Reconceptualizing the Primary Auditory Cortex: Learning, Memory and Specific Plasticity

Since 1985, attitudes about the role of the primary auditory cortex (AI) in learning, memory, and adult plasticity have changed from a denial, or studied disinterest, to an acceptance of these roles and, presently, to a new lack of interest. From the traditional assumption that AI is only an acoustic analyzer to the prevalent belief that learning-induced plasticity serves only to facilitate sensory analysis, auditory neuroscientists are expressing (more in private than in publication) a growing boredom with cortical plasticity. One worker wondered: “How much longer must we be subjected to endless demonstrations of plasticity?” From one viewpoint, this attitude is completely understandable, because (almost) every study of plasticity finds plasticity, first for acoustic frequency and, more recently, for any other acoustic parameter that has been used as a signal for reward or punishment. If all that has been gained is the continued compilation of plasticity demonstrations, boredom would be justified. But that is not all there is to it.

[1]  Henning Scheich,et al.  Macaque monkeys discriminate pitch relationships , 2004, Cognition.

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

[3]  J. Fritz,et al.  Differential Dynamic Plasticity of A1 Receptive Fields during Multiple Spectral Tasks , 2005, The Journal of Neuroscience.

[4]  G. Ryle,et al.  心的概念 = The concept of mind , 1962 .

[5]  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.

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

[7]  G. Berntson,et al.  The decerebrate human: Associative learning , 1983, Experimental Neurology.

[8]  A E Villa,et al.  Dynamical cell assemblies in the rat auditory cortex in a reaction-time task. , 1998, Bio Systems.

[9]  R. Zatorre,et al.  Behavioral and neural correlates of perceived and imagined musical timbre , 2004, Neuropsychologia.

[10]  M. Bear,et al.  Reward Timing in the Primary Visual Cortex , 2006, Science.

[11]  R. Ilmoniemi,et al.  Superior formation of cortical memory traces for melodic patterns in musicians. , 2001, Learning & memory.

[12]  Y Sakurai,et al.  Cells in the rat auditory system have sensory-delay correlates during the performance of an auditory working memory task. , 1990, Behavioral neuroscience.

[13]  G. Gerstein,et al.  Trial-to-Trial Variability and State-Dependent Modulation of Auditory-Evoked Responses in Cortex , 1999, The Journal of Neuroscience.

[14]  N. Suga,et al.  Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  N. Weinberger Correcting misconceptions of tuning shifts in auditory cortex , 2004, Nature Reviews Neuroscience.

[16]  Navzer D. Engineer,et al.  Cortical network reorganization guided by sensory input features , 2002, Biological Cybernetics.

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

[18]  A. R. McIntosh,et al.  The Application of Structural Modeling to Metabolic Mapping of Functional Neural Systems , 1992 .

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

[20]  N. Weinberger Retuning the brain by learning, literature, and logic: Reply to Suga , 2008 .

[21]  Norman M Weinberger,et al.  Encoding of learned importance of sound by magnitude of representational area in primary auditory cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. Majkowski,et al.  Evolution of average evoked potentials in cats during conditioning before and after tegmental lesions , 1975, Physiology & Behavior.

[23]  D. Irvine,et al.  Perceptual learning on an auditory frequency discrimination task by cats: association with changes in primary auditory cortex. , 2004, Cerebral cortex.

[24]  Henning Scheich,et al.  Learning-induced plasticity in animal and human auditory cortex , 2005, Current Opinion in Neurobiology.

[25]  N. Weinberger,et al.  Learning strategy determines auditory cortical plasticity , 2008, Neurobiology of Learning and Memory.

[26]  A. R. McIntosh,et al.  Network analysis of functional auditory pathways mapped with fluorodeoxyglucose: associative effects of a tone conditioned as a Pavlovian excitor or inhibitor , 1993, Brain Research.

[27]  E R JOHN,et al.  High nervous functions: brain functions and learning. , 1961, Annual review of physiology.

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

[29]  Catherine Semal,et al.  Learning to perceive pitch differences. , 2002, The Journal of the Acoustical Society of America.

[30]  M. Andrés Learning and behavior: A contemporary synthesis , 2008 .

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

[32]  J. Buchwald,et al.  Changes in cortical and subcortical unit activity during behavioral conditioning , 1966 .

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

[34]  T. Wagner,et al.  Categorical discrimination of direction in frequency-modulated tones by Mongolian gerbils , 1998, Behavioural Brain Research.

[35]  Norman M Weinberger,et al.  Increased lipolysis and altered lipid homeostasis protect γ-synuclein – null mutant mice from diet-induced obesity , 2013 .

[36]  D. Diamond,et al.  Initial events in conditioning: Plasticity in the pupillomotor and auditory systems , 1984 .

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

[38]  N. Weinberger,et al.  Modification of auditory and somatosensory system activity during pupillary conditioning in the paralyzed cat. , 1975, Journal of neurophysiology.

[39]  N. Weinberger,et al.  Evoked potential decrements in auditory cortex. I. Discrete-trial and continual stimulation. , 1976, Electroencephalography and clinical neurophysiology.

[40]  M. Merzenich,et al.  Role of cat primary auditory cortex for sound-localization behavior. , 1984, Journal of neurophysiology.

[41]  S. S. Stevens,et al.  Learning, motivation, and emotion , 2002 .

[42]  N. Weinberger,et al.  Neural correlates of asymptotic avoidance and classical conditioned leg felxion. , 1973, Experimental neurology.

[43]  F. Gonzalez-Lima,et al.  Network model of fear extinction and renewal functional pathways , 2007, Neuroscience.

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

[45]  I. Tetko,et al.  Spatiotemporal activity patterns of rat cortical neurons predict responses in a conditioned task. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[46]  M. Sams,et al.  Primary auditory cortex activation by visual speech: an fMRI study at 3 T , 2005, Neuroreport.

[47]  Gerald M. Edelman,et al.  Auditory function : neurobiological bases of hearing , 1988 .

[48]  D. Diamond,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, Behavioral neuroscience.

[49]  Norman M. Weinberger,et al.  Experience-Dependent Response Plasticity in the Auditory Cortex: Issues, Characteristics, Mechanisms, and Functions , 2004 .

[50]  Central Auditory System , 1993 .

[51]  N. Weinberger Auditory associative memory and representational plasticity in the primary auditory cortex , 2007, Hearing Research.

[52]  F. Morrell,et al.  Electrophysiological contributions to the neural basis of learning. , 1961, Physiological reviews.

[53]  A. McIntosh,et al.  Functional network interactions between parallel auditory pathways during Pavlovian conditioned inhibition , 1995, Brain Research.

[54]  J. Fritz,et al.  Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex , 2003, Nature Neuroscience.

[55]  T. Kuhn,et al.  The Structure of Scientific Revolutions. , 1964 .

[56]  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.

[57]  N. Schneiderman,et al.  Auditory cortex lesions prevent the extinction of Pavlovian differential heart rate conditioning to tonal stimuli in rabbits , 1989, Brain Research.

[58]  Amy Poremba,et al.  Metabolic Effects of Blocking Tone Conditioning on the Rat Auditory System , 1997, Neurobiology of Learning and Memory.

[59]  F. Gonzalez-Lima,et al.  Associative effects of Pavlovian differential inhibition of behaviour , 2001, The European journal of neuroscience.

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

[61]  J. T. Marsh,et al.  Amplitude changes in evoked auditory potentials during habituation and conditioning. , 1961, Electroencephalography and clinical neurophysiology.

[62]  Norman M. Weinberger,et al.  Learning-Induced Physiological Memory in Adult Primary Auditory Cortex: Receptive Field Plasticity, Model, and Mechanisms , 1998, Audiology and Neurotology.

[63]  J. Allman,et al.  The Anterior Cingulate Cortex , 2001, Annals of the New York Academy of Sciences.

[64]  N. Schneiderman,et al.  Role of auditory cortex in the acquisition of differential heart rate conditioning , 1988, Physiology & Behavior.

[65]  A. Halpern,et al.  Cerebral Substrates of Musical Imagery , 2001, Annals of the New York Academy of Sciences.

[66]  J. Edeline The thalamo-cortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems , 2003, Experimental Brain Research.

[67]  R. Zatorre,et al.  When that tune runs through your head: a PET investigation of auditory imagery for familiar melodies. , 1999, Cerebral cortex.

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

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

[70]  L. Dicara,et al.  Classical conditioning and instrumental learning of cardiac and gastrointestinal responses following removal of neocortex in the rat. , 1970, Journal of comparative and physiological psychology.

[71]  M. Domjan The principles of learning and behavior , 1982 .

[72]  Y. Sakurai Auditory working and reference memory can be tested in a single situation of stimuli for the rat , 1992, Behavioural Brain Research.

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

[74]  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.

[75]  F Gonzalez-Lima,et al.  Mapping Pavlovian conditioning effects on the brain: blocking, contiguity, and excitatory effects. , 2001, Journal of neurophysiology.

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

[77]  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.

[78]  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, Behavioral neuroscience.

[79]  Michael M Merzenich,et al.  Perceptual Learning Directs Auditory Cortical Map Reorganization through Top-Down Influences , 2006, The Journal of Neuroscience.

[80]  F. Gonzalez-Lima,et al.  Neural substrates for long-term habituation of the acoustic startle reflex in rats: A 2-deoxyglucose study , 1989, Neuroscience Letters.

[81]  D. P. Phillips,et al.  Central auditory onset responses, and temporal asymmetries in auditory perception , 2002, Hearing Research.

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

[83]  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.

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

[85]  Lutz Jäncke,et al.  Electrical brain imaging reveals spatio-temporal dynamics of timbre perception in humans , 2006, NeuroImage.

[86]  Douglas W. Barrett,et al.  Maturation of Extinction Behavior in Infant Rats: Large-Scale Regional Interactions with Medial Prefrontal Cortex, Orbitofrontal Cortex, and Anterior Cingulate Cortex , 2001, The Journal of Neuroscience.

[87]  F. Ohl,et al.  Fallacies in behavioural interpretation of auditory cortex plasticity , 2004, Nature Reviews Neuroscience.

[88]  G. Durup,et al.  I. L'électrencéphalogramme de l'homme. Observations psycho-physiologiques relatives à l'action des stimuli visuels et auditifs , 1935 .

[89]  H. Jasper,et al.  Habituation of the arousal reaction. , 1956, Brain : a journal of neurology.

[90]  N. Weinberger 3.11 Cortical Plasticity in Associative Learning and Memory , 2008 .

[91]  D. Diamond,et al.  Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response: II. Secondary field (AII). , 1984, Behavioral neuroscience.

[92]  N. Suga,et al.  Development of reorganization of the auditory cortex caused by fear conditioning: effect of atropine. , 2003, Journal of neurophysiology.

[93]  Sanjay S. P. Magavi,et al.  Associative learning shapes the neural code for stimulus magnitude in primary auditory cortex , 2004 .

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

[95]  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.

[96]  A. Lima-de-faria Change of pattern , 2003 .

[97]  R. Mark,et al.  Acoustically evoked potentials in the rat during conditioning. , 1967, Journal of neurophysiology.

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

[99]  H. Scheich,et al.  Multisensory processing via early cortical stages: Connections of the primary auditory cortical field with other sensory systems , 2006, Neuroscience.

[100]  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.

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

[102]  V. N. Dumenko,et al.  Spontaneous activity of auditory cortical neurons of waking cats at rest and during defensive conditioning , 2005, Neurophysiology.

[103]  Alan R. Palmer,et al.  The Oxford Handbook of Auditory Science: The Auditory Brain , 2010 .

[104]  C. Woody,et al.  Activity and excitability to electrical current of cortical auditory receptive neurons of awake cats as affected by stimulus association. , 1976, Journal of neurophysiology.

[105]  Douglas W. Barrett,et al.  Metabolic mapping of brain regions associated with behavioral extinction in preweanling rats , 2001, Brain Research.

[106]  Douglas W. Barrett,et al.  Metabolic Mapping of Mouse Brain Activity after Extinction of a Conditioned Emotional Response , 2003, The Journal of Neuroscience.

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

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

[109]  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.

[110]  F. Gonzalez-Lima,et al.  Learning-related activation in the auditory system of the rat produced by long-term habituation: a 2-deoxyglucose study , 1989, Brain Research.

[111]  G. J. Thomas Neurophysiology of learning. , 1962, Annual Review of Psychology.

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

[113]  J. Fritz,et al.  Active listening: Task-dependent plasticity of spectrotemporal receptive fields in primary auditory cortex , 2005, Hearing Research.

[114]  Yoshio Sakurai,et al.  The search for cell assemblies in the working brain , 1998, Behavioural Brain Research.

[115]  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.

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

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

[118]  B. Schwartz Psychology of Learning and Behavior , 1978 .

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

[120]  Christoph E. Schreiner,et al.  Reward-dependent plasticity in the primary auditory cortex of adult monkeys trained to discriminate temporally modulated signals , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[122]  David J. M. Kraemer,et al.  Musical imagery: Sound of silence activates auditory cortex , 2005, Nature.

[123]  Norman M. Weinberger,et al.  Remodeling the cortex in memory: Increased use of a learning strategy increases the representational area of relevant acoustic cues , 2010, Neurobiology of Learning and Memory.

[124]  Norman M. Weinberger,et al.  Dynamic Modulation of the Auditory System by Associative Learning , 1988 .

[125]  J. Saunders,et al.  Effects of appetitive drive on evoked potentials in cochlear nucleus and auditory cortex in cats. , 1969, Journal of comparative and physiological psychology.

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

[127]  Joseph E LeDoux,et al.  Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[128]  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.

[129]  J. D. McGaugh,et al.  Inactivation of Hippocampus or Caudate Nucleus with Lidocaine Differentially Affects Expression of Place and Response Learning , 1996, Neurobiology of Learning and Memory.

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

[131]  Frank Puga,et al.  Functional networks underlying latent inhibition learning in the mouse brain , 2007, NeuroImage.

[132]  Nobuo Suga,et al.  Multiparametric corticofugal modulation and plasticity in the auditory system , 2003, Nature Reviews Neuroscience.

[133]  Robert J. Zatorre,et al.  Mental Concerts: Musical Imagery and Auditory Cortex , 2005, Neuron.

[134]  A. Campbell Histological Studies on the Localisation of Cerebral Function , 2009 .

[135]  A Poremba,et al.  Classical conditioning modifies cytochrome oxidase activity in the auditory system , 1998, The European journal of neuroscience.

[136]  R B Masterton,et al.  Central auditory system. , 1993, ORL; journal for oto-rhino-laryngology and its related specialties.

[137]  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.

[138]  John H. Casseday,et al.  Behavioral Studies of Auditory Discrimination: Central Nervous System , 1975 .

[139]  Richard F. Thompson,et al.  Long-term storage of an associative memory trace in the cerebellum. , 2005, Behavioral neuroscience.

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

[141]  Norman M. Weinberger,et al.  Learning strategy trumps motivational level in determining learning-induced auditory cortical plasticity , 2010, Neurobiology of Learning and Memory.

[142]  N. Weinberger Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. , 2007, Learning & memory.

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

[144]  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.

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

[146]  W. Freeman,et al.  Change in pattern of ongoing cortical activity with auditory category learning , 2001, Nature.

[147]  D. Moore,et al.  Early and rapid perceptual learning , 2004, Nature Neuroscience.

[148]  Edward F Chang,et al.  Temporal plasticity in the primary auditory cortex induced by operant perceptual learning , 2004, Nature Neuroscience.