Emotion and the Human Brain

Popular ideas about the mind evolve over time: emotion came to have its contemporary meaning only in the late nineteenth century (Candland 1977). In current usage, the concept of emotion has two aspects. One pertains to a certain kind of subjective experience, "feeling." The other relates to expression, the public manifestation of feeling. These dual aspects of emotion -- the subjective and the expressive -- were represented a century ago in the writings of William JAMES (1884), who speculated on the neural and somatic basis of feeling, and Charles DARWIN (1872), who examined the evolution of emotional expression in various species. Most workers in this area have also pointed out that feelings and the actions that go with them are an essential part of an organism's relation to its environment. Thus, together with more elaborated cognition, emotions can be said to be the means by which an animal or person appraises the significance of stimuli so as to prepare the body for an appropriate response.

Emotion is traditionally distinguished from cognition, and for most of this century received little research attention in its own right -- excepting possibly studies of the brain mechanisms of aggression. Emotion per se has come to be embraced as a legitimate topic only in the last several decades. Its acceptance was probably due in part to Ekman's influential cross-cultural studies of human facial expression (Ekman, Sorenson, and Friesen 1969), which implied an innate, biological basis for emotional experience. Social factors have undoubtedly also facilitated the entry of emotion into the arena of neuroscience research, for current popular culture upholds emotion as a significant feature of human life (McCarthy 1989).

An additional factor in the acceptance of emotion as a neurobiological entity was MacLean's (1952) persuasive account of a brain system specialized for emotion. Building on earlier anatomical theories, MacLean grouped together certain evolutionarily ancient brain structures, primarily regions of medial cortex and interconnected subcortical regions such as the hypothalamus, and called them the "visceral brain." He suggested that activity in this region was responsible for the subjective aspect of emotional experience. Later, following terminology introduced by the anatomist BROCA, he called these structures the LIMBIC SYSTEM.

In the years following MacLean's account, researchers have debated exactly which structures can be said to be "limbic." Most often included are the AMYGDALA, septum, hippocampal formation, orbitofrontal cortex, and cingulate gyrus. However, it is now appreciated that no criteria -- be they anatomic, association with visceral function, or association with the behavioral manifestations of emotional experience -- bind the regions traditionally called "limbic" unequivocally and uniquely together, leaving the status of this proposal in doubt (LeDoux 1991). Indeed, James had asserted a century ago that there is no special brain system mediating emotional experience. Instead, he held, the bodily changes brought about by a stimulus are themselves experienced in turn through interoceptive pathways that project to sensory cortex; the latter somatic sensations "are" emotional experience. The role of afferent activity from the body in producing states of feeling continues to be emphasized: indeed, the idea that somatic sensations form the critical core of ongoing subjective experience has been repeatedly proposed by philosophers and psychologists. Most neuroscientists accept the idea that the body plays a role, but they also believe that there are particular structures in the human brain that are specialized for emotional experience and behavior.

There are several distinct themes in studies of the neural basis of human emotion. One pertains to the role of neural structures in producing states of feeling. In the 1950s, neurosurgeons demonstrated that subjective emotional experiences, especially fear, could be produced by electrical stimulation in the temporal lobes, particularly in the amygdala and hippocampal formation. The amygdala has come to the fore again in modern imaging studies that suggest that individuals with familial depression have increased metabolic activity in the left amygdala. Depression has been associated with both decreased and increased activity in orbitofrontal cortex. Several decades ago, before the rise of activity-dependent imaging techniques, there was an interest in the relation between mood and hemispheric side of brain lesions, with several researchers concluding that strokes involving the left hemisphere, particularly the frontal regions, produce depression, whereas strokes in the right produce euphoria. Although this interpretation of lesion data has been debated subsequently, stable differences in individual temperament have been attributed to differing patterns of activation of anterior frontal and temporal regions in the two hemispheres.

Links between emotion, memory, and learning have also attracted interest. Normal subjects seem to show a right hemisphere superiority for recall of affective material, and subjects with greater activation of the right amygdala appear to have a greater ability to recall emotional movies. Damasio (1994) has emphasized the role of central representations of relevant somatic states for acquiring appropriate responses to positive and negative situations. In support of his thesis, he has demonstrated that certain patients with orbitofrontal lesions, who seem unable to make appropriate decisions in real life situations, are also deficient in their autonomic responses to arousing stimuli.

A second major theme in emotion research relates to the production and understanding of expressive behavior. The right hemisphere appears to predominate for the production and the perception of expressions, both facial and vocal. Indeed, the temporal cortex of the right hemisphere may have a region specialized for decoding facial expression. Furthermore, some patients with bilateral damage to the amygdala are deficient in understanding facial expressions, especially expressions of fear. One such patient was also found to have difficulty interpreting emotional and non-emotional intonations of voice. These findings are consistent with a number of lesion studies carried out from the 1930s to the 1960s in nonhuman primates, involving structures such as the amygdala, orbital frontal cortex, and cortex of the temporal pole. Researchers had concluded, based on the animals' impaired ability to interpret social signals, that these structures are part of a brain system specialized for social responsiveness in primates (Kling and Steklis 1976). Indeed, case reports have repeatedly shown that humans with lesions in structures such as the hypothalamus, amygdala, cingulate gyrus, and orbitofrontal cortex exhibit altered social behavior and expressiveness. It is at present uncertain whether one should conceptualize the defective performance of patients with amygdala lesions in terms of a primary deficiency of emotional state (e.g., fear) or a primary deficiency of social communication (e.g., ability to interpret expression).

A third theme in emotion research is the neurochemistry of mood. The discovery that the antihypertensive drug reserpine induced depression gave rise to models of depression that invoked catecholamine transmission. Subsequently, the discovery of abnormally low levels of serotonin in the cerebrospinal fluid of suicide victims gave rise to hypotheses invoking serotonin. Both theories are supported by the efficacy of medications that enhance catecholaminergic and serotonergic transmission for the treatment of depression, but empirical confirmation of hypotheses regarding the specific sites and mechanisms of action remains lacking. Other workers have proposed a role for dopamine in disorders of mood. At present, the clear efficacy of antidepressant medications is not matched by an equally clear understanding of their mechanisms. Likewise, roles for GABAergic and serotonergic systems in anxiety have been postulated, based on the clinical effects of agents that interact with these neurotransmitters. Imaging studies show some promise of illuminating the relation between neurotransmitters and mood in the future.

There are some persisting uncertainties in emotion research. For one, workers have long debated the relative contributions of somatic states and cognition to emotional experience. A principled distinction between somatic states that are emotional and those that are not is impossible: as a result, emotion cannot be defined in terms of somatic states alone. Furthermore, there is general agreement that somatic changes cannot be specific enough by themselves to yield the various discriminable emotional experiences. But because somatic elements seem indispensable to emotion, researchers such as Schachter and Singer (1962) have argued that cognitive appraisal of the stimulus must be combined with physiological arousal in order for an emotion to be produced. However, the notion of appraisal itself is complex. Another area of uncertainty concerns which emotions deserve to be called "basic" (Ortony and Turner 1990). Finally, one of the pillars of the emotion concept is the idea of subjective experience -- feeling. This raises the thorny problem of QUALIA, a philosophical term for the felt nature of experience (cf. MIND-BODY PROBLEM). Nevertheless, despite -- or even because of -- these uncertainties, emotion will continue to attract interest as a topic in cognitive science.

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-- Leslie Brothers

References

Candland, D. (1977). The persistent problems of emotion. In D. Candland, J. Fell, E. Keen, A. Leshner, R. Tarpy, and R. Plutchik, Eds., Emotion. Monterey, CA: Brooks-Cole, pp. 2-84.

Damasio, A. (1994). Descartes' Error: Emotion, Reason, and the Human Brain. New York: G. P. Putnam's Sons.

Darwin, C. (1872). The Expression of the Emotions in Man and Animals.

Ekman, P., E. Sorenson, and W. Friesen. (1969). Pan-cultural elements in facial displays of emotion. Science 186:86-88.

James, W. (1884). What is an emotion? Mind 9:188-205.

Kling, A., and H. D. Steklis. (1976). A neural substrate for affiliative behavior in nonhuman primates. Brain, Behavior and Evolution 13:216-238.

LeDoux, J. (1991). Emotion and the limbic system concept. Concepts Neurosci. 2:169-199.

MacLean, P. (1952). Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalog. Clin. Neurophysiol. 4:407-418.

McCarthy, E. D. (1989). Emotions are social things: An essay in the sociology of emotions. In D. Franks and E. D. McCarthy, Eds., The Sociology of Emotions: Original Essays and Research Papers. Greenwich, CT: JAI Press, pp. 51-72.

Ortony, A., and T. Turner. (1990). What's basic about basic emotions? Psychological Review 97:315-331.

Schachter, S., and J. Singer. (1962). Cognitive, social, and physiological determinants of emotional state. Psychological Review 69:379-399.

Emotion and the Human Brain

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