Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex

We investigated the hypothesis that task performance can rapidly and adaptively reshape cortical receptive field properties in accord with specific task demands and salient sensory cues. We recorded neuronal responses in the primary auditory cortex of behaving ferrets that were trained to detect a target tone of any frequency. Cortical plasticity was quantified by measuring focal changes in each cell's spectrotemporal response field (STRF) in a series of passive and active behavioral conditions. STRF measurements were made simultaneously with task performance, providing multiple snapshots of the dynamic STRF during ongoing behavior. Attending to a specific target frequency during the detection task consistently induced localized facilitative changes in STRF shape, which were swift in onset. Such modulatory changes may enhance overall cortical responsiveness to the target tone and increase the likelihood of 'capturing' the attended target during the detection task. Some receptive field changes persisted for hours after the task was over and hence may contribute to long-term sensory memory.

[1]  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 .

[2]  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.

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

[4]  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.

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

[6]  S. Shamma,et al.  Organization of response areas in ferret primary auditory cortex. , 1993, Journal of neurophysiology.

[7]  C. Gilbert,et al.  Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex , 1995, Nature.

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

[9]  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.

[10]  Jane S. Paulsen Memory in the Cerebral Cortex: An Empirical Approach to Neural Networks in the Human and Nonhuman Primate , 1996 .

[11]  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.

[12]  J. Fuster Memory in the cerebral cortex : an empirical approach to neural networks in the human and nonhuman primate , 1996 .

[13]  S. Shamma,et al.  Analysis of dynamic spectra in ferret primary auditory cortex. I. Characteristics of single-unit responses to moving ripple spectra. , 1996, Journal of neurophysiology.

[14]  G. W. Huntley,et al.  Correlation between patterns of horizontal connectivity and the extend of short-term representational plasticity in rat motor cortex. , 1997, Cerebral cortex.

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

[16]  R. Metherate,et al.  Synaptic mechanisms in auditory cortex function. , 1998, Frontiers in bioscience : a journal and virtual library.

[17]  M. Hallett,et al.  Rapid plasticity of human cortical movement representation induced by practice. , 1998, Journal of neurophysiology.

[18]  J. Donoghue,et al.  Strengthening of horizontal cortical connections following skill learning , 1998, Nature Neuroscience.

[19]  M. Kilgard,et al.  Plasticity of temporal information processing in the primary auditory cortex , 1998, Nature Neuroscience.

[20]  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.

[21]  B. Connors,et al.  Sensory experience modifies the short-term dynamics of neocortical synapses , 1999, Nature.

[22]  S. Wise,et al.  Mechanisms of use-dependent plasticity in the human motor cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  E. Bizzi,et al.  Cortical correlates of learning in monkeys adapting to a new dynamical environment. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Munoz,et al.  t Immediate Neural Plasticity Shapes Motor Performance , 2000, The Journal of Neuroscience.

[25]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

[26]  L. Mannucci,et al.  Chemical Stimulation of Synaptosomes Modulates α-Ca2+/Calmodulin-Dependent Protein Kinase II mRNA Association to Polysomes , 2000, The Journal of Neuroscience.

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

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

[29]  S A Shamma,et al.  Spectro-temporal response field characterization with dynamic ripples in ferret primary auditory cortex. , 2001, Journal of neurophysiology.

[30]  N. Suga,et al.  Plasticity of bat's central auditory system evoked by focal electric stimulation of auditory and/or somatosensory cortices. , 2001, Journal of neurophysiology.

[31]  C. Gilbert,et al.  Learning to see: experience and attention in primary visual cortex , 2001, Nature Neuroscience.

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

[33]  C. Gilbert,et al.  The Neural Basis of Perceptual Learning , 2001, Neuron.

[34]  Mathew E. Diamond,et al.  The Cortical Distribution of Sensory Memories , 2001, Neuron.

[35]  E. Bizzi,et al.  Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field , 2001, Neuron.

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

[37]  N. Schmajuk Model Systems and the Neurobiology of Associative Learning , 2002 .

[38]  Lee M. Miller,et al.  Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. , 2002, Journal of neurophysiology.

[39]  I. Winkler,et al.  Top-down effects can modify the initially stimulus-driven auditory organization. , 2002, Brain research. Cognitive brain research.

[40]  Michael P. Kilgard,et al.  Order-sensitive plasticity in adult primary auditory cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[41]  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.

[42]  Karl J. Friston,et al.  Cholinergic Modulation of Experience-Dependent Plasticity in Human Auditory Cortex , 2002, Neuron.

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

[44]  N. Suga,et al.  Reorganization of the cochleotopic map in the bat's auditory system by inhibition , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[45]  I. Nelken,et al.  Processing of low-probability sounds by cortical neurons , 2003, Nature Neuroscience.

[46]  N. Suga,et al.  Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. , 2003, Journal of neurophysiology.

[47]  Ankoor S. Shah,et al.  Auditory Cortical Neurons Respond to Somatosensory Stimulation , 2003, The Journal of Neuroscience.

[48]  Jonathan Z. Simon,et al.  Robust Spectrotemporal Reverse Correlation for the Auditory System: Optimizing Stimulus Design , 2000, Journal of Computational Neuroscience.

[49]  E. Bizzi,et al.  Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamic environment. , 2004, Journal of neurophysiology.

[50]  George L. Gerstein,et al.  Reorganization in the auditory cortex of the rat induced by intracortical microstimulation: a multiple single-unit study , 1996, Experimental Brain Research.