs in reaction to the conditional stimulus alone) is conditional on a particular set of experiences. The elicitation of the conditional response by the conditional stimulus is termed a conditional reflex, the occurrence of which is reinforced by the presentation of the unconditional stimulus (food). In the absence of food, repeated presentation of the conditional stimulus alone will result in the gradual disappearance, or extinction, of its conditional response. In translation from the Russian, the terms “conditional” and “unconditional” became “conditioned” and “unconditioned,” and the verb “to condition” was soon introduced to describe the experimental activity.

      To the American psychologist Edward L. Thorndike (Thorndike, Edward L.) must go the credit for initiating the study of instrumental conditioning. Thorndike began his studies as a young research student, at about the time that Pavlov—already 50 years old and with an eminent body of research behind him—was starting his work on classical conditioning. Thorndike's typical experiment involved placing a cat (feline) inside a “puzzle box,” an apparatus from which the animal could escape and obtain food only by pressing a panel, opening a catch, or pulling on a loop of string. Thorndike measured the speed with which the cat gained its release from the box on successive trials. He observed that on early trials the animal would behave aimlessly or even frantically, stumbling on the correct response purely by chance; with repeated trials, however, the cat eventually would execute this response efficiently within a few seconds of being placed in the box.

      Thorndike's procedures were greatly refined by another U.S. psychologist, B.F. Skinner (Skinner, B.F.). Skinner delivered food to the animal inside the box via some automatic delivery device and could thus record the probability or rate at which the animal performed the designated response over long periods of time without having to handle the animal. He also adopted some of Pavlov's terminology, referring to his procedure as instrumental, or operant, conditioning; to the food reward as a reinforcer of conditioning; and to the decline in responding when the reward was no longer available as extinction. In Skinner's original experiments, a laboratory rat had to press a small lever protruding from one wall of the box in order to obtain a pellet of food. Subsequently, the “Skinner box” was adapted for use with pigeons, who were required to peck at a small, illuminated disk on one wall of the box in order to obtain some grain.

      In experiments on both classical conditioning and instrumental conditioning, the experimenter arranges a temporal relation between two events. In Pavlov's experiment the food was always preceded by the conditional stimulus; in Skinner's original experiment the delivery of food was always preceded by the rat's pressing the lever. Conditioning, or associative learning, is inferred if the animal's behaviour changes in certain ways and if that change can be attributed to the temporal relationship between these events. If the dog started salivating to the ticking of a metronome just because it had recently received food, rather than because the delivery of food had been signaled by the metronome, this should be regarded as an instance of sensitization rather than associative learning. One of the simplest ways of establishing that the change in behaviour results from the temporal relationship between the conditional stimulus and the unconditional stimulus in a classical experiment, or between the response and the reinforcer in an instrumental case, is to impose a delay between the two. A gap of even a few seconds between the rat's pressing the lever and the delivery of food will seriously interfere with the animal's ability to learn the connection. And although in some classical experiments evidence of conditioning can be found in spite of relatively long gaps between the conditional stimulus and the unconditional stimulus, increasing this interval beyond a certain point invariably causes a decline in conditioning.

Laws of associative learning
      The temporal relation between the conditional stimulus and the unconditional stimulus, or between the response and the reinforcer, was for a long time regarded as the primary determinant of conditioning. Conditioning is certainly a matter of associating temporally related events, but temporal contiguity is only one of several factors—and probably not the most important—that influences conditioning. A variety of experiments have shown that classical conditioning will occur only if the conditioned stimulus is the best predictor of the occurrence of the unconditional stimulus. In other words, it is the correlation between two events, just as much as their temporal contiguity, that establishes an association between them. A pigeon, for example, will learn by classical conditioning to peck an illuminated disk in a Skinner box if, whenever the disk is illuminated, food is delivered. This temporal relationship between the light and food can be preserved intact, but if the experimenter now arranges that food is equally available at other times (when the light is not on), the pigeon will not peck at the illuminated disk. Delivering food at other times destroys the correlation between light and food (although leaving the temporal relationship untouched) and abolishes conditioning.

      Although some conditioning will occur when the conditional stimulus is not perfectly correlated with the delivery of food (perhaps because on a proportion of trials the conditional stimulus is presented alone without food) or when the temporal relationship is less than perfect (there is a gap between the conditional stimulus and the delivery of food), this conditioning is abolished if the experimenter ensures that there is some better predictor always available. If a dog is conditioned to the ticking of a metronome paired with the delivery of food, the animal will salivate in response to the metronome even if the food is presented in no more than 50 percent of the trials. If, however, a light is illuminated on those trials when the metronome is accompanied by food, and not on the remaining 50 percent of the trials, the dog will become conditioned to the light and not to the metronome. Similarly, a pigeon will learn to peck at a disk illuminated with red light even if a gap of several seconds separates this response from the delivery of food. But if, during this interval, after the red light has been turned off and before food is delivered, a green light is turned on, the pigeon will never learn to peck at the red light. It is as though the pigeon attributes the occurrence of food to the most recent potential cause (now the green light rather than the red), and the dog attributes food to the stimulus best correlated with its delivery (the light rather than the metronome). Conditioning, in other words, occurs selectively to better predictors of reinforcement at the expense of worse predictors. This same principle explains the earlier observation of the role of correlation in general. The pigeon will not associate the illumination of the disk with food if food is equally probable both when the light is on and when it is switched off; from the pigeon's point of view, food occurs whenever the animal is placed in the Skinner box. The illumination of the light signals no increase in the probability of food, and the best predictor of food is the mere fact of being in the Skinner box.

      Temporal contiguity, therefore, is not necessarily the most important factor in successful conditioning. Moreover, there is yet another factor that should be stressed. It will hardly have escaped the reader's attention that there is an astonishing artificiality to the typical conditioning experiment conducted by Pavlov or Skinner. An animal is placed in a bare, confined space; lights are flashed on and off; the animal is permitted to operate some mechanical contrivance; some meat powder or a pellet of food is delivered. How could one possibly suppose that the ways in which animals learn anything of importance in the real world will be illuminated by this contrived and restrictive kind of experiment? This question raises large issues, some of which will recur at later points in this article. But one point should be acknowledged right away: the more restricted the range of experimental manipulations employed, the greater the chance that the investigator will completely miss important principles. Experiments with lights and metronomes failed to reveal the following important principle of conditioning: animals appear to have built-in biases toward associating some classes of stimuli with certain classes of consequences. The most dramatic instance of this principle is provided by conditioned food aversions. If rats (rat) eat some novel-flavoured substance and shortly thereafter are made mildly ill (for example, by an injection of a drug such as apomorphine or lithium chloride), they afterward will show a marked aversion to the novel food. Because they will show an aversion even though an interval of several minutes, or sometimes even hours, intervenes between eating the food and the onset of the illness, there has been some question as to whether this should be regarded as an instance of conditioning at all. But the parallels between food aversions and other forms of conditioning are so extensive that it is hard to believe that some common processes are not involved. And there is no question but that the length of the interval is important; other things being equal, rats will form a stronger aversion to a food they have eaten recently than to one they have eaten several hours earlier.

      The most interesting feature of such aversions is that they are, by and large, confined to foods. If rats suffer the unpleasant experience of being made ill, they are not likely to show an aversion to anything other than a novel-tasting food or drink they have recently ingested. As in other forms of conditioning, the novelty of the potential conditional stimulus is important. Rats will not show any marked aversion to a thoroughly familiar diet unless the experience of illness is repeatedly induced shortly after eating the daily ration, just as, in Pavlov's experiments, conditioning will proceed only slowly to the ticking of a metronome if the dog has heard this sound repeatedly before. The more striking restriction, however, is that it is the taste of the food or drink that is associated with illness. If rats drink plain tap water before being made ill, they will show little aversion to tap water (since there is no novelty here). But even if a novel buzzer is sounded while they are drinking and they are then made ill, they will not associate the buzzer with the illness. This is certainly not because rats are unable to associate the buzzer with an aversive consequence. If drinking water while the buzzer is sounded produces a mild electric shock, rats will rapidly learn to stop drinking whenever they hear the buzzer. In this case it is the flavour of the water that rats find difficult to associate with the shock; punishing rats with a mild shock whenever they drink sugar-flavoured water has little effect on their tendency to drink sugar-flavoured water. The flavour of food or drink is readily associated with subsequent illness, but only poorly associated with other painful consequences. Conversely, an external stimulus such as a buzzer or flashing light, which is readily established as a signal for shock, is only with great difficulty associated with illness. These relationships are summarized in the Table.

      The full explanation of this finding remains uncertain. It is known that even very young rats show such selectivity, so it cannot depend solely on any prior experience. What is easy to see is that this behaviour makes biological sense. Internal malaise, such as that caused in the psychologist's experiment by an injection of lithium, will in the real world usually be a consequence of eating spoiled or poisonous food or of drinking tainted water. The most reliable sign of such food or drink will be its taste, and animals predisposed to associate the taste of what they have ingested with subsequent illness are likely to be better equipped to avoid potentially harmful food in the future. On the other hand, painful injury, mimicked in the laboratory by a brief electric shock, is hardly likely to be a consequence of eating food of a particular flavour; it will usually be caused by external circumstances, such as contact with a sharp or very hot object or a narrow escape from a predator. The natural suggestion is that the function of conditioning is to enable animals to find out what causes certain events of biological significance. If this is so, a built-in bias toward associating certain classes of events together makes adaptive sense. Conditioning is not just a matter of associating two events because one happens to follow the other; it is more profitably seen as the process whereby animals discover the most probable causes of events of consequence to themselves.

Laws of performance
      Conditioning could have no function at all, however, if it did not involve changes in an animal's behaviour. Nor could scientists infer that conditioning has occurred unless they could observe, at some point, a change in an animal's behaviour attributable to certain conjunctions of events. So, although conditioning may involve the formation of associations between events or the attribution of particular events to their most probable antecedent causes, it must also include some mechanisms for translating these associations into changes in behaviour.

      For an earlier generation of behaviourists, the fundamental fact about conditioning was precisely that it changed behaviour, and the theories they advanced were determined by this fact. The description of conditioning as the establishment of a new response to a stimulus that had not previously elicited that response naturally suggested that conditioning was a matter of forming new stimulus–response connections. This conceptualization led to the development of the stimulus–response theory, variations of which long provided the dominant account of conditioning. One version of the stimulus–response theory suggested that the mere occurrence of a new response to a given stimulus, as when Pavlov's dog started salivating shortly after the metronome had started ticking, is in itself sufficient to strengthen the connection between the two. Thorndike, however, argued that the probability that a particular stimulus will repeatedly elicit a particular response depends on the perceived consequences of this response. According to this view, new stimulus–response connections are strengthened only if the response is followed by certain kinds of consequences.

      There are several questions raised here, and it is important to keep them distinct. One is whether responses are sometimes (or even always) modified by their consequences. Although denied by some theorists, their denial seems distinctly paradoxical. A rat whose presses on a lever are followed by the delivery of a food pellet will press the lever again; if the only consequence of pressing the lever is the delivery of a painful shock, the rat will desist from this action. Thorndike's law of effect—which stated that a behaviour followed by a satisfactory result was most likely to become an established response to a particular stimulus—was intended to summarize these observations, and it is surely an inescapable feature of understanding how and why humans and other animals behave. In keeping with this understanding, parents reward children for good behaviour and punish them for bad. When this fails to produce the desired behaviour, we are inclined to argue that the child is finding other sources of reward or does not find the intended punishment particularly unpleasant, or that the parents' behaviour is hopelessly inconsistent. We are far less likely to question the assumption that, other things being equal, people (and other animals) repeat actions that have desirable consequences and avoid repeating those that have undesirable consequences.

      Thorndike's law of effect was, however, also a theory of how reward and punishment modify behaviour. This theory, which states that behaviour normally is modified by changing the strength of stimulus–response connections, finds less general acceptance today. A simple experiment suggests one reason for this. A rat is trained to press a lever in a Skinner box, being rewarded with a small quantity of sucrose solution for each press of the lever. Once the response has been established, the rat is removed from the Skinner box. The next day, while in its home cage, the animal is given sucrose solution to drink and shortly thereafter is made ill by an injection of lithium. Once this treatment has established a strong aversion to the sucrose, the rat is returned to the Skinner box, where, despite the opportunity to do so, the animal does not press the lever again. The result is hardly surprising: there is no reason to expect the rat to perform a response whose sole consequence is the delivery of the now aversive sucrose solution. But this behaviour cannot be explained by Thorndike's theory, for according to Thorndike all that the rat learned in the first stage of the experiment was a new stimulus–response habit; stimuli from the Skinner box should, by Thorndike's reasoning, now elicit the response of pressing the lever. Thorndike's stimulus–response theory credits the rat with no acquired knowledge of the connection between pressing the lever and obtaining sucrose; the function of sucrose is merely to strengthen the stimulus–response connection.

      That responses are modified by their consequences, therefore, need not call for Thorndike's theoretical account of this fact. It is probably more reasonable to suppose that animals learn about the relationship between their actions and consequences (just as they can also learn about the relationship between any other classes of events), and that they then modify their actions in accordance with the current value of these consequences. The next question to consider is whether this is an entirely general principle of performance, or whether it applies only to some classes of response in some kinds of situations. Why, for example, does Pavlov's dog start salivating to the ticking of the metronome? Is it because the response of salivating is followed by a rewarding consequence? The response is, at first, elicited by the sight of food and is shortly followed by the rewarding consequence of chewing and swallowing the food. But another simple experiment suggests that salivating to the metronome is not strengthened because it is followed by food. The experimenter can turn on the metronome for five seconds on each trial, at the end of which time the dog receives food—but only if it did not start salivating before the arrival of food. Now the response of salivating to the metronome is followed by an undesirable consequence, the cancellation of the food that would otherwise have been delivered on that trial, but the dog still cannot help salivating (at least sometimes) to the metronome. The implication is that salivating is not a response modified by its consequences, but one reflexly elicited by food and also by any stimulus associated with food. Voluntary responses can be modified by their consequences; involuntary responses (such as blushing when a person is embarrassed or the release of adrenalin when a person is angry or afraid) cannot. The reason Pavlov's dog starts salivating to the metronome is, just as Pavlov himself supposed, that the association between metronome and food means that the metronome can substitute for food. To put it another way, the metronome now produces activity in neural centres normally responsive to the delivery of food, activity that is reflexly connected to the salivary response.

      It should not be thought that only autonomic, glandular responses are involuntary in this sense. If a small light is always illuminated for five seconds before the delivery of food to a hungry pigeon, the pigeon will learn, by classical conditioning, to approach and peck at the light. Exactly the same experiment as that described above can be undertaken, with food delivered only on those trials when the pigeon does not approach and peck the light during the initial five seconds. The pigeon cannot help doing so. Pavlovian conditioning appears to be a widespread phenomenon, applying to a relatively wide range of responses.

Functions of conditioning
      The behaviour of the dog and pigeon in the above experiments seems maladaptive, precisely because it violates the law of effect. If the way to obtain food is to refrain from performing a particular response, then that is what the law of effect says the animal should do. The law of effect makes obvious adaptive sense; several writers, indeed, have pointed to the analogy between the law of effect and natural selection. Just as natural selection favours those variations that happen to increase fitness, so the law of effect selects those responses that happen to be followed by certain consequences.

      The fact that Pavlovian conditioning may result in apparently maladaptive behaviour in the artificial confines of the experimental psychologist's laboratory, however, does not mean that it is not adaptive in the real world. The pigeon's behaviour provides a clue. In a normal classical conditioning experiment, where the illumination of a small light regularly precedes the delivery of food, the pigeon will rapidly learn to approach and direct pecks at the light. Approach and pecking are food-related activities: what is happening is that a simple process of Pavlovian conditioning is ensuring that responses related to food are being elicited by stimuli associated with food. It is not difficult to appreciate the adaptive significance of a process that results in animals approaching places where they have found food in the past, or in learning that a particular novel object is in fact an example of food, and directing food-related activity toward these stimuli in the future.

      Pavlovian conditioning also affects other significant behaviours. For example, it probably provides the basic process by which animals learn to avoid poisonous foods. If a novel food is associated with illness, its taste will elicit responses of disgust or nausea, ensuring that the substance will subsequently be rejected after the first taste. In territorial birds and fish, aggressive displays and attacks can become conditioned to stimuli that regularly precede the appearance of a rival male. A male already primed to threaten and attack an intruder, because he has learned that certain signs herald the appearance of the intruder, should be more successful in defense of his territory than the male that is unprepared. Experimental analysis has, in fact, nicely confirmed this expectation. In general, any pattern of defensive behaviour that is adaptive in response to an intruder or predator—such as displaying or fighting, fleeing or taking other evasive action, or freezing into immobility or feigning death—will be even more adaptive if performed in advance, at the first reliable signal of the predator's or intruder's appearance.

      The process of Pavlovian conditioning thus often enables animals to behave appropriately in anticipation of events of biological significance, without involving any direct modification of that behaviour by its success or failure. But further modification must sometimes be of further advantage. For instance, it is not always enough just to approach a stimulus associated with food; if that stimulus is a prey species, it may take evasive action that will require much more elaborate behaviour on the part of the predator. This can be seen in the feeding behaviour of the oystercatchers (oystercatcher), a group of birds that eat bivalve mollusks. Oystercatchers first catch their pray by probing down the hole made by the bivalve in the mud; the sight of the hole must be rapidly established as a conditional stimulus for food. But the birds must then perform a complex series of actions to get at the mollusk's flesh, and this skilled sequence of responses also must be learned, presumably in accordance with the law of effect. Similarly, many animals have a wide range of defensive behaviour patterns; in the laboratory, at least, which one eventually predominates in any given situation normally depends on which one successfully enables the animal to escape or to avoid aversive consequences. In all these cases, it appears that instrumental conditioning serves to modify, via the law of effect, initial responses that owed their origin to Pavlovian conditioning.

      The adaptive value of instrumental conditioning is an area of research that has seen some fruitful collaboration among experimental psychologists, ethologists, and behavioral ecologists. From ecology has come the “optimal foraging theory,” the idea that efficient foraging behaviour should maximize an animal's net rate of food intake. From ethology and experimental psychology has come the idea that an animal's instrumental behaviour in any given situation is a product of competition between various possible activities, a competition whose resolution depends on weighing the costs and benefits of increasing one activity at the expense of another. Both in the laboratory and in more natural settings, for example, the proportion of time spent searching for one kind of food depends not only on the probability of finding that food and on its value when found but also on the probability of the animal finding an alternative food if it looks elsewhere. There is also abundant evidence that animals improve their foraging efficiency with practice; this clearly must depend on learning which stimuli signal the availability of which kinds of food, the most efficient way of taking a given food, and the most effective distribution of time between alternatives.

Spatial learning
      One of the major problems many animals must confront is how to find their way around their world—for example, to know where a particular resource is and how to get to it from their present location, or what is a safe route home to avoid a predator. Such spatial learning may cover only the highly restricted confines of an animal's home range or territory, or it may embrace a migration route of several hundreds or even thousands of miles. Although some forms of navigational behaviour may be explicable in relatively simple terms, not necessarily requiring appeal to processes more complex than those of simple conditioning, others suggest some quite new principles.

Maze learning
      In the psychologist's laboratory, the primary method of studying spatial learning has been to put a rat in a maze and watch how it finds its way to the goal box, where it is fed. As befits the analytic (some would say sterile) approach so popular in experimental psychology, the elaborate and complex mazes used in earlier studies (the very first published experiment used a scaled-down replica of the maze at Hampton Court, London) soon gave way to something very much simpler, a T-maze or Y-maze. A rat placed at the end of one arm must run to the central choice-point, from where it has to enter one of the two remaining arms. Although extremely simple, even this apparatus allows for a number of possible modes of solution. One possibility is that the rat learns to execute a particular response, a left turn or a right turn, at the choice-point, because that response is followed by food. A second possible solution is that the rat learns that the two alternative arms differ in some particular way and further learns to associate one of the arms with food and hence to choose it. The third and most interesting possibility is that the rat learns to define the rewarded arm not in terms of its own intrinsic characteristics but by its spatial relationship to an array of landmarks outside the maze. Thus the rat might learn that the correct arm is the one pointing to the left of a window and away from a table with a lamp on it. Experiments show that whenever such landmarks are available, this third solution mode is the one used.

      Perhaps the most convincing demonstration that rats can find their way to a particular location—one defined solely in terms of its spatial relation to various external landmarks—has been provided by experiments in which the animals are placed in a large circular tank of water and must swim to a transparent platform submerged somewhere in the middle of the tank. They can rapidly learn to do this, regardless of where they are initially put into the tank and even though the platform itself is invisible. (The invisibility of the platform is shown by the following: if the platform is moved, the rat will swim straight past it, heading instead toward the position it used to occupy.)

      Rats in these experiments are not simply approaching a single landmark; they locate their goal by reference to its spatial relationship with a whole series of landmarks, no one of which is necessary. This can be established by using half a dozen arbitrary but easily identified objects as landmarks during maze training. Removal of any one or two of them in no way disrupts the rat's behaviour. If all the landmarks are systematically rotated around the room, the rat will identify a new arm of the maze as correct (the one that has the same relationship to the landmarks as the initially correct arm). If, however, the landmarks are rearranged in such a way as to destroy their original spatial relationship to one another, the rat does not know which arm to choose.

      The processes involved in this sort of learning are not well understood. Some psychologists have been sufficiently impressed by the rat's flexibility in these experiments to argue that the animal is constructing a map of its environment—not, obviously, a written map but an internal, maplike representation that encodes a complete set of spatial relationships between major landmarks. The best evidence for such a maplike representation would be if a rat could take an unfamiliar route when its original route to a goal is blocked. Unfortunately, there is little evidence of such performance in rats, except in the not especially critical case where the goal, or a stimulus very close to it, is clearly visible from the choice-point. On the other hand, studies of long-range navigation have shown that some animals can do just this.

       salmon return from the ocean to spawn in the stream in which they were hatched; swallows return to the same nest sites in northern Europe each spring from wintering in southern Africa. These and other examples of large-scale migrations (migration) have long fascinated students of animal behaviour, and experimental intervention has produced some remarkable results. A Manx shearwater was taken in an airplane from its breeding site on the island of Skokholm, off south Wales, to Boston, Mass. It returned to Skokholm within 13 days of being released in Boston; the direct distance between these two points is 3,050 miles, which implies (assuming that the bird did not fly at night) a minimum average speed in excess of 20 miles per hour. An albatross flew from a release site in the Philippines to its home in Midway Island, a direct distance of 4,120 miles, in 32 days.

      How do these animals navigate across such great distances? Numerous cues have been implicated in different instances. Near to home, animals probably rely on local cues quite different from those used at a distance. For example, experiments show that salmon distinguish their home streams on the basis of smell, although this sense can hardly come into play while the fish are swimming in the open ocean. Other investigations have demonstrated that diurnal birds use visual information derived from the position of the Sun, while those that migrate at night rely on the pattern of the stars. There have been several suggestions that certain long-range migrators are sensitive to the Earth's magnetic forces; sensitivity to auditory cues has also been suggested in some cases.

      The most intensive analysis of long-range navigation has been undertaken with homing pigeons. These birds are trained by being released from sites progressively further from their home loft. Just what the pigeons learn on these training flights is not entirely clear. In part, they obviously learn the visual landmarks immediately surrounding the home loft, but experimental evidence suggests that they use such landmarks only very close to home. Once some training has been given, however, a pigeon can be taken 100 miles or more in any direction from home, and it will, within a few minutes of its release, start flying in a homeward direction.

      One general class of theory on homing behaviour postulates that the pigeon detects a discrepancy between a particular set of stimuli observed at the release site and its stored knowledge of what that set of stimuli should be like at home, and it then flies in such a direction as to reduce this discrepancy. Different versions of this theory appeal to different sets of stimuli that might be used to guide the pigeon home. At one time, a popular idea was that the pigeon used the Sun's height in the sky in combination with an internal clock (biological rhythm). At any given season and time of day, the Sun's height in the sky—and, by extrapolation from its current rate of climb, its maximum height—are unique to a single place (in this case, the pigeon's home). Assuming that the pigeon's home loft and the release site are both in the Northern Hemisphere, then if the Sun's maximum height is lower at the release site, the release site is north of home; if higher, then the release site is south of home. If the Sun will reach its maximum height later than at home, the release site is west of home; if earlier, the site is east of home. If released at noon at a site in the Northern Hemisphere 200 miles northeast of home, the pigeon must fly so as to raise the maximum height of the Sun (i.e., south), and so as to stop the Sun falling (i.e., west).

      This explanation is immensely ingenious and, although calling for some astonishingly fine sensory discriminations on the part of the pigeon, not impossible in principle. Unfortunately, it is probably wrong. Two critical experiments have produced results quite at variance with its predictions. The first suggested that pigeons do not rely on the height of the Sun to navigate at all. In this experiment, the pigeons were confined to a laboratory from which they could see the Sun for only a relatively short time around noon each day, and the apparent height of the Sun above the horizon was raised or lowered by allowing the birds to view the Sun only through a complex series of mirrors. This should have had drastic effects on their perception of the true position of their home; for instance, an increase of 70′ in the apparent height of the Sun at noon would correspond to an 80-mile southward relocation of the home. The pigeons were then taken from home and released 40 miles south, where they saw the real Sun for the first time in several weeks. If the Sun's height was indeed a critical stimulus in navigation, the pigeons would be expected to fly south rather than north. In fact, they correctly flew north.

      The second experiment involved shifting the birds' internal clock, by confining them indoors and exposing them to a new light–dark cycle. Independent observations had shown that this procedure is entirely successful: if a bird is confined indoors for a few weeks with the lights switched on every day at midnight and switched off at noon, its clock soon will be entrained on this new cycle, so that 6:00 AM is regarded as the middle of the day. In the critical experiment, the bird was taken out of the laboratory and released at 6:00 AM (true time) from a site 50 miles south of home. The Sun, now seen for the first time in several weeks, was just rising; but, according to the pigeon's internal clock, the time at home was noon. This implied that the release site was a long way west of home, and if the pigeon were using the height of the Sun as a cue to guide it home, it should have flown east. In fact, the pigeon flew west.

      The result of the second experiment indicates that the pigeon was using the position of the Sun in the sky, and that the clock shift had been effective (for the pigeon was not flying in the direction of home). This is readily explained by the hypothesis that the pigeon used the Sun as a compass. If we allow, for the sake of argument, that the pigeon knew that the release site was south of home, then it should have tried to fly north. In the Northern Hemisphere at noon, the Sun is due south; therefore, the pigeon—whose internal clock said it was noon—should fly away from the Sun. But although the pigeon's shifted clock said that it was noon, the true local time was 6:00 AM, and the Sun was in the east. Flying away from the Sun, the pigeon flew west. This experiment then suggests first, that the pigeon was not using the height of the Sun at all; second, that it used the Sun's horizontal position, or azimuth, to provide a compass bearing; and, third, and most important, that the pigeon had some other map that told it that the release site was south of home. In general, a compass is of no use without a map.

      The basis for the map component of the pigeon's navigational skill remains extremely obscure. There is evidence from studies of many migratory birds that the compass component is in some sense innate, but that a map of the relative positions of the summer and winter habitats and of other places in between (or even not in between) develops only with the experience of migration. For example, starlings (starling) that breed around the Baltic Sea fly southwest in autumn to winter in southern England, northern France, and Belgium. When captured during this autumn migration and released in Switzerland (some 500 miles south of their normal route), experienced, adult birds flew back to northern France and Belgium—even though they had presumably never flown over any part of this route before. Young birds, however, for whom this was the first migration, flew southwest from Switzerland and ended up in southern France or northern Spain. They clearly had a compass that told them which direction was southwest; what they lacked was any knowledge of the spatial relationship between their present location in Switzerland and their goal in northern France.

Perceptual learning
      According to Thorndike's stimulus–response theory, learning, which is reducible to the strengthening and weakening of the tendency to perform a particular response in the presence of a particular stimulus, occurs only when that response is performed; learning, in other words, depends on trial and error. Even in the realm of simple conditioning, there are good reasons to question this restriction. Conditioning is better conceptualized as the acquisition of knowledge about temporal relationships between events rather than as the acquisition of behaviour. Spatial learning seems to be a matter of learning about spatial relationships between objects and places in one's environment and, apparently, the construction of some sort of map that will subsequently permit the animal to perform a new sequence of actions across unknown territory. This section considers other examples of learning, in which at least part of what an animal appears to acquire is the recognition of a more or less complex set of stimuli that subsequently can be used to guide its actions.

Imitation and observational learning
      One reason why Thorndike adopted such a narrow, behavioral view of learning was that he looked for evidence of other forms of learning without success. Having taught one cat to escape from the puzzle box by operating a latch, he looked to see whether a second cat would acquire the correct solution simply by watching the first. A series of such experiments produced uniformly negative results, and Thorndike concluded that trial and error was the only form of learning available to animals other than humans.

      Why Thorndike should have been so unsuccessful is something of a mystery, for later experiments have established quite convincingly that animals can often benefit from watching another member of their species perform a particular task. Casual observation in natural settings, for instance, reveals that young chimpanzees intently watch their elders perform intricate tasks; this certainly suggests that learning by observation is very common in some species.

      Experimental analysis has revealed a number of important distinctions concerning the role of observation in behaviour. For example, domestic chickens (chicken) that have eaten to satiation a particular source of food will start eating again if they observe other chickens feeding. Although the observation of conspecifics engaged in a particular activity has clearly affected the tendency of the satiated chicken to engage in that activity, it is not clear what they might have learned from this observation. They already know how to peck, and they already know that the grain before them is palatable food. It is probably more appropriate to regard this as an instance of “social facilitation” and to say that one of the stimuli that elicits feeding in chickens is the sight of other chickens feeding.

      The example above demonstrates the minimum requirement for establishing that an animal has learned by observation: in the absence of the opportunity to observe another, the animal must have been unlikely to have performed a particular response, and the reason for this must reside in lack of knowledge. An artificial, laboratory example of observational learning would be to allow an observer rat to watch a demonstrator rat pressing a lever for food. If the observer has never before pressed a lever and, given the opportunity, now does so much more rapidly than another rat denied the opportunity to observe the demonstrator, surely some genuine observational learning has occurred. But even here it remains difficult to establish exactly what it is that the observer has learned by watching the demonstrator, and more elaborate experiments may be required to elucidate this. An experiment with two monkeys (monkey) showed how this may be done. The monkeys took turns acting as demonstrator and observer. The demonstrator's task was to choose between two objects, one of which contained some hidden food. Since the objects were changed on each new trial for the demonstrator, there was no way for the animal to know which choice was correct, and it necessarily picked one at random. The observer, however, could watch the demonstrator's trial and thus could find out which of the two objects in a particular set was correct. Given an opportunity to choose between the two, the observer more often than not chose correctly. That the observer was not simply watching the demonstrator, but was in fact looking to see the outcome of the choice, is established by the finding that the observer performed somewhat more accurately on those trials when the demonstrator's choice was wrong than on those when it was right.

      This last finding points to a further distinction, that between observing the actions of another and imitating those actions. In this particular experiment, the monkeys clearly were not imitating one another, or they would have copied each other's choices even when these were wrong. A demonstration of imitation is provided by the behaviour of oystercatchers feeding on mussels. Having found a mussel, an adult oystercatcher obtains the food from within either by inserting its beak in the right place and cutting the muscle that holds the shell together or by pecking a hole in the weakest point of the shell. Young birds develop the method employed by their parents, but experiments in which chicks were fostered by adults with a different habit from that of the natural parents have established that this behaviour is not genetically determined. Rather, the young birds imitate the actions they observe being performed by their foster parents.

      The best known natural example of such imitation was provided by a troop of macaques (macaque) in Japan. In order to lure the monkeys out of the forest and into the open, where their behaviour could be better studied, scientists routinely left sweet potatoes and wheat on the beach. The monkeys ate this food but clearly disliked the fact that it had become liberally mixed with sand. A young female member of the troop, however, discovered that sweet potatoes could readily be washed free of sand, and that a handful of wheat and sand could be thrown into a pool, where the sand would sink, leaving the wheat floating behind. Both customs spread through the troop, first to the immediate family and young companions of the original inventor, and last of all (an interesting touch) to the old, conservative males. Other examples of observational learning are readily apparent in the behaviour of animals in the field, but in many cases, as in some of the laboratory studies cited above, it remains difficult to elucidate just what it is that has been learned.

song learning
      A special case of observational learning is that of young birds acquiring their species-typical song. Numerous species of animals, including many birds, produce species-typical calls or other vocalizations as adults; in many cases, however, there is little evidence that learning plays any significant role in their development. In many species of crickets, for example, the song is stereotyped, and the pattern of neural activity that produces the song can be detected even in young animals who neither sing nor apparently react to the adult song. But in most songbirds, there is reason to believe that learning has a significant effect on the development of the adult song.

      The interesting feature of this learning is that it sometimes occurs in two distinct phases separated by several months. The first of these can be regarded as purely observational learning, the second as the perfection of the song through practice (i.e., as imitation of a model). Song sparrows, for example, do not develop a normal adult song unless they have the opportunity to hear the song during their first autumn. There is thus a sensitive period during which they must hear their species' song if they are to develop normally, but it is important to note that they do not themselves sing at all during the first autumn. It is not until the next spring that they start practicing the song. At this point, they do not need to hear other sparrows singing, but they do need to hear themselves. If the bird is deafened before it starts practicing, only a very crude song emerges. The implication is that, during exposure in the first autumn, the sparrow learns to identify the detailed song and establishes a template of it; the following spring, the sparrow starts singing and needs practice to match its output to the stored template.

      The song sparrow provides an example of a particularly clear separation between observation and imitation. In other species, such as the chaffinch, the young bird learns from exposure to song in the first autumn, but refinement of the song is produced by further exposure to other chaffinches singing during the following spring. In yet others, such as indigo buntings, the adult bird learns its song from territorial neighbours. But even where there is no temporal separation between the two aspects of learning, it still seems valid to distinguish between the learning involved in establishing the template and that involved in perfecting the motor skill.

      If song learning consists solely of the young bird learning to reproduce the adult, species-typical song, one might wonder why any learning should be necessary at all. Why should the song not develop simply through maturation, or, in other words, why is not the template, at least, genetically laid down in the bird's brain? In fact, studies indicate that a relatively crude template is innately determined in most species. There are very strict limits to the range of songs that a bird of one species can learn. Moreover, among chaffinches and certain other species, even if a young bird hears no song at all it will still develop a crude song that has recognizable features of the full, species-typical one. The degree of this innate specification varies widely from species to species: at one extreme are such birds as cuckoos, which develop a standard call with no prior exposure at all; at the other extreme are such birds as marsh warblers, which develop idiosyncratic songs picked up, it seems, from any other species they come in contact with during the sensitive period.

      Species whose song acquisition involves a great deal of individual learning are probably those in which individual birds develop slightly different songs. In some species, such as song sparrows, there are recognizable local “dialects” that the young birds learn from adults living in the same region. In other species, there is even more variation between individuals. If one function of the song is to attract a mate, then an interplay is called for between a song that simply advertises the singer's species and one that establishes his individual identity. The importance of individual learning, then, depends on the role of the song in the mating patterns of the species.

      The young of many species are born relatively helpless: in songbirds, rats, cats, dogs, and primates, the hatchling or newborn infant is wholly dependent on its parents. These are altricial species. In other species, such as domestic fowl, ducks, geese, ungulates, and guinea pigs, the hatchling or newborn is at a more advanced stage of development. These are precocial species, and their young are capable, among other things, of walking independently within a few minutes or hours of birth, and therefore of wandering away from their parents. Since mammals are dependent on their mothers for nourishment, and even birds are still dependent on parental guidance and protection, it is important that the precocial infant not get lost in this way. The phenomenon of filial imprinting ensures that, in normal circumstances, the precocial infant forms an attachment to its mother and never moves too far away.

      Although imprinting was first studied by the Englishman Douglas Spalding in the 19th century, Konrad Lorenz (Lorenz, Konrad) is usually, and rightly, credited with having been the first not only to experiment on the phenomenon but also to study its wider implications. Lorenz found that a young duckling (duck) or gosling learns to follow the first conspicuous, moving object it sees within the first few days after hatching. In natural circumstances, this object would be the mother bird; but Lorenz discovered that he himself could serve as an adequate substitute, and that a young bird is apparently equally ready to follow a model of another species or a bright red ball. Lorenz also found that such imprinting affected not only the following response of the infant but also many aspects of the young bird's later behaviour, including its sexual preferences as an adult.

      Imprinting, like song learning, involves a sensitive period during which the young animal must be exposed to a model, and the learning that occurs at this time may not affect behaviour until some later date. In other words, one can distinguish between a process of perceptual or observational learning, when the young animal is learning to identify the defining characteristics of the other animal or object to which it is exposed, and the way in which this observational learning later affects behaviour. In the case of song learning, observation establishes a template that the bird then learns to match. In the case of imprinting, observation establishes, in Lorenz' phrase, a model of a companion, to which the animal subsequently directs a variety of patterns of social behaviour.

      With imprinting, as with song acquisition, one can ask why learning should be necessary at all. Would it not be safer to ensure that the young chick or lamb innately recognized its mother? There are, in fact, genetic constraints on the range of stimuli to which most precocial animals will imprint. A model of a Burmese jungle fowl (the species whose domestication produced domestic chickens) serves as a more effective imprinting object for a young chick than does a red ball; there is even evidence that imprinting in the latter case involves different neural circuits from those involved in imprinting to more natural stimuli. Nonetheless, it is clear that the innate constraints are not very tight and that a great deal of learning normally occurs. The most plausible explanation, as in the case of song learning, is that imprinting involves some measure of individual identification. Lorenz argued that one of the unique characteristics of imprinting was that it involved learning the characteristics of an entire species. It is true that imprinting results in the animal directing its social and mating behaviour toward other members of its own species, and not necessarily toward the particular individuals to which it was exposed when imprinting occurred. But learning usually involves some generalization to other instances, and there does not seem to be anything peculiar to imprinting here. The primary function of imprinting, however, is to enable the young animal to recognize its own mother from among the other adults of its species. This no doubt is particularly important in the case of such animals as sheep, which live in large flocks. Only learning could produce this result.

      There is also an important element of individual recognition in at least some cases of imprinting's effects on sexual behaviour. Experiments with Japanese quail have shown that their sexual preferences as adults are influenced by the precise individuals to whom they are exposed at an earlier age. Their preferred mate is one like, but not too like, the individuals on whom they imprinted. The preference for some similarity presumably ensures that they attempt to mate with members of their own species. The preference for some difference is almost certainly a mechanism for reducing inbreeding, since young birds will normally imprint on their own immediate relatives.

      The difference between imprinting and song learning lies in the consequences of observational learning. The effect of imprinting is the formation of various forms of social attachment. But what mechanism causes the young chick or duckling to follow its mother? Lorenz thought that imprinting was unrewarded, yet the tendency of a young bird to follow an object on which it has been imprinted in the laboratory can be enhanced by rewarding the bird with food. Rewards also occur outside the laboratory: the mother hen not only scratches up food for her young chicks, she also provides a source of warmth and comfort. Moreover, following is also rewarded by a reduction in anxiety. As chicks develop over the first few days of life, they show increasing fear of unfamiliar objects; they allay this anxiety by avoiding novel objects and approaching a familiar one. This latter object must be one to which they have already been exposed—in other words, one on which they have imprinted. Imprinting works because newly hatched birds do not show any fear of unfamiliar objects, perhaps because something can be unfamiliar only by contrast with something else that is familiar. On the contrary, the newly hatched birds are attracted toward salient objects, particularly ones that move. Once, however, a particular object has been established as familiar and its features identified, different objects will be discriminated from it. These will be perceived as relatively unfamiliar, and hence they will provoke anxiety and the attempt to get as close as possible to the more familiar object. The imprinting of the young bird on one object necessarily closes down the possibility of its imprinting on others, as these will always be relatively less familiar. Thus, there is normally a relatively restricted period in the first few hours or days of life during which imprinting can occur. The only way to prolong this period is to confine the newly hatched bird to a dark box where it is exposed to no stimuli; prevented from imprinting during this period of confinement, the bird imprints on the first salient object it sees after emerging.

Complex problem solving
      Experimental psychologists who study conditioning are the intellectual heirs of the traditional associationist philosophers. Both believe that the complexity of the human or animal mind is more apparent than real—that complex ideas are built from simple ideas by associating simple elements into apparently more complex wholes. According to this perspective, the only relationship between these ideas is their association, and the determinants of these associations are themselves relatively simple and few in number. Neither conditioning theorists nor associationist philosophers, however, have lacked for critics, who claim that intelligent problem solving cannot be reduced to mere association. Although allowing that the behaviour of invertebrates, and perhaps that of birds and fish, may be understood in terms of instincts and simple forms of nonassociative and associative learning, these critics maintain that the human mind is an altogether more subtle affair, and that the behaviour of animals more closely related to man—notably apes and monkeys, and perhaps other mammals as well—will share more features in common with human behaviour than with that of earthworms, insects, and mollusks.

      The idea that animals might differ in intelligence, with those more closely related to humans sharing more of their intellectual abilities, is commonly traced back to Charles Darwin (Darwin, Charles). This is because the acceptance of Darwin's theory of evolution was at the expense of the ideas of the French philosopher René Descartes, who held that there is a rigid distinction between man, who has a soul and can think and speak rationally, and all other animals, who are mere automatons. The Cartesian view had, in fact, been challenged long before Darwin's time by those who believed (as seems obvious from even the most casual observations) that some animals are notably more complicated than others, in ways that probably include differences in behaviour and intelligence. It was, however, the publication of Darwin's Descent of Man (1871) that stimulated scientific interest in the question of mental continuity between man and other animals. Darwin's young colleague, George Romanes, compiled a systematic collection of stories and anecdotes about the behaviour of animals, upon which he built an elaborate theory of the evolution of intelligence. It was largely in reaction to this anecdotal tradition, with its uncritical acceptance of tales of astounding feats by pet cats and dogs, that Thorndike undertook his studies of learning under relatively well-controlled laboratory conditions. Thorndike's own conclusions, already noted above, were distinctly Cartesian: animals ranging from chickens to monkeys all learned in essentially the same way, by trial and error or simple instrumental conditioning. Unlike man, none could reason.

      This controversy actually involves two questions, which are worth keeping apart. The first is whether theories of learning based on the results of, say, simple conditioning experiments are sufficient to explain all forms of learning and problem solving in animals. The second question is whether new and more complex processes operate only in some animals, that is to say, whether some animals are more intelligent than others. The distinction between these questions is not always easy to preserve, for they are clearly related, and an answer to one usually has implications for the other. The remainder of this article is organized around the first question; in cases where the behaviour of an animal does, in fact, seem to indicate that more complex processes are involved, the second question is also considered.

discrimination of relational and abstract stimuli
      Laboratory studies of habituation and conditioning usually employ very simple stimuli, such as lights, buzzers, and ticking metronomes in Pavlov's experiments. Some of the other examples of learning considered earlier have already suggested that animals can actually respond to additional, more complex stimuli. Even the solution of simple spatial discriminations in the laboratory requires the animal to learn about spatial relationships between different landmarks; migration or navigation over hundreds of miles demands abilities at least as complex as this. Song learning requires the young bird to discriminate between different sequences of subtly varying notes and calls, and the individual recognition involved in imprinting requires response to elaborate configurations of features.

      Thus, one way in which a problem may become more difficult is if its solution depends on response to more subtle changes in stimuli. Numerous laboratory studies have examined the abilities of a variety of animals to perform such discriminations. The phenomenon of transposition, first studied in chicks by the Gestalt psychologist Wolfgang Köhler (Köhler, Wolfgang), suggests that animals may solve even simple discriminations in ways more complex than the experimenter had imagined. Köhler trained his chicks to perform simple discriminations—say, to choose a large white circle (five centimetres in diameter) in preference to a small white circle (three centimetres in diameter). He then sought to discover whether the animal was responding to the relationship between the two stimuli or to the absolute characteristics of the stimuli. In other words, had the chick learned to select the larger of the two circles, or had it learned to pick the five-centimetre circle? If the former were the case, Köhler reasoned that given the choice between the five-centimetre circle and an even larger one (eight centimetres in diameter), the animal should transpose the relationship and choose the larger circle. This was indeed the result, demonstrating that the animal was responding in terms of the relationship between stimuli rather than, or at least in addition to, their absolute properties.

      Transposition experiments show that animals can respond to relationships between stimuli varying along a particular continuum of physical characteristics: size, brightness, hue, etc. Another question is whether animals can respond to an abstract property of a stimulus array, independent of the actual physical stimuli making up that array. In experiments on counting, the animal must choose between an array containing, say, five stimuli and one containing three. The actual stimuli in the array vary from trial to trial, in order to rule out the possibility that the animal is responding in terms of other features, such as differences in total area or brightness, between the arrays. Counting experiments have been tried on birds more frequently than on any other class of animal, and several species, notably ravens, rooks, and jackdaws, have solved this type of problem. This success may not be entirely by chance, for there is reason to believe that the stimulus that controls when a female bird stops laying eggs is something to do with the number of eggs already laid and in the nest. Chimpanzees, however, have been trained to label pictures of various objects (e.g., spoons, shoes, padlocks, and balls) with the numeral specifying the number of objects in the picture. Moreover, rats and other standard laboratory animals have solved similarly abstract discriminations, for example, of temporal duration. A rat can learn to perform one response after a stimulus has been turned on for two seconds and a different response after the stimulus has been turned on for five seconds. The nature of the actual stimuli employed can vary without disrupting the rat's discrimination, suggesting that it is the duration of the stimuli to which the rat responds.

      Concept (concept formation) learning makes up another class of discriminations that may be solved by the abstraction of a particular property or set of properties from a very wide array of individual stimuli. In a typical experiment, a pigeon is shown a large number of colour photographs of natural scenes: half of these contain, somewhere within the scene, all or part of a tree or group of trees; the other half contain no tree (although there might be flowers, a climbing rose, or other plants). Responding to the pictures of trees is rewarded, but responding to the remaining pictures is not. Pigeons rapidly learn the discrimination. In one sense, perhaps this is not surprising: birds that roost in trees, one is inclined to argue, must be able to recognize them. But pigeons can learn other discriminations with almost equal facility; for example, they can be trained to distinguish between underwater scenes containing a fish and similar views with no fish present. In such cases, the class of stimuli in question is one for which their evolutionary history can hardly have prepared pigeons. The question, of course, is how the pigeons solve such problems. Are they, in some sense, abstracting a conceptual rule for categorizing the world into classes of stimuli? Or are they responding to what is no doubt a very large number of particular features that differentiate trees or fish from other objects in the world?

      Pigeons, in common with most birds, rely more heavily on vision, and certainly have better developed colour vision, than most mammals—with the exception of primates. There is evidence that monkeys can solve the concept discriminations that have been set to pigeons, but there is no evidence that other mammals can. For extensive comparative analysis, therefore, it is necessary to turn to different kinds of tasks. One that has been studied almost to excess is discrimination reversal. In reversal tasks, an animal is first trained on a simple discriminative problem: for example, to choose the left-hand arm of a T-maze, where it is rewarded, rather than the right arm, where it is not. Once the animal has solved the problem, the experimenter reverses the reward assignments, so that the food is now in the right arm rather than the left. Training continues until the animal has learned this reversal, whereupon the assignment of reward is switched back to the left arm. And so on. Rats trained on this series of reversals eventually become extremely adept at the task. Although the initial reversal causes considerable problems, with animals making many more errors than on the original discrimination, after a few more reversals these difficulties vanish. Eventually, rats solve each new reversal in fewer trials than they took to solve the original discrimination, often with no more than a single error.

      Similarly efficient performance has been observed in a relatively wide range of mammals. More interesting was the early suggestion that the few species of fish ( goldfish, African mouthbreeders, and Paradise fish) trained on similar problems showed no evidence of the increase in efficiency displayed by mammals. The fish would learn the first reversal slowly and laboriously, and the 20th reversal equally slowly. Subsequent experiments have established that this was an unfairly pessimistic assessment, for improvements in experimental techniques have been accompanied by a significant improvement in the fish's performance, a finding that highlights the extreme difficulty of assessing the relative efficiency of widely differing animals on supposedly the same task. Nevertheless, it remains doubtful that goldfish are as adept at reversal tasks as rats are.

      The theoretical question, however, is how rats attain such efficiency. What processes allow them eventually to learn the reversal of a discrimination faster than they originally learned the discrimination itself, and often with only a single error? The most plausible suggestion is that they develop a “win–stay, lose–shift” strategy. They learn, in other words, to characterize the alternatives between which they must choose not in terms of their physical features but in terms of whether or not they chose it on the previous trial. They then learn that, if the alternative they chose on the last trial was rewarded, choice of that alternative will be rewarded again on the current trial; while, if it was not, choice of the other alternative will now be rewarded. A variety of other experiments have shown that rats can rapidly learn to use the outcome of one trial to predict the outcome of the next, and hence keep track of regular sequential dependencies in the availability of food or other rewards.

Generalized rule learning
      Second only to the reversal task in popularity as a tool for the comparative analysis of learning has been the learning set task. The latter is designed to measure the animal's ability “to learn to learn”—in other words, to discover whether after having learned a new behaviour the animal can then more readily learn other related behaviours. For example, an animal is trained on a simple discrimination between two objects, A and B. Once the problem has been solved, the experimenter substitutes a new pair of objects, C and D, for the original pair; when the animal has solved this new problem, yet another new pair, E and F, is substituted, and so on. Rhesus monkeys (rhesus monkey) trained on such a series of problems become progressively more efficient at solving each new problem. Like rats trained on reversal tasks, the monkeys eventually solve each new problem after a single trial, choosing at random on the first trial with each new pair of stimuli but thereafter selecting with essentially perfect accuracy.

      Performance on learning sets, as on reversals, was once thought to discriminate between more intelligent and less intelligent animals. Apes and rhesus monkeys were extremely efficient at such tasks, more so even than New World monkeys, who were, in turn, more efficient than any nonprimate mammals. Again, however, there are grave difficulties in the way of making valid comparisons. Primates (primate) have better developed visual systems than most other mammals, so it is not surprising that they should be better at solving a series of visual discrimination problems. Even the difference in performance between rhesus and cebus monkeys (Old World versus New World monkeys) turns out to be attributable to differences in colour vision more than anything else. Rats appear to solve learning set tasks very efficiently if olfactory stimuli are used.

      Nevertheless, there may be important intellectual differences also underlying the differences in performance. One reason for thinking so arises from consideration of the processes probably involved in mastering learning sets. The win–stay, lose–shift strategy that explains the progressive improvement in reversal learning can also explain the same improvement in the learning set task—but only if the animal can generalize the strategy to novel stimuli. Successful performance requires that the animal learn that the alternative chosen on the last trial, and the outcome of that choice, predict which alternative will be rewarded on this trial, whatever the nature of the alternatives. Some evidence suggests that primates can generalize rules of this sort more readily than many other animals can. Monkeys trained on a series of reversals of a single discrimination will learn the reversal of any new discrimination with equal facility. By contrast, cats trained on comparable problems show little evidence of such transfer.

      A discriminative problem widely used in the study of transfer is the “matching-to-sample” discrimination. A pigeon, for example, is required to choose between two disks, one illuminated with red light and the other with green light. The correct alternative on any one trial depends on the value of a sample stimulus, which is also part of each trial. If this third light is red, then the red disk is correct; if green, then green is correct. The correct alternative is the one that matches the sample. Although naturally more difficult than the simple red–green discrimination, matching-to-sample discriminations are learned readily enough by a wide variety of animals; however, there appear to be differences among animals in their capabilities to transfer this learning to a new set of stimuli. Primates and dolphins have shown good evidence of such transfer, but pigeons have shown at best only limited transfer. If pigeons are trained with two or three colours to the point where they are responding with essentially no errors, a substitution of a new colour for one of the trained colours may result in a complete breakdown in the discrimination; there is even some question as to whether they can learn a new matching-to-sample discrimination with new stimuli any faster than pigeons with no prior experience of matching problems.

      The abilities to respond in terms of certain relationships between stimuli, to abstract those relationships and invariant features from a complex and changing array of stimuli, and, above all perhaps, to transfer such learning to a completely novel set of physical stimuli seem to be some of the more important processes underlying the solution of complex discriminative problems. The fact that certain evidence suggests that animals may differ in some of these abilities has implications for studies of other forms of problem solving.

insight and reasoning
      Köhler's (Köhler, Wolfgang) best known contribution to animal psychology arose from his studies of problem solving in a group of captive chimpanzees (chimpanzee). Like other Gestalt psychologists, Köhler was strongly opposed to associationist interpretations of psychological phenomena, and he argued that Thorndike's analysis of problem solving in terms of associations between stimuli and responses was wholly inadequate. The task he set his chimpanzees was usually one of obtaining a banana that was hanging from the ceiling of their cage or lying out of reach outside the cage. After much fruitless endeavour, the chimpanzees would apparently give up and sit quietly in a corner, but some minutes later they might jump up and solve the problem in an apparently novel manner—for example, by using a bamboo pole to rake in the banana from outside or, if one pole was not long enough, by fitting one pole into another to form a longer rake. Other chimpanzees reached the banana hanging from the ceiling by using a wooden box, or a series of boxes stacked precariously on top of one another, as a makeshift ladder.

      Köhler believed that his chimpanzees had shown insight into the nature of the problem and the means necessary to solve it. According to Köhler's interpretation, the solution depended on a perceptual reorganization of the chimpanzee's world—seeing a pole as a rake, or a series of boxes as a ladder—rather than on forming any new associations. But subsequent experimental analysis has cast some doubts on Köhler's claims. The critical observation is that the sorts of solutions that Köhler took as evidence of insight quite clearly depend on relevant prior experience. Chimpanzees will not fit two poles together to form a rake or stack boxes up to form a ladder unless they have had a great deal of prior experience with those objects. This experience may well occur during play, when the young chimpanzee discovers that using a stick can extend the reach of an arm, or that standing on a box can put one within reach of high objects. Thus, what Köhler was studying, without knowing it, was probably the transfer of earlier instrumental conditioning to new situations. As we have already seen, the ability to transfer an old solution to a new stimulus situation is an important one, relevant to a wide range of problem-solving activities. This ability is not at all well understood, but it will not necessarily be greatly illuminated by describing it as insight. Certainly it is not a process unique to the great apes: if the component tasks are sufficiently well-structured, even pigeons can put together two independently learned patterns of behaviour to solve a novel problem.

      Combining information from separate sources to reach a new conclusion is one form of reasoning (reason). The paradigm case of reasoning is the solution of syllogisms; for example, when we conclude that Socrates is mortal given the two separate premises that Socrates is a man and that all men are mortal. Employing transitive inference, we can use the premises that Adam is taller than Bertram and that Bertram is taller than Charles to conclude that Adam must be taller than Charles. Reasoning has often been regarded as a uniquely human faculty, one of the few factors, along with the possession of language, that distinguishes us from the rest of the animal kingdom.

      But are humans the only animals that can reason? The unsatisfying answer must be that it depends on what is meant by reasoning. In a very general sense, most animals appear perfectly able to arrive at a conclusion based on combining information obtained on two separate occasions. A formal demonstration is provided by an experiment on instrumental conditioning discussed earlier. If rats learn that pressing a lever provides sucrose pellets and later learn that eating sucrose pellets makes them ill, they will subsequently put these two pieces of information together and refrain from pressing the lever. Monkeys and chimpanzees, however, have been trained to solve problems that appear more similar to transitive inference. They are first given discriminative training between pairs of coloured boxes, called, for example, A, B, C, D, E. Confronted with the choice between A and B, they learn that choice of A is rewarded and B is not. When B and C are the alternatives, they learn that B is correct; when C and D are the alternatives, C is correct; and so on. Although choice of A is always rewarded, and that of E never is, the remaining three boxes each are associated equally often with reward and with nonreward. Nonetheless, given a choice between B and D on a test trial, the animals choose B.

      Syllogistic and transitive inference are not the only forms of reasoning: humans also reason inductively or by analogy. Indeed, analogical reasoning problems (black is to white as night is to —?) form a staple ingredient of some IQ tests. One chimpanzee, a mature female called Sarah, was tested by David Premack and his colleagues on a series of analogical reasoning tasks. Sarah previously had been extensively trained in solving matching-to-sample discriminations, to the point where she could use two plastic tokens, one meaning same, which she would place between any two objects that were the same, and another meaning different, which she would place between two different objects. For her analogical reasoning tasks, Sarah was shown four objects grouped into two pairs, with each pair symmetrically placed on either side of an empty space. If the relationship between the paired objects on the left was the same as the relationship between those on the right, her task was to place the same token in the space between the two pairs. Thus in one series of geometrical analogies, a simple problem would display a blue circle and a red circle on the left and a blue triangle and a red triangle on the right; the correct answer, of course, was same. But Sarah was equally correct on more complex problems, even when the relationships in question were functional rather than simply perceptual. For example, she correctly answered same when the two objects on the left were a tin can and a can opener and the two on the right a padlock and a key.

      Solution of analogies requires one to see that the relationship between one pair of items (whether they are words, diagrams, pictures, or objects) is the same as the relationship between a different pair of items. If simple matching-to-sample requires animals to see that one comparison stimulus is the same as the sample and another is different, solving analogies requires them to match relationships between stimuli. The difficulties encountered in training pigeons (pigeon) to generalize simple matching-to-sample discriminations does not encourage one to believe that they would find analogies very easy.

Language learning
      The ability to speak was regarded by Descartes as the single most important distinction between humans and other animals (animal communication), and many modern linguists, most notably Noam Chomsky, have agreed that language is a uniquely human characteristic. Once again, of course, there are problems of definition. Animals of many species undoubtedly communicate with one another. Honeybees communicate the direction and distance of a new source of nectar; a male songbird informs rival males of the location of his territory's boundaries and lets females know of the presence of a territory-owning potential mate; vervet monkeys give different calls to signal to other members of the troop the presence of a snake, a leopard, or a bird of prey. None of these naturally occurring examples of communication, however, contains all of the most salient features of human language. In human language, the relationship between a word and its referent is a purely arbitrary and conventional one, which must be learned by anyone wishing to speak that language; many words, of course, have no obvious referent at all. Moreover, language can be used flexibly and innovatively to talk about situations that have never yet arisen in the speaker's experience—or indeed, about situations that never could arise. Finally, the same words in a different order may mean something quite different, and the rules of syntax that dictate this change of meaning are general ones applying to an indefinite number of other sequences of words in the language.

 During the first half of the 20th century, several psychologists bravely attempted to teach human language to chimpanzees. They were uniformly unsuccessful, and it is now known that the structure of the ape's vocal tract differs in critical ways from that of a human, thus dooming these attempts to failure. Since then, however, several groups of investigators have employed the idea of teaching a nonvocal language to apes. Some have used a gestural sign language widely used by the deaf to communicate with one another; others have used plastic tokens that stand for words; still others have taught chimpanzees to press symbols on a keyboard. All have had significant success, and several apes have acquired what appears to be a vocabulary of several dozen, and in some cases 100 or 200, “words.”

      Washoe, a female chimpanzee trained by Beatrice and Allan Gardner, learned to use well over 150 signs. Some apparently were used as nouns, standing for people and objects in her daily life, such as the names of her trainers, various kinds of food and drink, clothes, dolls, etc. Others she used as requests, such as please, hurry, and more; and yet others as verbs, such as come, go, tickle, and so on. Sarah, the chimpanzee trained by Premack to use plastic tokens as words, also apparently learned to use tokens for nouns, verbs (give, take, put), adjectives (red, round, large), and prepositions (in, under). But do these signs or tokens really function as words? Does the ape using them, or obeying instructions from a trainer who uses them, really understand their meaning? Or is the ape simply performing various arbitrary instrumental responses in the presence of particular stimuli because she had previously been rewarded for doing so?

 There can be little doubt that chimpanzees do have some understanding of what their “words” refer to. Sarah responded appropriately with her token for red if asked the question “What colour of apple?” both when an actual red apple was shown as part of the question and when only the token for an apple (which happened to be a blue triangle) was presented. To Sarah, the blue triangle surely stood for, or was associated with, the red apple. In another study, after two chimpanzees had been taught the meaning of a number of symbols for different kinds of food and different tools, they were able not only to fetch the appropriate but absent object when requested to do so, but they could also sort the symbols into two groups, one for foods and one for tools. In another series of studies, a pygmy chimpanzee named Kanzi demonstrated remarkable linguistic abilities. Unlike other apes, he learned to communicate using keyboard symbols without undergoing long training sessions involving food rewards. Even more impressive, he demonstrated an understanding of spoken English words under rigorous testing conditions in which gestural clues from his trainers were eliminated.

      As noted above, human language is more than a large number of unrelated words: in accordance with certain implicitly understood syntactic rules, humans combine words to form sentences that communicate a more or less complex meaning to a listener. Can apes understand or use sentences? Undoubtedly they can put together several gestures or tokens in a row. A chimpanzee named Lana, who was trained to press symbols on a keyboard, could type out “Please machine give Lana drink”; Washoe and other chimpanzees trained in gestural sign language frequently produced strings of gestures such as “You me go out,” “Roger tickle Washoe,” and so on. Skeptical critics, however, have raised doubts about the significance of these strings of signs and symbols. They have pointed out, for example, that when Lana pressed a series of coloured symbols on her keyboard, it was humans who interpreted her actions as the production of a sentence meaning “Please machine give Lana drink.” Might it not be equally reasonable to say that she learned to perform an arbitrary sequence of responses in order to obtain a drink? Pigeons can be trained to press four coloured keys—red, white, yellow, and green—in a particular order to obtain food. Psychologists do not feel any temptation to interpret this behaviour as the production of a sentence. What is it about Lana's behaviour that requires this richer interpretation?

      In the case of apes trained to use sign language, two other doubts have been raised. First, there is some reason to believe that a disappointingly high proportion of the apes' gestures may be direct imitations of gestures recently executed by their trainers. Second, a sequence of gestures interpreted as a single sentence is often just as readily interpreted as a number of independent gestures, each prompted, in turn, by a gesture from the trainer. Both these conclusions are based on careful examinations of video recordings of interactions between trainers and apes. Whether they will turn out to be generally true remains an open, and heatedly debated, question.

      Without any explicit training, apes have nevertheless learned to produce strings of two or three signs in certain preferred orders: “more drink” or “give me,” for example, rather than “drink more” or “me give.” Do the animals understand that a string of signs in one order means something different from the same signs in a different order? The following anecdote is suggestive. A chimpanzee called Lucy was accustomed to instructing her trainer, Roger Fouts, by gesturing “Roger tickle Lucy.” One day, instead of complying with this request, Fouts signed back “No, Lucy tickle Roger.” Although at first nonplussed, after several similar exchanges Lucy eventually did as asked. A simple instance of this sort proves little or nothing, but it may suggest what is needed—namely, that Lucy should understand that changing the order of a set of signs alters their meaning in certain predictable ways. She must generalize the rule that the relationship between the meanings of the signs A-B-C and C-B-A (the same signs in reverse order) is similar to the relationship between the meanings of certain other triplets of signs in her vocabulary when their order is reversed.

      The research on language in apes forcefully illustrates a conflict, or tension, that is common to many other areas of research on learning in animals. If the investigators are interested in language and communication, they can attempt to communicate as naturally and informally as possible with their apes. This approach involves treating an ape as a fellow social being, with whom one plays and interacts as far as possible as one would with a human child; it also, almost inevitably, results in a style of research where it is exceptionally difficult to control precisely the cues that the ape may be using and even hard to avoid an overly rich, anthropomorphic interpretation of the ape's behaviour. If, on the other hand, the researchers are interested in rigorous experimental control and economical interpretation of the processes underlying the ape's performances, they are likely to set the ape formal problems to solve, with rewards for correct responses and no rewards for errors. But such an approach, however scientific it may seem, must run the risk of missing the point. This is not language; the investigators are not communicating with the ape in the way they would communicate with a child. The very nature of the experimental problems ensures that the ape will not use its language in the way that a child does: to communicate shared interests, to attract a parent's attention to what the child has seen or is doing, to comment on a matter of concern to both.

      There is no resolution to this conflict, for both approaches have their virtues as well as their dangers, and both are therefore necessary. In just the same way, the study of a rat pressing a lever in a Skinner box or of a dog salivating to the ticking of a metronome seems to many critics a sterile and narrow approach to animal learning—one that simply misses the point that, if the ability to learn or profit from experience has evolved by natural selection, it must have done so in particular settings or environments because it paid the learner to learn something. It would be foolish to deny this obvious truism: of course it pays animals to learn. Indeed, it may pay them to learn quite particular things in specific situations, and different groups of animals may be particularly adapted to learning rather different things in similar situations. None of this should be forgotten, and the study of such questions requires the scientist to forsake the laboratory for the real world, where animals live and struggle to survive. But few sciences can afford to miss the opportunity to manipulate and experiment under laboratory conditions where this is possible, and none can afford to forget the benefits of precise observation under controlled conditions.

Additional Reading

General works
Historical background is provided by Robert Boakes, From Darwin to Behaviourism: Psychology and the Minds of Animals (1984). See also T.R. Halliday and P.J.B. Slater (eds.), Animal Behaviour, vol. 3: Genes, Development, and Learning (1983); Robert A. Hinde, Animal Behaviour: A Synthesis of Ethology and Comparative Psychology, 2nd ed. (1970); J.E.R. Staddon, Adaptive Behavior and Learning (1983); and David McFarland, Animal Behavior: Psychology, Ethology, and Evolution (1985).

Simple nonassociative learning
Gabriel Horn and Robert A. Hinde (eds.), Short-Term Changes in Neural Activity and Behaviour (1970); and Harman V.S. Peeke and Michael J. Herz (eds.), Habituation, 2 vol. (1973).

Associative learning and conditioning
Anthony Dickinson, Contemporary Animal Learning Theory (1980); Michael Domjan and Barbara Burkhard, The Principles of Learning and Behavior, 2nd ed. (1986); N.J. Mackintosh, The Psychology of Animal Learning (1974), and Conditioning and Associative Learning (1983); and Barry Schwartz, Psychology of Learning and Behavior, 2nd ed. (1984).

Biological functions of and constraints on learning
Robert A. Hinde and J. Stevenson-Hinde (eds.), Constraints on Learning: Limitations and Predispositions (1973); Timothy D. Johnston, “Contrasting Approaches to a Theory of Learning,” Behavioral and Brain Sciences, 4(1):125–173 (March 1981); and J.R. Krebs and N.B. Davies, An Introduction to Behavioural Ecology (1981).

Physiological basis of learning
Daniel L. Alkon and Joseph Farley (eds.), Primary Neural Substrates of Learning and Behavioral Change (1984); and Eric R. Kandel, Cellular Basis of Behavior: An Introduction to Behavioral Neurobiology (1976).

Spatial learning and navigation
P. Robin Baker, Bird Navigation: The Solution of a Mystery? (1984); John O'Keefe and Lynn Nadel, The Hippocampus as a Cognitive Map (1978); and K. Schmidt-Koenig and W.T. Keeton (eds.), Animal Migration, Navigation, and Homing (1978).

Song learning and imprinting
P.P.G. Bateson, “The Imprinting of Birds,” in S.A. Barnett (ed.), Ethology and Development (1973); Howard S. Hoffman, “Experimental Analysis of Imprinting and Its Behavioral Effects,” The Psychology of Learning and Motivation, 12:1–39 (1978); Donald E. Kroodsma, “Aspects of Learning in the Development of Bird Song,” in Gordon M. Burghardt and Marc Bekoff (eds.), The Development of Behavior: Comparative and Evolutionary Aspects (1978); and P.J.B. Slater, “Bird Song Learning: Theme and Variations,” in Alan H. Brush and George A. Clark, Jr. (eds.), Perspectives in Ornithology (1983).

Comparative psychology and complex training
E.M. Macphail, Brain and Intelligence in Vertebrates (1982); R.E. Passingham, The Human Primate (1982); and H.L. Roitblat, T.G. Bever, and H.S. Terrace (eds.), Animal Cognition (1985).Nicholas John Mackintosh

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