emotion, motivation, and the limbic system

PART VI. THEORETICAL OVERVIEWS

EMOTION, MOTIVATION, A N D THE LIMBIC SYSTEM

Magda B. Arnold Behavior Laboratory, Loyola University

Chicago, Il l .

In the theoretical literature. the relation between emotion and motivation is not at all clear. Over and over again, it is said that emotion motivates; but hardly ever does anyone come out and say unambiguously just how this is done.

Perhaps emotion and motivation must be set in the context of the ongoing sequence from perception to action before it is possible t o give a precise description of the mechanism involved. Furthermore, unless we can give a precise description of the psychological activities within that sequence, it will be impossible to identify the structures that make emotion and motivation possible. Classically, the reflex arc served as a model for psychology: the receptor link mediates perception, the connector link serves “internal states,” including pre- sumably emotion and motivation, and the effector link takes care of the initiation of action. Although the reflex arc concept has been respectfully retired, our analysis of the psychological and neural connection from perception to action has not advanced much beyond it. And the more we concentrate on the parameters of stimulus and response, the more difficult does it become to work out the structures that could mediate intraorganismic activity.

This does not matter too much, perhaps, as long as we are content with a psychology of the “empty” organism. But as soon as we begin to consider the brain functions involved in the reception of the stimulus and the choice of response, it becomes imperative to look for clues by which such functions could be identified. Since the stimulus-response paradigm will not serve, we have the choice between various recent models ( the cybernetic feedback, the computer model) and a careful phenomenologica1 analysis of the sequence of psychological activities from perception to action. Neither the cybernetic model nor the computer model is really appropriate. Human action is influenced by feedback information but does not completely depend on it: it has been shown that aiming, for instance, is more accurate when done quickly, spontaneously (as in the newly revived “quick-kill” technique) so that the weapon becomes an extension of the arm. It has also been shown that imaginary practice (e.g., in dart throwing) is as effective as actual practice, although no feedback is involved at all.

Similarly, the computer does not solve a problem as the human being does, by ordering various possibilities into categories and comparing them; rather, its lightning speed makes it possible to compare each alternative with every other, register the fitting combination, and produce the solution in a fraction of the time required by human beings. As everv engineer knows, a particular aim can be achieved in many different ways. The cybernetic circuit and the computer represent one way, the human mind and brain another. There is no evidence at all that terms derived from one model will be adequate to explain a mechanism that is built differently. To call sense experience “scanning” and to talk about “analyzers” instead of sensory receptors may sound more scientific if science is patterned after mechanistic or electronic models; but it serves only to confuse the issue when psychological activities have to be investigated. To analyze human experience, the

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language derived from experience is far superior to any terminology derived from mechanical models.

Even animals must have some of the experiences we concede to human beings. They can learn and thus must be able to sense, to remember, and even to imagine, for they seem to expect food or shock. An analysis of such experience, a phenomenological analysis, is not introspection as we usually understand it. Introspec- tion, whether used clinically or experimentally, reports subjective experience, however much at variance with the experience of others. Phenomenological analysis explores what goes on; it takes a given activity (e.g., a learned response) and specifies what has to happen psychologically before this result can be achieved. Subjective experience is used as a clue to be checked by the experience of every other observer. Just as sensory experience is considered a hallucina- tion unless comparable observers in the same situation have the same experience, so a phenomenological analysis can only be considered valid if others have the same experience and thus can agree.

I propose to use such a phenomenological analysis as a guide in interpreting some of the research findings of the past years on brain lesions and brain stimulation, and so tentatively to identify the circuits that mediate motivation and emotion.

When something is perceived, the sensory experience is not only felt but inter- preted. This means that the situation here and now must be compared with similar past experiences, i.e., such experiences must be remembered. But what was experienced in the past a k o includes the effect of this experience o n us. In other words, there must be a memory of benefit or harm as well as a memory of sights, sounds, touches, odors, and the like. Thus, we can distinguish between tnodality- specific and affective memory. In addition, the present experience and the relevant memories must be used to make a guess at the future: will this hurt me or benefit me this time? This requires imaginution and cippraisal. Furthermore, the individual must make some plan, must imagine possible ways of coping with this situation: then he must appraise or evaluate them. The choice of one alternative appraised as best here and now, finally leads to action. Of course, this sequence may be run through almost instantaneously, ending in precipitate action (as in panic) or it may be repeated over and over as different aspects of a situation are perceived and evaluated before it leads to the final choice of action (e.g., in difficult decisions).

Appraisal

The object or situation may be appraised as good, bad, or indifferent. If found good, it is felt as attractive, if bad, as repulsive, if considered indifferent, it is disregarded altogether. This appraisal is as direct as sense experience, even though it is experienced only as a liking or dislike, as a favorable or unfavorable attitude toward something. The appraisal itself is unconscious, unwitting, as opposed to a conscious and deliberate judgment of value. The human being, as distinct from the animal, experiences not only direct attractions and repulsions but can also make a reflective value judgment. Whether intuitive appraisal or deliberate value judgment, this judgment sets the thing appraised in relation to the subject and gauges its effect on the subject here and now. Thus, appraisal complements and completes perception, and produces a tendency to deal with the object in some way.

The stimulus-response psychologist usually considers that the object somehow produces approach or avoidance. But such a formulation cannot explain why a

Arnold: Motivation and the Limbic System 1043

given object does not produce approach in every subject, or even in the same subject all the time. To explain such vagaries by “conditioning” simply begs the question. Before a stimulus can become conditioned to a given response, it has to be evaluated as announcing food or shock. I f mechanical linkages were sufficient, we would not have $0 much trouble devising proper “shaping procedures” to make sure the animal makes the “proper” association.

To react to any stimulus, even the most primitive one, requires an estimate as to its effect on the subject. Even the so-called “orienting reflex” requires an appraisal that this thing is important enough to be investigated. When the stimulus is repeated several times, the animal soon fails to pay attention to it: the stimulus has become unimportant, irrelevant, inconsequential. This is not simple fatigue or adaptation of nerve tissue, for a new stimulus of the same modality will restore the orienting reflex to its original strength. Rather, it results from the appraisal that this thing has no particular effect (for it is followed by neither reward nor punishment) and so is indifferent. When the stimulus changes, there is a new appraisal producing renewed attention, another “orienting reflex,” With repetition, this stimulus will again be disregarded.

Affective Memory

Another point should be considered: very few situations can be felt as pleasur- able or painful the first time. Only very few stimuli, all of them somesthetic, elicit a response from the neonate who has no memories: according to Watson, when the newborn infant is gently stroked, he shows “love.” anger when he is forcibly restrained, and fear (or better, startle) when he is dropped. He also cries when in pain or uncomfortable. All these stimuli have a direct impact on the body: they immediately affect the infant’s well-being and thus arouse an emotional response the first time they are cxperienced.

By contrast, visual or auditory expericnces indicate things as yet in the distance. What we see and hear must have touched us in the past before we respond to it emotionally: its physical impact on us must be remembered. This memory is not a visual, auditory, or other sensory image. Rather, it is a revival of the impact of the past situation on us. We can call it affective memory, provided we realize that all that we experience is an immediate liking or dislike of something, often without the recognition that we have encountered this thing before. Once the child has felt pain in the dentist’s chair, he is afraid to go to the dentist, even if he knows he only needs an x-ray and there will be no pain. This fear, like any other fear, is based on an affective memory, the living remnant of a hurt felt before and expected again. Freud has explained such aftereffects of emotional experiences as repressed traumatic memories. But the same effect follows upon experiences that have not been represscd, such as the fear of the dentist. The burned child remembers the burn but does not necessarily connect his fear of fire with the pain he has felt before. In time, he may forget the burn altogether. but the reluctance to go near a fire will remain.

Moreover, the burned child is afraid of any fire, even a magnesium flare, just as the child who is afraid of the dentist is afraid every time, even when he knows there will be no pain. This phenomcnon is sometimes called “stimulus generalization.” But just how does it happen that a stimulus is generalized in this way? Only a phenomenological analysis can give the answer to this question. If we refuse to ask it and are content with the label, we deprive ourselves of the possibility of discovering both the psychological process responsible for the fact and


its neural mediation. When a rat jumps toward a circle and refuses to jump toward a square, it does so because the circle has led to food and the square has meant pain in earlier trials. The circle has been evaluated as good, leading to food, the square as bad, leading to harm. Learning occurs because the circle is recognized as being like the past situation that has led to food (modality-specific memory) ; and because what it led to was liked, the circle has acquired a positive value (affective memory). When an ellipse and a square, or a polyhedron and a square are shown, the rat will jump toward the ellipse and the polyhedron because they are sufficiently similar to the circle to arouse the same affective memory, which in this case overrides visual memory, for the affective memory is felt as an immediate tendency to approach. However, when the positive stimulus is a circle and the negative stimulus an ellipse, and the ellipse is gradually made more circular, there comes a point where the animal will refuse to jump because the affective memory of harm connected with the ellipse is now reactiviated by both figures.

Not only can the notion of affective memory explain the mechanisms behind stimulus generalization, it can shed light on some other puzzling experimental facts. For instance, take the different reactions of animals to an active and a passive avoidance situation. In passive uvoidunce, the animal receives an electric shock as he touches the food mash. H e may approach the food the next day, but if he is shocked again, he usually will refuse to approach the food cup for days and weeks afterwards. In cictive avoidance, he is given an electric shock in the home compartment of the shuttle box shortly after a light is flashed or a buzzer is sounded. He can escape the shock by crossing over into another compartment, but it will take many trials before the shock will be avoided by escaping as soon as light or buzzer come on. Why the difference between the two learning situations? It used to be said that ordinary conditioning is slow, requiring many trials, as compared to “emotional” conditioning which is often learned in one trial if the emotion is strong enough. But surely, emotion is involved in both active and passive avoidance, so the difference cannot be sought in emotional versus unemotional learning. Rather, in active avoidance, both sensory and affective memory are revived as soon as the animal is brought into the home compartment. The whole situation is intensely frightening, and the light is but one feature in it: to appraise the light alone as bad, to be avoided, will require considerable experience of “compartment with light” as harmless, and “compartment without light” as harmful, before the animal will learn to cross over as soon as the light goes on.*

In the passive avoidance situation, the animal is also afraid as soon as he is brought into the compartment, but all he has to d o is to keep away from the cup, the occasion of the shock experienced before. The revived affective memory results in fear and refusal to approach after one or two shocks. It is not the pres- ence or absence of emotion, nor the fact that passive avoidance or active jumping is required, that makes the difference in learning. Neither is it the intensity of shock in the two situations. In fact, the shock has to be held at low intensity in the active avoidance situation to prevent too intense emotional disturbance. If the shock level is raised, the increased disturbance makes the problem even more difficult for the animal. In passive avoidance, the shock can be maximal because the fear it produces implements the correct response so that the rat keeps away

* Interestingly enough, Lazarus (1967) has recently reported a study with human subjects in which the general apprehension aroused by the experimental situation made it impossible to distinguish the disturbance caused by emotional stimuli from the reaction to the total threatening situation.


from the cup. In the active avoidance situation, the emotion interferes with the correct response. Thus, the difference in the two learning situations is solely in the effect of emotional disturbance on the response to be learned.

Emotion, Motivotion, and Affect ive Memory

Appraisal and affective memory produce an affective tendency toward or away from the object; when this is intense, it is called an emotion. With the exception of the simple enjoyment or dislike of somesthetic and taste experiences, ranging to the extremes of pleasure and pain, and the anger produced by physical restraint, a11 emotions seem to require affective memory as the basis of the appraisal here and now which produces them. Just as we cannot feel fear unless the expected harm or the threatened deprivation has been experienced before, so we cannot feel confidence unless we have had occasion to cope successfully, and we cannot feel love unless we have felt the delight of close contact before. Sadness depends on past loves whose objects have disappeared, joy, on past longings that have now been satisfied.

Similarly, motivated behavior would be impossible without affective memory. When animals are induced by hunger to learn to run a maze or work a lever, they d o so because the correct turns in the maze and the correct cue-lever combination have led to food before. They have acquired a positive valence and now arouse the same positive reaction felt before because the animal is reliving in anticipation the satisfaction experienced when the food was found in the goal box or was delivered by lever pressing. We may call it positive reinforcement, or reward, or anything we like, but these terms will not give us a clue to the way in which the postulated reward produces its effects. By contrast, as soon as we see motivated behavior as an instance of affective memory, we recognize it as a link in the sequence from perception to action and can ask and, perchance, discover what the structures are that make it possible.

Brain Function f r o m Perception 10 Action

When we try to identify the structures and circuits that mediate the psychological sequence from perception to action, we must d o so on the basis of the large number of reports mentioning behavioral consequences of brain lesions and brain stimulation. Of course, it is obvious that a particular impairment after a lesion does not mean that the missing brain tissue had “generated” or “elaborated” the behavior that is now defective. But it may mean that all lesions resulting in such impairment, no matter where located, have damaged structures or circuits that are required for normal responses. Similarly, electrical stimulation of some point in the brain does not mean that the behavior so produced is necessarily the normal behavior mediated by a “center.” It may mean that the electrode has stimulated points in a circuit that normally mediate such behavior or that these connections have been preempted by the stimulating current and now cannot be used for the subject’s normal behavior. Keeping these facts in mind, let us now see whether it is possible to sketch the pathways that seem to be used for normal functioning.

If it is true, as I am suggesting, that every perception includes recall, imagination, and appraisal, and leads to some response tendency, we would expect the existence of brain structures and circuits that make such a sequence possible. We know that sensory and motor areas must be connected by a subcortical route because crosshatching of the cortex does not prevent learning as long as the subcortical connections are intact; but when the cortex is undercut so that it is


separated from its subcortical connections, there are gross memory losses (Cragg & Temperley, 1955).

Registration of Information When anything is experienced at all, the sensory cortex serving the experienced

sense modality is activated together with the neighboring association cortex. It is generally accepted that visual experience is mediated by area 17 in the occipital cortex, hearing by areas 41 and 42 in the superior temporal cortex, touch and kinesthesis by areas 1 , 2, 3. and taste by area 43, all in the parietal lobe. Although we know that smell is mediated by the olfactory lobe, the primary cortical repre- sentation is not equally certain. It ‘is also known that area 4 in the frontal area activates voluntary and involuntary muscles. Accordingly, the various modalities seem to be mediated by different areas in the cortex. Although it is true that in recent years motor responses have been produced by electrical stimulation of somesthetic and even visual areas, the longer reaction times obtained are com- patible with the concept of a circuit that runs from every sensory area through subcortical connections to the motor cortex. Thus the motor cortex would be the last cortical relay station, rather than an autonomous “center” initiating movement.

A phenomenological analysis of experience will show that memory and imagination must be modality-specific like sensation. We are well aware of being able to form visual, auditory, and motor images: we can visualize a picture or building, can hear a tune or the remark of a friend in imagination, and can “mentally” practice a golf stroke or rehearse an important address. We are also acquainted with olfactory, touch, and taste images, although we are often inclined to take them for factual experiences. These images, whether fantasy or memory images, must be derived from actual sensory experiences which can be reactivated, either exactly (in recall) or in new combinations (in fantasy). From various research report we can infer that visual impressions are registered in the visual association cortex, somesthetic impressions in the somesthetic association area, and auditory, olfactory, gustatory, and motor experiences in their respective association areas. This inference is suggested not only by Nielsen’s (1943, 1954) studies with brain injured patients, but also by a series of ingenious experiments with monkeys reported by the Yale group of Pribram and his associates: a visual discrimination habit was lost after ablation of the inferior edge of the temporal lobe and the preoccipital cortex (Pribram & Mishkin, 1955; Pribrani & Barry, 1956); a learned auditory discrimination habit was lost after removal of the posterior temporal cortex (Weiskrantz & Mishkin, 1958) ; and a learned somesthetic discrimination habit (touch and weight) was lost after loss of the parieto-occipital association area (Wilson, 1957). A learned alternation habit was lost after destruction of the lateral frontal cortex (Mishkin & Pribram, 1955), and conditioned taste discrimination was lost after destruction of the somesthetic association area for the tongue (Bagshaw & Pribram, 1953). From Allen’s findings (1940) and the known distribution of the olfactory fibers, we may conclude that the orbital (rather than the prepyriform) cortex is necessary for conditioned olfactory discrimination. It should be noted that these defects were permanent, suggesting that the engrams were destroyed rather than a circuit that might activate them.

Information Retrieval Usually, when psychologists speak of the brain structures involved in learning

and memory, they mean the areas serving the registration of sense impressions.


But for psychological experimentation, the retrieval of information is actually more important than the registration of the original experience. Whatever is learned remains unknown to the experimenter until such learning is demonstrated in performance. This has given rise to the notion of ‘‘latent’’ learning-which is latent only for the experimenter, not the subject. To demonstrate learning by performing the learned task, the rzquired information has to be retrieved, i.e., the cue must be recognized and the required action recalled and carried out. Recognition of the cue and recall of the required response are two separate processes. In paired associate learning, for instance, the stimulus member of the pair can usually be recognized long before the associated member can be produced. On the assumption that recognition is a sign that the registration of information has occurred, i t seems reasonable to conclude that both members of each pair were registered; but the registered information cannot easily be retrieved by the subject although it can be recognized as familiar.

Since the retrieval process is so important for testing learning, it would seem important to identify the circuit in the brain that can reactivate the registered impressions. Whatever the cortical changes that are produced when an experience is registered, the retrieval process must make it possible to revive or reactivate these changes in the same pattern in which they were laid down. Only in this way can an experience be recalled in the proper order and correct time sequence. On the basis of a great number of neurophysiological studies reported in the literature, 1 have suggested (Arnold, 1960) that modality-specific memory is recalled via a “memory circuit” which includes relays from association cortex to limbic areas, indusium griseum, and hippocampus and connects via fornix and hypothalamus with the midbrain from where relays go via thalamic sensory nuclei to various cortical association areas, thus closing the circuit. The responses made in various situations are recalled via a motor memory circuit with relays from limbic cortex to hippocampus, midbrain, and cerebellum. and via ventral thalamic nuclei to the frontal cortex.

The Appraisril and A flective Memory System Since appraisal is included in every perception, completing the sense experience

and giving it personal meaning, we might expect that the system mediating such appraisal would be connected with all sensory cortical areas. The limbic system, SO zealously researched during the past twenty years, would fulfill this require- ment. It has been called a “reward system” because an animal will keep up self- stimulation via electrodes implanted in limbic cortex and connected subcortical structures without any other reward. The term “reward,” I might point out, is merely the preferred objective-sounding label for the subjective experience of pleasure or satisfaction. Whatever the response-eating, mating, or brain stimulation-it must be rewarding or satisfying to the animal or the animal would not keep on making it.

That the limbic system, particularly the cingulate gyrus, serves affective reactions, is shown by several experiments. MacLean (1954) found that electrical and chemical stimulation of the posterior cingulate gyrus aroused increased pleasure reactions to petting in cats. Ward (1948) noted that monkeys which had the anterior cingulate gyrus removed did not groom other monkeys nor show affection in any other way. These monkeys took food out of other monkeys’ hands, walked or sat on them and then seemed suprised when their companions attacked. From these and many other experimental reports, Arnold (1960) con- cluded that the subcallosal gyrus mediates the appraisal of odors, the anterior


cingulate gyrus (and the anterior insula) mediate the appraisal of actions and action impulses, while the posterior cingulate and retrosplenial gyri (as well as the posterior insula) seem to mediate the appraisal of somesthetic impressions. Such appraisal, as discussed previously, is experienced merely as liking or dis- liking.

These limbic areas should be connected with a circuit which allows the revival of such affective appraisals, a circuit which should lead back to the limbic cortex if past experience is to be integrated with the appraisal of the present situation. Pribram and MacLean (1953) have shown that the limbic cortex (subcallosal, cingulate, retrosplenial, and hippocampal gyrus) actually receives impulses from cortical sensory and association areas. The cingulum, which connects these areas with the hippocampus and fornix, sends relays via the mamillary body to the anterior thalamic nucleus and the cingulate cortex. This could be the circuit mediating affective memory. If that is so, an object would be appraised when relays from the sensory and association areas reach the limbic cortex. This affective reaction would be relived when impulses from the cingulum are relayed back to the limbic cortex (via fornix, mamillary bodies, and anterior thalamic nuclei). The memory of successful or unsuccessful bodily movement would be revived when these relays reach the anterior cingulate gyrus, the memory of pleasant or painful bodily touch, when they reach the posterior cingulate and retrosplenial gyrus, while the memory of an unpleasant noise and painful bright- ness would be reexperienced when these impulses reach the hippocampal gyrus. Finally, the memory of an unpleasant taste would be revived when impulses from limbic insular areas are relayed back to the posterior insula, and the memory of pleasant or painful head movement, when relays f rom the anterior insula go via subcortical structures back to the anterior insula.

According to our phenomenological analysis, imagination is necessary for the expectation of what will happen this t ime. 1 have suggested that a circuit from the limbic cortex via amygdala and thalamic association nuclei to cortical association areas could serve this purpose. Such a circuit would make i t possible to revive memory traces in any order. as contrasted with the recall circuit which, as suggested above, seems to connect with the cortical association areas via the sensory thalamic nuclei and so reactivates the original pattern (FIGURE 1 ).

: an evaluation of possible alternatives of coping with the situation, and a choice of action. The “action circuit” mediating the final impulse to action seems to run from the limbic cortex via hippocampus and fornix to the hypothalamus, midbrain, cerebellum, ventral thalamic nuclei, and frontal lobe. For the evidence on which the suggested circuits are based, please refer to volume 2 of my book Etnotion and Personality ( I 960) in which this is fully documented.

All I can do here is discuss the appraisal and affective memory system which is mediated, I believe, by the limbic cortex and the affective memory circuit. Since this system is the basis of both emotion and motivation, it deserves to be discussed in relation to the conflicting research reports of the past two decades. It is clear that my view of limbic function is part of a larger theory of brain function, as I have indicated above. At first glance, this theory will seem to conflict with views based on isolated stimulation or ablation experiments. But perhaps such a view is worthy of attention if the theory, although complex, can integrate the results of studies that would otherwise remain contradictory.

Take, for instance, the notion that the precallosal and anterior cingulate gyrus mediate the appraisal of bodily movement and that the posterior cingulate medi-

Finally, there has to


FIGURE 1. The imagination circuit and the revival of affect. Identification of object by recalling similar things (via memory circuit) and their effects on us (via affective memory circuit VI) results in iniagiriing what might happen and what can be done about (imagination circuits I-V). (Reproduced by permission of Columbia University Press.)

I visual imagination. 11 auditory imagination. 111 somesthetic imagination (including taste). IV motor imagination. V olfactory imagination. VI affective memory. AM amygdala. ANT anterior thalamic nucleus. B brain stem. CING cingulate gyrus. DM dorsomedial thalamic nucleus. H habenula. HlPP hippocampus. M mammillary body. OLF olfactory bulb. PULV pulvinor. S septal area. STRIA TERM stria terminalis.

ates the appraisal of bodily pain and pleasure, and contrast it with McCleary’s (1961) view that the subcallosal and precallosal cortex represent a motor in- hibitory area and that the cingulate gyrus represents a motor facilitatory area. Kaada had reported in 1951 that stimulation of the area around and below the genu of the corpus callosum (pre- and subcallosal gyrus) produced inhibition of cortically induced movements and autonomic responses, while stimulation in the medial and anterior cingulate gyrus produced facilitation. McCleary (1961) found that bilateral septal and precallosal lesions in cats produced a deficit in passive avoidance but did not interfere with active avoidance, while bilateral lesions of the cingulate gyrus impaired active avoidance and left passive avoidance intact.

But is it really justified to equate the inhibition of cortically induced movements in the anesthetized animal with general motor inhibition abolished by septal lesions which produce incorrect approach responses in the passive avoidance situation? It is simplistic to assume that increased reactivity must be the result of a loss of “inhibition.” In addition to the increased “emotional reactivity” reported in animals with septal lesions (Brady & Nauta, 1953, 1955) and the impairment of passive avoidance reported by McCleary, there is also severe impairment in olfactory, visual and auditory discrimination and in single alteration (Arnold, 1967). Consequently, the impairment seems more like a loss of discrimination (i. e., modality-specific memory) than like a facilitation of action. If septal lesions, which always damage the precommissural and often the postcommissural fornix, impair the recall of earlier impressions but, according to my theory, leave the imagination circuit intact, it is easy to explain the increased emotional reactivity


after such lesions. If every situation is completely unfamiliar, the animal will be induced not only to explore it, but also to attack i t on the slightest provocation.

The facilitation of movement induced by cortical stimulation, as observed by Kaada, may also have very little to do with a general motor facilitation which is supposedly abolished by precallosal and anterior cingulate lesions. For instance, a lesion of the “facilitatory” cingulate gyrus may inhibit active avoidance but n o other responses. Thomas and Slotnick ( 1962) found that lesions severing projec- tion fibers from the anterior thalamic nucleus to the cingulate cortex produced active avoidance deficits but did not impair maze learning in rats. Later (1963), these investigators found that rats with cingulate lesions acquire active avoidance as easily as d o intact rats, provided they are hungry. The deficit is noticeable, however, when they are sated. These rats also crossed over spontaneously to the compartment in which they had been shucked (passive avoidance deficit): this happened more often when they were hungry than when they were sated. In other words, when hungry, the rats had no active avoidance deficit but did have an impairment in passive avoidance; when sated, they had little passive avoidance - deficit but considerable active avoidance impairment.

These findings cannot easily be explained as the result of damage to a facilitatory system; but they can be explained as the result of damage to the appraisal and affective memory system. After a large lesion of the posterior cingulate gyrus, somesthetic experiences in the rat’s body and hind legs can no longer be appraised as pleasant or unpleasant. At the very least, the dislike of shock will be materially reduced. Since affective memory is reduced proportionally, the pain of shock felt in the past will no longer arouse an immediate impulse to avoid it: the rats will show little fear of the shock compartment. If the hippocampal rudiment has also been damaged (which is likely in such large ablations of the cingulate gyrus), the animals also would not be able to remember what they had done before. Without affective memory, at any rate, they will not try to avoid the shock compartment. But when hungry, animals have an urge to find food and so would move to the next compartment as soon as the light goes on-all that is necessary is the visual stimulus, appraised as “good to explore and find food” (no active avoidance deficit). When sated, they had no such impulse to move, and stayed in their compartment (active avoidance deficit). When in need of food, they might cross over spontaneously because the pain connected with shock in the other compartment was only a vague memory (passive avoidance deficit) ; when sated, nothing urged them toward the opposite compartment (no passive avoidance deficit). As Thomas and Slotnick (1963) noted, hunger activated the animals in this situation. But it restored active avoidance not because it counteracted “freezing,” as they suggest, but because it substituted for the defective fear drive. Surely, freezing is not an independent mechanism but a behavioral sign of fear or uncer- tainty. And hunger had induced approach in the passive avoidance situation (thus demonstrating an impairment) because the reduced fear made it possible to approach the other compartment. Accurately speaking, the animals approached the food not because they were now “activated” (whatever that may mean) but because their affective memory of the pain of past shocks was now impaired, so that hunger alone moved them.

The passive avoidance deficit in Thomas and Slotnick’s rats with cingulate gyrus lesions was genuine enough, although it was only demonstrated when the animals were hungry. But these rats were shocked through their feet, while McCleary’s cats with equivalent lesions but no passive avoidance deficit were shocked through the mouth. Affective recall on the basis of impressions from


mouth and probably forelegs seem to be mediated by the posterior insula and claustrum rather than the posterior cingulate gyrus. Thus, cingulate lesions would leave the memory of pain felt through the mouth intact. (Both experimenters shocked the animals through the feet in the active avoidance situation).

That shock applied to the animal’s mouth is experienced and remembered via the insula can be inferred from a report by Kaada et al. (1962) . According to this study, rats with small lesions of the insula (limbic cortex overlying the claustrum) with or without simultaneous damage to the pyriform cortex, showed a passive avoidance deficit, i.e., they did not avoid drinking from the dish through which they had been shocked.

Further evidence of deficits produced by lesions in what I have called the “affective memory circuit” is provided by another series of experiments. Thomp- son and Langer (1963) reported that lesions of the mamillary bodies, the mamillothalamic tract, or anterior thalamus of rats impaired the reversal of a previous position habit in a T-maze in which incorrect turns were punished by shock to the feet. These lesions damaged the very structures that form relay stations in the proposed circuit. However, Thompson and Langer also reported that postcommissural fornix lesions did not produce such impairment; and Thompson and Hawkins ( 1961 ) found that bilateral lesions of the mamillary bodies left a learned active avoidance response unimpaired, although lesions of the lateral hypothalamic area resulted in the loss of this response.

These reports are difficult to interpret because it is not stated whether the hippocampal rudiment, the superior fornix, or other parts of the modality-specific memory circuit were damaged in any of the lesions. Theoretically, the reversal could be learned as long as both memory circuits are intact. However, Nauta (1956) reported that some fornix fibers are relayed from the hippocampus directly to the anterior and medial thalamic nuclei-which could mean that affective experience might still be revived even after damage to mamillary bodies or mamillothalamic tracts. To explain Thompson and Langer’s results, we would have to assume either that there was additional impairment in the modality-specific circuit in the animals that showed defective reversal after lesions of mamillary bodies or mamillothalamic tracts, or that the direct fornix fibers from hippocampus to medial and anterior thalamus are more numerous in some animals than in others; thus, animals with numerous such fibers might relive affective experience even after damage to the postcommissural fornix.

Thompson and Langer’s ( 1963) additional report that bilateral precallosal limbic cortex lesions produced a significant deficit in reversal of a position habit in a T-maze can be explained easily enough: after such lesions, body movement can n o longer be appraised effectively, and the rat would repeat the turn learned before, which is now incorrect. Similarly, lesions of the precommissural fornix, medial septa1 nuclei, and medial forebrain bundle produced a deficit because they destroyed sections of the modality-specific memory circuit.+ A report by Thompson and Hawkins (1961 ) that bilateral lesions of the lateral hypothalamic area resulted in the loss of an active avoidance response can be accounted for as the result of damage inflicted on the hypothalamic link of the “action circuit” which prevented the bodily disturbance connected with fear; without such bodily reverberation, fear loses its urgency and no longer leads to action.

t This seems to be confirmed by our finding that rats with precommissural fomix lesions (with or without additional damage to hippocampal rudiment or postcommissural fornix) showed severe impairment in olfactory, visual, and auditory discrimination as well as in singIe alternation learning and retention (Arnold, 1967).


More recently, Thomas et al. (1963) reported significant deficits in active avoidance after bilateral transection of the mamillothalamic tract (MTT) in a two-way shuttle box. Krieckhaus (1964) repeated the experiment and also found significant impairment, correlated with the extent of the lesion. But when he lesioned a comparable group of cats which had been trained in a one-way shuttle box, no reliable impairment could he demonstrated. Krieckhaus discussed the possibility that the lesions might produce accelerated fear extinction but decided against this hypothesis because most deficit animals showed the usual autonomic signs of fear. yet did not jump, while cats that made the avoidance response were “nonchalant and relaxed.” H e also noted that “freezing” in the two-way box usually occurred some trials after the first error-which speaks against the hypothesis of Thomas et al. that M T T lesions potentiate the freezing response and so prevent avoidance.

Both Krieckhaus and Thomas et al. pointed out that the avoidance deficit after M T T lesions cannot he attributed to a loss of memory because postoperative retention of a visual discrimination habit was unimpaired after such lesions; also, the avoidance response in the one-way shuttle box was retained. Indeed, even in the two-way shuttle box the animals made the correct avoidance response once or twice but soon gave up: on the following days, they again jumped in the begin- ning of the session. It seems clear that they remembered the response they had made to the CS; hut to go on making it, the animal must feel an impulse to escape from the “bad” compartment. This impulse, I suggest, is reduced because of the impairment in affective memory.

However, fear includes not only an impulse to escape but a bodily disturbance. The pain produced by the electric shock initiated a number of autonomic changes connected with the impulse to escape. These changes are apparently mediated by relays from the posterior cingulate gyrus to the autonomic system via the hypothalamus, one branch of the “action circuit” (see Arnold, 1960, vol. 2, p. 80f.) Even though the MTT is transected, the direct fibers connecting the fornix with the anterior thalamic nucleus (Nauta, 1956) could still mediate the reinstatement of these changes, i.e., the bodily disturbance and a reduced impulse to jump. After MTT destruction, the CS would initiate recall of the correct motor response (via precommissural fornix) and also the bodily disturbance connected with fear (via direct fornix fibers to anterior thalamic nucleus); the only component missing would be the escape tendency which depends on the affective memory that this compartment is bad (to-be-avoided). In the two-way shuttle box, however, this emotional disturbance would be felt in both com- partments, for the animal has heen shocked in both. The avoidance response does not bring relief and the animal soon “freezes” with all signs of fear. In the one- way box, on thc contrary, relief is experienced as soon as the animal has jumped into the safe compartment because shock has never been applied here.

T o test the notion of an affective memory circuit directly, we have conducted a series of experiments in which bilateral lesions were placed at various points in the postulated circuit, namely the cingulum, the anterior and posterior insula, and the anterior thalamic nucleus. Rats were trained in five successive discriminations, one in each modality: visual, auditory, tactual, olfactory, and motor. The olfactory discrimination consisted of a box with a glass front: a moving tray with small cups of water appeared underneath the glass front, one cup at a time. The animal had to sniff at the cup and drink. When the odor was positive, the cup contained plain water; when negative, a quinine solution, which the rat avoided. The motor problem was a single alternation T-maze. Visual and auditory

Arnold: Motivation and the Limbic System 1053 discriminations were tested in a Skinner box with flashing versus steady light as visual stimulus, a buzzer as auditory stimulus. Tactual discrimination was tested in the same box, with a slight shock delivered to the grid as the only cue. The animal learned to press rapidly when he felt no shock, at which time a cup with water appeared. H e learned to slow down as soon as he felt a shock to his feet, at which time the cup with water did not appear. The shocks were delivered at variable intervals. Although analysis of the data has not been completed, pre- liminary analysis has shown the following results:

Cingulum Lesions nt the Genu of the Corpus Callosum

Of 15 rats with bilateral lesions, all showed some retention deficit in the visual, auditory, tactual, and motor problems; in the olfactory discrimination, 13 animals showed some deficit. When the retention scores of each animal before and after the lesion were compared separately, it was found that two animals showed significant impairment in olfactory discrimination, three in the tactual, six in the auditory, seven in the motor problem, and eight in visual discrimination ( p between < .05 and < -01).

Cingulum Lesions at the Junction Between Motor and Sensory Cortex

Eleven animals with bilateral lesions showed impairment in retaining the visual, auditory, tactual, and motor problems, as compared with their own performance in a retention test before operation. However, they either remained stationary or improved in olfactory discrimination. Three of these animals refused to run in the single alternation T-maze postoperatively. They spent the time either in the start box or in the straightway, but they did not seem to be frightened nor did they try to hide. This type of behavior also occurred in 50% of the animals with comparable lesions in another experiment, both in the single alternation and the olfactory discrimination problem.

All these lesions were comparatively small, from 1 m m to a maximum of 2.5 m m in fronto-caudal extent, thus, considerably smaller than the lesions made by McCleary or Thomas. In each task, great care was taken to have a single modality cue as the only discriminandum.

According to my theory, both lesions damaged the area mediating appraisal of body movements in the anterior cingulate gyrus, and thus also interfered with affective memory which makes such movements seem immediately desirable or undesirable. The impairment after such lesions seems to be rather general in all modalities, because all modalities depend on motor performance to demonstrate learning or retention. However, the tasks showing impairment in the greatest number of animals are single alternation and visual discrimination. The “refusal” of some of the animals to perform the single alternation of olfactory discrimination should not be confused with the “freezing” often observed in avoidance experiments. Rather, the animal seems to feel no desire either to run the maze or to approach the cup in the olfactory discrimination; he does not crouch and seems quite unconcerned.

The impairment after such lesions is shown dramatically by the increased difficulty in “shaping” the animals (data from this learning study are not yet analyzed). For instance, in the olfactory discrimination, which intact animals usually learn in the first session, the lesioned animals often do not approach the glass front of the box even after they have found water in the cup. It takes many


trials before they learn to approach the cup immediately, although the discrimination of odors does not seem to present additional difficulties.

Passive Avoidance Retention After Anterior Cingctlum Lesions This lack of affective memory for bodily movement is illustrated by another

experiment. Sixteen rats with lesions at the midcingulum were trained in passive avoidance in an apparatus similar to that of McCleary (1961) except for its smaller size. They were trained successively with (1 ) shock to the face as soon as they touched the water in the drinking cup and ( 2 ) shock to the hind legs as soon as they started drinking ( the forelegs had t o rest on a n insulated step to reach the cup) . This variation was devised to test whether shock t o the hindlegs would result in greater impairment, since the theory postulates that touch to the hindlegs is appraised via the posterior cingulate gyrus but touch to the face via the posterior insula.

In the group of 16 animals with either unilateral or bilateral lesions, there was not the slightest impairment when shock to the face was given. With shock to the hind feet, one animal showed a significant difference between retention of passive avoidance before and after the lesion. Eight animals without apparent impairment in other tested discriminations were then given another lesion of the cingulum at the genu of the corpus callosum. After this second lesion, none of the animals were significantly impaired when shock to the face was given, but two more animals (three in all) showed a significant deficit in retention ( p < .02 to < .01) with shock of the feet.

However, we noticed another phenomenon which is highly relevant. In both situations (shock to face and shock to feet) , the animals would approach the cup and stop with head held straight above the cup; then, instead of drinking, they would quickly withdraw. This behavior is rarely observed in intact animals although such animals may approach part of the way. In the lesioned animals, this curious behavior may result from the same loss of affective memory for appropriate bodily movement. Since the animals were thirsty and remembered that the cup contained water, they approached. But when they detected the odor and saw the water, they did not dip the head into the water because the pain brought on by such movements before was now relived and resulted in hasty retreat. AC- cording to my theory, the appraisal of head movements as desirable or undesirable is mediated via the anterior insula, and so is the affective memory for the success or punishment connected with such movements. The anterior insula was intact in these animals.

When the number of such almost-complete approaches in the postoperative retention period was compared with their number before the operation, it was found that three animals showed a significant difference with face shock, and three with feet shock after the first lesion, After the second lesion, four additional animals showed a significant difference with face shock but none with shock to the feet. Considering these results, it is not surprising that even animals who received shock to the feet could in most instances refrain from drinking. However, in learning a passive avoidance response, animals with anterior cingulum lesions seem to be impaired more drastically. In both situations, with shock to the face and shock to the feet, another group of 17 rats with mid-cingulum lesions showed significant impairment when compared with intact controls ( p < .01 and .05). Apparently, it is so difficult for these animals to appraise and so restrain body movement that they are led by thirst to approach and drink. It takes considerable time before the affective memory of pain after drinking can inhibit this response.

Arnold: Motivation and the Limbic System

Active Avoidance after Anterior Cingulum Lesions Only two out of 16 animals showed a significant retention deficit after lesions

of the midcingulum. None of the other animals, not even those given a second lesion at the genu, showed any impairment. In this situation, the animal faced the opening, remembered the cue stimulus (via intact modality-specific memory circuit); and the affective memory of leg shock (via posterior cingulate) produced the impulse to jump. Although this impulse could not be effectively appraised because of the anterior cingulum lesion, jumping was the correct response and SO did not demonstrate the deficit. In one of the two animals that showed a retention deficit, the lesion destroyed the hippocampal rudiment; in the other, the lesion damaged the superior fornix and septa1 area. Thus, in both animals the modality-specific memory circuit was damaged, which accounts for their impairment.

Comparing our results with those of McCleary and Krieckhaus, we can agree that lesions of the precallosal and anterior cingulate gyrus (which always damage the cingulum or fibers from the precallosal gyrus to the cingulum) produce n o significant deficit in active avoidance, but d o produce such a deficit in passive avoidance. But we may infer from our findings that the deficit in passive avoidance results from the difficulty in restraining bodily movement based on the lack of affective memory connected with such movement. This deficit cannot be demonstrated in active avoidance because n o inhibition of movement is required. Even in passive avoidance, this deficit can in many cases (particularly when the habit has been learned preoperatively) be compensated for at the last moment, because head movement can still be appraised as long as the anterior insula and its pathways are intact.

1055

Cingulum Lesions at the Splenium o f the Corpus Callosum Fourteen rats showed severe impairment in learning the single alternation

T-maze and some impairment in learning the olfactory discrimination ( p < ,005 and < .025) , as compared with sham-operated controls. They also were significantly inferior to sham-opmated controls in learning the active avoidance problem ( p < .005). These animals were trained in four other discriminations as well, but these data are not available as yet.

This experiment confirms earlier reports that active avoidance is impaired by posterior cingulate and cingulum lesions. In this situation, the animal is n o longer able to relive the pain connected with shock to the legs and, therefore, no longer has an immediate impulse to escape from the shock compartment.

On the supposition that the cingulum is composed of fibers which run from the genu of the corpus callosum to the splenium, fornix, and hippocampal gyrus, the impairment in learning the single alternation and olfactory discrimination problems can be explained in the same way as similar impairment after lesions of the anterior cingulum. However, there is some evidence that most of the cingulum fibers dip into the subcortex a short distance from their point of entry (Adey. 1951; Adey & Meyer, 1952). In that case, the lesion at the splenium would only have destroyed some of the fibers originating in the precallosal o r anterior cingulate gyrus, but this was apparently sufficient to confuse the animal in learning the two discriminations.

Anterior Insula Lesions That the anterior insula is necessary for the appraisal of head, but not of body,

movement can be inferred from another experiment. Five animals with bilateral


lesions of the anterior insula showed no significant impairment in learning the single alternation and active avoidance habit as compared with sham-operated controls. However, they did show a significant deficit in the olfactory discrimination ( p <.00.5). As mentioned before, here the animals have to appraise their head movement (whether to drink at this particular moment). When the anterior insula is damaged, this appraisal is impaired, according to my theory, and head movement can no longer be restrained when the odor is the negative stimulus. For the same reason, rats with such lesions have a passive avoidance deficit, i.e., they keep o n drinking from a dish through which they have been shocked (Kaada et a/., 1962). By contrast, active avoidance is unimpaired because the appraisal of shock and affective memory of pain (via posterior cingulate) is unimpaired.

Anterior Thalamic Nucleus Lesions Sixteen animals with partial or complete lesions showed some retention deficits

in every problem except the olfactory discrimination. All animals but one showed some impairment, and all animals with bilateral lesions showed a significant deficit in postoperative retention of the single alternation problem, compared with their own preoperative retention ( p from < .05 to < . O O O O l ) . All animals but one had some impairment in postoperative retention of the visual and tactual discrimination; this deficit was significant in five animals for visual and in four animals for tactual discrimination. Eight animals had some retention deficit in auditory discrimination, which was significant in one animal.

This lesion, like the cingulum lesions, had produced a general impairment in all discrimination problems, an impairment which seems to be based on the same interference with affective memory we have hypothesized in lesions of the cingulum. The intact olfactory discrimination in these animals seems to indicate that the affective memory circuit for the appraisal of head movements lies outside the circuit including cingulum, fornix, mamillothalamic tract, and anterior thalamic nucleus.

Conclusion

Lesions of the anterior cingulate gyrus and anterior thalamic nucleus produce an impairment in all modalities tested; this impairment seems to represent a defect in affective memory resulting in inability to restrain body movement or make the correct response when there is another alternative. This defect in appraisal of body movement is not apparent in situations in which only one positive response is required (active avoidance). Moreover, the defect is often masked, even in situations that should demonstrate it, if the consummatory response requires head movement (passive avoidance and olfactory discrimination), because the appraisal of head movements seems to be mediated by the anterior insula. After lesions of this structure, leaving the cingulum and anterior thalamic nucleus intact, the appraisal of head movements is defective, which produces decrements in situations in which the consummatory response requires head movement (olfactory discrimination and passive avoidance). Finally, after lesions of the posterior cingulate and cingulum, there is impairment of performance in tasks which require body movement to avoid shock: this seems to be the result of an interference with affective memory (of pain) so that there is n o longer an immediate impulse to escape. However, when hunger supplies the missing impulse, this impairment is masked. (see pp. 1049-1050).

Although an appraisal of food, water, or shock is necessary before the animal will respond, there must also be a n appraisal of the movements by which the


goal can be achieved if the response is to be adequate. These appraisals are unwitting, unconscious, and are perpetuated by affective memory reinstating earlier approach-avoidance attitudes. When motivation and emotion are thus analyzed in depth, it becomes clear that the affective memory of pain or pleasure is the basis for most action impulses including emotions, and that the affective memory of appropriate or inappropriate movements is necessary for the smooth performance of learned action. At the same time, such analysis will make it possible to trace the brain structures that mediate motivated actions.

Admittedly, the explanations given here are complicated; but we must not expect a simple link from sensory to motor cortex to mediate complex activities like learning and motivation. Unless we work out a theory broad enough to account for the findings that are published in such profusion, yet precise enough to be testable, experimental investigation will amass isolated facts that will become increasingly chaotic as time goes on.

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emotion, motivation, and the limbic system

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