Emotion and the Animal Brain

Emotion, long ignored within the field of neuroscience, has at the end of the twentieth century been experiencing a renaissance. Starting around mid-century, brain researchers began to rely on the limbic system concept as an explanation of where emotions come from (MacLean 1949), and subsequently paid scant attention to the adequacy of that account. Riding the wave of the cognitive revolution (Gardner 1987), brain researchers have instead concentrated on the neural basis of perception, memory, attention, and other cognitive processes. However, starting in the 1980s, studies of a particular model of emotion, classical fear conditioning, began to suggest that the limbic system concept could not provide a meaningful explanation of the emotional brain (LeDoux 1996). The success of these studies in identifying the brain pathways involved in a particular kind of emotion has largely been responsible for the renewed interest in exploring more broadly the brain mechanisms of emotion, including a new wave of studies of emotion and the human brain. This article briefly reviews the neural pathways involved in fear conditioning, and then considers how the organization of the fear pathways provides a neuroana-tomical framework for understanding emotional processing, including emotional stimulus evaluation (appraisal), emotional response control, and emotional experience (feelings).

The brain circuits involved in fear conditioning have been most thoroughly investigated for situations involving an auditory conditioned stimulus (CS) paired with foot-shock (see LeDoux 1996; Davis 1992; Kapp et al. 1992;

McCabe et al. 1992; Fanselow 1994). In order for conditioning to take place and for learned responses to be evoked by the CS after conditioning, the CS has to be relayed through the auditory system to the amygdala. If the CS is relatively simple (a single tone), it can reach the amygdala either from the auditory thalamus or the auditory cortex. In more complex stimulus conditions that require discrimination or CATegorization, the auditory cortex becomes involved, though the exact nature of this involvement is poorly understood (see Jarrell et al. 1987; Armony et al. 1997).

CS information coming from either the auditory THALAMUS or the cortex arrives in the lateral nucleus of the amygdala and is then distributed to the central nucleus by way of internal amygdala connections that have been elucidated in some detail (Pitkanen et al. 1997). The central nucleus, in turn, is involved in the control of the expression of conditioned responses through its projections to a variety of areas in the brainstem. These behavioral (e.g., freezing, escape, fighting back), autonomic (e.g. blood pressure, heart rate, sweating), and hormonal (adrenaline and cortisol released from the adrenal gland) responses mediated by the central nucleus are involuntary and occur more or less automatically in the presence of danger (though they are modulated somewhat by the situation).

other brain areas implicated in fear conditioning are the hippocampus and prefrontal cortex. The hippocampus is important in conditioning to contextual stimuli, such as the situation in which an emotional event occurs. Its role is more of that of a high-level sensory/cognitive structure that integrates the situation into a spatial or conceptual "context" rather than that of an emotional processor per se (Kim and Fanselow 1992; Phillips and LeDoux 1992; LeDoux 1996). The medial area of the prefrontal cortex is important for extinction, the process by which the CS stops eliciting emotional reactions when its association with the shock is weakened (Morgan and LeDoux 1995). Fear/anxiety disorders, where fear persists abnormally, may involve alterations in the function of this region (LeDoux 1996).

The fear pathways can be summarized very succinctly. They involve the transmission of information about external stimuli to the amygdala and the control of emotional responses by way of outputs of the amygdala. The simplicity of this scheme suggests a clear mapping of certain psychological processes (stimulus evaluation and response control) onto brain circuits, and leads to hypotheses about how other aspects of emotion (feeling or experience) come about. However, it is important to point out that the ideas in the discussion that follows mainly pertain to the fear system of the brain, inasmuch as other emotions have not been studied in sufficient detail to allow these kinds of relations to be discussed.

Stimulus evaluation or appraisal is a key concept in the psychology of emotion (Lazarus 1991; Scherer 1988; Frijda 1986). Although most psychological work treats appraisal as a high-level cognitive process, often involving conscious access to underlying evaluations, it is clear from studies of animals and people that stimuli are first evaluated at a lower (unconscious) level prior to, and perhaps independent of, higher-level appraisal processes (see LeDoux 1996). In particular, the amygdala, which sits between sensory processes

(including low-level sensory processes originating precorti-cally and higher-level cortical processes) and motor control systems, is likely to be the neural substrate of early (unconscious) appraisal in the fear system. Not only do cells in the amygdala respond to conditioned fear stimuli, but they also learn the predictive value of new stimuli associated with danger (Quirk, Repa, and LeDoux 1995; Rogan, Staubli, and LeDoux 1997).

The amygdala receives inputs from a variety of cortical areas involved in higher cognitive functions. These areas project to the basal and accessory basal nuclei of the amygdala (Pitkanen et al. 1997). Thus, the emotional responses controlled by the amygdala can be triggered by low-level physical features of stimuli (intensity, color, form), higher-level semantic properties (objects), situations involving configurations of stimuli, and thoughts or memories about stimuli, and imaginary stimuli or situations. In this way higher-level appraisal processes can be critically involved in the functioning of this system. It is important to note that these hypotheses about the neural substrate of higher-level processes have emerged from a detailed elucidation of the physiology of lower-level processes. A bottom-up approach can be very useful when it comes to figuring out how psychological processes are represented in the brain.

Involuntary emotional responses are EVOLUTION's immediate solution to the presence of danger. Once these responses occur, however, higher-level appraisal mechanisms are often activated. We begin planning what to do, given the circumstances. We then have two kinds of response possibilities. Habits are well-practiced responses that we have learned to use in routine situations. Emotional habits can enable us to avoid danger and escape from it once we are in it. These kinds of responses may involve the amygdala, cortex, and basal ganglia (see LeDoux 1996; Everitt and Robbins 1992; McDonald and White 1993). Finally, there are emotional actions, such as choosing to run away rather than to stay put in the presence of danger, given our assessment of the possible outcomes of each course of action. These voluntary actions are controlled by cortical decision processes, most likely in the frontal lobe (Damasio 1994; Goldman-Rakic 1992; Georgopolous et al. 1989). Voluntary processes allow us to override the amygdala and become emotional actors rather than simply reactors (LeDoux 1996). The ability to shift from emotional reaction to action is an important feature of primate and especially human evolution.

The problem of feelings is really the problem of CONsciousness (LeDoux 1996). Emotion researchers have been particularly plagued by this problem. Although we are nowhere near solving the problem of consciousness (feelings), there have been some interesting ideas in the area of consciousness that may be useful in understanding feelings. In particular, it seems that consciousness is closely tied up with the process we call WORKING MEMORY (Baddeley 1992), a mental workspace where we think, reason, solve problems, and integrate disparate pieces of information from immediate situations and long-term memory (Kosslyn and Koenig 1992; Johnson-Laird 1988; Kihlstrom 1987). In light of this, we might postulate that feelings result when working memory is occupied with the fact that one's brain and body are in a state of emotional arousal. By integrating immediate stimuli with long-term memories about the occurrence of such stimuli in the past, together with the arousal state of the brain and feedback from the bodily expression of emotion, working memory might just be the stuff that feelings are made of.

Ever since William james raised the question of whether we run from the bear because we are afraid or whether we are afraid because we run, the psychology of emotion has been preoccupied with questions about where fear and other conscious feelings come from. Studies of fear conditioning have gone a long way by addressing James's other question —what causes bodily emotional responses (as opposed to feelings)? Although James was correct in concluding that rapid-fire emotional responses are not caused by feelings of fear, he did not say much about how these come about. However, as we now see, by focusing on the responses we have been able to get a handle on how the system works, and even have gotten some ideas about where the feelings come from.


—Joseph LeDoux and Michael Rogan References

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Further Readings

Davis, M., W. A. Falls, S. Campeau, and M. Kim. (1994). Fear potentiated startle: A neural and pharmacological analysis. Behavioral Brain Research 53: 175-198.

Gray, J. A. (1987). The Psychology of Fear and Stress, vol. 2. New York: Cambridge University Press.

LeDoux, J. E. (1994). Emotion, memory and the brain. Scientific American 270: 32-39.

Maren, S., and M. S. Fanselow. (1996). The amygdala and fear conditioning: Has the nut been cracked? Neuron 16: 237-240.

Ono, T., and H. Nishijo. (1992). Neurophysiological basis of the Kulver-Bucy Syndrome: Responses of monkey amygdaloid neurons to biologically significant objects. In J. P. Aggleton, Ed., The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. New York: Wiley-Liss, pp. 167-191.

Rolls, E. T. (1992). Neurophysiology and functions of primate amygdala. In J. P. Aggleton, Ed., The Amygdala: Neurobiologi-cal Aspects of Emotion, Memory, and Mental Dysfunction. New York: Wiley-Liss, pp. 143-166.

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Brain Blaster

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