Learning-Induced Receptive Field Plasticity in the Primary Auditory Cortex

Abstract Primary sensory cortex in the adult is modified by learning. The primary auditory cortex is retuned when a tone is paired with a behaviorally relevant reinforcer. Frequency receptive fields are shifted toward or to the frequency of the signal stimulus, yielding enhanced processing and representation of important frequencies. Receptive field plasticity constitutes “physiological memory” because, like much memory, it is associative, highly specific, rapidly-induced, and retained indefinitely, at least for months. The basal forebrain cholinergic system may be a substrate because its paired activation is sufficient to induce receptive field plasticity in the absence of actual behavioral learning experiences.

[1]  D. Diamond,et al.  Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. , 1989, Behavioral neuroscience.

[2]  J. Coyle,et al.  Evidence for a cholinergic projection to neocortex from neurons in basal forebrain. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Henning Scheich,et al.  Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. II. Auditory cortex plasticity , 1986, Behavioural Brain Research.

[4]  J. Edeline,et al.  Non-awaking basal forebrain stimulation enhances auditory cortex responsiveness during slow-wave sleep , 1994, Brain Research.

[5]  B. Schreurs,et al.  A functional anatomical study of associative learning in humans. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[6]  N. Weinberger,et al.  Analysis of response systems in Pavlovian conditioning reveals rapidly versus slowly acquired conditioned responses: Support for two factors, implications for behavior and neurobiology , 1992, Psychobiology.

[7]  J. Edeline,et al.  Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat , 1993, Neuroscience.

[8]  Norman M. Weinberger,et al.  Classical conditioning rapidly induces specific changes in frequency receptive fields of single neurons in secondary and ventral ectosylvian auditory cortical fields , 1986, Brain Research.

[9]  J. Edeline,et al.  Rapid development of learning-induced receptive field plasticity in the auditory cortex. , 1993, Behavioral neuroscience.

[10]  D. Diamond,et al.  Physiological plasticity in auditory cortex: Rapid induction by learning , 1987, Progress in Neurobiology.

[11]  P. Kelly,et al.  Regional decreases of cortical choline acetyltransferase after lesions of the septal area and in the area of nucleus basalis magnocellularis , 1982, Neuroscience.

[12]  Y Sakurai,et al.  Involvement of auditory cortical and hippocampal neurons in auditory working memory and reference memory in the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  N. Weinberger Dynamic regulation of receptive fields and maps in the adult sensory cortex. , 1995, Annual Review of Neuroscience.

[14]  Norman M. Weinberger,et al.  Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig , 1990, Brain Research.

[15]  N. Weinberger,et al.  Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[16]  M. Merzenich,et al.  Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  R. Rescorla Behavioral studies of Pavlovian conditioning. , 1988, Annual review of neuroscience.

[18]  Norman M. Weinberger,et al.  Sensitization induced receptive field plasticity in the auditory cortex is independent of CS-modality , 1992, Brain Research.

[19]  N. Weinberger,et al.  Cholinergic modulation of frequency receptive fields in auditory cortex: I. Frequency‐specific effects of muscarinic agonists , 1989, Synapse.

[20]  F. Ohl,et al.  Differential Frequency Conditioning Enhances Spectral Contrast Sensitivity of Units in Auditory Cortex (Field Al) of the Alert Mongolian Gerbil , 1996, The European journal of neuroscience.

[21]  Norman M. Weinberger,et al.  Induction of receptive field plasticity in the auditory cortex of the guinea pig during instrumental avoidance conditioning. , 1996 .

[22]  J. Bakin,et al.  Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[23]  N. Mackintosh,et al.  Conditioning And Associative Learning , 1983 .

[24]  R. Metherate,et al.  Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors , 1991, Brain Research.

[25]  E. Gibson,et al.  Principles of Perceptual Learning and Development , 1973 .

[26]  R. Racine,et al.  Kindling mechanisms: Current progress on an experimental epilepsy model , 1986, Progress in Neurobiology.

[27]  N. Weinberger,et al.  A comparison of nonspecific and nictitating membrane conditioned responses: Additional support for two-factor theories , 1994, Psychobiology.

[28]  N. Weinberger,et al.  Cholinergic modulation of responses to single tones produces tone‐specific receptive field alterations in cat auditory cortex , 1990, Synapse.

[29]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[30]  Norman M. Weinberger,et al.  Retuning the brain by fear conditioning. , 1995 .

[31]  J. Edeline,et al.  Conditioned changes in the basal forebrain: Relations with learning-induced cortical plasticity , 1995, Psychobiology.

[32]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

[33]  N. Weinberger,et al.  Habituation produces frequency-specific plasticity of receptive fields in the auditory cortex. , 1991, Behavioral neuroscience.

[34]  A. Levey,et al.  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 , 1983, The Journal of comparative neurology.

[35]  Norman M. Weinberger,et al.  Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. , 1989 .

[36]  Norman M. Weinberger,et al.  Retuning auditory cortex by learning: A preliminary model , 1990 .

[37]  N. Weinberger,et al.  Cholinergic modulation of frequency receptive fields in auditory cortex: II. Frequency‐specific effects of anticholinesterases provide evidence for a modulatory action of endogenous Ach , 1989, Synapse.

[38]  J. Kaas,et al.  Receptive-field properties of deafferentated visual cortical neurons after topographic map reorganization in adult cats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  B. Kapp,et al.  Neuronal activity within the nucleus basalis and conditioned neocortical electroencephalographic activation , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  E. Boring A History of Experimental Psychology. , 1930 .

[41]  J. Edeline,et al.  Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. , 1993, Behavioral neuroscience.

[42]  E. Kehoe,et al.  Classical conditioning of the rabbit nictitating membrane response can be fast or slow: Implications for Lennartz and Weinberger’s (1992) two-factor theory , 1994, Psychobiology.

[43]  R. Metherate,et al.  Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex , 1993, Synapse.