Abstract
The discipline of affective neuroscience is concerned with the neural bases of emotion and mood. The past 30 years have witnessed an explosion of research in affective neuroscience that has addressed questions such as: which brain systems underlie emotions? How do differences in these systems relate to differences in the emotional experience of individuals? Do different regions underlie different emotions, or are all emotions a function of the same basic brain circuitry? How does emotion processing in the brain relate to bodily changes associated with emotion? And, how does emotion processing in the brain interact with cognition, motor behaviour, language and motivation?
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References
James, W. What is an emotion? Mind 9, 188–205 (1884).
Darwin, C. The Expression of the Emotions in Man and Animals (Chicago Univ. Press, Chicago, 1872/1965).
Cannon, W. B. The James–Lange theory of emotions: a critical examination and an alternative theory. Am. J. Psychol. 39, 106–124 (1927).
Cannon, W. B. Against the James–Lange and the thalamic theories of emotions. Psychol. Rev. 38, 281–295 (1931).
Bard, P. A diencephalic mechanism for the expression of rage with special reference to the central nervous system. Am. J. Physiol. 84, 490–513 (1928).
Bard, P. & Rioch, D. M. A study of four cats deprived of neocortex and additional portions of the forebrain. John Hopkins Med. J. 60, 73–153 (1937).
Papez, J. W. A proposed mechanism of emotion. Arch. Neurol. Psychiatry 38, 725–743 (1937).
MacLean, P. D. Psychosomatic disease and the 'visceral brain': recent developments bearing on the Papez theory of emotion. Psychosom. Med. 11, 338–353 (1949).
Darwin, C. On the Origin of Species by Means of Natural Selection (Murray, London, 1859).
Ekman, P. (ed.) Darwin and Facial Expression: a Century of Research in Review (Academic, New York, 1973).
Lange, C. in The Emotions (ed. Dunlap, E.) 33–90 (Williams & Wilkins, Baltimore, Maryland, 1885).
Ekman, P., Levenson, R. W. & Friesen, W. Autonomic nervous system activity distinguishes among emotions. Science 221, 1208–1210 (1983).
Harro, J. & Vasar, E. Cholecystokinin-induced anxiety: how is it reflected in studies on exploratory behavior? Neurosci. Biobehav. Rev. 15, 473–477 (1991).
Kluver, H. & Bucy, P. C. 'Psychic blindness' and other symptoms following bilateral temporal lobectomy. Am. J. Physiol. 119, 254–284 (1937).
MacLean, P. D. in The Neurosciences. Second Study Program. (ed. Schmidt, F. O.) 336–349 (Rockefeller Univ. Press, New York, 1970).
MacLean, P. D. Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalogr. Clin. Neurophysiol. 4, 407–418 (1952).
LeDoux, J. E. The Emotional Brain: the Mysterious Underpinning of Emotional Life (Simon & Schuster, New York, 1996).
Calder, A. J., Lawrence, A. D. & Young, A. W. Neuropsychology of fear and loathing. Nature Rev. Neurosci. 2, 352–363 (2001).
Weiskrantz, L. Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J. Comp. Physiol. Psychol. 49, 381–391 (1956).
Rosvold, H. E., Mirsky, A. F., Sarason, I., Bransome, E. D. & Beck, L. H. A continious performance test of brain damage. J. Consult. Psychol. 20, 343–350 (1956).
Murray, E. A., Gaffan, E. A. & Flint, R. W. Anterior rhinal cortex and amygdala: dissociation of their contributions to memory and food preference in rhesus monkeys. Behav. Neurosci. 110, 30–42 (1996).
Meunier, M., Bachevalier, J., Murray, E. A., Malkova, L. & Mishkin, M. Effects of aspiration vs neurotoxic lesions of the amygdala on emotional reactivity in rhesus monkeys. Soc. Neurosci. Abstr. 13, 5418–5432 (1996).
Aggleton, J. P. in The Amygdala (ed. Aggleton, J. P.) 485–503 (Wiley-Liss, New York/Chichester, 1992).
Terzian, H. & Ore, G. D. Syndrome of Kluver-Bucy reproduced in man by bilateral removal of temporal lobes. Neurology 5, 373–380 (1955).
Jacobson, R. Disorders of facial recognition, social behaviour and affect after combined bilateral amygdalotomy and subcaudate tractotomy — a clinical and experimental study. Psychol. Med. 16, 439–450 (1986).
Leonard, C. M., Rolls, E. T., Wilson, F. A. W. & Baylis, C. G. Neurons in the amygdala of the monkey with responses selective for faces. Behav. Brain Res. 15, 159–176 (1985).
Brothers, L., Ring, B. & Kling, A. Response of neurons in the macaque amygdala to complex social stimuli. Behav. Brain Res. 41, 199–213 (1990).
Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372, 669–672 (1994).
Young, A. W. et al. Face processing impairments after amygdalotomy. Brain 118, 15–24 (1995).
Calder, A. J. et al. Facial emotion recognition after bilateral amygdala damage: Differentially severe impairment of fear. Cognit. Neuropsychol. 13, 699–745 (1996).
Morris, J. S. et al. A differential neural response in the human amygdala of fearful and happy facial expressions. Nature 383, 812–815 (1996).
Breiter, H. C. et al. Response and habituation of the human amygdala during visual processing of facial emotion. Neuron 17, 875–887 (1996).
Scott, S. K. et al. Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature 385, 254–257 (1997).
Whalen, P. J. et al. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci. 18, 411–418 (1998).
Morris, J., Ohman, A. & Dolan, R. J. Modulation of human amygdala activity by emotional learning and conscious awareness. Nature 393, 467–470 (1998).
Morris, J. S., DeGelder, B., Weiskrantz, L. & Dolan, R. J. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 124, 1241–1252 (2001).
Pessoa, L., McKenna, M., Gutierrez, E. & Ungerleider, L. G. Neural processing of emotional faces requires attention. Proc. Natl Acad. Sci. USA 99, 11458–11463 (2002).
Blanchard, D. C. & Blanchard, R. J. Innate and conditioned reactions to threat in rats with amygdaloid lesions. J. Comp. Physiol. Psychol. 81, 281–290 (1972).
LeDoux, J. E. Emotion: clues from the brain. Annu. Rev. Psychol. 46, 209–235 (1995).
LeDoux, J. E. in Handbook of Emotions (eds Lewis, M. & Haviland, J. M.) 109–118 (The Guilford Press, New York, 1993).
LeDoux, J. E. Cognitive–emotional interactions in the brain. Cognit. Emotion 3, 267–289 (1989).
LeDoux, J. E. in Handbook of Physiology, Nervous System. Vol. 5 (eds Mountcastle, V. & Plum, F.) 419–459 (American Physiological Society, Washington DC, 1987).
LeDoux, J. E. Sensory systems and emotion: a model of affective processing. Integr. Psychiatry 4, 237–248 (1986).
Zajonc, R. B. Feeling and thinking: preferences need no inferences. Am. Psychol. 35, 151–175 (1980).
Angrilli, A. et al. Startle reflex and emotion modulation impairment after right amygdala lesion. Brain 119, 1991–2000 (1996).
Bechara, A., Tranel, D., Damasio, H. & Adolphs, R. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269, 1115–1118 (1995).
Morris, J., Ohman, A. & Dolan, R. J. A subcortical pathway to the right amygdala mediating unseen fear. Proc. Natl Acad. Sci. USA 96, 1680–1685 (1999).
Gallagher, M. S., Graham, P. W. & Holland, P. C. The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behaviour. J. Neurosci. 10, 1906–1911 (1990).
Cahill, L., Babinsky, R., Markowitsch, H. J. & McGaugh, J. L. The amygdala and emotional memory. Nature 377, 295–296 (1995).
Adolphs, R., Cahill, L., Schul, R. & Babinsky, R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn. Mem. 4, 291–300 (1997).
Cahill, L. et al. Amygdala activity at encoding correlated with long-term free recall of emotional information. Proc. Natl Acad. Sci. USA 93, 8016–8021 (1996).
Hamann, S. B., Ely, T. D., Grafton, S. T. & Kilts, C. D. Amygdala activity related to enhanced memory for pleasant and aversive material. Nature Neurosci. 2, 289–293 (1999).
Anderson, A. & Phelps, E. A. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411, 305–309 (2001).
Harlow, J. M. Recovery of the passage of an iron bar through the head. Publ. Mass. Med. Soc. 2, 327–334 (1868).
Rolls, E. T. The orbitofrontal cortex. Phil. Trans. R. Soc. Lond. B 351, 1433–1443 (1996).
Rolls, E. T. The Brain and Emotion (Oxford Univ. Press, Oxford, 1999).
Rolls, E. T. A theory of emotion, and its application to understanding the neural basis of emotion. Cognit. Emotion 4, 161–190 (1990).
Mowrer, O. H. Learning Theory and Behavior (Wiley, New York, 1960).
Schachter, S. & Singer, J. E. Cognitive, social, and physiological determinants of emotional state. Psychol. Rev. 69, 379–399 (1962).
Mandler, G. Mind and Emotion (Wiley, New York, 1975).
Damasio, A. R., Tranel, D. & Damasio, H. in Frontal Lobe Function and Dysfunction (eds Levin, H. S., Eisenberg, H. M. & Bemton, A. L.) 217–219 (Oxford Univ. Press, New York, 1991).
Damasio, A. R. Descartes' Error (Putnam, New York, 1994).
Damasio, A. R. The somatic marker hypothesis and the possible functions of the prefrontal cortex. Phil. Trans. R. Soc. Lond. B 351, 1413–1420 (1996).
Damasio, A. R. Towards a neuropathology of emotion and mood. Nature 386, 769–770 (1997).
Nauta, W. J. H. The problem of the frontal lobe: a reinterpretation. J. Psychiatr. Res. 8, 167–187 (1971).
Pribram, K. H. in Feelings and Emotions: The Loyola Symposium (ed. Arnold, M. B.) 41–53 (Academic, New York, 1970).
Saver, J. L. & Damasio, A. R. Preserved access and processing of social knowledge in a patient with acquired sociopathy due to ventromedial frontal damage. Neuropsychologia 29, 1241–1249 (1991).
Bechara, A., Damasio, A. R., Damasio, H. & Anderson, S. W. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7–15 (1994).
Bechara, A., Tranel, D. & Damasio, H. Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain 123, 2189–2202 (2000).
Davidson, R. J. in Emotions, Cognition and Behavior (eds Kagan, J., Izard, C. E. & Zajonc, R. B.) 320–365 (Cambridge Univ. Press, Cambridge/New York, 1984).
Davidson, R. J. in Approaches to Emotion (eds Scherer, K. R. & Ekman, P.) 39–58 (Erlbaum, Hillsdale, New Jersey, 1984).
Davidson, R. J. in Handbook of Emotions (eds Lewis, M. & Haviland, J. M.) 143–154 (The Guilford Press, New York, 1993).
Davidson, R. J., Ekman, P., Saron, C., Senulis, J. & Friesen, W. V. Approach-withdrawal and cerebral asymmetry: emotional expression and brain physiology I. J. Pers. Soc. Psychol. 58, 330–341 (1990).
Davidson, R. J. & Irwin, W. The functional neuroanatomy of affective style. Trends Cognit. Sci. 3, 11–21 (1999).
Ochsner, K. N., Bunge, S. A., Gross, J. J. & Gabrieli, J. D. E. Rethinking feelings: an fMRI study of the cognitive regulation of emotion. J. Cognit. Neurosci. 14, 1215–1219 (2002).
Bush, G., Luu, P. & Posner, M. I. Cognitive and emotional influences in anterior cingulate cortex. Trends Cognit. Sci. 4, 215–222 (2000).
Davidson, R. J. et al. Neural and behavioral substrates of mood and mood regulation. Biol. Psychiatry 52, 478–502 (2002).
Lane, R. D. et al. Neural correlates of levels of emotional awareness: evidence of an interaction between emotion and attention in the anterior cingulate cortex. J. Cognit. Neurosci. 10, 525–535 (1998).
Critchley, H. D., Elliot, R., Mathias, C. J. & Dolan, R. J. Neural activity relating to generation and representation of galvanic skin responses: a functional magnetic resonance imaging study. J. Neurosci. 20, 3033–3040 (2000).
Phan, K. L., Wager, T., Taylor, S. F. & Liberzon, I. Functional neuroanatomy of emotion: a metaanalysis of emotion activation studies in PET and fMRI. Neuroimage 16, 331–348 (2002).
Murphy, F. C., Nimmo-Smith, I. & Lawrence, A. D. Functional neuroanatomy of emotions:a meta-analysis. Cognit. Affect. Behav. Neurosci. 3, 207–233 (2003).
Hess, W. R. & Brugger, M. in Biological Order and Brain Organization: Selected Works of W. R. Hess (ed. Akert, K.) 183–202 (Springer, Berlin, 1943/1981).
Olds, J. & Milner, P. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J. Comp. Physiol. Psychol. 47, 419–427 (1954).
Heath, R. G. Pleasure and brain activity in man. J. Nerv. Ment. Dis. 154, 3–18 (1972).
Baxter, M. G. & Murray, E. A. The amygdala and reward. Nature Rev. Neurosci. 3, 563–573 (2002).
Robbins, T., Cador, M., Taylor, J. R. & Everitt, B. J. Limbic-striatal interactions in reward-related processes. Neurosci. Biobehav. Rev. 13, 155–162 (1989).
Teitelbaum, P. & Epstein, A. N. The lateral hypothalamic syndrome: recovery of feeding and drinking after lateral hypothalamic lesions. Psychol. Rev. 69, 74–90 (1962).
Stellar, E. The physiology of motivation. Psychol. Rev. 61, 5–22 (1954).
Mills, C. K. The cortical representation of emotion, with a discussion of some points in the general nervous system mechanism of expression in its relation to organic nervous disease and insanity. Proc. Am. Medico-Psychol. Assoc. 19, 297–300 (1912).
Sackeim, H. A. & Gur, R. C. Lateral asymmetry in intensity of emotional expression. Neuropsychologia 16, 473–481 (1978).
Sackheim, H. A., Gur, R. C. & Saucy, M. C. Emotions are expressed more intensely on the left side of the face. Science 202, 434–436 (1978).
Schwartz, G. E., Davidson, R. J. & Maer, F. Right hemisphere lateralization from emotion in the human brain: interactions with cognition. Science 190, 286–288 (1975).
Schwartz, G. E., Ahern, G. L. & Brown, S. L. Lateralized facial muscle response to positive and negative emotional stimuli. Psychophysiology 16, 561–571 (1979).
Adolphs, R., Damasio, H., Tranel, D. & Damasio, A. R. Cortical systems for the recognition of emotion in facial expression. J. Neurosci. 16, 7678–7687 (1996).
Schneirla, T. C. in Nebraska Symposium on Motivation (ed. Jones, M. R.) 1–42 (Univ. Nebraska Press, Lincoln, 1959).
Cloninger, C. A systematic method for clinical description and classification of personality variants. Arch. General Psychiatry 44, 573–588 (1987).
Gray, J. A. The Neuropsychology of Anxiety: an Enquiry into the Function of the Septo–Hippocampal System (Clarendon, Oxford, 1982).
Lang, P. J., Bradley, M. M. & Cuthbert, B. N. Emotion, attention, and the startle reflex. Psychol. Rev. 97, 377–395 (1990).
Izard, C. E. The Face of Emotion (Appleton-Century-Crofts, New York, 1971).
Panksepp, J. Toward a general psychobiological theory of emotions. Behav. Brain Sci. 5, 407–467 (1982).
Tomkins, S. S. in Approaches to Emotion (eds Scherer, K. R. & Ekman, P.) 163–196 (Erlbaum, Hillsdale, New Jersey, 1982).
Ekman, P. An argument for basic emotions. Cogn. Emotion 6, 169–200 (1992).
Damasio, A. R. et al. Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neurosci. 3, 1049–1056 (2000).
Schmolck, H. & Squire, L. R. Impaired perception of facial emotions following bilateral damage to the anterior temporal lobe. Neuropsychology 15, 30–38 (2001).
Adolphs, R. et al. Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia 37, 1111–1117 (1999).
Phillips, M. L. et al. A specific neural substrate for perceiving facial expressions of disgust. Nature 389, 495–498 (1997).
Penfield, W. & Faulk, M. E. The insula: further observations of its function. Brain 78, 445–470 (1955).
Calder, A. J., Keane, J., Manes, F., Antoun, N. & Young, A. W. Impaired recognition and experience of disgust following brain injury. Nature Neurosci. 3, 1077–1078 (2000).
Sprengelmayer, R. et al. Loss of disgust: perception of faces and emotions in Huntingdon's disease. Brain 119, 1647–1665 (1996).
Gray, J. M., Young, A. W., Barker, W. A., Curtis, A. & Gibson, D. Impaired recognition of disgust in Huntingdon's disease gene carriers. Brain 120, 2029–2038 (1997).
Calder, A. J., Keane, J., Lawrence, A. D. & Manes, F. Impaired recognition of anger following damage to the ventral striatum. Brain (in the press).
Lawrence, A. D., Calder, A. J., McGowan, S. V. & Grasby, P. M. Selective disruption of the recognition of facial expressions of anger. Neuroreport 13, 881–884 (2002).
Izard, C. E. Four systems for emotion activation: cognitive and noncognitive processes. Psychol. Rev. 100, 68–90 (1993).
Power, M. J. & Dalgleish, T. Cognition and Emotion: From Order to Disorder (Psychology, Hove, 1997).
Dalgleish, T. Cognitive approaches to posttraumatic stress disorder (PTSD): the evolution of multi-representational theorizing. Psychol. Bull. 130, 228–260 (2004).
Dalgleish, T. & Power, M. J. The I of the storm: relations between self and conscious emotion experience. Psychol. Rev. (in the press).
Lambie, J. A. & Marcel, A. J. Consciousness and the varieties of emotion experience: a theoretical framework. Psychol. Rev. 109, 219–259 (2002).
Hariri, A. R. et al. Serotonin transporter 1tic variation and the response of the human amygdala. Science 297, 400–403 (2002).
Davidson, R. J., Putnam, K. M. & Larson, C. L. Dysfunction in the neural circuitry of emotion regulation — a possible prelude to violence. Science 289, 591–595 (2000).
Mayberg, H. S. Limbic-cortical dysregulation: a proposed model of depression. J. Neuropsychiatry Clin. Neurosci. 9, 471–481 (1997).
Lazarus, R. S. Thoughts on the relationship between emotion and cognition. Am. Psychol. 37, 1019–1024 (1982).
Panksepp, J. A critical role for 'affective neuroscience' in resolving what is basic about emotions. Psychol. Rev. 99, 554–560 (1992).
Martin, J. H. Neuroanatomy: Text and Atlas 2nd edn (Appleton & Lange, Stamford, Connecticut, 1996).
Acknowledgements
I would like to acknowledge A. Lawrence for advice and comments throughout the preparation of this manuscript. This work was funded by the UK Medical Research Council.
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Dalgleish, T. The emotional brain. Nat Rev Neurosci 5, 583–589 (2004). https://doi.org/10.1038/nrn1432
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DOI: https://doi.org/10.1038/nrn1432
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