Emotion Circuits in the Brain

Annual Review of Neuroscience - Tập 23 Số 1 - Trang 155-184 - 2000
Joseph E. LeDoux1
1Center for Neural Science, New York University, New York, New York 10003

Tóm tắt

The field of neuroscience has, after a long period of looking the other way, again embraced emotion as an important research area. Much of the progress has come from studies of fear, and especially fear conditioning. This work has pinpointed the amygdala as an important component of the system involved in the acquisition, storage, and expression of fear memory and has elucidated in detail how stimuli enter, travel through, and exit the amygdala. Some progress has also been made in understanding the cellular and molecular mechanisms that underlie fear conditioning, and recent studies have also shown that the findings from experimental animals apply to the human brain. It is important to remember why this work on emotion succeeded where past efforts failed. It focused on a psychologically well-defined aspect of emotion, avoided vague and poorly defined concepts such as “affect,” “hedonic tone,” or “emotional feelings,” and used a simple and straightforward experimental approach. With so much research being done in this area today, it is important that the mistakes of the past not be made again. It is also time to expand from this foundation into broader aspects of mind and behavior

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Tài liệu tham khảo

10.1016/S0092-8674(00)81904-2

10.1523/JNEUROSCI.15-09-05879.1995

Aggleton JP, ed. 1992.The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction.New York: Wiley-Liss

Aggleton JP, Mishkin M. 1986. The amygdala: sensory gateway to the emotions. InEmotion: Theory, Research and Experience,ed. R Plutchik, H Kellerman, 3:281–99. Orlando, FL: Academic

Amaral DG, Price JL, Pitkänen A, Carmichael ST. 1992. Anatomical organization of the primate amygdaloid complex. See Aggleton 1992, pp. 1–66

Armony JL, LeDoux JE. 1999. How danger is encoded: towards a systems, cellular, and computational understanding of cognitiveemotional interactions in fear circuits. See Gazzaniga 1999. In press

10.1523/JNEUROSCI.18-07-02592.1998

Armony JL, Servan-Schreiber D, Cohen JC, LeDoux JE. 1996. Emotion and cognition interactions in the thalalmo-cortico-amygdala network: theory and model.Cogn. Neurosci. Soc. Abstr.3:76

Armony JL, Servan-Schreiber D, Romanski LM, Cohen JD, LeDoux JE. 1997. Stimulus generalization of fear responses: effects of auditory cortex lesions in a computational model and in rats.Cereb. Cortex7:157–65

10.1016/S0079-6123(08)61877-4

10.1038/2836

10.1126/science.1736359

Barnes CA. 1995. Involvement of LTP in memory: Are we searching under the streetlight?Neuron15:751–54

10.1126/science.7652558

Bernard JF, Besson JM. 1990. The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes.J. Neurophysiol.63:473–89

Blanchard RJ, Blanchard DC, Fial RA. 1970. Hippocampal lesions in rats and their effect on activity, avoidance, and aggression.J. Comp. Physiol. Psychol.71(1):92–102

Bliss TVP, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus.Nature361:31–39

10.1113/jphysiol.1973.sp010273

1998, Learn. Mem., 5, 365, 10.1101/lm.5.4.365

10.1016/0092-8674(94)90400-6

Braver TS, Cohen JD, Jonides J, Smith EE, Noll DC. 1997. A parametric study of prefrontal cortex involvement in human working memory.NeuroImage5(1):49–62

10.1016/S0896-6273(00)80219-6

Brodal A, ed. 1982.Neurological Anatomy.New York: Oxford Univ. Press

Buchel C, Morris J, Dolan RJ, Friston KJ. 1998. Brain systems mediating aversive conditioning: an event-related fMRI study.Neuron20:947–57

10.1002/cne.903350402

10.1016/S0166-2236(97)01214-9

Calder AJ, Young AW, Rowland D, Perrett D, Hodges JR, Etcoff NL. 1996. Facial emotion recognition after bilateral amygdala damage: differentially severe impairment of fear.Cogn. Neuropsychol.13:699–745

10.1523/JNEUROSCI.15-03-02301.1995

Canteras NS, Swanson LW. 1992. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat.J. Comp. Neurol.324:180–94

10.1111/j.1749-6632.1999.tb09270.x

10.1126/science.280.5364.747

10.1152/jn.1996.76.5.3038

10.1002/syn.890110406

10.1002/syn.890060306

Christianson SA. 1989. Flashbulb memories: special, but not so special.Mem. Cogn.17:435–43

Clugnet MC, LeDoux JE. 1990. Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body.J. Neurosci.10:2818–24

Damasio A, 1994.Descarte’s Error: Emotion, Reason, and the Human Brain.New York: Gosset/Putnam

1999, Trends Cogn. Sci., 3, 211

Davis M. 1992. The Role of the Amygdala in Conditioned Fear. See Aggleton 1992, pp. 255–306

de Olmos J, Alheid G, Beltramino C. 1985. Amygdala. InThe Rat Nervous System,ed. G Paxinos, pp. 223–334. Orlando, FL: Academic

Dudai Y. 1989.The Neurobiology of Memory.New York: Oxford Univ. Press

Eichenbaum H. 1994. The hippocampal system and declarative memory in humans and animals: experimental analysis and historical origins. InMemory Systems,ed. DL Schacter, E Tulving, pp. 147–201. Cambridge, MA: MIT Press

10.1038/378131a0

Ekman P, Davidson R. 1994.The Nature of Emotion: Fundamental Questions.New York: Oxford Univ. Press

Everitt BJ, Robbins TW. 1992. Amygdala-ventral striatal interactions and reward-related processes. See Aggleton 1992, pp. 401–29

10.3758/BF03210947

10.1016/S0896-6273(00)80775-8

10.1037//0735-7044.112.4.863

10.1006/nlme.1998.3852

Gaffan D. 1992. Amygdala and the memory of reward. See Aggleton 1992, pp. 471–83

Gallagher M, Holland PC. 1994. The amygdala complex: multiple roles in associative learning and attention.Proc. Natl. Acad. Sci. USA91:11771–76

Gardner H. 1987.The Mind’s New Science: A History of the Cognitive Revolution.New York: Basic Books

Gazzaniza MS, ed. 1999.The Cognitive Neurosciences.Cambridge, MA: MIT Press. In press

Gean P-W, Chang F-C, Hung C-R. 1993. Usedependent modification of a slow NMDA receptor-mediated synaptic potential in rat amygdalar slices. J. Neurosci. Res.34:635– 41

Gentile CG, Jarrell TW, Teich A, McCabe PM, Schneiderman N. 1986. The role of amygdaloid central nucleus in the retention of differential Pavlovian conditioning of bradycardia in rabbits. Behav. Brain Res.20:263–73

Gewirtz JC, Davis M. 1997. Second-order fear conditioning prevented by blocking NMDA receptors in amygdala. Nature388:471–74

Goddard AW, Gorman JM, Charney DS. 1998. Neurobiology of panic disorder. InPanic Disorder and its Treatment,ed. JF Rosenblaum, MH Pollack, pp. 57–92. New York: Dekker

Goldman-Rakic PS. 1996. Regional and cellular fractionation of working memory. Proc. Natl. Acad. Sci. USA93:13473–80

Gray JA. 1982.The Neuropsychology of Anxiety.New York: Oxford Univ. Press

Helmstetter FJ, Bellgowan PS. 1994. Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats. Behav. Neurosci.108:1005–9

Hitchcock J, Davis M. 1986. Lesions of the amygdala but not of the cerebellum or red nucleus block conditioned fear as measured with the potentiated startle paradigm. Behav. Neurosci.100:11–22

Holland PC, Gallagher M. 1999. Amygdala circuitry in attentional and representational processes. Trends Cogn. Sci.3:65–73

Huang YY, Kandel ER. 1998. Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron21:169–78

Huang YY, Nguyen PV, Abel T, Kandel ER. 1996. Long-lasting forms of synaptic potentiation in the mamalian hippocampus. Learn. Mem.3:74–85

Isaacson RL. 1982.The Limbic System.New York: Plenum

10.1016/0006-8993(86)90020-X

Jarrell TW, Gentile CG, Romanski LM, McCabe PM, Schneiderman N. 1987. Involvement of cortical and thalamic auditory regions in retention of differential bradycardia conditioning to acoustic conditioned stimulii in rabbits. Brain Res.412:285–94

Josselyn SA, Carlezon, WA, Shi C, Neve RL, Nestler EJ, Davis M. 1998. Overexpression of CREB in the amygdala of rats facilitates long term memory formation. Soc. Neurosci. Abs.

Kaada BR. 1960. Cingulate, posterior orbital, anterior insular and temporal pole cortex. InHandbook of Physiology: Neurophysiology II,ed. J Field, HJ Magoun, VE Hall, pp. 1345–72. Washington, DC: Am. Physiol. Soc.

Kandel ER. 1997. Genes, synapses, and longterm memory. J. Cell Physiol.173:124–25

Kapp BS, Frysinger RC, Gallagher M, Haselton J. 1979. Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol. Behav.23:1109–17

Kapp BS, Whalen PJ, Supple WF, Pascoe JP. 1992. Amygdaloid contributions to conditioned arousal and sensory information processing. See Aggleton 1992, pp. 229–54

Kihlstrom JF. 1987. The cognitive unconscious. Science237:1445–52

Killcross S, Robbins TW, Everitt BJ. 1997. Different types of fear-conditioned behavior mediated by separate nuclei within amygdala. Nature388:377–80

10.1126/science.1585183

Kotter R, Meyer N. 1992. The limbic system: a review of its empirical foundation.Behav. Brain Res.52:105–27

10.1002/cne.901780205

LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA. 1998. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study.Neuron20:937–45

LaBar KS, LeDoux JE, Spencer DD, Phelps EA. 1995. Impaired fear conditioning following unilateral temporal lobectomy in humans. J. Neurosci.15:6846–55

LeDoux JE. 1987. Emotion. InHandbook of Physiology. 1: The Nervous System,ed. F Plum, pp. 419–60. Bethesda, MD: Am. Physiol. Soc.

LeDoux JE. 1991. Emotion and the limbic system concept. Concepts Neurosci.2:169–99

LeDoux JE. 1992. Emotion and the Amygdala. See Aggleton 1992, pp. 339–51

LeDoux JE, ed. 1996.The Emotional Brain.New York: Simon & Schuster

LeDoux JE, Cicchetti P, Xagoraris A, Romanski L-M. 1990a. The lateral amygdaloid nucleus: Sensory interface of the amygdala in fear conditioning. J. Neurosci.10:1062– 69

LeDoux JE, Farb CF, Ruggiero DA. 1990b. Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J. Neurosci.10:1043–54

LeDoux JE, Iwata J, Cicchetti P, Reis DJ. 1988. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J. Neurosci.8:2517–29

LeDoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ. 1987. Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J. Comp. Neurol.264:123– 46

Lee H, Kim JJ. 1998. Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. J. Neurosci.18:8444–54

Lewis M, Haviland J, eds. 1992.Handbook of Emotions.New York: Guilford

Li X, Phillips RG, LeDoux JE. 1995. NMDA and non-NMDA receptors contribute to synaptic transmission between the medial geniculate body and the lateral nucleus of the amygdala. Exp. Brain Res.105:87–100

Li XF, Stutzmann GE, LeDoux JL. 1996. Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors:in vivointracellular and extracellular recordings in fear conditioning pathways.Learn. Mem.3:229–42

Livingston KE, Escobar A. 1971. Anatomical bias of the limbic system concept. Arch. Neurol.24:17–21

Lynch G, ed. 1986.Synapses, Circuits, and the Beginnings of Memory.Cambridge, MA: MIT Press

MacLean PD. 1949. Psychosomatic disease and the “visceral brain”: recent developments bearing on the Papez theory of emotion. Psychosom. Med.11:338–53

MacLean PD. 1952. Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalogr. Clin. Neurophysiol.4:407–18

MacLean PD. 1970. The triune brain, emotion and scientific bias. See Schmitt 1970, pp. 336–49

Majidishad P, Pelli DG, LeDoux JE. 1996. Disruption of fear conditioning to contextual stimuli but not to a tone by lesions of the accessory basal nucleus of the amygdala. Soc. Neurosci. Abstr.22:1116

Maren S, Aharonov G, Fanselow MS. 1997. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav. Brain Res.88:261–74

Maren S, Aharonov G, Stote DL, Fanselow MS. 1996. N-methyl-d-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of the conditional fear in rats. Behav. Neurosci.110:1365–74

Maren S, Fanselow MS. 1995. Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulationin vivo. J. Neurosci.15:7548–64

Maren S, Poremba A, Gabriel M. 1991. Basolateral amygdaloid multi-unit neuronal correlates of discriminative avoidance learning in rabbits. Brain. Res.549:311–16

Marks I, ed. 1987.Fears, Phobias, and Rituals: Panic, Anxiety and Their Disorders.New York: Oxford Univ. Press

Mascagni F, McDonald AJ, Coleman JR. 1993. Corticoamygdaloid and corticocortical projections of the rat temporal cortex: a phaseolus vulgaris leucoagglutinin study. Neuroscience57:697–715

Mayford M, Bach ME, Huang Y-Y, Wang L, Hawkins RD, Kandel ER. 1996. Control of memory formation through regulated expression of a CaMKII transgene. Science274:1678–83

McDonald AJ. 1998. Cortical pathways to the mammalian amygdala. Prog. Neurobiol.55:257–332

McDonald RJ, White NM. 1993. A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav. Neurosci.107:3–22

McGaugh JL, Mesches MH, Cahill L, Parent MB, Coleman-Mesches K, Salinas JA. 1995. Involvement of the amygdala in the regulation of memory storage. InPlasticity in the Central Nervous System,ed. JL McGaugh, F Bermudez-Rattoni, RA PradoAlcala, pp. 18–39. Mahwah, NJ: Erlbaum

McKernan MG, Shinnick-Gallagher P. 1997. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature390:607–11

Miserendino MJD, Sananes CB, Melia KR, Davis M. 1990. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature345:716–18

Morgan MA, Romanski LM, LeDoux JE. 1993. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci. Lett.163:109–13

Morris JS, Ohman A, Dolan RJ. 1998. Conscious and unconscious emotional learning in the human amygdala. Nature393:467– 70

Morris JS, Ohman A, Dolan RJ. 1999. A subcortical pathway to the right amygdala mediating “unseen” fear. Proc. Natl. Acad. Sci. USA96:1680–85

Muller J, Corodimas KP, Fridel Z, LeDoux JE. 1997. Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit CS and to contextual stimuli. Behav. Neurosci.111:683–91

Nader K, LeDoux JE. 1997. Is it time in invoke multiple fear learning system?Trends Cogn. Sci.1:241–44

Nauta WJH. 1979. Expanding borders of the limbic system concept. InFunctional Neurosurgery,ed. T Rasmussen, R Marino, pp. 7–23. New York: Raven

Nauta WJH, Karten HJ. 1970. A general profile of the vertebrate brain, with sidelights on the ancestry of cerebral cortex. See Schmitt 1970, pp. 7–26

Neisser U. 1967.Cognitive Psychology.Englewood Cliffs, NJ: Prentice Hall

Nicoll RA, Malenka RC. 1995. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature377:115–18

Öhman A. 1992. Fear and anxiety as emotional phenomena: clinical, phenomenological, evolutionary perspectives, and informationprocessing mechanisms. See Lewis & Haviland, pp. 511–36

Ono T, Nishijo H. 1992. Neurophysiological basis of the Kluver-Bucy syndrome: responses of monkey amygdaloid neurons to biologically significant objects. See Aggleton 1992, pp. 167–90

Packard MG, Cahill L, McGaugh JL. 1994. Amygdala modulation of hippocampaldependent and caudate nucleus-dependent memory processes. Proc. Natl. Acad. Sci. USA91:8477–81

Panksepp J. 1998.Affective Neuroscience: The Foundations of Human and Animal Emotions.New York: Oxford Univ. Press

Paré D, Smith Y, Paré JF. 1995. Intra-amygdaloid projections of the basolateral and basomedial nuclei in the cat:Phaseolus vulgaris–leucoagglutinin anterograde tracing at the light and electron microscopic level.Neuroscience69:567–83

Pascoe JP, Kapp BS. 1985. Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit. Behav. Brain. Res.16:117–33

Pavlov IP. 1927.Conditioned Reflexes.New York: Dover

Phelps EA, Anderson AK. 1997. Emotional memory: What does the amygdala do?Curr. Biol.7:311–14

Phillips RG, LeDoux JE. 1992. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci.106:274–85

Pitkänen A, Savander V, LeDoux JL. 1997. Organization of intra-amygdaloid circuitries: an emerging framework for understanding functions of the amygdala. Trends Neurosci.20:517–23

Pitman RK, Orr SP. 1999. Post-traumatic stress disorder: emotion, conditioning, and memory. See Gazzaniga 1999. In press

Pribram KH, Melges FT. 1969. Psychophysiological basis of emotion. InHandbook of Clinical Neurology,ed. PJ Vinken, GW Bruyn, pp. 316–42. Amsterdam: NorthHolland Publ.

Pribram KH, Reitz S, McNeil M, Spevack AA. 1979. The effect of amygdalectomy on orienting and classical conditioning in monkeys. Pavlov. J. Biol. Sci.14:203–17

Quirk GJ, Armony JL, LeDoux JE. 1997. Fear conditioning enhances different temporal components of toned-evoked spike trains in auditory cortex and lateral amygdala.Neuron19:613–24

Quirk GJ, Repa JC, LeDoux JE. 1995. Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron15:1029–39

Rogan M, Staubli U, LeDoux J. 1997. Fear conditioning induces associative long-term potentiation in the amygdala. Nature390:604–7

Rogan MT, LeDoux JE. 1995. LTP is accompanied by commensurate enhancement of auditory—evoked responses in a fear conditioning circuit. Neuron15:127–36

Rolls ET. 1992. Neurophysiology and functions of the primate amygdala. See Aggleton 1992, pp. 143–65

Rolls ET. 1999.The Brain and Emotion.New York: Oxford Univ. Press

10.1523/JNEUROSCI.12-11-04501.1992

Romanski LM, LeDoux JE. 1993. Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat.Cereb. Cortex.3:515–32

Romanski LM, LeDoux JE, Clugnet MC, Bordi F. 1993. Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav. Neurosci.107:444–50

1999, Learn. Mem., 6, 97, 10.1101/lm.6.2.97

Schmitt FO, ed. 1970.Neurosciences: Second Study Program.New York: Rockefeller Univ. Press

10.1038/385254a0

Scoville WB, Milner B. 1957. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Psychol.20:11–21

Seligman MEP. 1971. Phobias and preparedness. Behav. Ther.2:307–20

Shi C, Davis M. 1998. Pain pathways involved in fear conditioning measured with fear potentiated startle: lesion studies.J. Neurosci.19:420–30

Siegel A, Edinger H. 1981. Neural control of aggression and rage behavior. InHandbook of the Hypothalamus.Vol. 3.Behavioral Studies of the Hyphothalamus,ed. PJ Morgane, J Panksepp, pp. 203–40. New York: Dekker

10.1016/S0149-7634(98)00040-2

Squire LR, Knowlton B, Musen G. 1993. The structure and organization of memory. Annu. Rev. Psychol.44:453–95

Stevens CF. 1998. A million dollar question: Does LTP = memory?Neuron20:1–2

Swanson LW. 1983. The hippocampus and the concept of the limbic system. InNeurobiology of the Hippocampus,ed. W Seifert, pp. 3–19. London: Academic

Turner BH, Mishkin M, Knapp M. 1980. Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J. Comp. Neurol.191:515–43

Turner BH, Zimmer J. 1984. The architecture and some interconnections of the rat amygdala and lateral periallocortex. J. Comp. Neurol.227:540–57

10.1016/0306-4522(95)00125-3

van de Kar LD, Piechowski RA, Rittenhouse PA, Gray TS. 1991. Amygdaloid lesions: differential effect on conditioned stress and immobilization-induced increases in corticosterone and renin secretion.Neuroendocrinology54:89–95

10.1073/pnas.95.25.15003

Weinberger NM. 1995. Retuning the brain by fear conditioning. InThe Cognitive Neurosciences,ed. MS Gazzaniga, pp. 1071– 90. Cambridge, MA: MIT Press

Weinberger NM. 1998. Physiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiol. Learn. Mem.70:226–51

Weisskopf MG, Bauer E, LeDoux JE. 1999. L-type voltage gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala.J. Neurosci.10512–19

10.1152/jn.1999.81.2.930

10.1523/JNEUROSCI.18-01-00411.1998

Wilensky AE, Schafe GE, LeDoux JE. 1999. Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation.J. Neurosci.19 RC48 1–5