The level of cholinergic nucleus basalis activation controls the specificity of auditory associative memory

Neurobiology of Learning and Memory

Volumn 86, Issue 3, 2006, Pages 270-285

  Weinberger, Norman M ^a   Miasnikov, Alexandre A ^a   Chen, Jemmy C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholine; Association; Auditory cortex; Encoding

Indexed keywords

ACETYLCHOLINE;

ACETYLCHOLINE RELEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; ASSOCIATIVE MEMORY; AUDITORY MEMORY; AUDITORY STIMULATION; BREATHING RATE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAM; MALE; NEUROMODULATION; NONHUMAN; OLIVARY NUCLEUS; RAT;

ANIMALS; ASSOCIATION LEARNING; AUDITORY PERCEPTION; BASAL NUCLEUS OF MEYNERT; BEHAVIOR, ANIMAL; CHOLINERGIC FIBERS; ELECTRIC STIMULATION; ELECTROENCEPHALOGRAPHY; MALE; MENTAL RECALL; NEURONAL PLASTICITY; PRACTICE (PSYCHOLOGY); RATS; RATS, SPRAGUE-DAWLEY;

EID: 33748924505     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2006.04.004     Document Type: Article

References (97)

1. Barkai E., and Hasselmo M.H. Acetylcholine and associative memory in the piriform cortex. Molecular Neurobiology 15 1 (1997) 17-29
2. Başar E., Başar-Eroǧlu C., Karakaş S., and Schürmann M. Brain oscillations in perception and memory. International Journal of Psychophysiology 35 2-3 (2000) 95-124
3. Berntson G.G., Shafi R., and Sarter M. Specific contributions of the basal forebrain corticopetal cholinergic system to electroencephalographic activity and sleep/waking behaviour. European Journal of Neuroscience 16 12 (2002) 2453-2461
4. Bertrand O., and Tallon-Baudry C. Oscillatory gamma activity in humans: a possible role for object representation. International Journal of Psychophysiology 38 3 (2000) 211-223
5. Bigl V., Woolf N.J., and Butcher L.L. Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Research Bulletin 8 6 (1982) 727-749
6. Brett B., and Barth D.S. Subcortical modulation of high-frequency (gamma band) oscillating potentials in auditory cortex. Journal of Neurophysiology 78 2 (1997) 573-581
7. Brett B., Krishnan G., and Barth D.S. The effects of subcortical lesions on evoked potentials and spontaneous high frequency (gamma-band) oscillating potentials in rat auditory cortex. Brain Research 721 1-2 (1996) 155-166
8. Cape E.G., Manns I.D., Alonso A., Beaudet A., and Jones B.E. Neurotensin-induced bursting of cholinergic basal forebrain neurons promotes γ and θ cortical activity together with waking and paradoxical sleep. Journal of Neuroscience 20 22 (2000) 8452-8461
9. Casamenti F., Deffenu G., Abbamondi A.L., and Pepeu G. Changes in cortical acetylcholine output induced by modulation of the nucleus basalis. Brain Research Bulletin 16 5 (1986) 689-695
10. Celesia G.G., and Jasper H.H. Acetylcholine released from cerebral cortex in relation to state of activation. Neurology 16 11 (1966) 1053-1063
11. Chernyshev B.V., and Weinberger N.M. Acoustic frequency tuning of neurons in the basal forebrain of the waking guinea pig. Brain Research 793 1-2 (1998) 79-94
12. Christian K.M., and Thompson R.F. Neural substrates of eyeblink conditioning: acquisition and retention. Learning and Memory 10 6 (2003) 427-455
13. Condon C.D., and Weinberger N.M. Habituation produces frequency-specific plasticity of receptive fields in the auditory cortex. Behavioral Neuroscience 105 3 (1991) 416-430
14. Davis M., Falls W.A., Campeau S., and Kim M. Fear-potentiated startle: a neural and pharmacological analysis. Behavioural Brain Research 58 1-2 (1993) 175-198
15. Détári L., Juhász G., and Kukorelli T. Effect of stimulation of vagal and radial nerves on neuronal activity in the basal forebrain area of anaesthetized cats. Acta Physiologica Hungarica 61 3 (1983) 147-154
16. Détári L., Juhász G., and Kukorelli T. Firing properties of cat basal forebrain neurones during sleep-wakefulness cycle. Electroencephalography and Clinical Neurophysiology 58 4 (1984) 362-368
17. Détári L., Juhász G., and Kukorelli T. Neuronal firing in the pallidal region: firing patterns during sleep-wakefulness cycle in cats. Electroencephalography and Clinical Neurophysiology 67 2 (1987) 159-166
18. Détári L., Rasmusson D.D., and Semba K. The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex. Progress in Neurobiology 58 3 (1999) 249-277
19. Deutsch J.A. The cholinergic synapse and the site of memory. Science 174 11 (1971) 788-794
20. Diamond M.E., Petersen R.S., and Harris J.A. Learning through maps: functional significance of topographic organization in primary sensory cortex. Journal of Neurobiology 41 1 (1999) 64-68
21. Duque A., Balatoni B., Détári L., and Zaborszky L. EEG correlation of the discharge properties of identified neurons in the basal forebrain. Journal of Neurophysiology 84 3 (2000) 1627-1635
22. Dykes R.W. Mechanisms controlling neuronal plasticity in somatosensory cortex. Canadian Journal of Physiology and Pharmacology 75 5 (1997) 535-545
23. Edeline J.-M. The thalamo-cortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems. Experimental Brain Research 153 4 (2003) 554-572
24. Edeline J.-M., Hars B., Maho C., and Hennevin E. Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex. Experimental Brain Research 97 3 (1994) 373-386
25. Edeline J.-M., Maho C., Hars B., and Hennevin E. Non-awaking basal forebrain stimulation enhances auditory cortex responsiveness during slow-wave sleep. Brain Research 636 2 (1994) 333-337
26. Feldman D.E., and Brecht M. Map plasticity in somatosensory cortex. Science 310 5749 (2005) 810-815
27. Flood J.F., Landry D.W., and Jarvik M.E. Cholinergic receptor interactions and their effects on long-term memory processing. Brain Research 215 1-2 (1981) 177-185
28. Freund T.F., and Meskenaite V. γ-Aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex. Proceedings of the National Academy of Sciences of the United States of America 89 2 (1992) 738-742
29. Giocomo L.M., and Hasselmo M.E. Nicotinic modulation of glutamatergic synaptic transmission in region CA3 of the hippocampus. European Journal of Neuroscience 22 6 (2005) 1349-1356
30. Giovannini M.G., Rakovska A., Benton R.S., Pazzagli M., Bianchi L., and Pepeu G. Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106 1 (2001) 43-53
31. Greenberg D.L., and Rubin D.C. The neuropsychology of autobiographical memory. Cortex 39 4-5 (2003) 687-728
32. Hars B., Maho C., Edeline J.-M., and Hennevin E. Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat. Neuroscience 56 1 (1993) 61-74
33. Hasselmo M.E., Anderson B.P., and Bower J.M. Cholinergic modulation of cortical associative memory function. Journal of Neurophysiology 67 5 (1992) 1230-1246
34. Hasselmo M.E., Fransen E., Dickson C., and Alonso A.A. Computational modeling of entorhinal cortex. Annals of the New York Academy of Sciences 911 (2000) 418-446
35. Hasselmo M.E., and McGaughy J. High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Progress in Brain Research 145 (2004) 207-231
36. Heffner H.E., Heffner R.S., Contos C., and Ott T. Audiogram of the hooded Norway rat. Hearing Research 73 2 (1994) 244-247
37. Jasper H.H., and Tessier J. Acetylcholine liberation from cerebral cortex during paradoxical (REM) sleep. Science 172 3983 (1971) 601-602
38. Jefferys J.G.R., Traub R.D., and Whittington M.A. Neuronal networks for induced '40 Hz' rhythms. Trends in Neurosciences 19 5 (1996) 202-208
39. Jiménez-Capdeville M.E., Dykes R.W., and Myasnikov A.A. Differential control of cortical activity by the basal forebrain in rats: a role for both cholinergic and inhibitory influences. Journal of Comparative Neurology 381 1 (1997) 53-67
40. John E.R. High nervous functions: brain functions and learning. Annual Review of Physiology 23 (1961) 451-484
41. Johnston M.V., McKinney M., and Coyle J.T. Evidence for a cholinergic projection to neocortex from neurons in basal forebrain. Proceedings of the National Academy of Sciences of the United States of America 76 10 (1979) 5392-5396
42. Juhász G., Détári L., and Kukorelli T. Effects of hypnogenic vagal stimulation on thalamic neuronal activity in cats. Brain Research Bulletin 15 5 (1985) 437-441
43. Kaiser J., and Lutzenberger W. Cortical oscillatory activity and the dynamics of auditory memory processing. Reviews in the Neurosciences 16 3 (2005) 239-254
44. Kametani H., and Kawamura H. Alterations in acetylcholine release in the rat hippocampus during sleep-wakefulness detected by intracerebral dialysis. Life Sciences 47 5 (1990) 421-426
45. Kilgard M.P., Pandya P.K., Vazquez J., Gehi A., Schreiner C.E., and Merzenich M.M. Sensory input directs spatial and temporal plasticity in primary auditory cortex. Journal of Neurophysiology 86 1 (2001) 326-338
46. Kilgard M.P., and Merzenich M.M. Cortical map reorganization enabled by nucleus basalis activity. Science 279 5357 (1998) 1714-1718
47. Kukorelli T., Feuer L., Juhász G., and Détári L. Effect of glutaurine on sleep-wakefulness cycle and aggressive behaviour in the cat. Acta Physiologica Hungarica 67 1 (1986) 31-35
48. Luiten P.G.M., Gaykema R.P.A., Traber J., and Spencer Jr. D.G. Cortical projection patterns of magnocellular basal nucleus subdivisions as revealed by anterogradely transported Phaseolus vulgaris leucoagglutinin. Brain Research 413 2 (1987) 229-250
49. Mackintosh N.J. The psychology of animal learning (1974), Academic Press, New York
50. Marrosu F., Portas C., Mascia M.S., Casu M.A., Fà M., Giagheddu M., et al. Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Research 671 2 (1995) 329-332
51. McGaughy J., Koene R.A., Eichenbaum H., and Hasselmo M.E. Cholinergic deafferentation of the entorhinal cortex in rats impairs encoding of novel but not familiar stimuli in a delayed nonmatch-to-sample task. Journal of Neuroscience 25 44 (2005) 10273-10281
52. McIntyre C.K., Marriott L.K., and Gold P.E. Cooperation between memory systems: acetylcholine release in the amygdala correlates positively with performance on a hippocampus-dependent task. Behavioral Neuroscience 117 2 (2003) 320-326
53. McIntyre C.K., Pal S.N., Marriott L.K., and Gold P.E. Competition between memory systems: acetylcholine release in the hippocampus correlates negatively with good performance on an amygdala-dependent task. Journal of Neuroscience 22 3 (2002) 1171-1176
54. McLin, D. E., Miasnikov, A. A., & Weinberger, N. M. (2000). Potentials evoked in the primary auditory cortex by stimulation of the nucleus basalis that can induce receptive field plasticity. Abs. No. 73.5. Society for Neuroscience Abstracts, 26 (1), 194.
55. McLin III D.E., Miasnikov A.A., and Weinberger N.M. The effects of electrical stimulation of the nucleus basalis on the electroencephalogram, heart rate, and respiration. Behavioral Neuroscience 116 5 (2002) 795-806
56. McLin III D.E., Miasnikov A.A., and Weinberger N.M. Induction of behavioral associative memory by stimulation of the nucleus basalis. Proceedings of the National Academy of Sciences of the United States of America 99 6 (2002) 4002-4007
57. McLin III D.E., Miasnikov A.A., and 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. Neurobiology of Learning and Memory 79 2 (2003) 152-176
58. Mesulam M.-M., Mufson E.J., Wainer B.H., and Levey A.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10 4 (1983) 1185-1201
59. Metherate R., and Ashe J.H. Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Research 559 1 (1991) 163-167
60. Metherate R., and Ashe J.H. Nucleus basalis stimulation elicits neocortical activation and facilitates thalamocortical synaptic transmission: Intracellular and extracellular recordings in rat auditory cortex. Society for Neuroscience Abstracts 18 2 (1992) 975
61. Metherate R., and Ashe J.H. Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex. Synapse 14 2 (1993) 132-143
62. Metherate R., Cox C.L., and Ashe J.H. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. Journal of Neuroscience 12 12 (1992) 4701-4711
63. Metherate R., and Cruikshank S.J. Thalamocortical inputs trigger a propagating envelope of gamma-band activity in auditory cortex in vitro. Experimental Brain Research 126 2 (1999) 160-174
64. Metherate R., and Hsieh C.Y. Synaptic mechanisms and cholinergic regulation in auditory cortex. Progress in Brain Research 145 (2004) 143-156
65. Miasnikov, A. A., Chen, J. C., & Weinberger, N. M. (2006). Rapid induction of specific associative behavioral memory by stimulation of the nucleus basalis in the rat. Neurobiology of Learning and Memory, in press, doi:10.1016/j.nlm.2005.12.010.
66. Miasnikov A.A., McLin III D., and Weinberger N.M. Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity. NeuroReport 12 7 (2001) 1537-1542
67. Miasnikov, A. A., Poytress, B. S., Chen, J. C., & Weinberger, N. M. (2004). Stimulation of the nucleus basalis that induces behavioral memory in the rat is motivationally neutral. Prog. No. 207.6. In 2004 Abstract Viewer. Washington, DC: Society for Neuroscience.
68. In: Mostofsky D.I. (Ed). Stimulus generalization (1965), Stanford University Press, Palo Alto, CA
69. Ohl, F. W., & Scheich, H. (2004). Online correspondence: fallacies in behavioural interpretation of auditory cortex plasticity. Nature Reviews Neuroscience. Published online November 20, 2004 at .
70. Palmer C.V., Nelson C.T., and Lindley IV G.A. The functionally and physiologically plastic adult auditory system. Journal of the Acoustical Society of America 103 4 (1998) 1705-1721
71. Pavlov, I. P. (1960). Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex (G.V. Anrep, Trans.). New York: Dover Publications. (Original work published 1927).
72. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. 3rd ed. (1997), Academic Press, San Diego
73. Pennartz C.M.A. The ascending neuromodulatory systems in learning by reinforcement: comparing computational conjectures with experimental findings. Brain Research Reviews 21 3 (1995) 219-245
74. Phillis J.W., and York D.H. Pharmacological studies on a cholinergic inhibition in the cerebral cortex. Brain Research 10 3 (1968) 297-306
75. Power A.E., Vazdarjanova A., and McGaugh J.L. Muscarinic cholinergic influences in memory consolidation. Neurobiology of Learning and Memory 80 3 (2003) 178-193
76. Rasmusson D.D., Clow K., and Szerb J.C. Frequency-dependent increase in cortical acetylcholine release evoked by stimulation of the nucleus basalis magnocellularis in the rat. Brain Research 594 1 (1992) 150-154
77. Rasmusson D.D., Clow K., and Szerb J.C. Modification of neocortical acetylcholine release and electroencephalogram desynchronization due to brainstem stimulation by drugs applied to the basal forebrain. Neuroscience 60 3 (1994) 665-677
78. Rasmusson D.D., Szerb J.C., and Jordan J.L. Differential effects of α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid and N-methyl-d-aspartate receptor antagonists applied to the basal forebrain on cortical acetylcholine release and electroencephalogram desynchronization. Neuroscience 72 2 (1996) 419-427
79. Rauschecker J.P. Auditory cortical plasticity: a comparison with other sensory systems. Trends in Neurosciences 22 2 (1999) 74-80
80. Rugg M.D., and Yonelinas A.P. Human recognition memory: a cognitive neuroscience perspective. Trends in Cognitive Sciences 7 7 (2003) 313-319
81. Rutkowski R.G., and Weinberger N.M. Encoding of learned importance of sound by magnitude of representational area in primary auditory cortex. Proceedings of the National Academy of Sciences of the United States of America 102 38 (2005) 13664-13669
82. Rye D.B., Wainer B.H., Mesulam M.-M., Mufson E.J., and Saper C.B. Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 13 3 (1984) 627-643
83. Sommer F.T., and Wennekers T. Associative memory in networks of spiking neurons. Neural Networks 14 6-7 (2001) 825-834
84. Szerb J. The effect of tertiary and quaternary atropine on cortical acetylcholine output and on the electroencephalogram in cats. Canadian Journal of Physiology and Pharmacology 42 (1964) 303-314
85. Szymusiak R., and McGinty D. Sleep-related neuronal discharge in the basal forebrain of cats. Brain Research 370 1 (1986) 82-92
86. Thompson R.F., Patterson M.M., and Teyler T.J. The neurophysiology of learning. Annual Review of Psychology 23 (1972) 73-104
87. Trainor L.J., Shahin A., and Roberts L.E. Effects of musical training on the auditory cortex in children. Annals of the New York Academy of Sciences 999 (2003) 506-513
88. Wagner A.R., and Brandon S.E. Evolution of a structured connectionist model of Pavlovian conditioning (AESOP). In: Klein S.B., and Mowrer R.R. (Eds). Contemporary learning theories: Pavlovian conditioning and the status of traditional learning theory (1989), Lawrence Erlbaum Associates, Hillsdale, NJ 149-189
89. Weinberger N.M. Dynamic regulation of receptive fields and maps in the adult sensory cortex. Annual Review of Neuroscience 18 (1995) 129-158
90. Weinberger N.M. Physiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiology of Learning and Memory 70 1-2 (1998) 226-251
91. Weinberger N.M. The nucleus basalis and memory codes: auditory cortical plasticity and the induction of specific, associative behavioral memory. Neurobiology of Learning and Memory 80 3 (2003) 268-284
92. Weinberger N.M. Experience-dependent response plasticity in the auditory cortex: issues, characteristics, mechanisms, and functions. In: Parks T.N., Rubel E.W., Fay R.R., and Popper A.N. (Eds). Plasticity of the auditory system. Springer Handbook of Auditory Research Vol. 23 (2004), Springer, New York 173-227
93. Weinberger, N. M. (2004b). Online correspondence: correcting misconceptions of tuning shifts in auditory cortex. Nature Reviews Neuroscience. Published online November 20, 2004 at .
94. Weinberger N.M. Specific long-term memory traces in primary auditory cortex. Nature Reviews Neuroscience 5 4 (2004) 279-290
95. Weinberger N.M., Ashe J.H., Metherate R., McKenna T.M., Diamond D.M., and Bakin J. Retuning auditory cortex by learning: a preliminary model of receptive field plasticity. Concepts in Neuroscience 1 1 (1990) 91-132
96. Wenk G.L., Stoehr J.D., Quintana G., Mobley S., and Wiley R.G. Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats. Journal of Neuroscience 14 10 (1994) 5986-5995
97. Wilson F.A.W., and Ma Y.-Y. Reinforcement-related neurons in the primate basal forebrain respond to the learned significance of task events rather than to the hedonic attributes of reward. Cognitive Brain Research 19 1 (2004) 74-81