The Emotional Brain That Occur in Response to Emotive Stimuli
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PERSPECTIVES by rTMS of primary motor cortex. Curr. Biol. 14, 252–256 55. Shea, J. & Morgan, R. Contextual interference effects on Two fathers of affective neuroscience (2004). the acquisition, retention, and transfer of a motor skill. 44. Tong, C., Wolpert, D. M. & Flanagan, J. R. Kinematics J. Exp. Psychol. Hum. Learn. Mem. 5, 179–187 (1978). In 1872, Charles Darwin published a ground- and dynamics are not represented independently in 56. Simon, D. & Bjork, R. Metacognition in motor learning. breaking book — The Expression of the motor working memory: evidence from an interference J. Exp. Psychol. Learn. Mem. Cogn. 27, 907–912 2 study. J. Neurosci. 22, 1108–1113 (2002). (2001). Emotions in Man and Animals .It was the 45. Tong, C. & Flanagan, J. R. Task-specific internal models 57. Osu, R., Hirai, S., Yoshioka, T. & Kawato, M. Random culmination of 34 years of work on emotion for kinematic transformations. J. 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Press for helpful discus- humans, such as tears when upset or baring secondary-task effects on sequence learning. Psychol. sions, and to M. Casement and D. Cohen for their thoughtful Res. 60, 53–71 (1997). comments on this manuscript. The National Alliance for the teeth when angry, are vestigial patterns of 51. Shin, J. & Ivry, R. Concurrent learning of temporal and Research in Schizophrenia and Depression (E.M.R.), the National action. The second contribution was the spatial sequences. J. Exp. Psychol. Learn. Mem. Cogn. Institutes of Health (A.P.L.) the Goldberg Foundation (A.P.L.) and 28, 445–457 (2002). the Wellcome Trust (R.C.M.) financially supported this work. proposal that a limited set of fundamental or 52. Aizenstein, H. J. et al. Regional brain activation during ‘basic’ emotions are present across species concurrent implicit and explicit sequence learning. Cereb. Competing interests statement Cortex 14, 199–208 (2004). 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Around 10 years later, James, in his seminal TIMELINE paper entitled ‘What is an Emotion?’1,contro- versially proposed that emotions are no more than the experience of sets of bodily changes The emotional brain that occur in response to emotive stimuli. So, if we meet a bear in the woods, it is not the Tim Dalgleish case that we feel frightened and run; rather, running away follows directly from our The discipline of affective neuroscience is neuroscience uses functional neuroimaging, perception of the bear, and our experience of concerned with the neural bases of emotion behavioural experiments, electrophysiological the bodily changes involved in running is the and mood. The past 30 years have recordings, animal and human lesion studies, emotion of fear. Different patterns of bodily witnessed an explosion of research in and animal and human behavioural experi- changes thereby code different emotions. affective neuroscience that has addressed ments to seek a better understanding of Similar ideas were developed in parallel by questions such as: which brain systems emotion and mood at the neurobiological and Carl Lange in 1885 (REF.11),providing us with underlie emotions? How do differences in psychological levels and their interface. the James–Lange theory of emotions. these systems relate to differences in the In this article, I outline the historical The James–Lange theory was challenged emotional experience of individuals? Do development of affective neuroscience (see in the 1920s by Cannon3,4 on several grounds: different regions underlie different emotions, TIMELINE). I begin by reviewing the pioneer- total surgical separation of the viscera from or are all emotions a function of the same ing work of William James1 and Charles the brain in animals did not impair emotional basic brain circuitry? How does emotion Darwin2.This is followed by discussion of the behaviour; bodily or autonomic activity processing in the brain relate to bodily early functional neuroanatomical models cannot differentiate different emotional changes associated with emotion? And, of emotion of Walter Cannon and Philip states; bodily changes are typically too slow to how does emotion processing in the brain Bard3–6,James Papez7 and Paul MacLean8.I generate emotions; and artificial hormonal interact with cognition, motor behaviour, then briefly outline our current knowledge of activation of bodily activity is insufficient language and motivation? the contributions of key brain regions, to generate emotion. Recent research has including the prefrontal cortex (PFC), amyg- cast doubt on Cannon’s claims. Emotional How are emotions and moods embodied dala, hypothalamus and anterior cingulate responses can be distinguished (at least in the brain? This is the central question cortex (ACC), to the processing of emotions, partly) on the basis of autonomic activity12; that is posed by affective neuroscience — before considering contemporary theoretical emotions were less intense when the an endeavour that integrates the efforts accounts of how these regions might interact. brain was disconnected from the viscera of psychologists, psychiatrists, neurologists, Finally, some thought is given to the future in Cannon’s studies; and some artificial philosophers and biologists. Affective directions of affective neuroscience. manipulations of organ activity can induce 582 | JULY 2004 | VOLUME 5 www.nature.com/reviews/neuro PERSPECTIVES emotions — for instance, intravenous brain lesions to understand emotions, based model elaborated on Papez’s and Cannon and administration of cholecystokinin (a gastric on the logic that any changes after surgery Bard’s original ideas and integrated them with peptide) can provoke panic attacks13. must reflect processes that involved the the knowledge provided by the seminal work The James–Lange theory has remained lesioned part of the brain. of Kluver and Bucy. In 1939, Kluver and influential. Its main contribution is the Bucy14 had shown that bilateral removal emphasis it places on the embodiment of The Papez circuit. In 1937, James Papez of the temporal lobes in monkeys led to emotions, especially the argument that pro-posed a scheme for the central neural a characteristic set of behaviours (the changes in the bodily concomitants of circuitry of emotion — now known as the ‘Kluver–Bucy syndrome’) that included a loss emotions can alter their experienced ‘Papez circuit’7 (FIG. 2).Papez proposed that of emotional reactivity, increased exploratory intensity. Most contemporary affective sensory input into the thalamus diverged into behaviour, a tendency to examine objects neuroscientists would endorse a modified upstream and downstream — the separate with the mouth, hypersexuality and abnormal James–Lange view in which bodily feedback streams of ‘thought’ and ‘feeling’.The thought dietary changes, including