Specific long-term memory traces in primary auditory cortex

Nature Reviews Neuroscience

Volumn 5, Issue 4, 2004, Pages 279-290

  Weinberger, Norman M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUDITORY CORTEX; BRAIN FUNCTION; CHOLINERGIC SYSTEM; HUMAN; LEARNING; LONG TERM MEMORY; MEMORY; NERVE CELL PLASTICITY; NEUROBIOLOGY; NEUROPHYSIOLOGY; OLIVARY NUCLEUS; PRIORITY JOURNAL; REVIEW; SENSORY CORTEX; SOUND;

ANIMALS; AUDITORY CORTEX; BASAL NUCLEUS OF MEYNERT; CONDITIONING, OPERANT; HUMANS; LEARNING; MEMORY; NEURONAL PLASTICITY; NEURONS; SENSATION;

EID: 1842731927     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn1366     Document Type: Article

References (135)

1. Galambos, R., Sheatz, G. & Vernier, V. Electrophysiological correlates of a conditioned response in cats. Science 123, 376–377 (1956).
2. Weinberger, N. M. & Diamond, D. M. Physiological plasticity in auditory cortex: rapid induction by learning. Prog. Neurobiol. 29, 1–55 (1987).
3. Rauschecker, J. P. Auditory cortical plasticity: a comparison with other sensory systems. Trends Neurosci. 22, 74–80 (1999).
4. Palmer, C. V., Nelson, C. T. & Lindley, G. A. The functionally and physiologically plastic adult auditory system. J. Acoust. Soc. Am. 103, 1705–1721 (1998).
5. Edeline, J. M. Learning-induced physiological plasticity in the thalamo-cortical sensory systems: a critical evaluation of receptive field plasticity, map changes and their potential mechanisms. Prog. Neurobiol. 57, 165–224 (1999).
6. Irvine, D. R. & Rajan, R. Injury- and use-related plasticity in the primary sensory cortex of adult mammals: possible relationship to perceptual learning. Clin. Exp. Pharmacol. Physiol. 23, 939–947 (1996).
7. Moore, D. R. et al. Auditory learning as a cause and treatment of central dysfunction. Audiol. Neurootol. 6, 216–220 (2001).
8. Scheich, H., Stark, H., Zuschratter, W., Ohl, F. W. & Simonis, C. E. Some functions of primary auditory cortex in learning and memory formation. Adv. Neurol. 73, 179–193 (1997).
9. Gonzalez-Lima, F. & Scheich, H. Neural substrates for toneconditioned bradycardia demonstrated with 2-deoxyglucose. II. Auditory cortex plasticity. Behav. Brain Res. 20, 281–293 (1986).
10. Carrascal, E., Ortin, A., Collia, F. & Arevalo, M. Metabolic activity changes in auditory system of the rat during associative learning. New Trends Exp. Clin. Psychiatry 6, 56–63 (1990).
11. Bakin, J. S. & Weinberger, N. M. Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res. 536, 271–286 (1990).
12. Weinberger, N. M., Diamond, D. M. & McKenna, T. M. in Neurobiology of Learning and Memory (eds Martinez, J. & Kesner, R.) 197–227 (Academic, New York, 1984).
13. Diamond, D. M. & Weinberger, N. M. Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. Behav. Neurosci. 103, 471–194 (1989).
14. Diamond, D. M. & Weinberger, N. M. Classical conditioning rapidly induces specific changes in frequency receptive fields of single neurons in secondary and ventral ectosylvian auditory cortical fields. Brain Res. 372, 357–360 (1986).
15. Bakin, J. S., Lepan, B. & Weinberger, N. M. Sensitization induced receptive field plasticity in the auditory cortex is independent of CS-modality. Brain Res. 577, 226–235 (1992).
16. Edeline, J. M. & Weinberger, N. M. Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. Behav. Neurosci. 107, 82–103 (1993).
17. Bakin, J. S., South, D. A. & Weinberger, N. M. Induction of receptive field plasticity in the auditory cortex of the guinea pig during instrumental avoidance conditioning. Behav. Neurosci. 110, 905–913 (1996).
18. Edeline, J.-M., Pham, P. & Weinberger, N. M. Rapid development of learning-induced receptive field plasticity in the auditory cortex. Behav. Neurosci. 107, 539–557 (1993).
19. Weinberger, N. M., Javid, R. & Lepan, B. Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. Proc. Natl Acad. Sci. USA 90, 2394–2398 (1993).
20. McGaugh, J. L. Memory: a century of consolidation. Science 287, 248–251 (2000).
21. Galvan, V. V., Chen, J. & Weinberger, N. M. Long-term frequency tuning of local field potentials in the auditory cortex of the waking guinea pig. J. Assoc. Res. Otolaryngol. 2, 199–215 (2001).
22. Galvan, V. V. & Weinberger, N. M. Long-term consolidation and retention of learning-induced tuning plasticity in the auditory cortex of the guinea pig. Neurobiol. Learn. Mem. 77, 78–108 (2002).
23. Kisley, M. A. & Gerstein, G. L. Daily variation and appetitive conditioning-induced plasticity of auditory cortex receptive fields. Eur. J. Neurosci. 13, 1993–2003 (2001).
24. Olds, J. Hypothalamic substrates of reward. Physiol. Rev. 42, 554–604 (1962).
25. Gao, E. & Suga, N. Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proc. Natl Acad. Sci. USA 97, 8081–8086 (2000).
26. Konorski, J. Integrative Activity of the Brain: An Interdisciplinary Approach (Univ. Chicago Press, Chicago, 1967).
27. Lennartz, R. C. & Weinberger, N. M. Analysis of response systems in Pavlovian conditioning reveals rapidly vs slowly acquired conditioned responses: support for two factors and implications for neurobiology. Psychobiology 20, 93–119 (1992).
28. Pavlov, I. P. Conditioned Reflexes (Dover Publications, New York, 1927).
29. Ohl, F. W. & Scheich, H. Differential frequency conditioning enhances spectral contrast sensitivity of units in auditory cortex (field A1) of the alert Mongolian gerbil. Eur. J. Neurosci. 8, 1001–1017 (1996).
30. Ohl, F. W. & Scheich, H. Learning-induced dynamic receptive field changes in primary auditory cortex of the unanaesthetized Mongolian gerbil. J. Comp. Physiol. A 181, 685–696 (1997).
31. Mackintosh, N. J. Conditioning and Associative Learning (Oxford Univ. Press, New York, 1983).
32. Mackintosh, N. J. in Memory Systems of the Brain: Animal and Human Cognitive Processes (eds Weinberger, N. M., McGaugh, J. L. & Lynch, G.) 335–350 (Guilford, New York, 1985).
33. Weinberger, N. M. in Springer Handbook of Auditory Research (eds Parks, E. R., Popper, A. & Fay, R.) (Springer, New York, in the press).
34. Weinberger, N. M. et al. Retuning auditory cortex by learning: a preliminary model of receptive field plasticity. Concepts Neurosci. 1, 91–131 (1990).
35. Recanzone, G. H., Schreiner, C. E. & Merzenich, M. M. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J. Neurosci. 13, 87–103 (1993).
36. Goldstone, R. L., Schyns, P. G. & Medin, D. L. Perceptual Learning (Academic, San Diego, 1997).
37. Brown, M., Irvine, D. R. F. & Park, V. N. Perceptual learning on an auditory frequency discrimination task by cats: association with changes in primary auditory cortex. Cereb. Cortex (in the press).
38. Bao, S., Chan, V. T. & Merzenich, M. M. Cortical remodeling induced by activity of ventral tegmental dopamine neurons. Nature 412, 79–83 (2001).
39. Bao, S., Chan, V. T., Zhang, L. I. & Merzenich, M. M. Suppression of cortical representation through backward conditioning. Proc. Natl Acad. Sci. USA 100, 1405–1408 (2003).
40. Rescorla, R. Pavlovian conditioning and its proper control procedure. Psychol. Rev. 74, 71–80 (1967).
41. Rutkowski, R. G., Than, K. H. & Weinberger, N. M. Evidence for area of frequency representation encoding stimulus importance in rat primary auditory cortex. Soc. Neurosci. Abstr. 28, 530 (2002).
42. Weinberger, N. M. The nucleus basalis and memory codes: auditory cortical plasticity and the induction of specific, associative behavioral memory. Neurobiol. Learn. Mem. 80, 268–284 (2003).
43. Weinberger, N. M. in Consolidation: Essays in Honor of James L. McGaugh (eds Gold, P. E. McGaugh, J. L., & Greenough, W. T.) 321–342 (American Psychological Association, Washington, DC, 2001).
44. Molchan, S. E., Sunderland, T., McIntosh, A. R., Herscovitch, P. & Schreurs, B. G. A functional anatomical study of associative learning in humans. Proc. Natl Acad. Sci. USA 91, 8122–8126 (1994).
45. Schreurs, B. G. et al. Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. J. Neurophysiol. 77, 2153–2163 (1997).
46. Morris, J. S., Friston, K. J. & Dolan, R. J. Experiencedependent modulation of tonotopic neural responses in human auditory cortex. Proc. R. Soc. Lond. B 265, 649–657 (1998).
47. Weinberger, N. M. et al. in Neurocomputation and Learning: Foundations of Adaptive Networks (eds Gabriel, M. & Moore, J.) 91–138 (Bradford Books/MIT Press, Cambridge, Massachusetts, 1990).
48. Suga, N. & Ma, X. Multiparametric corticofugal modulation and plasticity in the auditory system. Nature Rev. Neurosci. 4, 783–794 (2003).
49. Huang, C. L. & Winer, J. A. Auditory thalamocortical projections in the cat: laminar and areal patterns of input. J. Comp. Neurol. 427, 302–331 (2000).
50. Weinberger, N. M. Physiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiol. Learn. Mem. 70, 226–251 (1998).
51. Edeline, J. M. & Weinberger, N. M. Thalamic short-term plasticity in the auditory system: associative returning of receptive fields in the ventral medial geniculate body. Behav. Neurosci. 105, 618–639 (1991).
52. Gao, E. & Suga, N. Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proc. Natl Acad. Sci. USA 95, 12663–12670 (1998).
53. Guillery, R. W. & Harting, J. K. Structure and connections of the thalamic reticular nucleus: advancing views over half a century. J. Comp. Neurol. 463, 360–371 (2003).
54. Shosaku, A., Kayama, Y., Sumitomo, I., Sugitani, M. & Iwama, K. Analysis of recurrent inhibitory circuit in rat thalamus: neurophysiology of the thalamic reticular nucleus. Prog. Neurobiol. 32, 77–102 (1989).
55. Edeline, J. M., Neuenschwander-El Massioui, N. & Dutrieux, G. Discriminative long-term retention of rapidly induced multiunit changes in the hippocampus, medial geniculate and auditory cortex. Behav. Brain Res. 39, 145–155 (1990).
56. Edeline, J. M. & Weinberger, N. M. 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, 81–105 (1992).
57. Lennartz, R. C. & Weinberger, N. M. Frequency-specific receptive field plasticity in the medial geniculate body induced by Pavlovian fear conditioning is expressed in the anesthetized brain. Behav. Neurosci. 106, 484–497 (1992).
58. Wepsic, J. G. Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus. Exp. Neurol. 15, 299–318 (1966).
59. Lund, R. D. & Webster, K. E. Thalamic afferents from the spinal cord and the trigeminal nucleus. An experiment anatomic study in the rat. J. Comp. Neurol. 130, 313–328 (1967).
60. Gabriel, M., Miller, J. D. & Saltwick, S. E. Multiple unit activity of the rabbit medial geniculate nucleus in conditioning, extinction, and reversal. Physiol. Psychol. 4, 124–134 (1976).
61. Gabriel, M., Saltwick, S. E. & Miller, J. D. Conditioning and reversal of short-latency multiple-unit responses in the rabbit medial geniculate nucleus. Science 189, 1108–1109 (1975).
62. Ryugo, D. K. & Weinberger, N. M. Differential plasticity of morphologically distinct neuron populations in the medial geniculate body of the cat during classical conditioning. Behav. Biol. 22, 275–301 (1978).
63. Edeline, J. M., Neuenschwander-el Massioui, N. & Dutrieux, G. Discriminative long-term retention of rapidly induced multiunit changes in the hippocampus, medial geniculate and auditory cortex. Behav. Brain Res. 39, 145–155 (1990).
64. Edeline, J. M. Frequency-specific plasticity of single unit discharges in the rat medial geniculate body. Brain Res. 529, 109–119 (1990).
65. McEchron, M. D., McCabe, P. M., Green, E. J., Llabre, M. M. & Schneiderman, N. Simultaneous single unit recording in the medial nucleus of the medial geniculate nucleus and amygdaloid central nucleus throughout habituation, acquisition, and extinction of the rabbit’s classically conditioned heart rate. Brain Res. 682, 157–166 (1995).
66. McEchron, M. D. et al. Changes of synaptic efficacy in the medial geniculate nucleus as a result of auditory classical conditioning. J. Neurosci. 16, 1273–1283 (1996).
67. Lennartz, R. C. & Weinberger, N. M. Frequency-specific receptive field plasticity in the medial geniculate body induced by pavlovian fear conditioning is expressed in the anesthetized brain. Behav. Neurosci. 106, 484–497 (1992).
68. O’Connor, K. N., Allison, T. L., Rosenfield, M. E. & Moore, J. W. Neural activity in the medial geniculate nucleus during auditory trace conditioning. Exp. Brain Res. 113, 534–556 (1997).
69. Gerren, R. A. & Weinberger, N. M. Long term potentiation in the magnocellular medial geniculate nucleus of the anesthetized cat. Brain Res. 265, 138–142 (1983).
70. Weinberger, N. M., Javid, R. & Lepan, B. Heterosynaptic long-term facilitation of sensory-evoked responses in the auditory cortex by stimulation of the magnocellular medial geniculate body in guinea pigs. Behav. Neurosci. 109, 10–17 (1995).
71. Cruikshank, S. J., Edeline, J. M. & Weinberger, N. M. Stimulation at a site of auditory-somatosensory convergence in the medial geniculate nucleus is an effective unconditioned stimulus for fear conditioning. Behav. Neurosci. 106, 471–483 (1992).
72. LeDoux, J. E., Sakaguchi, A., Iwata, J. & Reis, D. J. Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli. Neuroscience 17, 615–627 (1986).
73. LeDoux, J. E., Iwata, J., Pearl, D. & Reis, D. J. Disruption of auditory but not visual learning by destruction of intrinsic neurons in the rat medial geniculate body. Brain Res. 371, 395–399 (1986).
74. Iwata, J., LeDoux, J. E., Meeley, M. P., Arneric, S. & Reis, D. J. 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 (1986).
75. McKernan, M. G. & Shinnick-Gallagher, P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390, 607–611 (1997).
76. Cahill, L., McGaugh, J. L. & Weinberger, N. M. The neurobiology of learning and memory: some reminders to remember. Trends Neurosci. 24, 578–581 (2001).
77. Cahill, L., Vazdarjanova, A. & Setlow, B. The basolateral amygdala complex is involved with, but is not necessary for, rapid acquisition of Pavlovian ‘fear conditioning’. Eur. J. Neurosci. 12, 3044–3050 (2000).
78. Vazdarjanova, A. Does the basolateral amygdala store memories for emotional events? Trends Neurosci. 23, 345–346 (2000).
79. Maren, S., Yap, S. A. & Goosens, K. A. The amygdala is essential for the development of neuronal plasticity in the medial geniculate nucleus during auditory fear conditioning in rats. J. Neurosci. 21, RC135 (2001).
80. Poremba, A. & Gabriel, M. Amygdalar efferents initiate auditory thalamic discriminative training-induced neuronal activity. J. Neurosci. 21, 270–278 (2001).
81. Edeline, J. M., Hars, B., Hennevin, E. & Cotillon, N. Muscimol diffusion after intracerebral microinjections: a reevaluation based on electrophysiological and autoradiographic quantifications. Neurobiol. Learn. Mem. 78, 100–124 (2002).
82. Maho, C. & Hennevin, E. Appetitive conditioning-induced plasticity is expressed during paradoxical sleep in the medial geniculate, but not in the lateral amygdala. Behav. Neurosci. 116, 807–823 (2002).
83. Teich, A. H. et al. Role of auditory cortex in the acquisition of differential heart rate conditioning. Physiol. Behav. 44, 405–412 (1988).
84. Romanski, L. M. & LeDoux, J. E. Equipotentiality of thalamoamygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning. J. Neurosci. 12, 4501–4509 (1992).
85. DiCara, L. V., Braun, J. J. & Pappas, B. A. Classical conditioning and instrumental learning of cardiac and gastrointestinal responses following removal of neocortex in the rat. J. Comp. Physiol. Psychol. 73, 208–216 (1970).
86. Mauk, M. D. & Thompson, R. F. Retention of classically conditioned eyelid responses following acute decerebration. Brain Res. 403, 89–95 (1987).
87. Norman, R. J., Villablanca, J. R., Brown, K. A., Schwafel, J. D. & Buchwald, J. S. Classical eyeblink conditioning in the bilaterally hemispherectomized cat. Exp. Neurol. 44, 363–380 (1974).
88. Berntson, G. G., Tuber, D. S., Ronca, A. E. & Bachman, D. S. The decerebrate human: associative learning. Exp. Neurol. 81, 77–88 (1983).
89. Manunta, Y. & Edeline, J. M. Effects of noradrenaline on frequency tuning of auditory cortex neurons during wakefulness and slow-wave sleep. Eur. J. Neurosci. 11, 2134–2150 (1999).
90. Manunta, Y. & Edeline, J. M. Effects of noradrenaline on frequency tuning of rat auditory cortex neurons. Eur. J. Neurosci. 9, 833–847 (1997).
91. Juckel, G., Hegerl, U., Molnar, M., Csepe, V. & Karmos, G. Auditory evoked potentials reflect serotonergic neuronal activity — a study in behaving cats administered drugs acting on 5-HT1A autoreceptors in the dorsal raphe nucleus. Neuropsychopharmacology 21, 710–716 (1999).
92. Stark, H. & Scheich, H. Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: a long-term microdialysis study of metabolites. J. Neurochem. 68, 691–697 (1997).
93. Johnston, M. V., McKinney, M. & Coyle, J. T. Evidence for a cholinergic projection to neocortex from neurons in basal forebrain. Proc. Natl Acad. Sci. USA 76, 5392–5396 (1979).
94. Mesulam, M.-M., Mufson, E. J., Levey, A. I. & Wainer, B. H. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area diagonal band nuclei, nucleus basalia (substantia innominata), and hypothalamus in the rhesus monkey. J. Comp. Neurol. 214, 170–197 (1983).
95. McKenna, T. M., Ashe, J. H. & Weinberger, N. M. Cholinergic modulation of frequency receptive fields in auditory cortex: I. Frequency-specific effects of muscarinic agonists. Synapse 4, 30–43 (1989).
96. Ashe, J. H., McKenna, T. M. & Weinberger, N. M. Cholinergic modulation of frequency receptive fields in auditory cortex: II. Frequency-specific effects of anticholinesterases provide evidence for a modulatory action of endogenous ACh. Synapse 4, 44–54 (1989).
97. Metherate, R. & Weinberger, N. M. Cholinergic modulation of responses to single tones produces tone-specific receptive field alterations in cat auditory cortex. Synapse 6, 133–145 (1990).
98. Metherate, R. & Ashe, J. H. Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Res. 559, 163–167 (1991).
99. Metherate, R. & Ashe, J. H. Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex. Synapse 14, 132–143 (1993).
100. Hars, B., Maho, C., Edeline, J.-M. & Hennevin, E. Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat. Neuroscience 56, 61–74 (1993).
101. Edeline, J. M., Maho, C., Hars, B. & Hennevin, E. Nonawaking basal forebrain stimulation enhances auditory cortex responsiveness during slow-wave sleep. Brain Res. 636, 333–337 (1994).
102. Edeline, J. M., Hars, B., Maho, C. & Hennevin, E. Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex. Exp. Brain Res. 97, 373–386 (1994).
103. Maho, C., Hars, B., Edeline, J.-M. & Hennevin, E. Conditioned changes in the basal forebrain: relations with learning-induced cortical plasticity. Psychobiology 23, 10–25 (1995).
104. Ji, W., Gao, E. & Suga, N. Effects of acetylcholine and atropine on plasticity of central auditory neurons caused by conditioning in bats. J. Neurophysiol. 86, 211–225 (2001).
105. Ma, X. & Suga, N. Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. J. Neurophysiol. 89, 90–103 (2003).
106. Ji, W. & Suga, N. Development of reorganization of the auditory cortex caused by fear conditioning: effect of atropine. J. Neurophysiol. 90, 1904–1909 (2003).
107. Thiel, C. M., Friston, K. J. & Dolan, R. J. Cholinergic modulation of experience-dependent plasticity in human auditory cortex. Neuron 35, 567–574 (2002).
108. Oh, J. D., Edwards, R. H. & Woolf, N. J. Choline acetyltransferase mRNA plasticity with Pavlovian conditioning. Exp. Neurol. 140, 95–99 (1996).
109. Pennartz, C. M. The ascending neuromodulatory systems in learning by reinforcement: comparing computational conjectures with experimental findings. Brain Res. Brain Res. Rev. 21, 219–245 (1995).
110. Mesulam, M. M., Mufson, E. J., Levey, A. I. & Wainer, B. H. Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12, 669–686 (1984).
111. Sarter, M. & Bruno, J. P. Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res. Brain Res. Rev. 23, 28–46 (1997).
112. Olds, J. & Peretz, B. A motivational analysis of the reticular activating system. Electroencephalogr. Clin. Neurophysiol. 12, 445–454 (1960).
113. Wester, K. Habituation to electrical stimulation of the thalamus in unanaesthetized cats. Electroencephalogr. Clin. Neurophysiol. 30, 52–61 (1971).
114. Bakin, J. S. & Weinberger, N. M. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl Acad. Sci. USA 93, 11219–11224 (1996).
115. Dimyan, M. A. & Weinberger, N. M. Basal forebrain stimulation induces discriminative receptive field plasticity in the auditory cortex. Behav. Neurosci. 113, 691–702 (1999).
116. Bjordahl, T. S., Dimyan, M. A. & Weinberger, N. M. Induction of long-term receptive field plasticity in the auditory cortex of the waking guinea pig by stimulation of the nucleus basalis. Behav. Neurosci. 112, 467–479 (1998).
117. Miasnikov, A. A., McLin, D. E. & Weinberger, N. M. Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity. Neuroreport 12, 1537–1542 (2001).
118. Kilgard, M. P. & Merzenich, M. M. Cortical map reorganization enabled by nucleus basalis activity. Science 279, 1714–1718 (1998).
119. Kilgard, M. P. et al. Sensory input directs spatial and temporal plasticity in primary auditory cortex. J. Neurophysiol. 86, 326–338 (2001).
120. McLin, D. E., Miasnikov, A. A. & Weinberger, N. M. Induction of behavioral associative memory by stimulation of the nucleus basalis. Proc. Natl Acad. Sci. USA 99, 4002–4007 (2002).
121. McLin, D. E., Miasnikov, A. A. & Weinberger, N. M. CS-specific gamma, theta, and alpha EEG activity detected in stimulus generalization following induction of behavioral memory by stimulation of the nucleus basalis. Neurobiol. Learn. Mem. 79, 152–176 (2003).
122. Jensen, O., Idiart, M. A. & Lisman, J. E. Physiologically realistic formation of autoassociative memory in networks with theta/gamma oscillations: role of fast NMDA channels. Learn. Mem. 3, 243–256 (1996).
123. Beitel, R. E., Schreiner, C. E., Cheung, S. W., Wang, X. & Merzenich, M. M. Reward-dependent plasticity in the primary auditory cortex of adult monkeys trained to discriminate temporally modulated signals. Proc. Natl Acad. Sci. USA 100, 11070–11075 (2003).
124. Karmarkar, U. R. & Buonomano, D. V. Temporal specificity of perceptual learning in an auditory discrimination task. Learn. Mem. 10, 141–147 (2003).
125. Carretta, D., Herve-Minvielle, A., Bajo, V. M., Villa, A. E. & Rouiller, E. M. c-Fos expression in the auditory pathways related to the significance of acoustic signals in rats performing a sensory-motor task. Brain Res. 841, 170–183 (1999).
126. Fritz, J., Shamma, S., Elhilali, M. & Klein, D. Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nature Neurosci. 6, 1216–1223 (2003).
127. Nelken, I., Fishbach, A., Las, L., Ulanovsky, N. & Farkas, D. Primary auditory cortex of cats: feature detection or something else? Biol. Cybern. 89, 397–406 (2003).
128. Ohl, F. W., Scheich, H. & Freeman, W. J. Change in pattern of ongoing cortical activity with auditory category learning. Nature 412, 733–736 (2001).
129. Blake, D. T., Strata, F., Churchland, A. K. & Merzenich, M. M. Neural correlates of instrumental learning in primary auditory cortex. Proc. Natl Acad. Sci. USA 99, 10114–10119 (2002).
130. Villa, A. E., Tetko, I. V., Hyland, B. & Najem, A. Spatiotemporal activity patterns of rat cortical neurons predict responses in a conditioned task. Proc. Natl Acad. Sci. USA 96, 1106–1111 (1999).
131. Hernandez-Peon, R., Scherrer, H. & Jouvet, M. Modification of electric activity in cochlear nucleus during ‘attention’ in unanesthetized cats. Science 123, 331–332 (1956).
132. Furedy, J. J. Explicity unpaired and truly-random CScontrols in human classical differential autonomic conditioning. Psychophysiology 8, 497–503 (1971).
133. Rescorla, R. A. Behavioral studies of Pavlovian conditioning. Annu. Rev. Neurosci. 11, 329–352 (1988).
134. Weinberger, N. M. Learning-induced receptive field plasticity in the primary auditory cortex. Sem. Neurosci. 9, 59–67 (1997).
135. Weinberger, N. M. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) 1071–1089 (MIT Press, Cambridge, Massachusetts, 1995).