The emotional brain, fear, and the amygdala

Cellular and Molecular Neurobiology

Volumn 23, Issue 4-5, 2003, Pages 727-738

  LeDoux, Joseph ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Amygdala; Emotion; Fear; Limbio system

Indexed keywords

AMYGDALOID NUCLEUS; AUTONOMIC NERVOUS SYSTEM; AVERSIVE BEHAVIOR; CONDITIONING; DEFENSIVE BEHAVIOR; EMOTION; ENVIRONMENTAL FACTOR; EXPERIENCE; FEAR; HUMAN; HUMAN TISSUE; LIMBIC SYSTEM; PRIORITY JOURNAL; REVIEW; STIMULUS RESPONSE; THALAMUS LATERAL NUCLEUS;

AMYGDALA; ANIMALS; CONDITIONING (PSYCHOLOGY); EMOTIONS; FEAR; HUMANS; LIMBIC SYSTEM; MODELS, ANIMAL; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; SENSATION;

EID: 0042317090     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1025048802629     Document Type: Review

References (131)

1. Abel, T., Nguyen, P. V., Barad, M., Deuel, T. A., Kandel, E. R., and Bourtchouladze, R. (1997). Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626.
2. Amaral, D. G., Price, J. L., Pitkänen, A., and Carmichael, S. T. (1992). Anatomical organization of the primate amygdaloid complex. In Aggleton, J. P. (ed.), The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, Wiley-Liss, New York, pp. 1-66.
3. Anagnostaras, S. G., Gale, G. D., and Fanselow, M. S. (2001). Hippocampus and contextual fear conditioning: Recent controversies and advances. Hippocampus 11:8-17.
4. Armony, J. L., Servan-Schreiber, D., Romanski, L. M., Cohen, J. D. and LeDoux, J. E. (1997). Stimulus generalization of fear responses: Effects of auditory cortex lesions in a computational model and in rats. Cereb. Cortex 7:157-165.
5. Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M., and Sweatt, J. D. (1998). The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1:602-609.
6. Baddley, A. (1998). Recent developments in working memory. Curr. Opin. Neurobiol. 8:234-238.
7. Bard, P. (1928). A diencephalic mechanism for the expression of rage with special reference to the sympathetic nervous system. Am. J. Physiol. 84:490-515.
8. Barnes, C. A. (1995). Involvement of LTP in memory: Are we "searching under the street light"? Neuron 15:751-754.
9. Bauer, E. P., Schafe, G. E., and LeDoux, J. E. (2002). NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J. Neurosci. 22:5239-5249.
10. Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., and Damasio, A. R. (1995). Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269:1115-1118.
11. Blair, H. T., Schafe, G. E., Bauer, E. P., Rodrigues, S. M., and LeDoux, J. E. (2001). Synaptic plasticity in the lateral amygdala: A cellular hypothesis of fear conditioning. Learn. Mem. 8:229-242.
12. Blanchard, R. J., Blanchard, D. C., and Fial, R. A. (1970). Hippocampal lesions in rats and their effect on activity, avoidance, and aggression. J. Comp. Physiol. Psychol. 71:92-102.
13. Bliss, T. V. P., and G. L. Collingridge. (1993). A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361:31-39.
14. Bliss, T. V., and T. Lomo. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond.) 232:331-356.
15. Bourtchouladze, R., Abel, T., Berman, N., Gordon, R., Lapidus, K., and Kandel, E. R. (1998). Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn. Mem. 5:365-374.
16. Bourtchouladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., and Silva, A. J. (1994). Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59-68.
17. Braver, T. S., Cohen, J. D., Jonides, J., Smith, E. E., and Noll, D. C. (1997). A parametric study of prefrontal cortex involvement in human working memory. Neuroimage 5(1):49-62.
18. Brodal, A. (1982). Neurological Anatomy, Oxford University Press, New York.
19. Buchel, C., Morris, J., Dolan, R. J., and Friston, K. J. (1998). Brain systems mediating aversive conditioning: An event-related fMRI study. Neuron 20:947-957.
20. Cahill, L., and McGaugh, J. L. (1998). Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 21:294-299.
21. Campeau, S., and Davis, M. (1995a). Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J. Neurosci. 15:2301-2311.
22. Campeau, S., and Davis, M. (1995b). Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J. Neurosci. 15:2312-2327.
23. Cannon, W. B. (1929). Bodily Changes in Pain, Hunger, Fear, and Rage, Appleton, New York.
24. Cannon, W. B., and Britton, S. W. (1925). Pseudoaffective medulliadrenal secretion. Am. J. Physiol. 72:283-294.
25. Canteras, N. S., and Swanson, L. W. (1992). Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: A PHAL anterograde tract-tracing study in the rat. J. Comp. Neurol. 324:180-194.
26. Carter, C. S., Braver, T. S., Barch, D. M., Botvinick, M. M., Noll, D., and Cohen, J. D. (1998). Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747-749.
27. Cavus, I., and Teyler, T. (1996). Two forms of long-term potentiation in area CA1 activate different signal transduction cascades. J. Neurophysiol. 76:3038-3047.
28. Chapman, P. F., and Bellavance, L. L. (1992). Induction of long-term potentiation in the basolateral amygdala does not depend on NMDA receptor activation. Synapse 11:310-318.
29. Chapman, P. F., Kairiss, E. W., Keenan, C. L., and Brown, T. H. (1990). Long-term synaptic potentiation in the amygdala. Synapse 6:271-278.
30. Clugnet, M. C., and LeDoux, J. E. (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. 10:2818-2824.
31. Collins, D. R., and Pare, D. (2000). Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS(+) and CS(-). Learn. Mem. 7:97-103.
32. Davidson, R. J., and Irwin, W. (1999). The functional neuroanatomy of emotion and affective style. Trends in Cog. Sci. 3:11-21.
33. Dudai, Y. (1989). Neurobiology of Memory, Oxford University Press, New York.
34. Eichenbaum, H. (1994). The hippocampal system and declarative memory in humans and animals: Experimental analysis and historical origins. In Schacter, D. L., and Tulving, E. (eds.), Memory Systems, MIT Press, Cambridge, MA, pp. 147-201.
35. Eichenbaum, H. (1995). The LTP-Memory connection. Nature 378:131-132.
36. Eichenbaum, H. (1997). To cortex: Thanks for the memories. Neuron 19:481-484.
37. Everitt, B. J., Parkinson, J. A., Olmstead, M. C., Arroyo, M., Robledo, P., and Robbins, T. W. (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, New York Academy of Sciences, New York, pp. 412-438.
38. Fendt, M. (2001). Injections of the NMDA receptor antagonist aminophosphonopentanoic acid into the lateral nucleus of the amygdala block the expression of fear-potentiated startle and freezing. J Neurosci. 21:4111-4115.
39. Frankland, P. W., Cestari, V., Filipkowski, R. K., and Silva, A. J. (1997). Hippocampal representation of context in fear conditioning. Soc. Neuro. Abstr. 23:1598.
40. Fuster, J. (1998). Linkage at the top. Neuron 21:1223-1229.
41. Gean, P.-W., Chang, F.-C., Huang, C.-C., Lin, J.-H. and Way, L.-J. (1993). Long-term enhancement of EPSP and NMDA receptor-mediated synaptic transmission in the amygdala. Brain Res. Bull. 31:7-11.
42. Gentile, C. G., Jarrell, T. W., Teich, A., McCabe, P. M., and Schneiderman, N. (1986). The role of amygdaloid central nucleus in the retention of differential Pavlovian conditioning of bradycardia in rabbits. Behav. Brain Res. 20:263-273.
43. Gewirtz, J. C., and Davis, M. (1997). Second-order fear conditioning prevented by blocking NMDA receptors in amygdala. Nature 388:471-474.
44. Goldman-Rakic, P. S. (1996). Regional and cellular fractionation of working memory. Proc. Natl. Acad. Sci. U.S.A. 93:13473-13480.
45. Helmstetter, F. J., and Bellgowan, P. S. (1994). Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats. Behav. Neurosci. 108:1005-1009.
46. Hitchcock, J., and 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.
47. Huang, Y. Y., and Kandel, E. R. (1998). Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21:169-78.
48. Huang, Y. Y., Nguyen, P. V., Abel, T., and Kandel, E. R. (1996). Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learn. Mem. 3:74-85.
49. Iwata, J., LeDoux, J. E., Meeley, M. P., Arneric, S., and Reis, D. J. (1986). Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli. Brain Res. 383:195-214.
50. Jarrell, T. W., Gentile, C. G., Romanski, L. M., McCabe, P. M., and Schneiderman, N. (1987). Involvement of cortical and thalamic auditory regions in retention of differential bradycardia conditioning to acoustic conditioned stimulii in rabbits. Brain Res. 412:285-294.
51. Johnson-Laird, P. N. (1993). A computational analysis of consciousness. In Marcel, A. J., and Bisiach, E. (eds.), Consciousness in Contemporary Science, Oxford University Press, Oxford, pp. 357-368.
52. Josselyn, S. A., Carlezon, W. A. J., R. Neve, S. C. J., Nestler, E. J., and Davis, M. (1998). Overexpression of CREB in the amygdala facilitates the formation of long-term memory measured with fear-potentiated startle in rats. Soc. Neurosci. Abstr. 24:926.
53. Kandel, E. R. (1997). Genes, synapses, and long-term memory. J. Cell. Physiol. 173:124-125.
54. Kandel, E. R. (1999). Biology and the future of psychoanalysis: A new intellectual framework for psychiatry revisited. Am. J. Psychiatry 156:505-524.
55. Kapp, B. S., Frysinger, R. C., Gallagher, M., and Haselton, J. R. (1979). Amygdala central nucleus lesions: Effect on heart rate conditioning in the rabbit. Physiol. Behav. 23:1109-1117.
56. Karplus, J. P., and Kreidl, A. (1927). Gehirn und Sympathicus. VII: Uber beziehungen der hypothalamuszentren zu blutdruck und innerer sekretion. Pfluegers Arch. Gesamte Physiol. Menschen Tiere 215:667-670.
57. Kihlstrom, J. F. (1987). The cognitive unconscious. Science 237:1445-1452.
58. Kim, J. J., and Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science 256:675-677.
59. Kluver, H. and Bucy, P. C. (1937). "Psychic blindness" and other symptoms following bilateral temporal lobectomy in rhesus monkeys. Am. J. Physiol. 119:352-353.
60. Kosslyn, S. M., and Koenig, O. (1992). Wet Mind: The New Cognitive Neuroscience. Macmillan, New York.
61. Kotter, R., and Meyer, N. (1992). The limbic system: A review of its empirical foundation. Behav. Brain. Res. 52:105-127.
62. LaBar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E., and Phelps, E. A. (1998). Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study. Neuron 20:937-945.
63. LaBar, K. S., LeDoux, J. E., Spencer, D. D., and Phelps, E. A. (1995). Impaired fear conditioning following unilateral temporal lobectomy in humans. J. Neurosci. 15:6846-6855.
64. LeDoux, J. E. (1987). Emotion. In Plum, F. (ed.), Handbook of Physiology. 1: The Nervous System, Vol V, Higher Functions of the Brain, American Physiological Society. Bethesda, pp. 419-460.
65. LeDoux, J. E. (1991). Emotion and the limbic system concept. Concepts Neurosci. 2:169-199.
66. LeDoux, J. E. (1996). The Emotional Brain, Simon and Schuster, New York.
67. LeDoux, J. E. (2000). Emotion circuits in the brain. Annu. Rev. Neurosci. 23:155-184.
68. LeDoux, J. E., Cicchetti, P., Xagoraris, A., and Romanski, L. M. (1990a). The lateral amygdaloid nucleus: Sensory interface of the amygdala in fear conditioning. J. Neurosci. 10:1062-1069.
69. LeDoux, J. E., Farb, C. F., and Ruggiero, D. A. (1990b). Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J. Neurosci. 10:1043-1054.
70. LeDoux, J. E., Iwata, J., Cicchetti, P. and Reis, D. J. (1988). Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J. Neurosci. 8:2517-2529.
71. Lee, H., and Kim, J. J. (1998). Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. J. Neurosci. 18:8444-8454.
72. Lynch, G. (1986). Synapses, Circuits, and the Beginnings of Memory, The MIT Press, Cambridge, Massachusetts.
73. MacLean, P. D. (1949). Psychosomatic disease and the "visceral brain": Recent developments bearing on the Papez theory of emotion. Psychosom. Med. 11:338-353.
74. MacLean, P. D. (1952). Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalogr. Clin. Neurophysiol 4:407-418.
75. Magee, J. C., and Johnston, D. (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275:209-213.
76. Majidishad, P., Pelli, D. G. and LeDoux, J. E. (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.
77. Malenka, R., and Nicoll, R. (1999). Neuroscience: Long-term potentiation - A decade of progress? Science 285:1870-1874.
78. Maren, S. (2000). Auditory fear conditioning increases CS-elicited spike firing in lateral amygdala neurons even after extensive overtraining. Eur. J. Neurosci. 12:4047-4054.
79. Maren, S. (2001). Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci. 24:897-931.
80. Maren, S., Aharonov, G., and Fanselow, M. S. (1997). Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav. Brain Res. 88:261-274.
81. Maren, S., and Fanselow, M. S. (1995). Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J. Neurosci. 15:7548-7564.
82. Maren, S., and Fanselow, M. S. (1996). The amygdala and fear conditioning: Has the nut been cracked? Neuron 16:237-240.
83. Maren, S., Poremba, A., and Gabriel, M. (1991). Basolateral amygdaloid multi-unit neuronal correlates of discriminative avoidance learning in rabbits. Brain Res. 549:311-316.
84. Martin, S. J., Grimwood, P. D., and Morris, R. G. M. (2000). Synaptic plasticity and memory: An evaluation of the hypothesis. Annu. Rev. Neurosci. 23:649-711.
85. Mascagni, F., McDonald, A. J., and Coleman, J. R. (1993). Corticoamygdaloid and corticocortical projections of the rat temporal cortex: A phaseolus vulgaris leucoagglutinin study. Neuroscience 57:697-715.
86. Mayford, M., Bach, M. E., Huang, Y. Y., Wang, L., Hawkins, R. D., and Kandel, E. R. (1996). Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683.
87. McDonald, A. J. (1998). Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 55:257-332.
88. McDonald, R. J., and White, N. M. (1993). A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behav. Neurosci. 107:3-22.
89. Miserendino, M. J., Sananes, C. B., Melia, K. R., and Davis, M. (1990). Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 345:716-718.
90. Morris, R. G. (1998). Synaptic plasticity. Down with novelty [News]. Nature 394:834-835.
91. Morris, J. S., Ohman, A., and Dolan, R. J. (1998). Conscious and unconscious emotional learning in the human amygdala. Nature 393:467-470.
92. Morris, J. S., Ohman, A., and Dolan, R. J. (1999). A subcortical pathway to the right amygdala mediating "unseen" fear. Proc. Natl. Acad. Sci. U.S.A. 96:1680-1685.
93. Muller, J., Corodimas, K. P., Fridel, Z., and LeDoux, J. E. (1997). Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behav Neurosci. 111:683-691.
94. Nicoll, R. A., and Malenka, R. C. (1995). Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377:115-118.
95. Packard, M. G., Cahill, L., and McGaugh, J. L. (1994). Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc. Natl. Acad. Sci. U.S.A. 91:8477-8481.
96. Pascoe, J. P., and Kapp, B. S. (1985). Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit. Behav. Brain Res. 16:117-133.
97. Phelps, E. A., and Anderson, A. K. (1997). Emotional memory: What does the amygdala do? Curr. Biol. 7:R311-R314.
98. Phillips, R. G., and LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106:274-285.
99. Pitkänen, A., Savander, V., and LeDoux, J. E. (1997). Organization of intra-amygdaloid circuitries in the rat: An emerging framework for understanding functions of the amygdala. Trends Neurosci. 20:517-523.
100. Quirk, G. J., Armony, J. L., and LeDoux, J. E. (1997). Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19:613-624.
101. Quirk, G. J., Repa, C., and LeDoux, J. E. (1995). Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: Parallel recordings in the freely behaving rat. Neuron 15:1029-1039.
102. Repa, J. C., Muller, J., Apergis, J., Desrochers, T. M., Zhou, Y., and LeDoux, J. E. (2001). Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat. Neurosci. 4:724-731.
103. Rodrigues, S. M., Bauer, E. P., Farb, C. R., Schafe, G. E., and LeDoux, J. E. (2002). The group I metabotropic glutamate receptor mGluR5 is required for fear memory formation and long-term potentiation in the lateral amygdala. J. Neurosci. 22:5219-5229.
104. Rogan, M. T., and LeDoux, J. E. (1995). LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit. Neuron 15:127-136.
105. Rogan, M. T., Staubli, U. V., and LeDoux, J. E. (1997). Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390:604-607.
106. Rolls, ET (1999). The Brain and Emotion, Oxford University Press, Oxford.
107. Romanski, L. M. and LeDoux, J. E. (1992). Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning. J. Neurosci. 12:4501-4509.
108. Romanski, L. M., and LeDoux, J. E. (1993). Information cascade from primary auditory cortex to the amygdala: Corticocortical and corticoamygdaloid projections of temporal cortex in the rat. Cereb. Cortex 3:515-532.
109. Romanski, L. M., LeDoux, J. E., Clugnet, M. C., and Bordi, F. (1993). Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav. Neurosci. 107:444-450.
110. Royer, S., Martina, M., and Pare, D. (1999). An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J. Neurosci. 19:10575-10583.
111. Schafe, G. E., Fitts, D. A., Thiele, T. E., LeDoux, J. E., and Bernstein, I. L. (2000). The induction of c-fos in the NTS after taste aversion learning is not correlated with measures of conditioned fear. Behav. Neurosci. 114:99-106.
112. Schafe, G. E., Nadel, N. V., Sullivan, G. M., Harris, A., and LeDoux, J. E. (1999). Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn. Mem. 6:97-110.
113. Schafe, G. E., Nader, K., Blair, H. T., and LeDoux, J. E. (2001). Memory consolidation of Pavlovian fear conditioning: A cellular and molecular perspective. Trends Neurosci. 24:540-546.
114. Shaywitz, A. J., and Greenberg, M. E. (1999). CREB: A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68:821-861.
115. Shi, C., and Davis, M. (1999). Pain pathways involved in fear conditioning measured with fear-potentiated startle: Lesion studies. J. Neurosci. 19:420-430.
116. Silva, A. J., Kogan, J. H., Frankland, P. W., and Kida, S. (1998). CREB and memory. Annu Rev. Neurosci. 21:127-148.
117. Squire, L. R., Knowlton, B., and Musen, G. (1993). The structure and organization of memory. Annu. Rev. Psychol. 44:453-495.
118. Stevens, C. F. (1998). A million dollar question: Does LTP = memory? Neuron 20:1-2.
119. Swanson, L. W. (1983). The hippocampus and the concept of the limbic system. In Seifert, W. (ed.), Neurobiology of the Hippocampus, Academic Press, London, pp. 3-19.
120. Sweatt, J. D. (2001). The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 76:1-10.
121. Tang, Y. P., Shimizu, E., Dube, G. R., Rampon, C., Kerchner, G. A., Zhuo, M., Liu, G., and Tsien, J. Z. (1999). Genetic enhancement of learning and memory in mice. Nature 401:63-69.
122. Turner, B., and Herkenham, M. (1991). Thalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing. J. Comp. Neurol. 313:295-325.
123. Turner, B. H., Mishkin, M., and Knapp, M. (1980). Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J. Comp. Neurol. 191:515-543.
124. Uwano, T., Nishijo, H., Ono, T., and Tamura, R. (1995). Neuronal responsiveness to various sensory stimuli, and associative learning in the rat amygdala. Neuroscience 68:339-361.
125. Van de Kar, L. D., Piechowski, R. A., Rittenhouse, P. A., and Gray, T. S. (1991). Amygdaloid lesions: Differential effect on conditioned stress and immobilization-induced increases in corticosterone and renin secretion. Neuroendocrinology 54:89-95.
126. Vazdarjanova, A., and McGaugh, J. L. (1998). Basolateral amygdala is not critical for cognitive memory of contextual fear conditioning. Proc. Natl. Acad. Sci. U.S.A. 95:15003-15007.
127. Weinberger, N. M. (1995). Retuning the brain by fear conditioning. In Gazzaniga, M. S. (ed.), The Cognitive Neurosciences, The MIT Press, Cambridge, MA, pp. 1071-1090.
128. Weinberger, N. M. (1998). Physiological memory in primary auditory cortex: Characteristics and mechanisms. Neurobiol. Learn. Mem. 70:226-251.
129. Weisskopf, M. G., Bauer, E. P., and LeDoux, J. E. (1999). L-type voltage-gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala. J. Neurosci. 19:10512-10519.
130. Wilensky, A. E., Schafe, G. E., and LeDoux, J. E. (1999). Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. J. Neurosci. 19:RC48.
131. Yin, J. C., Wallach, J. S., Del Vecchio, M., Wilder, E. L., Zhou, H., Quinn, W. G. and Tully, T. (1994). Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79:49-58.