Experience-Dependent Response Plasticity in the Auditory Cortex: Issues, Characteristics, Mechanisms, and Functions

The goal of this chapter is to provide a guide for understanding experience-dependent neuronal plasticity in the auditory cortex and its relation to behavior. (Unless otherwise noted, “auditory cortex” refers to the tonotopic primary auditory field, AI). It focuses on research that began in the mid-1980s concerning the question of how learning may alter the processing and representation of acoustic information in the primary auditory cortex. As used here, the term “plasticity” refers to systematic long-term (minutes to months) changes in the responses of neurons to sound as a result of experience. Plasticity at the level of altered neural responses is the result of various subcellular and molecular processes. Selected aspects of these substrates are included, particularly those relating to the cholinergic modulation of auditory cortical plasticity. Owing to lack of space, the subcortical auditory system cannot be reviewed, except as it directly pertains to mechanisms of cortical plasticity (see Birt et al. 1979; Cruickshank et al. 1992; Edeline and Weinberger 1992; Gonzalez-Lima and Scheich 1992; Hennevin et al. 1993; McKernan and Shinnick-Gallagher 1997).

[1]  Joseph E LeDoux,et al.  Differential Effects of Amygdala Lesions on Early and Late Plastic Components of Auditory Cortex Spike Trains during Fear Conditioning , 1998, The Journal of Neuroscience.

[2]  James L Olds,et al.  A motivational analysis of the reticular activating system. , 1960, Electroencephalography and clinical neurophysiology.

[3]  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.

[4]  R. Dykes,et al.  The effects of acetylcholine on response properties of cat somatosensory cortical neurons. , 1988, Journal of neurophysiology.

[5]  R. Lund,et al.  Thalamic afferents from the spinal cord and trigeminal nuclei. An experimental anatomical study in the rat. , 1967, The Journal of comparative neurology.

[6]  J. Edeline,et al.  Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex , 2004, Experimental Brain Research.

[7]  G. Pepeu,et al.  Changes in cortical acetylcholine output induced by modulation of the nucleus basalis , 1986, Brain Research Bulletin.

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

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

[10]  G. Karmos,et al.  Intracortical auditory evoked potentials during classical aversive conditioning in cats , 1988, Biological Psychology.

[11]  E. J. Green,et al.  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 , 1995, Brain Research.

[12]  T. Robbins,et al.  Central cholinergic systems and cognition. , 1997, Annual review of psychology.

[13]  D. Sparks,et al.  Unitary responses and discrimination learning in the squirrel monkey: The globus pallidus , 1968 .

[14]  T. Hattori,et al.  Separate neuronal populations of the rat globus pallidus projecting to the subthalamic nucleus, auditory cortex and pedunculopontine tegmental area , 1992, Neuroscience.

[15]  N Suga,et al.  Effects of acetylcholine and atropine on plasticity of central auditory neurons caused by conditioning in bats. , 2001, Journal of neurophysiology.

[16]  Karl J. Friston,et al.  Experience–dependent modulation of tonotopic neural responses in human auditory cortex , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  A. Vazdarjanova Does the basolateral amygdala store memories for emotional events? , 2000, Trends in Neurosciences.

[18]  M. Kurosawa,et al.  Stimulation of the nucleus basalis of Meynert increases acetylcholine release in the cerebral cortex in rats , 1989, Neuroscience Letters.

[19]  Norman M. Weinberger,et al.  Memory codes: New concept for old problem. , 2001 .

[20]  C. Schreiner,et al.  Sensory input directs spatial and temporal plasticity in primary auditory cortex. , 2001, Journal of neurophysiology.

[21]  C. Maho,et al.  Appetitive conditioning-induced plasticity is expressed during paradoxical sleep in the medial geniculate, but not in the lateral amygdala. , 2002, Behavioral neuroscience.

[22]  M. Miranda,et al.  Differential effects of 192IgG-saporin and NMDA-induced lesions into the basal forebrain on cholinergic activity and taste aversion memory formation , 1999, Brain Research.

[23]  J. Edeline,et al.  Discriminative long-term retention of rapidly induced multiunit changes in the hippocampus, medial geniculate and auditory cortex , 1990, Behavioural Brain Research.

[24]  C. H. Vanderwolf,et al.  The behavioral neurobiology of learning and memory: A conceptual reorientation , 1994, Brain Research Reviews.

[25]  D. Rasmusson The role of acetylcholine in cortical synaptic plasticity , 2000, Behavioural Brain Research.

[26]  N. Weinberger,et al.  Receptive-field plasticity in the adult auditory cortex induced by Hebbian covariance , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  K. Wester Habituation to electrical stimulation of the thalamus in unanaesthetized cats. , 1971, Electroencephalography and clinical neurophysiology.

[28]  J. W. Rudy,et al.  Scopolamine Administered before and after Training Impairs both Contextual and Auditory-Cue Fear Conditioning , 1996, Neurobiology of Learning and Memory.

[29]  N. Weinberger,et al.  Acoustic frequency tuning of neurons in the basal forebrain of the waking guinea pig , 1998, Brain Research.

[30]  D. Potter,et al.  Scopolamine impairs memory performance and reduces frontal but not parietal visual P3 amplitude , 2000, Biological Psychology.

[31]  N. Woolf,et al.  Choline Acetyltransferase mRNA Plasticity with Pavlovian Conditioning , 1996, Experimental Neurology.

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

[33]  N. Mackintosh The psychology of animal learning , 1974 .

[34]  D. Rasmusson,et al.  Frequency-dependent increase in cortical acetylcholine release evoked by stimulation of the nucleus basalis magnocellularis in the rat , 1992, Brain Research.

[35]  E. Ahissar,et al.  Differential Effects of Acetylcholine on Neuronal Activity and Interactions in the Auditory Cortex of the Guinea‐pig , 1997, The European journal of neuroscience.

[36]  J. Edeline,et al.  Stimulation at a site of auditory-somatosensory convergence in the medial geniculate nucleus is an effective unconditioned stimulus for fear conditioning. , 1992, Behavioral neuroscience.

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

[38]  H. Fibiger,et al.  The nucleus basalis magnocellularis: The origin of a cholinergic projection to the neocortex of the rat , 1980, Neuroscience.

[39]  H. Scheich,et al.  Learning-induced dynamic receptive field changes in primary auditory cortex of the unanaesthetized Mongolian gerbil , 1997, Journal of Comparative Physiology A.

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

[41]  W. Wickelgren Effect of state of arousal on click-evoked responses in cats. , 1968, Journal of neurophysiology.

[42]  A. Sillito,et al.  Cholinergic modulation of the functional organization of the cat visual cortex , 1983, Brain Research.

[43]  M. Delong,et al.  Nucleus basalis of Meynert neuronal activity during a delayed response task in monkey , 1986, Brain Research.

[44]  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.

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

[46]  Gary L. Wenk,et al.  The Nucleus Basalis Magnocellularis Cholinergic System: One Hundred Years of Progress , 1997, Neurobiology of Learning and Memory.

[47]  Norman M Weinberger,et al.  Long-Term Consolidation and Retention of Learning-Induced Tuning Plasticity in the Auditory Cortex of the Guinea Pig , 2002, Neurobiology of Learning and Memory.

[48]  N Suga,et al.  Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[49]  D. C. Teas,et al.  EVOKED RESPONSES FROM THE AUDITORY CERTEX. , 1964, Experimental neurology.

[50]  J. D. McGaugh,et al.  The neurobiology of learning and memory: some reminders to remember , 2001, Trends in Neurosciences.

[51]  R. Miettinen,et al.  Loss of cholinergic neurons in the nucleus basalis induces neocortical electroencephalographic and passive avoidance deficits , 1992, Neuroscience.

[52]  Joseph E LeDoux,et al.  Fear Conditioning Enhances Different Temporal Components of Tone-Evoked Spike Trains in Auditory Cortex and Lateral Amygdala , 1997, Neuron.

[53]  N. Weinberger,et al.  Differential plasticity of morphologically distinct neuron populations in the medical geniculate body of the cat during classical conditioning. , 1978, Behavioral biology.

[54]  K. Murata,et al.  THE ACTIVITY OF SINGLE CORTICAL NEURONES OF UNRESTRAINED CATS DURING SLEEP AND WAKEFULNESS. , 1963, Archives italiennes de biologie.

[55]  Heterosynaptic long-term facilitation of sensory-evoked responses in the auditory cortex by stimulation of the magnocellular medial geniculate body in guinea pigs. , 1995, Behavioral neuroscience.

[56]  A. Tunturi AUDIO FREQUENCY LOCALIZATION IN THE ACOUSTIC CORTEX OF THE DOG , 1944 .

[57]  J. Edeline,et al.  Thalamic short-term plasticity in the auditory system: associative returning of receptive fields in the ventral medial geniculate body. , 1991, Behavioral neuroscience.

[58]  C. Saper Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus , 1984, The Journal of comparative neurology.

[59]  N. Weinberger,et al.  Epinephrine enables Pavlovian fear conditioning under anesthesia. , 1984, Science.

[60]  C. Pennartz The ascending neuromodulatory systems in learning by reinforcement: comparing computational conjectures with experimental findings , 1995, Brain Research Reviews.

[61]  R. Dykes,et al.  Acetylcholine release in rat frontal and somatosensory cortex is enhanced during tactile discrimination learning , 1997, Psychobiology.

[62]  M. Miranda,et al.  Reversible inactivation of the nucleus basalis magnocellularis induces disruption of cortical acetylcholine release and acquisition, but not retrieval, of aversive memories. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[63]  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.

[64]  M. Merzenich,et al.  Cortical plasticity and memory , 1993, Current Opinion in Neurobiology.

[65]  H. Scheich,et al.  Dopaminergic and Serotonergic Neurotransmission Systems Are Differentially Involved in Auditory Cortex Learning: A Long‐Term Microdialysis Study of Metabolites , 1997, Journal of neurochemistry.

[66]  R. Russell,et al.  Accelerating behavioral recovery after cortical lesions. II. In vivo evidence for cholinergic involvement. , 1994, Behavioral and neural biology.

[67]  A. Duque,et al.  EEG correlation of the discharge properties of identified neurons in the basal forebrain. , 2000, Journal of neurophysiology.

[68]  Norman M. Weinberger,et al.  Long-Term Frequency Tuning of Local Field Potentials in the Auditory Cortex of the Waking Guinea Pig , 2001, Journal of the Association for Research in Otolaryngology.

[69]  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.

[70]  Henning Scheich,et al.  Advances in metabolic mapping techniques for brain imaging of behavioral and learning functions , 1992 .

[71]  Gastone G. Celesia,et al.  Acetylcholine released from cerebral cortex in relation to state of activation , 1966, Neurology.

[72]  Norman M. Weinberger,et al.  Rapid development of learning-induced receptive field plasticity in the auditory cortex. , 1993 .

[73]  F. Gonzalez-Lima,et al.  Classical conditioning enhances auditory 2-deoxyglucose patterns in the inferior colliculus , 1984, Neuroscience Letters.

[74]  F. Ohl,et al.  Some functions of primary auditory cortex in learning and memory formation. , 1997, Advances in neurology.

[75]  N. Weinberger,et al.  The effects of electrical stimulation of the nucleus basalis on the electroencephalogram, heart rate, and respiration. , 2002, Behavioral neuroscience.

[76]  M. Ahissar,et al.  Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. , 1992, Science.

[77]  E Ahissar,et al.  Possible involvement of neuromodulatory systems in cortical Hebbian-like plasticity , 1996, Journal of Physiology-Paris.

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

[79]  Donald Robertson,et al.  Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness , 1989, The Journal of comparative neurology.

[80]  R. Dykes,et al.  Mechanisms controlling neuronal plasticity in somatosensory cortex. , 1997, Canadian journal of physiology and pharmacology.

[81]  M. Dimyan,et al.  Basal forebrain stimulation induces discriminative receptive field plasticity in the auditory cortex. , 1999, Behavioral neuroscience.

[82]  M. Merzenich,et al.  Cortical remodelling induced by activity of ventral tegmental dopamine neurons , 2001, Nature.

[83]  JOHN W. Moore,et al.  Neural Activity in the Medial Geniculate Nucleus during Auditory Trace Conditioning , 1995 .

[84]  R. Dykes,et al.  Transient and prolonged effects of acetylcholine on responsiveness of cat somatosensory cortical neurons. , 1988, Journal of neurophysiology.

[85]  D. Michaelson,et al.  M1 Muscarinic Agonist Treatment Reverses Cognitive and Cholinergic Impairments of Apolipoprotein E‐Deficient Mice , 1998, Journal of neurochemistry.

[86]  B. Hars,et al.  Learning-induced plasticity in the medial geniculate nucleus is expressed during paradoxical sleep. , 1993, Behavioral neuroscience.

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

[88]  Coding the temporal structure of sounds in auditory cortex , 2001, Nature Neuroscience.

[89]  A. Gower Enhancement by secoverine and physostigmine of retention of passive avoidance response in mice , 2004, Psychopharmacology.

[90]  Henning Scheich,et al.  Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. I. Activation of auditory nuclei , 1984, Behavioural Brain Research.

[91]  A. Karni,et al.  Learning perceptual skills: behavioral probes into adult cortical plasticity , 1997, Current Opinion in Neurobiology.

[92]  M. Jarvik,et al.  Cholinergic receptor interactions and their effects on long-term memory processing , 1981, Brain Research.

[93]  Valéria Csépe,et al.  Auditory Evoked Potentials Reflect Serotonergic Neuronal Activity—A Study in Behaving Cats Administered Drugs Acting on 5-HT1A Autoreceptors in the Dorsal Raphe Nucleus , 1999, Neuropsychopharmacology.

[94]  L. Cahill,et al.  The basolateral amygdala complex is involved with, but is not necessary for, rapid acquisition of Pavlovian ‘fear conditioning’ , 2000, The European journal of neuroscience.

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

[96]  M. McKERNAN,et al.  Fear conditioning induces a lasting potentiation of synaptic currents in vitro , 1997, Nature.

[97]  W. Wickelgren Effect of acoustic habituation on click-evoked responses in cats. , 1968, Journal of neurophysiology.

[98]  P. Maldonado,et al.  Neuronal assembly dynamics in the rat auditory cortex during reorganization induced by intracortical microstimulation , 1996, Experimental Brain Research.

[99]  R. Dykes,et al.  Changes in cortical acetylcholine release in the rat during day and night: differences between motor and sensory areas , 1996, Neuroscience.

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

[101]  N. Weinberger,et al.  Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity , 2001, Neuroreport.

[102]  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.

[103]  N. Weinberger,et al.  Long term potentiation in the magnocellular medial geniculate nucleus of the anesthetized cat , 1983, Brain Research.

[104]  J. Bakin,et al.  Neural adaptive information processing: A preliminary model of receptive field plasticity in auditory cortex during Pavlovian conditioning , 1990 .

[105]  Henning Scheich,et al.  Auditory cortex: comparative aspects of maps and plasticity , 1991, Current Opinion in Neurobiology.

[106]  Robert M. Young,et al.  Mind, Brain and Adaptation in the Nineteenth Century , 1994 .

[107]  D. Birt,et al.  Separation of associative from non-associative short latency changes in medial geniculate and inferior colliculus during differential conditioning and reversal in rats , 1979, Brain Research.

[108]  J. Edeline Learning-induced physiological plasticity in the thalamo-cortical sensory systems: a critical evaluation of receptive field plasticity, map changes and their potential mechanisms , 1999, Progress in Neurobiology.

[109]  Larry L. Butcher,et al.  Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: A combined fluorescent tracer and acetylcholinesterase analysis , 1982, Brain Research Bulletin.

[110]  Russell L. Martin,et al.  Specificity of perceptual learning in a frequency discrimination task. , 2000, The Journal of the Acoustical Society of America.

[111]  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.

[112]  J. Wepsic,et al.  Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus. , 1966, Experimental neurology.

[113]  J. Edeline,et al.  Effects of Noradrenaline on Frequency Tuning of Rat Auditory Cortex Neurons , 1997, The European journal of neuroscience.

[114]  N. Weinberger,et al.  CS-specific gamma, theta, and alpha EEG activity detected in stimulus generalization following induction of behavioral memory by stimulation of the nucleus basalis , 2003, Neurobiology of Learning and Memory.

[115]  J. Edeline,et al.  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. , 1992, Behavioral neuroscience.

[116]  G L Gerstein,et al.  Daily variation and appetitive conditioning‐induced plasticity of auditory cortex receptive fields , 2001, The European journal of neuroscience.

[117]  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.

[118]  M. Mesulam,et al.  Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6) , 1983, Neuroscience.

[119]  F. Gonzalez-Lima,et al.  Brain Imaging of Auditory Learning Functions in Rats: Studies with Fluorodeoxyglucose Autoradiography and Cytochrome Oxidase Histochemistry , 1992 .

[120]  G. Di Chiara,et al.  Cocaine and Amphetamine Increase Extracellular Dopamine in the Nucleus Accumbens of Mice Lacking the Dopamine Transporter Gene , 2001, The Journal of Neuroscience.

[121]  L. C. Oatman Role of visual attention on auditory evoked potentials in unanesthetized cats. , 1971, Experimental neurology.

[122]  G. Berlucchi,et al.  CHANGES IN THE AUDITORY INPUT DURING AROUSAL IN CATS WITH TENOTOMIZED MIDDLE EAR MUSCLES. , 1964, Archives italiennes de biologie.

[123]  A. Starr,et al.  Modulation of auditory cortex unit activity during the performance of a conditioned response , 1978, Experimental Neurology.

[124]  Selene Cansino,et al.  Neuromagnetic fields reveal cortical plasticity when learning an auditory discrimination task , 1997, Brain Research.

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

[126]  D. Blozovski,et al.  Effects of antimuscarinic cholinergic drugs injected systemically or into the hippocampo-entorhinal area upon passive avoidance learning in young rats , 2004, Psychopharmacology.

[127]  L. Stratton,et al.  Post-trial injections of an anti-cholinesterase drug and maze learning in two strains of rats , 1963, Psychopharmacologia.

[128]  I. Introini-Collison,et al.  Modulation of memory by post-training epinephrine: involvement of cholinergic mechanisms , 2004, Psychopharmacology.

[129]  James L. McGaugh,et al.  Posttraining Intraamygdala Infusions of Oxotremorine and Propranolol Modulate Storage of Memory for Reductions in Reward Magnitude , 1997, Neurobiology of Learning and Memory.

[130]  R. Mark,et al.  Fear and the modification of acoustically evoked potentials during conditioning. , 1967, Journal of neurophysiology.

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

[132]  N. Weinberger,et al.  Sensory system neural activity during habituation of the pupillary orienting reflex. , 1975, Behavioral biology.

[133]  N. Weinberger Specific long-term memory traces in primary auditory cortex , 2004, Nature Reviews Neuroscience.

[134]  Merav Ahissar,et al.  Hebbian-like functional plasticity in the auditory cortex of the behaving monkey , 1998, Neuropharmacology.

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

[136]  ET Rolls,et al.  Learning and memory is reflected in the responses of reinforcement- related neurons in the primate basal forebrain , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[137]  G L Gerstein,et al.  Role of mammalian auditory cortex in the perception of elementary sound properties. , 2001, Journal of neurophysiology.

[138]  Stephen Maren,et al.  The Amygdala Is Essential for the Development of Neuronal Plasticity in the Medial Geniculate Nucleus during Auditory Fear Conditioning in Rats , 2001, The Journal of Neuroscience.

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

[140]  Eric I. Knudsen,et al.  Maps versus clusters: different representations of auditory space in the midbrain and forebrain , 1999, Trends in Neurosciences.

[141]  M. Kilgard,et al.  Cortical map reorganization enabled by nucleus basalis activity. , 1998, Science.

[142]  A R McIntosh,et al.  Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. , 1997, Journal of neurophysiology.

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

[144]  N. Kraus,et al.  The time course of auditory perceptual learning: neurophysiological changes during speech‐sound training , 1998, Neuroreport.

[145]  William D. Hopkins,et al.  Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response: I. Primary field (AI). , 1984 .

[146]  Josef P. Rauschecker,et al.  Auditory cortical plasticity: a comparison with other sensory systems , 1999, Trends in Neurosciences.

[147]  M M Merzenich,et al.  Alterations in correlated activity parallel ICMS-induced representational plasticity. , 1993, Neuroreport.

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

[149]  G. Gerstein,et al.  Reorganization in awake rat auditory cortex by local microstimulation and its effect on frequency-discrimination behavior. , 2001, Journal of neurophysiology.

[150]  Joseph E LeDoux,et al.  Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli , 1986, Brain Research.

[151]  N. Weinberger,et al.  Evoked potential decrements in auditory cortex. II. Critical test for habituation. , 1976, Electroencephalography and clinical neurophysiology.

[152]  G. Pepeu,et al.  Lesions of cholinergic forebrain nuclei: Changes in avoidance behavior and scopolamine actions , 1982, Pharmacology Biochemistry and Behavior.

[153]  Henry Gluck,et al.  Defensive conditioning of electrographic arousal with delayed and differentiated auditory stimuli. , 1959, Electroencephalography and clinical neurophysiology.

[154]  M. Dimyan,et al.  Induction of long-term receptive field plasticity in the auditory cortex of the waking guinea pig by stimulation of the nucleus basalis. , 1998, Behavioral neuroscience.

[155]  M. Gabriel,et al.  Conditioning and reversal of short-latency multiple-unit responses in the rabbit medial geniculate nucleus. , 1975, Science.

[156]  M. Tanaka,et al.  Further evidence for the specific involvement of the flocculus in the vertical vestibulo-ocular reflex (VOR). , 1996, Progress in brain research.

[157]  Amy Poremba,et al.  Amygdalar Efferents Initiate Auditory Thalamic Discriminative Training-Induced Neuronal Activity , 2001, The Journal of Neuroscience.

[158]  N. Schneiderman,et al.  Changes of synaptic efficacy in the medial geniculate nucleus as a result of auditory classical conditioning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[160]  Norman M. Weinberger,et al.  Physiological Memory in Primary Auditory Cortex: Characteristics and Mechanisms , 1998, Neurobiology of Learning and Memory.

[161]  W. R. Webster,et al.  Arousal effects on cochlear potentials: investigation of a two-factor hypothesis. , 1972, Brain research.

[162]  N. Weinberger,et al.  Frequency-specific receptive field plasticity in the medial geniculate body induced by Pavlovian fear conditioning is expressed in the anesthetized brain , 1992 .

[163]  N. Kraus,et al.  Speech Sound Representation, Perception, and Plasticity: A Neurophysiologic Perspective , 1998, Audiology and Neurotology.

[164]  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.

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

[166]  Drf Irvine,et al.  INJURY‐ AND USE‐RELATED PLASTICITY IN THE PRIMARY SENSORY CORTEX OF ADULT MAMMALS: POSSIBLE RELATIONSHIP TO PERCEPTUAL LEARNING , 1996, Clinical and experimental pharmacology & physiology.

[167]  C. Gilbert,et al.  Interactions between attention, context and learning in primary visual cortex , 2000, Vision Research.

[168]  R. Galamboš,et al.  Electrophysiological correlates of a conditioned response in cats. , 1956, Science.

[169]  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.

[170]  G. Pepeu,et al.  Enhanced acetylcholine release in the hippocampus and cortex during acquisition of an operant behavior , 1996, Brain Research.

[171]  C V Palmer,et al.  The functionally and physiologically plastic adult auditory system. , 1998, The Journal of the Acoustical Society of America.

[172]  J A Deutsch,et al.  The Cholinergic Synapse and the Site of Memory , 1971, Science.

[173]  N. Weinberger,et al.  In vivo Hebbian and basal forebrain stimulation treatment in morphologically identified auditory cortical cells , 2001, Brain Research.

[174]  N. Weinberger,et al.  Induction of behavioral associative memory by stimulation of the nucleus basalis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[175]  J. Edeline,et al.  Frequency-specific cellular changes in the auditory system during acquisition and reversal of discriminative conditioning , 1990, Psychobiology.