Rapid induction of specific associative behavioral memory by stimulation of the nucleus basalis in the rat

Neurobiology of Learning and Memory

Volumn 86, Issue 1, 2006, Pages 47-65

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

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Association; Auditory cortex; Evoked potentials; Frequency generalization gradients; Learning; Plasticity

Indexed keywords

ACETYLCHOLINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; ASSOCIATIVE MEMORY; AUDITORY CORTEX; BEHAVIOR; BRAIN DEPTH STIMULATION; BREATHING; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EVOKED RESPONSE; FREQUENCY MODULATION; HEART CONTRACTION; HORMONE RELEASE; MALE; NERVE CELL PLASTICITY; NERVE STIMULATION; NEUROMODULATION; NONHUMAN; OLIVARY NUCLEUS; RAT; WAKEFULNESS;

ACOUSTIC STIMULATION; ANIMALS; ASSOCIATION LEARNING; AUDITORY CORTEX; BASAL NUCLEUS OF MEYNERT; CONDITIONING, CLASSICAL; ELECTRIC STIMULATION; EVOKED POTENTIALS, AUDITORY; GENERALIZATION (PSYCHOLOGY); MALE; MEMORY; NEURAL PATHWAYS; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 33646852624     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2005.12.010     Document Type: Article

References (85)

1. Ashe J.H., McKenna T.M., and 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 1 (1989) 44-54
2. Bakin J.S., and Weinberger N.M. Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Research 536 1-2 (1990) 271-286
3. Bakin J.S., and Weinberger N.M. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proceedings of the National Academy of Sciences of the United States of America 93 20 (1996) 11219-11224
4. Bao S., Chan V.T., and Merzenich M.M. Cortical remodeling induced by activity of ventral tegmental dopamine neurons. Nature 412 6842 (2001) 79-83
5. Barth D.S., Kithas J., and Di S. Anatomic organization of evoked potentials in rat parietotemporal cortex: Somatosensory and auditory responses. Journal of Neurophysiology 69 6 (1993) 1837-1849
6. Beninger R.J., Wirsching B.A., Jhamandas K., and Boegman R.J. Animal studies of brain acetylcholine and memory. Archives of Gerontology and Geriatrics Supplement 1 (1989) 71-89
7. Bjordahl T.S., Dimyan M.A., and 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. Behavioral Neuroscience 112 3 (1998) 467-479
8. Christian K.M., and Thompson R.F. Long-term storage of an associative memory trace in the cerebellum. Behavioral Neuroscience 119 2 (2005) 526-537
9. 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
10. Deutsch J.A. The cholinergic synapse and the site of memory. Science 174 11 (1971) 788-794
11. Dimyan M.A., and Weinberger N.M. Basal forebrain stimulation induces discriminative receptive field plasticity in the auditory cortex. Behavioral Neuroscience 113 4 (1999) 691-702
12. Dykes R.W. Acetylcholine and neuronal plasticity in somatosensory cortex. In: Steriade M., and Biesold D. (Eds). Brain cholinergic systems (1990), Oxford University Press, New York 294-313
13. 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
14. 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
15. Edeline J.-M., Pham P., and Weinberger N.M. Rapid development of learning-induced receptive field plasticity in the auditory cortex. Behavioral Neuroscience 107 4 (1993) 539-551
16. Edeline J.-M., and Weinberger N.M. Discrimination training induces selective receptive field (RF) plasticity in the auditory cortex during both easy and difficult tasks. Abs. No. 146.13. Society for Neuroscience Abstracts 18 1 (1992) 339
17. 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
18. Galván V.V., Chen J., and Weinberger N.M. Long-term frequency tuning of local field potentials in the auditory cortex of the waking guinea pig. Journal of the Association for Research in Otolaryngology 2 3 (2001) 199-215
19. Galván V.V., and Weinberger N.M. Long-term consolidation and retention of learning-induced tuning plasticity in the auditory cortex of the guinea pig. Neurobiology of Learning and Memory 77 1 (2002) 78-108
20. 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
21. Hasselmo M.E., and Bower J.M. Acetylcholine and memory. Trends in Neurosciences 16 6 (1993) 218-222
22. Heffner H.E., Heffner R.S., Contos C., and Ott T. Audiogram of the hooded Norway rat. Hearing Research 73 2 (1994) 244-247
23. Jasper H.H., and Tessier J. Acetylcholine liberation from cerebral cortex during paradoxical (REM) sleep. Science 172 983 (1971) 601-602
24. Ji W., Gao E., and Suga N. Effects of acetylcholine and atropine on plasticity of central auditory neurons caused by conditioning in bats. Journal of Neurophysiology 86 1 (2001) 211-225
25. Ji W., and Suga N. Development of reorganization of the auditory cortex caused by fear conditioning: Effect of atropine. Journal of Neurophysiology 90 3 (2003) 1904-1909
26. Jimenez-Capdeville M.E., and Dykes R.W. Daily changes in the release of acetylcholine from rat primary somatosensory cortex. Brain Research 625 1 (1993) 152-158
27. 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
28. Juckel G., Hegerl U., Molnar M., Csepe V., and 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 6 (1999) 710-716
29. Kilgard M.P., and Merzenich M.M. Order-sensitive plasticity in adult primary auditory cortex. Proceedings of the National Academy of Sciences of the United States of America 99 (2002) 3205-3209
30. Kilgard M.P., and Merzenich M.M. Cortical map reorganization enabled by nucleus basalis activity. Science 279 5357 (1998) 1714-1718
31. Kilgard M.P., and Merzenich M.M. Plasticity of temporal information processing in the primary auditory cortex. Nature Neuroscience 1 8 (1998) 727-731
32. 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
33. Konorski J. Integrative activity of the brain: An interdisciplinary approach (1967), University of Chicago Press, Chicago
34. Kurosawa M., Sato A., and Sato Y. Stimulation of the nucleus basalis of Meynert increases acetylcholine release in the cerebral cortex in rats. Neuroscience Letters 98 1 (1989) 45-50
35. Lennartz R.C., and Weinberger N.M. Analysis of response systems in Pavlovian conditioning reveals rapidly versus slowly acquired conditioned responses: Support for two factors, implications for behavior and neurobiology. Psychobiology 20 2 (1992) 93-119
36. Ma X., and Suga N. Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. Journal of Neurophysiology 89 1 (2003) 90-103
37. Mackintosh N.J. The psychology of animal learning (1974), Academic Press, New York
38. Maho C., Hars B., Edeline J.-M., and Hennevin E. Conditioned changes in the basal forebrain: Relations with learning-induced cortical plasticity. Psychobiology 23 1 (1995) 10-25
39. Manunta Y., and Edeline J.-M. Effects of noradrenaline on frequency tuning of rat auditory cortex neurons. European Journal of Neuroscience 9 4 (1997) 833-847
40. Manunta Y., and Edeline J.-M. Effects of noradrenaline on frequency tuning of auditory cortex neurons during wakefulness and slow-wave sleep. European Journal of Neuroscience 11 6 (1999) 2134-2150
41. Martin S.J., Grimwood P.D., and Morris R.G.M. Synaptic plasticity and memory: An evaluation of the hypothesis. Annual Review of Neuroscience 23 (2000) 649-711
42. McKenna T.M., Ashe J.H., and Weinberger N.M. Cholinergic modulation of frequency receptive fields in auditory cortex: I. Frequency-specific effects of muscarinic agonists. Synapse 4 1 (1989) 30-43
43. 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
44. 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
45. 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
46. Mesulam M.M., Mufson E.J., Levey A.I., and Wainer B.H. Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. Journal of Comparative Neurology 214 2 (1983) 170-197
47. 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
48. Metherate R., and Ashe J.H. Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex. Synapse 14 2 (1993) 132-143
49. 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
50. Metherate R., Tremblay N., and Dykes R.W. Acetylcholine permits long-term enhancement of neuronal responsiveness in cat primary somatosensory cortex. Neuroscience 22 1 (1987) 75-81
51. Metherate R., and Weinberger N.M. Cholinergic modulation of responses to single tones produces tone-specific receptive field alterations in cat auditory cortex. Synapse 6 2 (1990) 133-145
52. 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
53. 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.
54. Morris J.S., Buchel C., and Dolan R.J. Parallel neural responses in amygdala subregions and sensory cortex during implicit fear conditioning. Neuroimage 13 6 Pt. 1 (2001) 1044-1052
55. Morris J.S., Friston K.J., and Dolan R.J. Experience-dependent modulation of tonotopic neural responses in human auditory cortex. Proceedings of the Royal Society B: Biological Sciences 265 1397 (1998) 649-657
56. Oh J.D., Edwards R.H., and Woolf N.J. Choline acetyltransferase mRNA plasticity with Pavlovian conditioning. Experimental Neurology 140 1 (1996) 95-99
57. Ohl F.W., and Scheich H. Differential frequency conditioning enhances spectral contrast sensitivity of units in auditory cortex (field Al) of the alert Mongolian gerbil. European Journal of Neuroscience 8 5 (1996) 1001-1017
58. Ohl F.W., and Scheich H. Learning-induced dynamic receptive field changes in primary auditory cortex of the unanaesthetized Mongolian gerbil. Journal of Comparative Physiology A: Sensory, Neural and Behavioral Physiology 181 6 (1997) 685-696
59. Ohl, F. W., Scheich, H. (2004). Fallacies in behavioral interpretation of auditory cortex plasticity. Nature Reviews Neuroscience. Published on November 20, 2004, at .
60. Olds J., and Peretz B. A motivational analysis of the reticular activating system. Electroencephalography and Clinical Neurophysiology 12 (1960) 445-454
61. Pantev, C., Dinnesen, A., Ross, B., Wollbrink, A., Knief, A. (2005). Dynamics of auditory plasticity after cochlear implantation: A longitudinal study. Cerebral cortex. Published on April 20, 2005, at .
62. Paxinos G., and Watson C. The rat brain: In stereotaxic coordinates. (3rd ed.) (1997), Academic Press, San Diego
63. Pennartz C.M. The ascending neuromodulatory systems in learning by reinforcement: Comparing computational conjectures with experimental findings. Brain Research Reviews 21 3 (1995) 219-245
64. 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
65. 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
66. Sharpless S., and Jasper H. Habituation of the arousal reaction. Brain 79 4 (1956) 655-680
67. Shaw N.A. The auditory evoked potential in the rat-a review. Progress in Neurobiology 31 1 (1988) 19-45
68. Shaw N.A. A simple technique for localizing the primary auditory cortex in the rat. Physiology and Behavior 48 1 (1990) 207-209
69. Sokolov E.N. Perception and the conditioned reflex (1958), Moscow University Press, Oxford, England
70. Stark H., and Scheich H. Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: A long-term microdialysis study of metabolites. Journal of Neurochemistry 68 2 (1997) 691-697
71. Stratton L.O., and Petrinovich L. Post-trial injections of an anti-cholinesterase drug and maze learning in two strains of rats. Psychopharmacologia 26 (1963) 47-54
72. Thiel C.M., Friston K.J., and Dolan R.J. Cholinergic modulation of experience-dependent plasticity in human auditory cortex. Neuron 35 3 (2002) 567-574
73. Tremblay N., Warren R.A., and Dykes R.W. Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. Journal of Neurophysiology 64 4 (1990) 1212-1222
74. Webster H.H., Rasmusson D.D., Dykes R.W., Schliebs R., Schober W., Bruckner G., et al. Long-term enhancement of evoked potentials in raccoon somatosensory cortex following co-activation of the nucleus basalis of Meynert complex and cutaneous receptors. Brain Research 545 1-2 (1991) 292-296
75. Weinberger N.M. Beyond neuronal excitability: Receptive field analysis reveals that association specifically modifies the representation of auditory information. In: Squire L.R., and Butters N. (Eds). Neuropsychology of Memory. 2nd ed. (1992), Guilford Press, New York 496-509
76. Weinberger N.M. Dynamic regulation of receptive fields and maps in the adult sensory cortex. Annual Review of Neuroscience 18 (1995) 129-158
77. 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
78. Weinberger, N. M. (2004a). Correcting misconceptions of tuning shifts in auditory cortex. Nature Reviews Neuroscience. Published on November 20, 2004, at .
79. Weinberger N.M. Experience-dependent response plasticity in the auditory cortex: Issues, characteristics, mechanisms and functions. In: Parks T.N., Rubel E.W., and Popper A.N. (Eds). Plasticity of the auditory system (2004), Springer-Verlag, New York 173-228
80. Weinberger N.M. Specific long-term memory traces in primary auditory cortex. Nature Reviews Neuroscience 5 4 (2004) 279-290
81. Weinberger N.M., Ashe J.H., Metherate R., McKenna T.M., Diamond D.M., Bakin J.S., et al. Neural adaptive information processing: A preliminary model of receptive field plasticity in auditory cortex during Pavlovian conditioning. In: Gabriel M.R., and Moore J. (Eds). Learning and computational neuroscience: Foundations of adaptive networks (1990), MIT Press, Cambridge, MA 91-138
82. Wester K. Habituation to electrical stimulation of the thalamus in unanaesthetized cats. Electroencephalography and Clinical Neurophysiology 30 1 (1971) 52-61
83. Wilson D.A., and Sullivan R.M. Respiratory airflow pattern at the rat's snout and an hypothesis regarding its role in olfaction. Physiology and Behavior 66 1 (1999) 41-44
84. Wilson F.A., 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
85. Winters R.W., McCabe P.M., and Schneiderman N. Functional utility and neurobiology of conditioned autonomic responses. In: Moore J.W. (Ed). A neuroscientist's guide to classical conditioning (2002), Springer-Verlag, New York 46-85