Progressive plasticity of auditory cortex during appetitive operant conditioning

In stimulus-response-outcome learning, different regions in the cortico-basal ganglia network are progressively involved according to the stage of learning. However, the involvement of sensory cortex remains ellusive even though massive cortical projections to the striatum imply its significant role in this learning. Here we show that the global tonotopic representation in the auditory cortex changed progressively depending on the stage of training in auditory operant conditioning. At the early stage, tone-responsive areas mainly in the core cortex expanded, while both the core and belt cortices shrank at the late stage as behavior became conditioned. Taken together with previous findings, this progressive global plasticity from the core to belt cortices suggests differentiated roles in these areas: the core cortex serves as a filter to better identify auditory objects for hierarchical computation within the belt cortex, while the belt stores auditory objects and affects decision making through direct projections to limbic system and higher association cortex. Thus, the progressive plasticity in the present study reflects a shift from identification to storage of a behaviorally relevant auditory object, which is potentially associated with a habitual behavior.

[1]  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.

[2]  J. Wickens,et al.  A cellular mechanism of reward-related learning , 2001, Nature.

[3]  C. I. Connolly,et al.  Building neural representations of habits. , 1999, Science.

[4]  J. Horvitz,et al.  Conditioned incentive properties of a food-paired conditioned stimulus remain intact during dopamine receptor blockade. , 1991 .

[5]  H. Heffner,et al.  Effect of unilateral and bilateral auditory cortex lesions on the discrimination of vocalizations by Japanese macaques. , 1986, Journal of neurophysiology.

[6]  J. Eggermont,et al.  Spectrally enhanced acoustic environment disrupts frequency representation in cat auditory cortex , 2006, Nature Neuroscience.

[7]  D. Irvine,et al.  Basal Forebrain Cholinergic Input Is Not Essential for Lesion-Induced Plasticity in Mature Auditory Cortex , 2005, Neuron.

[8]  Gonzalo H. Otazu,et al.  Engaging in an auditory task suppresses responses in auditory cortex , 2009, Nature Neuroscience.

[9]  M. Merzenich,et al.  Experience-Dependent Adult Cortical Plasticity Requires Cognitive Association between Sensation and Reward , 2006, Neuron.

[10]  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.

[11]  J. Eggermont,et al.  Spatial representation of neural responses to natural and altered conspecific vocalizations in cat auditory cortex. , 2007, Journal of neurophysiology.

[12]  R. Reale,et al.  Auditory cortical field projections to the basal ganglia of the cat , 1983, Neuroscience.

[13]  Joseph E LeDoux,et al.  Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. , 1993, Cerebral cortex.

[14]  J. Kaas,et al.  Auditory processing in primate cerebral cortex , 1999, Current Opinion in Neurobiology.

[15]  J. Winer Decoding the auditory corticofugal systems , 2005, Hearing Research.

[16]  J. Horvitz Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum , 2002, Behavioural Brain Research.

[17]  Shaowen Bao,et al.  Early experience impairs perceptual discrimination , 2007, Nature Neuroscience.

[18]  H. Read,et al.  Multiparametric auditory receptive field organization across five cortical fields in the albino rat. , 2007, Journal of neurophysiology.

[19]  Kimitaka Kaga,et al.  Distributed representation of sound intensity in the rat auditory cortex , 2004, Neuroreport.

[20]  M. Leon,et al.  Conditioned tone control of brain reward behavior produces highly specific representational gain in the primary auditory cortex , 2009, Neurobiology of Learning and Memory.

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

[22]  J. Galen Buckwalter,et al.  Regional differences in the expression of corticostriatal synaptic plasticity , 2001, Neuroscience.

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

[24]  H. Yin,et al.  The role of the basal ganglia in habit formation , 2006, Nature Reviews Neuroscience.

[25]  T. Robinson,et al.  Methamphetamine‐induced structural plasticity in the dorsal striatum , 2007, The European journal of neuroscience.

[26]  Mounya Elhilali,et al.  Task Difficulty and Performance Induce Diverse Adaptive Patterns in Gain and Shape of Primary Auditory Cortical Receptive Fields , 2009, Neuron.

[27]  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.

[28]  I. Nelken,et al.  Neurons and Objects: The Case of Auditory Cortex , 2008, Front. Neurosci..

[29]  Sabrina M. Tom,et al.  The Neural Correlates of Motor Skill Automaticity , 2005, The Journal of Neuroscience.

[30]  Ranulfo Romo,et al.  Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex , 2009, Proceedings of the National Academy of Sciences.

[31]  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.

[32]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

[33]  R. Passingham,et al.  The Time Course of Changes during Motor Sequence Learning: A Whole-Brain fMRI Study , 1998, NeuroImage.

[34]  Anne K. Churchland,et al.  Neural correlates of instrumental learning in primary auditory cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  W. D. Neff,et al.  Role of auditory cortex in discrimination of changes in frequency. , 1957, Journal of neurophysiology.

[36]  H. Scheich,et al.  Nonauditory Events of a Behavioral Procedure Activate Auditory Cortex of Highly Trained Monkeys , 2005, The Journal of Neuroscience.

[37]  Michael Davis,et al.  Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear- potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  J. Partridge,et al.  Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. , 2000, Journal of neurophysiology.

[39]  Joseph E LeDoux,et al.  Bilateral destruction of neocortical and perirhinal projection targets of the acoustic thalamus does not disrupt auditory fear conditioning , 1992, Neuroscience Letters.

[40]  Kimitaka Kaga,et al.  Interfield differences in intensity and frequency representation of evoked potentials in rat auditory cortex , 2005, Hearing Research.

[41]  Rui M. Costa,et al.  Rapid Alterations in Corticostriatal Ensemble Coordination during Acute Dopamine-Dependent Motor Dysfunction , 2006, Neuron.

[42]  Nobuo Suga,et al.  Specific and Nonspecific Plasticity of the Primary Auditory Cortex Elicited by Thalamic Auditory Neurons , 2009, The Journal of Neuroscience.

[43]  J. Horikawa,et al.  Tonotopic Representation in the Rat Auditory Cortex , 1988 .

[44]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[45]  M. West,et al.  Loss of Lever Press-Related Firing of Rat Striatal Forelimb Neurons after Repeated Sessions in a Lever Pressing Task , 1997, The Journal of Neuroscience.

[46]  Johannes C. Dahmen,et al.  Learning to hear: plasticity of auditory cortical processing , 2007, Current Opinion in Neurobiology.

[47]  O. Hikosaka,et al.  Two types of dopamine neuron distinctly convey positive and negative motivational signals , 2009, Nature.

[48]  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.

[49]  J. Horvitz,et al.  Extended Habit Training Reduces Dopamine Mediation of Appetitive Response Expression , 2005, The Journal of Neuroscience.

[50]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[51]  H Scheich,et al.  Bilateral ablation of auditory cortex in Mongolian gerbil affects discrimination of frequency modulated tones but not of pure tones. , 1999, Learning & memory.

[52]  John M. Ennis,et al.  A neurobiological theory of automaticity in perceptual categorization. , 2007, Psychological review.

[53]  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.

[54]  D. Margoliash,et al.  Neuronal populations and single cells representing learned auditory objects , 2003, Nature.

[55]  B. Hu,et al.  Distinct forms of cholinergic modulation in parallel thalamic sensory pathways , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[56]  W. Penfield,et al.  THE BRAIN'S RECORD OF AUDITORY AND VISUAL EXPERIENCE. A FINAL SUMMARY AND DISCUSSION. , 1963, Brain : a journal of neurology.

[57]  D. Pandya,et al.  Architectonic parcellation of the temporal operculum in rhesus monkey and its projection pattern , 1973, Zeitschrift für Anatomie und Entwicklungsgeschichte.