Emotion Systems and the Brain

Transcription

1 Emotion Systems and the Brain 903 Emotion Systems and the Brain J LeDoux, New York University, New York, NY, USA ã 2009 Elsevier Ltd. All rights reserved. Introduction In 1884, William James asked, What is an emotion? Although his answer was not universally accepted, the way James framed the problem continues to influence how we think about emotions today. Particularly important was James distinction between the bodily expression of emotions and conscious emotional experiences or feelings. James goal was to explain feelings. But to do so, he felt he had to first dispel the common sense notion that feelings cause us to behave in certain ways. He argued that this was flat out wrong in fact, backwards. In his view, the expression of an emotion in behavior and other physiological responses of the body actually determinewhatwefeel.james papergaverisetotwo questions that have occupied emotion researchers and theorists ever since. One is, how do emotional stimuli elicit emotional responses? The other is, what are feelings? The first is a relatively straightforward empirical question. The second is considerably more complicated. In this overview of emotion concepts, this article begins by summarizing progress that has been made on these two questions. This article also discusses how the two questions sometimes get confused. How Do Emotional Stimuli Elicit Emotional Responses? James put his finger on a very important point when he rejected the idea that feelings cause emotional responses. Because different emotions (say, fear vs. joy) are elicited by different kinds of stimuli, the brain must have already determined the emotional nature of the situation before the feeling or the response occurs. James did not dwell on this, since he wanted to know what causes feelings. But implicit in his formulation was the notion that emotional responses are elicited on the basis of unconscious processing of emotional stimuli, since the conscious aspect of emotion, the feeling, does not emerge until the responses are expressed. Regardless of whether you accept James theory, unless you accept the common sense view, that feelings cause responses, unconscious emotional processing must be the basis of the responses. The following sections, outline how emotional stimuli, via unconscious processes, lead to the expression of emotional responses. Then, research aimed at revealing the brain mechanisms is summarized through which emotional responses are controlled by external stimuli. Unconscious Emotional Processing In the first half of the twentieth century, behaviorists eliminated consciousness from psychology and only allowed the description of psychological processes in terms of observable behavior. With the rise of cognitive science, the possibility arose for viewing psychological functions in terms of internal representations, without equating those internal processes with consciousness. That is, psychological functions involve information processing. Such processing could, but does not have to, lead to conscious experiences. Information processing, in other words, is by definition unconscious. This notion was originally about cognitive processes such as perception and memory, but it was subsequently extended to emotional processing. The processing of emotional stimuli is typically referred in psychology to as evaluative processing, or appraisal. Appraisal is said to underlie both the emotional responses and the conscious feelings that occur in the presence of emotional stimuli. Nevertheless, appraisal theorists have traditionally focused on the role of appraisals in feelings, and have viewed appraisals in terms of higher cognitive processes. However, as we will see, basic evaluative or appraisal mechanisms that operate unconsciously are also involved in the elicitation of emotional responses by external stimuli. Everyone has, in some situation, found his or her heart pounding before recognizing the nature of the eliciting event. Considerable scientific evidence also supports the idea that unconsciously processed stimuli can control emotional responses. This does not mean that conscious appraisal never occurs. It simply means that conscious appraisal is not necessary for the elicitation of emotional responses. The idea that emotional responses are based on unconscious appraisal processes is actually of tremendous value from the point of view of brain research. It allows us to do research on emotional behavior without having to first solve the mind body problem, and allows us to treat the control of emotional responses in animals and humans similarly. There are two basic ways in which emotional stimuli can elicit emotional responses by activating appraisal mechanisms. Some appraisals are hardwired by evolution and others are learned through individual experience. All organisms, including humans, have innate appraisal capacities that help ensure their survival. Stimuli that signal sexual partners, palatable

2 904 Emotion Systems and the Brain and poisonous foods, painful stimulation, predators, or aggressive members of one s own species are common examples. Such stimuli activate innate appraisal mechanisms and lead directly to the expression of species-typical responses and accompanying autonomic responses. For example, a rat that encounters a cat for the first time will express signs of fear, even if it was reared in a laboratory and never previously exposed to a cat. When organisms encounter stimuli that innately activate appraisal mechanisms they often form associations (through Pavlovian conditioning) with other stimuli present, since these may be predictive of harm or benefit in the future. These conditioned stimuli acquire the capacity to elicit species-typical emotional responses. Species-typical behavioral and autonomic responses are often just the first stage of emotional responding to an innate or conditioned emotional stimulus. In addition to these reactions, organisms also often perform instrumental actions. Avoidance behavior is a canonical example of a learned aversive instrumental action. Thus, when you encounter an innate or conditioned danger signal, your first reaction may be to freeze. But you may also try to escape from or avoid the danger. Sometimes avoidance of danger becomes pathological, as when a patient with panic disorder stays inside her home in order to reduce the chances of having an attack. Positive instrumental responses are also important. We seek stimuli and situations that lead to desirable outcomes. But these too can have pathological consequences. Eating disorders and drug addiction are common examples. Instrumental responses are often learned through trial-and-error processes in which the probability of the response changes depending on the rewarding or punishing consequences of the behavior. Once learned, these are performed as habits. However, instrumental responses can also be based on spontaneous decisions; cognitive estimation of outcomes eliminates the need for trial-and-error leaning. In summary, the brain unconsciously appraises the value of external stimuli. Some stimuli are significant because of innate wiring, while the significance of others is learned through experience. Stimuli that are appraised as significant then lead to the expression of responses. Both innate and learned stimuli can lead to the expression of hard-wired species-typical emotional responses. These reactions are then often followed by instrumental responses that reflect past learning or spontaneous decisions. Brain Mechanisms of Emotional Processing William James not only speculated about the nature of emotion, he also proposed the first modern brain theory of emotion. By the late nineteenth century researchers had discovered sensory and motor regions in the cortex. James therefore asked whether an emotion center was yet to be discovered or whether it might be possible to explain emotions as functions of cortical sensory and motor areas. He preferred the latter idea, arguing that emotional stimuli elicit emotional responses by way of sensory cortex activation of motor cortex. This idea was then challenged by Walter Cannon on the basis of studies showing that emotional reactions were preserved in decorticate animals, but were disrupted after damage to the hypothalamus. On the basis of these and other observations, Papez, in 1937, proposed a circuit theory of emotion involving the hypothalamus, anterior thalamus, cingulate gyrus, and hippocampus. Later, MacLean then named the structures of the Papez circuit, together with several additional regions (amygdala, septal nuclei, orbitofrontal cortex, portions of the basal ganglia), the limbic system, which he viewed as a general-purpose system involved in behaviors that ensure survival of the individual and the species. MacLean s writings were very persuasive and for many years the problem of relating emotion to brain mechanisms seemed solved at the level of anatomical systems. However, the limbic system concept is now believed to suffer from imprecision at both the structural and the functional levels. For example, it has proved impossible to provide unequivocal criteria for defining which structures and pathways should be included in the limbic system. A standard criterion is connectivity with the hypothalamus. However, because studies have shown that the hypothalamus is connected with structures at all levels of the central nervous system, from the neocortex to the spinal cord, the limbic system would occupy much of the brain. Further, classic limbic areas, such as the hippocampus and mammillary bodies, have proved to be far more important for cognitive processes, such as declarative memory, than for emotional processes. The post-jamesian theories of the emotional brain were fairly consistent in their view of how sensory stimuli lead to the expression of emotional responses. Sensory information transmitted from the thalamus and/or cortex to specialized subcortical emotion circuits regulates the expression of emotional responses. In these theories, the subcortical circuits were centered on the hypothalamus. Electrical stimulation studies provided strong support for the role of the hypothalamus in the control of emotional responses, including autonomic responses. Today, the emphasis has shifted from the hypothalamus to the amygdala, especially in the control

3 Emotion Systems and the Brain 905 of the bodily responses that occur during fear reactions in both animals and humans. The animal studies indicate that one region of the amygdala, the lateral nucleus, receives sensory information from the thalamus and cortex. It then connects with the central amygdala, which in turn connects with lower areas, including the hypothalamus, that then connect with specific motor neuron groups that control emotional responses. Circuits within the amygdala in essence mediate the appraisal of danger, including learning about stimuli associated with danger. The amygdala has also been implicated in appraising positive emotional stimuli, but the circuit details are less well understood. The scenario just described mainly applies to aversive emotional responses that are elicited automatically in response to a stimulus. But, as noted earlier, in addition to reacting in an automatic fashion to emotional events, organisms also perform instrumental responses. The amygdala is also involved in instrumental responses, but in a different way than for automatically elicited responses. Specifically, the central amygdala and its connectivity with lower brain regions is not involved. Instead, connections from the lateral nucleus to the basal amygdala, and from there to the striatum, seem to be important. A prominent idea in recent years has been that the prefrontal cortex, especially the ventromedial prefrontal cortex, interacts with the amygdala in the regulation of emotional responses. The amygdala is often thought of as an emotional accelerator and the prefrontal cortex as the brakes. Prefrontal cortex is also likely to play an important role in the decisionmaking processes through which instrumental behavior is regulated in emotional situations. In summary, much has been learned about the neural circuits through which sensory stimuli come to elicit emotional responses. Progress has been made for both negative and positive emotions, and for both automatic and instrumental responses. What Are Feelings? As noted previously, what William James really cared about was the nature of feelings. And throughout the following century, up to this day, there has been much debate about just what feelings are, both in psychology and brain science. The Psychology of Feelings After several decades of acceptance, James theory of feelings was dethroned by Walter Cannon. He rejected the idea that feelings are due to feedback from responses, since, he said, the bodily responses would be too slow and too vague to define the difference between fear and joy and love and grief. The debate stalled for decades, but took a new turn in the 1960s when Stanley Schachter and Jerome Singer proposed that both James and Cannon were right. Cannon was right that body arousal is not specific enough. James was right that body arousal was important. The solution, they said, was that through cognitive processes we interpret nonspecific body arousal in light of the context which exists at the moment. Later theories eliminated the need for bodily responses at all, emphasizing the importance of cognitive processing. By the 1980s, emotion had become a full-fledged cognitive process. Some, such as Robert Zajonc, felt this went too far. On the basis of the results of clever experiments he performed, Zajonc argued that feelings are the products of unconscious affect. Because he objected to the cognitive take over of emotion, he avoided the use of the term unconscious processing. Nevertheless, his work made the idea that conscious feelings might be based on unconscious appraisal palatable. Feelings and the Brain The various aforementioned theories of the emotional brain each proposed that feelings are products of information processing in the cerebral cortex. For Cannon, feelings occurred in this way: sensory information split at the thalamus, with some going to the hypothalamus and some to the cortex. The hypothalamus then communicated with the cortex. When hypothalamic information interacted with sensory information in the cerebral cortex, a feeling was the result. Papez had a similar theory, but with more anatomical specificity, proposing that feelings occurred when the cingulate cortex integrated external sensory information with information processed by the hypothalamus. For MacLean, feelings resulted in the limbic system when the hippocampal cortex integrated information from the internal and external environments. After several decades of dormancy, research and theory on the brain mechanisms of emotion began to pick up in 1980s. For the most part, this work was focused on emotional learning and the control of emotional behavior. However, attention was also returning to questions about the nature of feelings. William James, you ll recall, proposed that feelings result when the cortex perceives body sensations produced during an emotional reaction. Thus, fear feels different from love because these two emotions have different effects on the body. Although James emphasized the entire bodily response, critics such

4 906 Emotion Systems and the Brain as Cannon focused on the autonomic nervous system response. While autonomic responses are indeed slow and nonspecific, feedback from the muscles through proprioception can be fast and specific. A contemporary theory that emphasizes such responses is the facial feedback hypothesis. This theory proposes that the specific facial responses associated with certain emotions provide feedback to the brain that determines what we feel. Another feedback theory was proposed in 1994 by Antonio Damasio. Building on James, Damasio argued that we use gut feelings to figure out what we are feeling, and that this information plays an important role in the way we make decisions. For example, when trying to decide between two courses of action, we play these out in our minds and the body sensations that result in one versus the other, according to Damasio, help us decide which to choose (which one feels better). According to Damasio, the orbitofrontal cortex and the body-sensing regions of the cortex (somatosensory and insular regions) are involved in feeling states. From authors viewpoint, feedback from the body such as that described by James and Damasio adds intensity and duration to emotional experiences, but the quality of the experience is a product of working memory. Because working memory is believed to be the cognitive operation that makes consciousness possible, it may be the basis of conscious feelings as well as cognitive states of consciousness. The basic idea is that we have one mechanism of consciousness, and qualitatively different states of consciousness are defined by the kind of information that we are conscious of at the moment. Through working memory we are able to integrate the way something looks and sounds with past memories of this thing, and with the way this thing is making us feel at the moment. If you encounter a rattlesnake on a path, for example, the following kinds of information will likely come to be present in working memory: a visual representation of the snake, an auditory representation of the rattling sound, information retrieved from longterm memory (things known about snakes as well as experiences with them), and information about the state of your brain (the fact that a certain emotion system is activated and that you are aroused). These will combine to produce an integrated representation in working memory of the entire experience. The cognitive appraisal of this experience in working memory is the initial feeling. At the same time, bodily responses, which are slower to occur, are expressed. These then feed back to the brain and add to the feeling that is evolving. The difference between an emotional conscious experience and a nonemotional one is simply that working memory is working with additional information in the case of the emotional experience namely, information about the emotional aspects of the experience. The difference between different kinds of emotional experiences (fear vs. joy) is due to the particular emotion system that is active at the moment and monopolizing consciousness. Considerable evidence implicates the dorsolateral prefrontal cortex (PFC) in working memory. While the brain networks of working memory were once narrowly viewed as mainly involving the dorsolateral PFC, this is no longer the case. The various medial areas of PFC, including the orbital cortex and anterior cingulate, as well as insular cortex, are now viewed as being involved, especially in emotional situations. This broader view of working memory overlaps with Damasio s somatic hypothesis but without placing too much burden on peripheral feedback. Can Responses Tell Us about Feelings? A final issue to consider is the relation of responses and feelings. This issue has two parts. One has already been discussed: do responses cause feelings? James and Damasio emphasize this view. Others take issue with it. But the part that we want to consider here is this: can responses tell us what other organisms are feeling? Some years ago, Nagel pointed out that each species is likely to have its own kind of subjective experience of world. Because working memory plays a key role in human conscious awareness of the world, the brain mechanisms of working memory may give us clues about the kinds of experiences different organisms can have. Interestingly, the brain regions involved in working memory are more highly developed in humans than in other primates and more highly developed in other primates than in other mammals. Adding in the fact that language is likely to change the way experiences are interpreted (and appraised), and that only humans have natural language, we are led to the conclusion that whatever kinds of experiences other organisms have, they are likely to be distinct from those typical of humans. The bottom line is that two organisms may have identical behavioral and autonomic responses but have completely different conscious experiences. You can trust to some extent that when another human is acting fearful or joyful they are likely to be feeling what you refer to as fear or joy. The reason we can trust this conclusion is because we have the same basic brain plan as do other members of our species. We can therefore take what we know from our own experiences and apply it to others. We do this all the time in social interactions. People also often do this for pets and other animals. The reason this anthropomorphic reasoning is inappropriate was

5 Emotion Systems and the Brain 907 explained earlier: because the brain mechanisms of consciousness are likely to be different in different organisms, mainly because of the development of the prefrontal cortex in primates and language in humans, conscious experiences are likely to be different. Conclusion This brief survey, much of it including historical material, provides an overview of some of the major concepts of emotion that are relevant to the pursuit of brain mechanisms of emotion. Many of these concepts have been explored in depth in the large body of literature on emotion theory. See also: Aggression: Hormonal Basis; Aggression: Neurochemical and Molecular Mechanisms; Amygdala: Contributions to Fear; Aversive Emotions: Molecular Basis of Unconditioned Fear; Aversive Emotions: Genetic Mechanisms of Serotonin; Emotion and Vigilance; Emotion in Speech; Emotion: Neuroimaging; Emotion: Computational Modeling; Emotional Disorders: Treatment; Emotional Hormones and Memory Modulation; Emotional Influences on Memory and Attention; Emotional Control of the Autonomic Nervous System; Genetics of Human Anxiety and Its Disorders; Social Emotion: Neuroimaging. Further Reading Aggleton JP and Mishkin M (1986) The amygdala: Sensory gateway to the emotions. In: Plutchik R and Kellerman H (eds.) Emotion: Theory, Research and Experience, vol. 3, pp Orlando: Academic Press. Amorapanth P, LeDoux JE, and Nader K (2000) Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nature Neuroscience 3: Arnold MB (1960) Emotion and Personality. New York: Columbia University Press. Baars BJ (1997) In the theatre of consciousness. Journal of Consciousness Studies 4: Bandler RJ (1982) Induction of rage following microinjection of glutamate into midbrain but not hypothalamus of cats. Neuroscience Letters 30: Bard P (1929) The central representation of the sympathetic system: As indicated by certain physiological observations. Archives of Neurology and Psychiatry 22: Blanchard CD and Blanchard RJ (1972) Innate and conditioned reactions to threat in rats with amygdaloid lesions. Journal of Comparative Physiological Psychology 81: Brodal A (1982) Neurological Anatomy. New York: Oxford University Press. Cannon WB (1929) Bodily Changes in Pain, Hunger, Fear, and Rage. New York: Appleton. Cohen NJ and Eichenbaum H (1993) Memory, Amnesia, and the Hippocampal System. Cambridge, MA: MIT Press. Damasio A (1994) Descartes Error: Emotion, Reason, and the Human Brain. New York: Gosset/Putnam. Damasio AR and van Hoesen G (1983) Emotional disturbances associated with focal lesions of the limbic frontal lobe. In: Heilman KM and Satz P (eds.) Neuropsychology of Human Emotion, pp New York: Guilford. Davis M and Whalen PJ (2001) The amygdala: Vigilance and emotion. Molecular Psychiatry 6: Ekman P (1993) Facial expression and emotion. American Psychologist 48: Erdelyi MH (1985) Psychoanalysis: Freud s Cognitive Psychology. New York: Freeman. Everitt BJ, Parkinson JA, Olmstead MC, et al. (1999) Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. In: McGintry J (ed.) Advancing from the Ventral Striatum to the Extended Amygdala, pp New York: New York Academy of Sciences. Fanselow MS and Poulos AM (2005) The neuroscience of mammalian associative learning. Annual Review of Psychology 56: Frijda N (1986) The Emotions. Cambridge: Cambridge University Press. Gray JA (1982) The Neuropsychology of Anxiety. New York: Oxford University Press. Hilton SM and Zbrozyna AW (1963) Amygdaloid region for defense reactions and its efferent pathway to the brainstem. Journal of Physiology 165: Holland PC and Gallagher M (1999) Amygdala circuitry in attentional and representational processes. Trends in Cognitive Sciences 3: Irwin W, Davidson RJ, Lowe MJ, et al. (1996) Human amygdala activation detected with echo-planar functional magnetic resonance imaging. NeuroReport 7: Isaacson RL (1982) The Limbic System. New York: Plenum. Izard CE (1971) The Face of Emotion. New York: Appleton- Century-Crofts. James W (1884) What is an emotion? Mind 9: James W (1890) Principles of Psychology. New York: Holt. Kaada BR (1960) Cingulate, posterior orbital, anterior insular and temporal pole cortex. In: Field J, Magoun HJ, and Hall VE (eds.) Handbook of Physiology: Neurophysiology II, pp Washington, DC: American Physiological Society. Kapp BS, Pascoe JP, and Bixler MA (1984) The amygdala: A neuroanatomical systems approach to its contributions to aversive conditioning. In: Buttlers N and Squire LR (eds.) Neuropsychology of Memory, pp New York: Guilford. Kihlstrom JF (1987) The cognitive unconscious. Science 237: Lazarus R and McCleary R (1951) Autonomic discrimination without awareness: A study of subception. Psychological Review 58: Lazarus RS (1984) On the primacy of cognition. American Psychologist 39: LeDoux JE (1984) Cognition and emotion: Processing functions and brain systems. In: Gazzaniga MS (ed.) Handbook of Cognitive Neuroscience, pp New York: Plenum. LeDoux JE (1987) Emotion. In: Plum F (ed.) Handbook of Physiology. 1: The Nervous System. Volume V, Higher Functions of the Brain, pp Bethesda: American Physiological Society. LeDoux JE (1996) The Emotional Brain. New York: Simon and Schuster. LeDoux JE (2000) Emotion circuits in the brain. Annual Review of Neuroscience 23: LeDoux JE (2002) Synaptic Self: How Our Brains Become Who We Are. New York: Viking. MacLean PD (1949) Psychosomatic disease and the visceral brain : Recent developments bearing on the Papez theory of emotion. Psychosomatic Medicine 11:

6 908 Emotion Systems and the Brain MacLean PD (1952) Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalography and Clinical Neurophysiology 4: Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annual Review of Neuroscience 24: Mishkin M and Aggleton J (1981) Multiple functional contributions of the amygdala in the monkey. In: Ben-Ari Y (ed.) The Amygdaloid Complex, pp Amsterdam: Elsevier/ North-Holland Biomedical Press. Mowrer OH (1956) Two-factor learning theory reconsidered, with special reference to secondary reinforcement and the concept of habit. Psychological Review 63: Nader K and LeDoux JE (1997) Is it time to invoke multiple fear learning system? Trends in Cognitive Sciences 1: Nagel T (1974) What is it like to be a bat? Philosophical Review 83: Neisser U (1967) Cognitive Psychology. Englewood Cliffs, NJ: Prentice-Hall. Norman DA and Shallice T (1980) Attention to action: Willed and automatic control of behavior. In: Davidson RJ, Schwartz GE, and Shapiro D (eds.) Consciousness and Self-Regulation, pp New York: Plenum. Ohman A and Mineka S (2001) Fears, phobias, and preparedness: Toward an evolved module of fear and fear learning. Psychological Review 108: Ono T and Nishijo H (1992) Neurophysiological basis of the Kluver Bucy syndrome: Responses of monkey amygdaloid neurons to biologically significant objects. In: Aggleton JP (ed.) The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, pp New York: Wiley-Liss. Ortony A, Clore GL, and Collins A (1988) The Cognitive Structure of Emotions. Cambridge: Cambridge University Press. Panksepp J (1982) Toward a general psychobiological theory of emotions. Behavioral and Brain Sciences 5: Panksepp J (1998) Affective Neuroscience. New York: Oxford University Press. Papez JW (1937) A proposed mechanism of emotion. Archives of Neurology and Psychiatry 79: Phelps EA and LeDoux JE (2005) Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron 48: Quirk GJ, Russo GK, Barron JL, et al. (2000) The role of ventromedial prefrontal cortex in the recovery of extinguished fear. Journal of Neuroscience 20: Rolls ET (1999) The Brain and Emotion. Oxford: Oxford University Press. Schachter S (1975) Cognition and centralist peripheralist controversies in motivation and emotion. In: Gazzaniga MS and Blakemore CB (eds.) Handbook of Psychobiology, pp New York: Academic Press. Schachter S and Singer JE (1962) Cognitive, social, and physiological determinants of emotional state. Psychological Review 69: Shallice T (1988) Information processing models of consciousness. In: Marcel A and Bisiach E (eds.) Consciousness in Contemporary Science, pp Oxford: Oxford University Press. Siegel A and Edinger H (1981) Neural control of aggression and rage behavior. In: Morgane PJ and Panksepp J (eds.) Handbook of the Hypothalamus, Vol. 3: Behavioral Studies of the Hypothalamus, pp New York: Dekker. Sotres-Bayon F, Cain CK, and Ledoux JE (2006) Brain mechanisms of fear extinction: Historical perspectives on the contribution of prefrontal cortex. Biological Psychiatry 60: Squire LR (1987) Memory: Neural organization and behavior. In: Plum F (ed.) Handbook of Physiology, Section 1: The Nervous System. Vol. V: Higher Functions of the Brain, pp Bethesda: American Physiological Society. Swanson LW (1983) The hippocampus and the concept of the limbic system. In: Seifert W (ed.) Neurobiology of the Hippocampus, pp London: Academic Press. Whalen PJ, Rauch SL, Etcoff NL, et al. (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience 18: Zajonc RB (1984) On the primacy of affect. American Psychologist 39: