The neuroscience of mammalian associative learning

Annual Review of Psychology

Volumn 56, Issue , 2005, Pages 207-234

  Fanselow, Michael S ^a   Poulos, Andrew M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Amygdala; Cerebellum; Eyeblink; Fear; Hippocampus; Pavlovian conditioning

Indexed keywords

ANIMAL; BLINKING; BRAIN; CEREBELLUM; CONDITIONED REFLEX; FEAR; HUMAN; LEARNING; METHODOLOGY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROSCIENCE; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX;

ANIMALS; ASSOCIATION LEARNING; BLINKING; BRAIN; CEREBELLUM; CONDITIONING, CLASSICAL; FEAR; HUMANS; NERVE NET; NEURONAL PLASTICITY; NEUROSCIENCES; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX;

EID: 14544267665     PISSN: 00664308     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.psych.56.091103.070213     Document Type: Review

References (182)

1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, et al. 1994. Deficient cerebellar longterm depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-88
2. Aizenman CD, Linden DJ. 2000. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat. Neurosci. 3:109-11
3. Albus JS. 1971. A theory of cerebellar function. Math. Biosci. 10:25-61
4. Allen MT, Steinmetz JE. 1996. A nitric oxide synthase inhibitor delays the formation of learning-related neural activity in the cerebellar interpositus nucleus during rabbit eyelid conditioning. Pharmacol. Biochem. Behav. 53:147-53
5. Amaral DG, Price JL, Pitkanen A, Carmichael ST. 1992. Anatomical organization of the primate amygdaloid complex. In The Amygdala: Neurological Aspects of Emotion, Memory and Mental Dysfunction, ed. JP Aggleton, pp. 1-66. New York: Wiley-Liss
6. Amorapanth P, LeDoux JE, Nader K. 2000. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat. Neurosci. 3(1):74-79
7. Anagnostaras SG, Maren S, Fanselow MS. 1999. Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J. Neurosci. 19:1106-14
8. Antonov I, Antonova I, Kandel ER, Hawkins RD. 2003. Activity-dependent presynaptic facilitation and Hebbian LTP are both required and interact during classical conditioning in aplysia. Neuron 37(1):135-47
9. Attwell PJ, Rahman S, Ivarsson M, Yeo CH. 1999. Cerebellar cortical AMPA-kainate receptor blockade prevents performance of classically conditioned nictitating membrane responses. J. Neurosci. 19:RC45
10. Attwell PJ, Rahman S, Yeo CH. 2001. Acquisition of eyeblink conditioning is critically dependent on normal function in cerebellar cortical lobule HVI. J. Neurosci. 21:5715-22
11. Bailey DJ, Kim JJ, Sun W, Thompson RF, Helmstetter FJ. 1999. Acquisition of fear conditioning in rats requires the synthesis of mRNA in the amygdala. Behav. Neurosci. 113(2):276-78
12. Bao S, Chen L, Kim JJ, Thompson RF. 2002. Cerebellar cortical inhibition and classical eyeblink conditioning. Proc. Natl. Acad. Sci. USA 99:1592-97
13. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR. 1995. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269:1115-18
14. Benarroch EE. 2001. Pain-autonomic interactions: a selective review. Clin. Auton. Res. 11(6):343-49
15. Berry SD, Thompson RF. 1979. Medial septal lesions retard classical conditioning of the nicitating membrane response in rabbits. Science 205:209-11
16. Berthier NE, Moore JW. 1986. Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response. Exp. Brain Res. 63:341-50
17. Berthier NE, Moore JW. 1990. Activity of deep Cerebellar nuclear cells during classical conditioning of nictitating membrane extension in rabbits. Exp. Brain Res. 83:44-54
18. Beylin AV, Gandhi CC, Wood GE, Talk AC, Matzel LD, Shors TJ. 2001. The role of the hippocampus in trace conditioning: temporal discontinuity or task difficulty? Neurobiol. Learn. Mem. 76:447-61
19. Bi G, Poo M. 2001. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu. Rev. Neurosci. 24:139-66
20. Blaxton TA, Zeffiro TA, Gabrieli JD, Bookheimer SY, Carrillo MC, et al. 1996. Functional mapping of human learning: a positron emission tomography activation study of eyeblink conditioning. J. Neurosci. 16:4032-34
21. Bliss TV, Gardner-Medwin AR. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232(2):357-74
22. Bliss TV, Lomo T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232:331-56
23. Boehning D, Snyder SH. 2003. Novel neural modulators. Annu. Rev. Neurosci. 26:105-31
24. Bracha V, Irwin KB, Webster ML, Wunderlich DA, Stachowiak MK, Bloedel JR. 1998. Microinjections of anisomycin into the intermediate cerebellum during learning affects the acquisition of classically conditioned responses in the rabbit. Brain Res. 788:169-78
25. Brunzell DH, Kim JJ. 2001. Fear conditioning to tone, but not to context, is attenuated by lesions of the insular cortex and posterior extension of the intralaminar complex in rats. Behav. Neurosci. 115(2):365-75
26. Bucci DJ, Phillips RG, Burwell RD. 2000. Contributions of postrhinal and perirhinal cortex to contextual information processing. Behav. Neurosci. 114(5):882-94
27. Burstein R, Potrebic SJ. 1993. Retrograde labeling of neurons in the spinal cord that project directly to the amygdala or the orbital cortex in the rat. Comp. Neural. 335(4):469-85
28. Burwell RD, Saddoris MP, Bucci DJ, Wiig KA. 2004. Corticohippocampal contributions to spatial and contextual learning. J. Neurosci. 24(15):3826-36
29. Canli T, Brown TH. 1996. Amygdala stimulation enhances the rat eyeblink reflex through a short-latency mechanism. Behav. Neurosci. 110(1):51-59
30. Chapman PF, Kairiss EW, Keenan CL, Brown TH. 1990. Long-term synaptic potentiation in the amygdala. Synapse 6(3):271-78
31. Chen C, Thompson RF. 1995. Temporal specificity of long-term depression in parallel fiber-Purkinje synapses in rat cerebellar slice. Learn. Mem. 2:185-98
32. Chen G, Steinmetz JE. 2000a. Intra-cerebellar infusion of NMDA receptor antagonist AP5 disrupts classical eyeblink conditioning in rabbits. Brain Res. 887:144-56
33. Chen G, Steinmetz JE. 2000b. Microinfusion of protein kinase inhibitor H7 into the cerebellum impairs the acquisition but not the retention of classical eyeblink conditioning in rabbits. Brain Res. 856:193-201
34. Cheng DT, Knight DC, Smith CN, Stein EA, Helmstetter FJ. 2003. Functional MRI of human amygdala activity during Pavlovian fear conditioning: stimulus processing versus response expression. Behav. Neurosci. 117:3-10
35. Christian KM, Thompson RF. 2003. Neural substrates of eyeblink conditioning: acquisition and retention. Learn. Mem. 10:427-55
36. Clark RE, Lavond DO. 1993. Reversible lesions of the red nucleus during acquisition and retention of a classically conditioned behavior in rabbits. Behav. Neurosci. 107:264-70
37. Clark RE, Squire LR. 1998. Classical conditioning and brain systems: the role of awareness. Science 280:77-81
38. Clark RE, Zhang AA, Lavond DG. 1992. Reversible lesions of the cerebellar interpositus nucleus during acquisition and retention of a classically conditioning behavior. Behav. Neurosci. 106:879-88
39. 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(8):2818-24
40. Collingridge GL, Kehl SJ, McLennan H. 1983. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol. 334:33-46
41. Daum I, Schugens MM, Ackermann H, Lutzenberger W, Dichgans J, Birbaumer N. 1993. Classical conditioning after cerebellar lesions in humans. Behav. Neurosci. 107:748-56
42. Dayan P, Balleine BW. 2002. Reward, motivation, and reinforcement learning. Neuron 36(2):285-98
43. DeOlmos JS, Alheid GF, Beltramino CA. 1985. Amygdala. In The Rat Nervous System, ed. G Paxinos, pp 223-334. Orlando, FL: Academic
44. Edeline JM, Pham P, Weinberger MM. 1993. Rapid development of learning-induced receptive field plasticity in the auditory cortex. Behav. Neurosci. 107(4):539-51
45. Edeline JM, Weinberger NM. 1992. Associative retuning in the thalamic source of input to the amygdala and auditory cortex: receptive field plasticity in the medial division of the medial geniculate body. Behav. Neurosci. 106(1):81-105
46. Fanselow MS. 1980. Conditional and unconditional components of post-shock freezing in rats. Pavlov. J. Biol. Sci. 15:177-82
47. Fanselow MS. 1991. The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety. In The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Immunohistochemical Organization, ed. A Depaulis, R Bandler, pp 151-73. New York: Plenum
48. Fanselow MS. 1998. Pavlovian conditioning, negative feedback, and blocking: mechanisms that regulate association formation. Neuron 20:625-27
49. Fanselow MS, Gale GD. 2003. The amygdala, fear and memory. Ann. NY Acad. Sci. 985:125-34
50. Fanselow MS, Kim JJ. 1994. Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist D,L-2-amino-5-phosphonovaleric acid to the basolateral amygdala. Behav. Neurosci. 108:210-12
51. Feldman S, Weidenfeld J. 1998. The excitatory effects of the amygdala on hypothalamopituitary-adrenocortical responses are mediated by hypothalamic norepinephrine, serotonin, and CRF-41. Brain Res. Bull. 45(4):389-93
52. Freeman JH Jr., Scharenberg AM, Olds JL, Schreurs BG. 1998. Classical conditioning increases membrane-bound protein kinase C in rabbit cerebellum. Neuroreport9:2669-73
53. French SJ, Totterdell S. 2003. Individual nucleus accumbens-projection neurons receive both basolateral amygdala and ventral subicular afferents in rats. Neuroscience 119(1):19-31
54. Gale GD, Anagnostaras SG, Godsil BP, Mitchell S, Nozawa T, et al. 2004. Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J. Neurosci. 24:3810-15
55. Garcia KS, Mauk MD. 1998. Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology 37:471-80
56. Garcia KS, Steele PM, Mauk MD. 1999. Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. J. Neurosci. 19:10940-47
57. Gauriau C, Bernard JF. 2002. Pain pathways and parabrachial circuits in the rat. Exp. Physiol. 87(2):251-58
58. Gomi H, Sun W, Finch CE, Itohara S, Yoshimi K, Thompson RF. 1999. Learning induces a CDC2-related protein kinase, KKIAMRE. J. Neurosci. 19: 9530-37
59. Goosens KA, Holt W, Maren S. 2000. A role for amygdaloid PKA and PKC in the acquisition of long-term conditional fear memories in rats. Behav. Brain Res. 114(1-2):145-52
60. Goossens J, Daniel H, Rancillac A, van der Steen J, Oberdick J, et al. 2001. Expression of protein kinase C inhibitor blocks cerebellar long-term depression without affecting Purkinje cell excitability in alert mice. J. Neurosci. 21:5813-23
61. Gould TJ, Steinmetz JE. 1994. Multiple-unit activity from rabbit cerebellar cortex and interpositus nucleus during classical discrimination/reversal eyelid conditioning. Brain Res. 652:98-106
62. Han CJ, O'Tuathaigh CM, van Trigt L, Quinn JJ, Fanselow MS, et al. 2003. Trace but not delay fear conditioning requires attention and the anterior cingulate cortex. Proc. Natl. Acad. Sci. USA 100:13087-92
63. Hansel C, Linden DJ, D'Angelo E. 2001. Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat. Neurosci. 4:467-75
64. Hauge SA, Tracy JA, Baudry M, Thompson RF. 1998. Selective changes in AMPA receptors in rabbit cerebellum following classical conditioning of the eyelid-nictitating membrane response. Brain Res. 803:9-18
65. Huang YY, Kandel ER. 1998. Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21(1): 169-78
66. Huff NC, Rudy JW. 2004. The amygdala modulates hippocampus-dependent context memory formation and stores cue-shock associations. Behav. Neurosci. 118(1):53-62
67. Hunt PS. 1999. A further investigation of the developmental emergence of fear-potentiated startle in rats. Dev. Psychobiol. 34(4):281-91
68. Hunt PS, Campbell BA. 1997. Developmental dissociation of the components of conditioned fear. In Learning, Motivation, and Cognition: The Functional Behaviorism of Robert C. Bolles, ed. ME Bouton, MS Fanselow, pp. 53-74. Washington, DC: Am. Psychol. Assoc.
69. Impey S, Smith DM, Obrietan K, Donahue R, Wade C, Storm DR. 1998. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat. Neurosci. 1(7):595-601
70. Isaac JT, Nicoll RA, Malenka RC. 1995. Evidence for silent synapses: implications for the expression of LTP. Neuron 15(2):427-34
71. Ito M. 2002. The molecular organization of cerebellar long-term depression. Nat. Neurosci. Rev. 3:896-902
72. Ito M, Kano M. 1982. Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neurosci. Lett. 33:253-58
73. Ivkovich D, Lockard JM, Thompson RF. 1993. Interpositus lesion abolition of the eyeblink conditioned response is not due to effects on performance. Behav. Neurosci. 107:530-32
74. Jasmin L, Granato A, Ohara PT. 2004. Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J. Comp. Neurol. 468(3):425-40
75. Jolkkonen E, Miettinen R, Pikkarainen M, Pitkanen A. 2002. Projections from the amygdaloid complex to the magnocellular cholinergic basal forebrain in rat. Neuroscience 111(1):133-49
76. Josselyn SA, Shi C, Carlezon WA Jr., Neve RL, Nestler EJ, Davis M. 2001. Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J. Neurosci. 21(7):2404-12
77. Kapp BS, Frysinger RC, Gallagher M, Haselton JR. 1979. Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol. Behav. 23:1109-17
78. Kida S, Josselyn SA, de Ortiz SP, Kogan JH, Chevere I, et al. 2002. CREB required for the stability of new and reactivated fear memories. Nat. Neurosci. 5(4):348-55
79. Killcross S, Robbins TW, Everitt BJ. 1997. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 388(6640):377-80
80. Kim JJ, Clark RE, Thompson RF. 1995. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav. Neurosci. 109:195-203
81. Kim JJ, Fanselow MS. 1992. Modality specific retrograde amnesia of fear following hippocampal lesions. Science 256:675-77
82. King DA, Krupa DJ, Foy MR, Thompson RF. 2001. Mechanisms of neuronal conditioning. Int. Rev. Neurobiol. 45:313-37
83. Kleim JA, Freeman JH Jr., Bruneau R, Nolan BC, Cooper NR, et al. 2002. Synapse formation is associated with memory storage in the cerebellum. Proc. Natl. Acad. Sci. USA 99:13228-31
84. Knight DC, Cheng DT, Smith CN, Stein EA, Helmstetter FJ. 2004. Neural substrates mediating human delay and trace fear conditioning. J. Neurosci. 24:218-28
85. Koekkoek SK, Hulscher HC, Dortland BR, Hensbroek RA, Elgersma Y, et al. 2003. Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science 301:1736-39
86. Krupa DJ, Thompson JK, Thompson RF. 1993. Localization of a memory trace in the mammalian brain. Science 260:989-91
87. Krupa DJ, Thompson RF. 1995. Inactivation of the superior cerebellar peduncle blocks expression but not acquisition of the rabbit's classically conditioned eye-blink response. Proc. Natl. Acad. Sci. USA 92:5097-101
88. Krupa DJ, Thompson RF. 1997. Reversible inactivation of the cerebellar interpositus nucleus completely prevents acquisition of the classically conditioned eye-blink response. Learn. Mem. 3:545-56
89. 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. Neuron 20:937-45
90. Lanuza E, Nader K, LeDoux JE. 2004. Unconditioned stimulus pathways to the amygdala: effects of posterior thalamic and cortical lesions on fear conditioning. Neuroscience 125(2):305-15
91. Lavond DG, Hembree TL, Thompson RF. 1985. Effect of kainic acid lesions of the cerebellar interpositus nucleus on eyelid conditioning in the rabbit. Brain Res. 326:179-82
92. Lavond DG, Kim JJ, Thompson RF. 1993. Mammalian brain substrates of aversive classical conditioning. Annu. Rev. Psychol. 44:317-42
93. Lavond DG, Lincoln JS, McCormick DA, Thompson RF. 1984. Effect of bilateral lesions of the dentate and interpositus cerebellar nuclei on conditioning of heart-rate and nictitating membrane/eyelid responses in the rabbit. Brain Res. 305:323-30
94. Lavond DG, Steinmetz JE. 1989. Acquisition of classical conditioning without cerebellar cortex. Behav. Brain Res. 33:113-64
95. LeDoux JE, Farb CR, Romanski LM. 1991. Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex. Neurosci. Lett. 134(1):139-44
96. LeDoux JE, Iwata J, Cicchetti P, Reis DJ. 1988. Different projections of the central amygdaloid nucleus mediate autonomic and be havioral correlates of conditioned fear. J. Neurosci. 8(7):2517-29
97. Lee T, Kim JJ. 2004. Differential effects of cerebellar, amygdalar, and hippocampal lesions on classical eyeblink conditioning in rats. J. Neurosci. 24:3242-50
98. Lemieux SK, Woodruff-Pak DR 2000. Functional MRI studies of eyeblink classical conditioning. See Woodruff-Pak & Steinmetz 2000, Vol. 1, pp. 71-93
99. Liao D, Hessler NA, Malinow R. 1995. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375(6530):400-4
100. Lindquist DH, Jarrard LE, Brown TH. 2004. Perirhinal cortex supports delay fear conditioning to rat ultrasonic social signals. J. Neurosci. 24(14):3610-17
101. Lisman J. 2003. Long-term potentiation: outstanding questions and attempted synthesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358(1432):829-42
102. Logan CG, Grafton ST. 1995. Functional anatomy of human eyeblink conditioning determined with regional cerebral glucose metabolism and positron-emission tomography. Proc. Natl. Acad. Sci. USA 92:7500-4
103. Logan CG, Lavond DG, Wong JT, Thompson RF. 1994. Acquisition of classically conditioned eyeblink response following bilateral lesions of flocculus and paraflocculus. Behav. Neural. Biol. 61:102-6
104. Lye RH, O'Boyle DJ, Ramsden RT, Schady W. 1988. Effects of unilateral cerebellar lesions on the acquisition of eye-blink conditioning in man. J. Physiol. 403:58P
105. Lynch MA. 2004. Long-term potentiation and memory. Physiol. Rev. 84(1):87-136
106. Malinow R, Malenka RC. 2002. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25:103-26
107. Malinow R, Miller JP. 1986. Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation. Nature 320(6062):529-30
108. Maren S, Fanselow MS. 1995. Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J. Neurosci. 15:7548-64
109. Maren S, Yap SA, Goosens KA. 2001. The amygdala is essential for the development of neuronal plasticity in the medial geniculate nucleus during auditory fear conditioning in rats. J. Neurosci. 21(6):RC135
110. Marr D. 1969. A theory of cerebellar cortex. J. Physiol. 202:437-70
111. Martinez JL Jr., Derrick BE. 1996. Long-term potentiation and learning. Annu. Rev. Psychol. 47:173-203
112. Mauk MD, Steinmetz JE, Thompson RF. 1986. Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc. Natl. Acad. Sci. USA 83:5349-53
113. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER. 1996. Control of memory formation through regulated expression of a CaMKII transgene. Science 274(5293):1678-83
114. McCormick DA, Lavond DG, Clark GA, Kettner RE, Thompson RF. 1981. The engram found? Role of the cerebellum in classical conditioning of the nictitating membrane and eyelid responses. Bull. Psychon. Soc. 28:769-75
115. McCormick DA, Lavond DG, Thompson RF. 1983. Neuronal responses of the rabbit brainstem during performance of the classically conditioned nictitating membrane (NM)/eyelid response. Brain Res. 271:73-88
116. McCormick DA, Steinmetz JE, Thompson RF. 1985. Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Res. 359:120-30
117. McGlinchey-Berroth R. 2000. Eyeblink classical conditioning in amnesia. See Woodruff-Pak & Steinmetz 2000, Vol. 1, pp. 205-27
118. McGlinchey-Berroth R, Carrillo MC, Gabrieli JD, Brawn CM, Disterhoft JF. 1997. Impaired trace eyeblink conditioning in bilateral, medial-temporal lobe amnesia. Behav. Neurosci. 111:873-82
119. McIntosh AR, Schreurs BG. 2000. Functional networks underlying human eyeblink con ditioning. See Woodruff-Pak & Steinmetz 2000, Vol. 1, pp. 51-77
120. McKernan MG, Shinnick-Gallagher P. 1997. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390(6660):607-11
121. Medina JF, Garcia KS, Mauk MD. 2001. A mechanism for savings in the cerebellum. J. Neurosci. 21:4081-89
122. Miserendino MJ, Sananes CB, Melia KR, Davis M. 1990. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 345(6277):716-18
123. Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT. 2003. Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37(3):485-97
124. Molchan SE, Sunderland T, McIntosh AR, Herscovitch P, Schreurs BG. 1994. A functional anatomical study of associative learning in humans. Proc. Natl. Acad. Sci. USA 91:8122-26
125. Muller D, Nikonenko I, Jourdain P, Alberi S. 2002. LTP, memory and structural plasticity. Curr. Mol. Med. 2(7):605-11
126. Murthy VN, De Camilli 2003. Cell biology of the presynaptic terminal. Annu. Rev. Neurosci. 26:701-28
127. Perrett SP, Ruiz BP, Mauk MD. 1993. Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J. Neurosci. 13:1708-18
128. Pickard L, Noel J, Duckworth JK, Fitzjohn SM, Henley JM, et al. 2001. Transient synaptic activation of NMDA receptors leads to the insertion of native AMPA receptors at hippocampal neuronal plasma membranes. Neuropharmacology 41(6):700-13
129. Pittenger C, Kandel ER. 2003. In search of general mechanisms for long-lasting plasticity: aplysia and the hippocampus. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358(1432):757-63
130. Poremba A, Gabriel M. 2001. Amygdalar efferents initiate auditory thalamic discriminative training-induced neuronal activity. J. Neurosci. 21(1):270-78
131. Poulos AM, Robleto K, Thompson RF. 2002. Effects of sensory stimulation and learning on excitability of the interpositus nucleus. Abstr. Soc. Neurosci. 28:79.10
132. Poulos AM, Thompson RF. 2004. Timing of conditioned responses utilizing electrical stimulation in the region of the interpositus nucleus as a CS. Integ. Physiol. Behav. Sci. In press
133. Quinn JJ, Oommen SS, Morrison GE, Fanselow MS. 2002. Post-training excitotoxic lesions of the dorsal hippocampus attenuate forward trace, backward trace, and delay fear conditioning in a temporally specific manner. Hippocampus 12:495-504
134. Quirk GJ, Armony JL, LeDoux JE. 1997. Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19(3):613-24
135. Racine RJ, Wilson DA, Gingell R, Sunderland D. 1986. Long-term potentiation in the interpositus and vestibular nuclei in the rat. Exp. Brain Res. 63:158-62
136. Rescorla RA. 1974. Effect of inflation of the unconditioned stimulus value following conditioning. J Comp. Physiol. Psychol. 86:101-6
137. Richardson R, Fan M. 2002. Behavioral expression of learned fear in rats is appropriate to their age at training, not their age at testing. Anim. Learn. Behav. 30(4):394-404
138. Roberts AC, Glanzman DL. 2003. Learning in aplysia: looking at synaptic plasticity from both sides. Trends Neurosci. 26(12):662-70
139. Rodrigues SM, Farb CR, Bauer EP, LeDoux JE, Schafe GE. 2004. Pavlovian fear conditioning regulates Thr286 autophosphorylation of Ca2+/calmodulin-dependent protein kinase II at lateral amygdala synapses. J. Neurosci. 24(13):3281-88
140. Rogan MT, Staubli UV, LeDoux JE. 1997. Fear conditioning induces associative longterm potentiation in the amygdala. Nature 390(6660):604-7
141. Rogers RF, Britton GB, Steinmetz JE. 2001. Learning-related interpositus activity is conserved across species as studied during eye blink conditioning in the rat. Brain Res. 905:171-77
142. Romanski LM, Clugnet MC, Bordi F, LeDoux JE. 1993. Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav. Neurosci. 107(3):444-50
143. Romanski LM, LeDoux JE. 1992. Equipotentiality of thalamo-amygdala and thalamocortico-amygdala circuits in auditory fear conditioning. J. Neurosci. 12(11):4501-9
144. Rosen JB, Davis M. 1990. Enhancement of electrically elicited startle by amygdaloid stimulation. Physiol. Behav. 48(2):343-49
145. Rosen JB, Fanselow MS, Young SL, Sitcoske M, Maren S. 1998. Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning. Brain Res. 196:132-42
146. Rosen JB, Hitchcock JM, Sananes CB, Miserendino MJ, Davis M. 1991. A direct projection from the central nucleus of the amygdala to the acoustic startle pathway: anterograde and retrograde tracing studies. Behav. Neurosci. 105(6):817-25
147. Salvatierra AT, Berry SD. 1989. Scopolamine disruption of septo-hippocampal activity and classical conditioning. Behav. Neurosci. 103:715-21
148. Schafe GE, LeDoux JE. 2000. Memory consolidation of auditory Pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J. Neurosci. 20(18):RC96
149. Schreurs BG, McIntosh AR, Bahro M, Herscovitch P, Sunderland T, Molchan SE. 1997. Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. J. Neurophysiol. 77:2153-63
150. Schultz W, Montgomery EB Jr., Marini R. 1979. Proximal limb movements in response to microstimulation of primate dentate and interpositus nuclei mediated by brain-stem structures. Brain 102:127-46
151. Seidenbecher T, Laxmi TR, Stork O, Pape HC. 2003. Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301(5634):846-50
152. Shi C, Davis M. 1999. Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J. Neurosci. 19(1):420-30
153. Shibuki K, Gomi H, Chen L, Bao S, Kim JJ, et al. 1996. Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron 16:587-99
154. Shibuki K, Okada D. 1991. Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349:326-28
155. Shimizu E, Tang YP, Rampon C, Tsien JZ. 2000. NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Science 290(5494):1170-74
156. Shinkman PG, Swain RA, Thompson RF. 1996. Classical conditioning with electrical stimulation of cerebellum as both conditioned and unconditioned stimulus. Behav. Neurosci. 110:914-21
157. Silva AJ. 2003. Molecular and cellular cognitive studies of the role of synaptic plasticity in memory. J. Neurobiol. 54(1):224-37
158. Solomon PR, Gottfried KE. 1981. The septohippocampal cholinergic system and classical conditioning of the rabbit's nictitating membrane response. J. Comp. Physiol. Psychol. 95:322-30
159. Solomon PR, Pomerleau D, Bennett L, James J, Morse DL. 1989. Acquisition of the classically conditioned eyeblink response in humans over the life span. Psychol. Aging 4:34-41
160. Solomon PR, Solomon SD, Schaaf EV, Perry HE. 1983. Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science 220:329-31
161. Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ. 1986. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav. Neurosci. 100:729-44
162. Steinmetz JE, Lavond DG, Ivkovich D, Logan CG, Thompson RF. 1992. Disruption of clas sical eyelid conditioning after cerebellar lesions: damage to a memory trace system or a simple performance deficit? J. Neurosci. 12:4403-26
163. Steinmetz JE, Logan CG, Rosen DJ, Thompson JK, Lavond DG, Thompson RF. 1987. Initial localization of the acoustic conditioned stimulus projection system to the cerebellum essential for classical eyelid conditioning. Proc. Natl. Acad. Sci. USA 84:3531-35
164. Steinmetz JE, Rosen DJ, Chapman PF, Lavond DG, Thompson RF. 1986. Classical conditioning of the rabbit eyelid response with a mossy-fiber stimulation CS: I. Pontine nuclei and middle cerebellar peduncle stimulation. Behav. Neurosci. 100:878-87
165. Stole DL, Fanselow MS. 2004. NMDA receptor modulation of incidental learning in Pavlovian context conditioning. Behav. Neurosci. 118:253-57
166. Swanson LW, Petrovich GD. 1998. What is the amygdala? Trends Neurosci. 21(8):323-31
167. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, et al. 1999. Genetic enhancement of learning and memory in mice. Nature 401(6748):63-69
168. Thompson RF, Krupa DJ. 1994. Organization of memory traces in the mammalian brain. Annu. Rev. Neurosci. 17:519-49
169. Topka H, Valls-Sole J, Massaquoi SG, Hallett M. 1993. Deficit in classical conditioning in patients with cerebellar degenerations. Brain 116:961-69
170. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, et al. 2002. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420(6917): 788-94
171. Tracy JA, Britton GB, Steinmetz JE. 2001. Comparison of single unit responses to tone, light, and compound conditioned stimuli during rabbit classical eyeblink conditioning. Neurobiol. Learn. Mem. 76:253-67
172. Tracy JA, Thompson JK, Krupa DJ, Thompson RF. 1998. Evidence of plasticity in the pontocerebellar conditioned stimulus pathway during classical conditioning of the eyeblink response in the rabbit. Behav. Neurosci. 112:267-85
173. Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY. 2002. Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 34(2):289-300
174. Tully T. 1997. Regulation of gene expression and its role in long-term memory and synaptic plasticity. Proc. Natl. Acad. Sci. USA 94(9):4239-41
175. Walker DL, Toufexis DJ, Davis M. 2003. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur. J. Pharmacol. 463(1-3):199-216
176. Wang YT, Linden DJ. 2000. Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25:635-47
177. Wei F, Qiu CS, Liauw J, Robinson DA, Ho N, et al. 2002. Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nat. Neurosci. 5(6):573-79
178. Woodruff-Pak DS, Steinmetz JE, eds. 2000. Eyeblink Classical Conditioning: Applications in Humans. Norwell, MA: Kluwer Acad.
179. Yaniv D, Schafe GE, LeDoux JE, Richter-Levin G. 2000. Perirhinal cortex and thalamic stimulation induces LTP in different areas of the amygdala. Ann. NY Acad. Sci. 911:474-76
180. Yeo CH, Hardiman MJ, Glickstein M. 1985. Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei. Exp. Brain Res. 60:87-98
181. Young SL, Bohenek DL, Fanselow MS. 1994. NMDA processes mediate anterograde amnesia of contextual fear conditioning induced by hippocampal damage: immunization against amnesia by contextual preexposure. Behav. Neurosci. 108:19-29
182. Zhen X, Du W, Romano AG, Friedman E, Harvey JA. 2001. The p38 mitogen-activated protein kinase is involved in associative learning in rabbits. J. Neurosci. 21:5513-19