Animal studies of amygdala function in fear and uncertainty: Relevance to human research

Biological Psychology

Volumn 73, Issue 1, 2006, Pages 49-60

  Rosen, Jeffrey B ^a   Donley, Melanie P ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Amygdala; egr 1; Fear; Fear conditioning; Predator; Uncertainty; Unconditioned fear

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANXIETY; ANXIETY DISORDER; ARTICLE; AVERSIVE BEHAVIOR; BRAIN FUNCTION; BRAIN REGION; CONDITIONED REFLEX; CONDITIONING; EMOTION; FEAR; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; LEARNING; MEDICAL RESEARCH; MEMORY; NEUROBIOLOGY; NEUROIMAGING; NOISE; NONHUMAN; PERCEPTION; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; UNCERTAINTY;

AMYGDALA; ANIMALS; AROUSAL; ASSOCIATION LEARNING; BRAIN; CONDITIONING, CLASSICAL; EARLY GROWTH RESPONSE PROTEIN 1; FEAR; GENE EXPRESSION; HUMANS; NERVE NET; RATS; RNA, MESSENGER; SPECIES SPECIFICITY; UNCERTAINTY;

EID: 33646523377     PISSN: 03010511     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2006.01.007     Document Type: Article

References (117)

1. Adolphs R., Tranel D., and Damasio A.R. The human amygdala in social judgment. Nature 393 6684 (1998) 470-474
2. Adolphs R., Tranel D., Damasio H., and Damasio A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372 6507 (1994) 669-672
3. Adolphs R., Tranel D., Damasio H., and Damasio A.R. Fear and the human amygdala. Journal of Neuroscience 15 (1995) 5879-5891
4. Adolphs R., Tranel D., Hamann S., Young A.W., Calder A.J., Phelps E.A., et al. Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia 37 10 (1999) 1111-1117
5. Aggleton J.P. The contribution of the amygdala to normal and abnormal emotional states. Trends of Neuroscience 16 8 (1993) 328-333
6. Aggleton J.P., and Passingham R.E. Syndrome produced by lesions of the amygdala in monkeys (macaca mulatta). Journal of Comparative and Physiological Psychology 95 6 (1981) 961-977
7. Aggleton J.P., and Young A.W. The enigma of the amygdala: on its contribution to human emotion. In: Lane R.D., and Nadel L. (Eds). Cognitive Neuroscience of Emotion (2000), Oxford University Press, New York 106-128
8. Amorapanth P., LeDoux J.E., and Nader K. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nature Neuroscience 3 (2000) 74-79
9. Anderson A.K., Christoff K., Panitz D., De Rosa E., and Gabrieli J.D. Neural correlates of the automatic processing of threat facial signals. Journal of Neuroscience 23 13 (2003) 5627-5633
10. Anderson A.K., Christoff K., Stappen I., Panitz D., Ghahremani D.G., Glover G., et al. Dissociated neural representations of intensity and valence in human olfaction. Nature Neuroscience 6 2 (2003) 196-202
11. Anderson A.K., and Phelps E.A. Expression without recognition: contributions of the human amygdala to emotional communication. Psychological Science 11 (2000) 106-111
12. Anderson A.K., and Phelps E.A. Perceiving emotion: there's more than meets the eye. Current Biology 10 15 (2000) R551-R554
13. Anderson A.K., and Phelps E.A. Is the human amygdala critical for the subjective experience of emotion? Evidence of intact dispositional affect in patients with amygdala lesions. Journal of Cognitive Neuroscience 14 5 (2002) 709-720
14. Baxter M.G., and Murray E.A. The amygdala and reward. Nature Reviews Neuroscience 3 (2002) 563-573
15. Bechara A., Tranel D., Damasio H., Adolphs R., Rockland C., and Damasio A.R. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269 5227 (1995) 1115-1118
16. Blair H.T., Schafe G.E., Bauer E.P., Rodrigues S.M., and LeDoux J.E. Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learning and Memory 8 (2001) 229-242
17. Blanchard D.C., and Blanchard R.J. Innate and conditioned reactions to threat in rats with amygdaloid lesions. Journal of Comparative and Physiological Psychology 81 (1972) 281-290
18. Bouton M.E., Mineka S., and Barlow D.H. A modern learning theory perspective on the etiology of panic disorder. Psychological Review 108 (2001) 4-32
19. Breiter H.C., Etcoff N.L., Whalen P.J., Kennedy W.A., Rauch S.L., Buckner R.L., et al. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17 (1996) 875-887
20. Broks P., Young A.W., Maratos E.J., Coffey P.J., Calder A.J., Isaac C.L., et al. Face processing impairments after encephalitis: Amygdala damage and recognition of fear. Neuropsychologia 36 1 (1998) 59-70
21. Buchel C., and Dolan R.J. Classical fear conditioning in functional neuroimaging. Current Opinion in Neurobiology 10 (2000) 219-223
22. Buchel C., Morris J., Dolan R.J., and Friston K.J. Brain systems mediating aversive conditioning: An event-related fMRI study. Neuron 20 5 (1998) 947-957
23. Cahill L., Babinsky R., Markowitsch H.J., and McGaugh J.L. The amygdala and emotional memory. Nature 377 6547 (1995) 295-296
24. Cahill L., Vazdarjanova A., and Setlow B. The basolateral amygdala complex is involved with, but not necessary for, rapid acquisition of pavlovian "fear conditioning". European Journal of Neuroscience 12 (2000) 3044-3050
25. Cahill L., Weinberger N.M., Roozendaal B., and McGaugh J.L. Is the amygdala a locus of "conditioned fear"?. Neuron 23 (1999) 227-228
26. Carlsson K., Petersson K.M., Lundqvist D., Karlsson A., Ingvar M., and Ohman A. Fear and the amygdala: manipulation of awareness generates differential cerebral responses to phobic and fear-relevant (but nonfeared) stimuli. Emotion 4 4 (2004) 340-353
27. Cheng D.T., Knight D.C., Smith C.N., Stein E.A., and Helmstetter F.J. Functional mri of human amygdala activity during pavlovian fear conditioning: stimulus processing versus response expression. Behavioural Neuroscience 117 1 (2003) 3-10
28. Damasio A.R. Descartes' Error: Emotion, Reason, and the Human Brain (1994), Grosset/Ptnam, New York
29. Davis M. The role of the amygdala in conditioned fear. In: Aggleton J.P. (Ed). The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction (1992), Wiley-Liss, New York 255-306
30. Davis M., and Whalen P.J. The amygdala: vigilance and emotion. Molecular Psychiatry 6 (2001) 13-34
31. Day H.E., Masini C.V., and Campeau S. The pattern of brain c-fos mrna induced by a component of fox odor, 2,5-dihydro-2,4,5-trimethylthiazoline (TMT), in rats, suggests both systemic and processive stress characteristics. Brain Research 1025 1-2 (2004) 139-151
32. Dayas C.V., Buller K.M., and Day T.A. Neuroendocrine responses to an emotional stressor: Evidence for involvement of the medial but not the central amygdala. European Journal of Neuroscience 11 (1999) 2312-2322
33. Dielenberg R.A., Hunt G.E., and McGregor I.S. 'when a rat smells a cat': distribution of fos immunoreactivty in rat brain following exposure to predatory odor. Neuroscience 104 (2001) 1085-1097
34. Dolan R.J. Emotion, cognition, and behavior. Science 298 5596 (2002) 1191-1194
35. Donley, M.P. & Rosen, J.B. Effect of handling on egr-1 expression in the amygdala: Impact of uncertainty, submitted for publication.
36. Dragunow M. A role for immediate-early transcription factors in learning and memory. Behavior Genetics 26 (1996) 293-299
37. Fanselow M.S. Associative vs topographical accounts of the immediate shock freezing deficit in rats: implication for the response selection rules governing species-specific defensive reactions. Learning and Motivation 17 (1986) 16-39
38. Fanselow M.S. Factors governing one trial contextual conditioning. Animal Learning and Behavior 18 (1990) 264-270
39. Fanselow M.S., and Bolles R.C. Naloxone and shock-elicited freezing in the rat. Journal of Comparative and Physiological Psychology 93 4 (1979) 736-744
40. Fanselow M.S., and LeDoux J.E. Why we think plasticity underlying pavolvian fear conditioning occurs in the basolateral amygdala. Neuron 23 (1999) 229-232
41. Fendt M., Endres T., and Apfelbach R. Temporary inactivation of the bed nucleus of the stria terminalis but not of the amygdala blocks freezing induced by trimethylthiazoline, a component of fox feces. Journal of Neuroscience 23 (2003) 23-28
42. Fox R.J., and Sorenson C.A. Bilateral lesions of the amygdala attenuate analgesia induced by diverse environmental challenges. Brain Research 648 (1994) 215-221
43. Gale G.D., Anagnostaras S.G., Godsil B.P., Mitchell S., Nozawa T., Sage J.R., et al. Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. Journal of Neuroscience 24 15 (2004) 3810-3815
44. Goldstein L.E., Rasmusson A.M., Bunney B.S., and Roth R.H. Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. Journal of Neuroscience 16 15 (1996) 4787-4798
45. Gray T.S. Functional and anatomical relationships among the amygdala, basal forebrain, ventral striatum, and cortex. An integrative discussion. Annals of the New York Academy of Science 877 (1999) 439-444
46. Hall J., Thomas K.L., and Everitt B.J. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nature Neuroscience 3 (2000) 533-535
47. Hamann S.B., Cahill L., McGaugh J.L., and Squire L.R. Intact enhancement of declarative memory for emotional material in amnesia. Learning and Memory 4 3 (1997) 301-309
48. Hamann S.B., Stefanacci L., Squire L.R., Adolphs R., Tranel D., Damasio H., et al. Recognizing facial emotion. Nature 379 6565 (1996) 497
49. Herdegen T., and Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by jun, fos and krox, and creb/atf proteins. Brain Research Reviews 28 (1998) 370-490
50. Holahan M.R., and White N.M. Amygdala c-fos induction corresponds to unconditioned and conditioned aversive stimuli but not to freezing. Behavioural Brain Research 152 1 (2004) 109-120
51. Holstege G. The basic, somatic, and emotional components of the motor system in mammals. In: Paxinos G. (Ed). The Rat Nervous System. 2nd ed. (1995), Academic Press, San Diego 137-154
52. Kalin N.H., Shelton S.E., Davidson R.J., and Kelley A.E. The primate amygdala mediates acute fear but not the behavioral and physiological components of anxious temperament. Journal of Neuroscience 21 (2001) 2067-2074
53. Kapp B.S., Whalen P.J., Supple Jr. W.F., and Pascoe J.P. Amygdaloid contributions to conditioned arousal and sensory information processing. In: Aggleton J.P. (Ed). The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (1992), Wiley, New York 229-254
54. Kim M., and Davis M. Lack of a temporal gradient of retrograde amnesia in rats with amygdala lesions assessed with the fear-potentiated startle paradigm. Behavioural Neuroscience 107 6 (1993) 1088-1092
55. Kling A.S., and Brothers L.A. The amygdala and social behavior. In: Aggleton J. (Ed). The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction (1992), John Wiley and Sons, New York 353-377
56. Kluver H., and Bucy P.C. Preliminary analysis of functions of the temporal lobes in monkeys. Archives of Neurology and Psychiatry 42 (1939) 979-1000
57. Knight D.C., Smith C.N., Cheng D.T., Stein E.A., and Helmstetter F.J. Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning. Cognitive, Affective & Behavioural Neuroscience 4 3 (2004) 317-325
58. LaBar K.S., Gatenby J.C., Gore J.C., LeDoux J.E., and Phelps E.A. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20 5 (1998) 937-945
59. LaBar K.S., LeDoux J.E., Spencer D.D., and Phelps E.A. Impaired fear conditioning following unilateral temporal lobectomy in humans. Journal of Neuroscience 15 10 (1995) 6846-6855
60. Lattal K.M., and Abel T. An immediate-shock freezing deficit with discrete cues: a possible role for unconditioned stimulus processing mechanisms. Journal of Experimental Psychology: Animal Behavior Processes 27 (2001) 394-406
61. LeDoux J.E. The Emotional Brain (1996), Simon and Schuster, New York
62. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 23 (2000) 155-184
63. Li C.I., Maglinao T.L., and Takahashi L.K. Medial amygdala modulation of predator odor-induced unconditioned fear in the rat. Behavioural Neuroscience 118 2 (2004) 324-332
64. Malkani S., and Rosen J.B. Induction of ngfi-b following contextual fear conditioning and its blockade by diazepam. Molecular Brain Research 80 (2000) 153-165
65. Malkani S., and Rosen J.B. Specific induction of immediate early growth response gene 1 (egr-1) in the lateral nucleus of the amygdala following contextual fear conditioning in rats. Neuroscience 97 (2000) 693-702
66. Malkani S., Wallace K.J., Donley M.P., and Rosen J.B. An egr-1 (zif268) antisense oligodeoxynucleotide infused into the amygdala disrupts fear conditioning. Learning and Memory 11 (2004) 617-624
67. Maren S. Overtraining does not mitigate contextual fear conditioning deficits produced by neurotoxic lesions of the basolateral amygdala. Journal of Neuroscience 18 (1998) 3088-3097
68. Maren S., and Quirk G.J. Neuronal signalling of fear memory. Nature Review Neuroscience 5 11 (2004) 844-852
69. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience 27 (2004) 1-28
70. McGregor I.S., Hargreaves G.A., Apfelbach R., and Hunt G.E. Neural correlates of cat odor-induced anxiety in rats: region-specific effects of the benzodiazepine midazolam. Journal of Neuroscience 24 17 (2004) 4134-4144
71. McGregor I.S., Schrama L., Ambermoon P., and Dielenberg R.A. Not all 'predator odours' are equal: Cat odour but not 2,4,5-trimethylthiazoline (TMT: Fox odour) elicits specific defensive behaviours in rats. Behavioural Brain Research 129 (2002) 1-16
72. Mineka S., and Ohman A. Phobias and preparedness: the selective, automatic, and encapsulated nature of fear. Biological Psychiatry 52 10 (2002) 927-937
73. Morris J.S., Buchel C., and Dolan R.J. Parallel neural responses in amygdala subregions and sensory cortex during implicit fear conditioning. Neuroimage 13 6 Pt 1 (2001) 1044-1052
74. Morris J.S., Ohman A., and Dolan R.J. Conscious and unconscious emotional learning in the human amygdala. Nature 393 6684 (1998) 467-470
75. Morris J.S., Ohman A., and Dolan R.J. A subcortical pathway to the right amygdala mediating "unseen" fear. Proceedings of the National Academy of Science of the United States of America 96 4 (1999) 1680-1685
76. Murphy F.C., Nimmo-Smith I., and Lawrence A.D. Functional neuroanatomy of emotions: a meta-analysis. Cognitive, Affective & Behavioural Neuroscience 3 3 (2003) 207-233
77. Nauta W.J., and Domesick V.B. Afferent and efferent relationships of the basal ganglia. CIBA Foundation Symposium 107 (1984) 3-29
78. Phan K.L., Wager T., Taylor S.F., and Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16 2 (2002) 331-348
79. Phelps E.A., and Anderson A.K. Emotional memory: what does the amygdala do?. Current Biology 7 (1997) R311-R320
80. Pitkanen A. Connectivity of the rat amygdaloid complex. In: Aggleton J.P. (Ed). The Amygdala: A Functional Analysis. second ed. (2000), Oxford University Press, New York 31-116
81. Pitkanen A., Savander V., and LeDoux J.E. Organization of intra-amygdaloid circuitries in the rat: An emerging framework for understanding functions of the amygdala. Trends in Neuroscience 20 (1997) 517-523
82. Quirk G.J., Armony J.L., and LeDoux J.E. Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19 (1997) 613-624
83. Quirk G.J., Likhtik E., Pelletier J.G., and Pare D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. Journal of Neuroscience 23 (2003) 8800-8807
84. Quirk G.J., Repa C., and LeDoux J.E. Fear conditioning enhances short latency auditory responses of lateral amygdala neurons: parallel recordings in the freely moving rat. Neuron 15 (1995) 1029-1039
85. Radulovic J., Kammermeier J., and Spiess J. Relationship between fos production and classical fear conditioning: effects of novelty, latent inhibition, and unconditioned stimulus preexposure. Journal of Neuroscience 18 (1998) 7452-7561
86. Rauch S.L., Shin L.M., and Wright C.I. Neuroimaging studies of amygdala function in anxiety disorders. Annals of the New York Academy of Science 985 (2003) 389-410
87. Ressler K.J., Paschall G., Zhou X.L., and Davis M. Regulation of synaptic plasticity genes during consolidation of fear conditioning. Journal of Neuroscience 22 (2002) 7892-7902
88. Ricardo J.A., and Koh E.T. Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Research 153 (1978) 1-26
89. Rodrigues S.M., Schafe G.E., and LeDoux J.E. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44 1 (2004) 75-91
90. Romanski L.M., and LeDoux J.E. Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of the temporal cortex in the rat. Cerebral Cortex 3 (1993) 515-532
91. Rosen J.B. The neurobiology of conditioned and unconditioned fear: A neurobehavioral system analysis of the amygdala. Behavioral and Cognitive Neuroscience Reviews 3 (2004) 23-41
92. Rosen J.B., Adamec R.E., and Thompson B.L. Expression of egr-1 (zif268) in rat brain following exposure to a predator. Behavioural Brain Research 162 (2005) 279-288
93. Rosen J.B., Fanselow M.S., Young S.L., Sitcoske M., and Maren S. Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning. Brain Research 796 (1998) 132-142
94. Rosen J.B., and Schulkin J. From normal fear to pathological anxiety. Psychological Review 105 (1998) 325-350
95. Rudy J.W., Huff N.C., and Matus-Amat P. Understanding contextual fear conditioning: Insights from a two-process model. Neuroscience Biobehavioural Reviews 28 7 (2004) 675-685
96. Sander D., Grafman J., and Zalla T. The human amygdala: an evolved system for relevance detection. Reviews in the Neurosciences 14 4 (2003) 303-316
97. Sato W., Kubota Y., Okada T., Murai T., Yoshikawa S., and Sengoku A. Seeing happy emotion in fearful and angry faces: Qualitative analysis of facial expression recognition in a bilateral amygdala-damaged patient. Cortex 38 5 (2002) 727-742
98. Siebert M., Markowitsch H.J., and Bartel P. Amygdala, affect and cognition: evidence from 10 patients with urbach-wiethe disease. Brain 126 Pt 12 (2003) 2627-2637
99. Sigmundi R.A., Bouton M.E., and Bolles R.C. Conditioned freezing in the rat as a function of shock intensity and cs modularity. Bulletin of the Psychonomic Society 15 (1980) 254-256
100. Small D.M., Gregory M.D., Mak Y.E., Gitelman D., Mesulam M.M., and Parrish T. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39 4 (2003) 701-711
101. Stark R., Schienle A., Walter B., Kirsch P., Sammer G., Ott U., et al. Hemodynamic responses to fear and disgust-inducing pictures: an fMRI study. International Journal of Psychophysiology 50 3 (2003) 225-234
102. Swanson L.W. Cerebral hemisphere regulation of motivated behavior (1). Brain Research 886 (2000) 113-164
103. Swanson L.W., and Petrovich G.D. What is the amygdala?. Trends in Neuroscience 21 (1998) 323-331
104. Tranel D., and Damasio H. Intact electrodermal skin conductance responses after bilateral amygdala damage. Neuropsychologia 27 4 (1989) 381-390
105. Vazdarjanova A., Cahill L., and McGaugh J.L. Disrupting basolateral amygdala function impairs unconditioned freezing and avoidance in rats. European Journal of Neuroscience 14 4 (2001) 709-718
106. Walker D.L., and Davis M. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. Journal of Neuroscience 17 (1997) 9375-9383
107. Wallace K.J., and Rosen J.B. Neurotoxic lesions of the lateral nucleus of the amygdala decrease conditioned fear, but not unconditioned fear of a predator odor: comparison to electrolytic lesions. Journal of Neuroscience 21 (2001) 3619-3627
108. Weiskrantz L. Behavioral changes associated with ablation of the amygdaloid complex in monkeys. Journal of Comparative and Physiological Psychology 49 (1956) 381-391
109. Whalen P.J. Fear, vigilance and ambiguity: initial neuroimaging studies of the human amygdala. Current Directions in Psychological Science 7 (1998) 177-188
110. Whalen P.J., Rauch S.L., Etcoff N.L., McInerney S.C., Lee M.B., and Jenike M.A. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience 18 1 (1998) 411-418
111. Whalen P.J., Shin L.M., McInerney S.C., Fischer H., Wright C.I., and Rauch S.L. A functional mri study of human amygdala responses to facial expressions of fear versus anger. Emotion 1 1 (2001) 70-83
112. Winston J.S., O'Doherty J., and Dolan R.J. Common and distinct neural responses during direct and incidental processing of multiple facial emotions. Neuroimage 20 1 (2003) 84-97
113. Winston J.S., Gottfried J.A., Kilner J.M., and Dolan R.J. Integrated neural representations of odor intensity and affective valence in human amygdala. Journal of Neuroscience 25 (2005) 8903-8907
114. Yim C.Y., and Mogenson G.J. Response of nucleus accumbens neurons to amygdala stimulation and its modification by dopamine. Brain Research 239 (1982) 401-415
115. Yu A.J., and Dayan P. Expected and unexpected uncertainty: ach and ne in the neocortex. In: Becker S., Thrun S., and Obermayer K. (Eds). Advances in Neural Information Processing Systems vol. 15 (2003), MIT Press, Cambridge, MA 173-180
116. Yu A.J., and Dayan P. Uncertainty, neuromodulation, and attention. Neuron 46 4 (2005) 681-692
117. Zald D.H. The human amygdala and the emotional evaluation of sensory stimuli. Brain Research Review 41 1 (2003) 88-123