Asynchronous inputs alter excitability, spike timing, and topography in primary auditory cortex

Correlation-based synaptic plasticity provides a potential cellular mechanism for learning and memory. Studies in the visual and somatosensory systems have shown that behavioral and surgical manipulation of sensory inputs leads to changes in cortical organization that are consistent with the operation of these learning rules. In this study, we examine how the organization of primary auditory cortex (A1) is altered by tones designed to decrease the average input correlation across the frequency map. After one month of separately pairing nucleus basalis stimulation with 2 and 14 kHz tones, a greater proportion of A1 neurons responded to frequencies below 2 kHz and above 14 kHz. Despite the expanded representation of these tones, cortical excitability was specifically reduced in the high and low frequency regions of A1, as evidenced by increased neural thresholds and decreased response strength. In contrast, in the frequency region between the two paired tones, driven rates were unaffected and spontaneous firing rate was increased. Neural response latencies were increased across the frequency map when nucleus basalis stimulation was associated with asynchronous activation of the high and low frequency regions of A1. This set of changes did not occur when pulsed noise bursts were paired with nucleus basalis stimulation. These results are consistent with earlier observations that sensory input statistics can shape cortical map organization and spike timing.

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

[2]  M. Kilgard,et al.  Spectral Features Control Temporal Plasticity in Auditory Cortex , 2001, Audiology and Neurotology.

[3]  R. Metherate,et al.  Intracortical pathways determine breadth of subthreshold frequency receptive fields in primary auditory cortex. , 2004, Journal of neurophysiology.

[4]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[5]  T. Bonhoeffer,et al.  Pairing-Induced Changes of Orientation Maps in Cat Visual Cortex , 2001, Neuron.

[6]  M. Merzenich,et al.  Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. , 1990, Journal of neurophysiology.

[7]  Y. Dan,et al.  Stimulus Timing-Dependent Plasticity in Cortical Processing of Orientation , 2001, Neuron.

[8]  M. Merzenich,et al.  Reorganization of somatosensory area 3b representations in adult owl monkeys after digital syndactyly. , 1991, Journal of neurophysiology.

[9]  G. Bi,et al.  Synaptic modification by correlated activity: Hebb's postulate revisited. , 2001, Annual review of neuroscience.

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

[11]  Li I. Zhang,et al.  A critical window for cooperation and competition among developing retinotectal synapses , 1998, Nature.

[12]  W. Singer,et al.  Reduced Synchronization in the Visual Cortex of Cats with Strabismic Amblyopia , 1994, The European journal of neuroscience.

[13]  C E Schreiner,et al.  Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  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.

[15]  G. Recanzone,et al.  Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. , 1992, Journal of neurophysiology.

[16]  D. Feldman,et al.  Timing-Based LTP and LTD at Vertical Inputs to Layer II/III Pyramidal Cells in Rat Barrel Cortex , 2000, Neuron.

[17]  M. Law,et al.  Eye-specific termination bands in tecta of three-eyed frogs. , 1978, Science.

[18]  G. Recanzone,et al.  Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. , 1992, Journal of neurophysiology.

[19]  Y. Chino,et al.  Effects of rearing kittens with convergent strabismus on development of receptive-field properties in striate cortex neurons. , 1983, Journal of neurophysiology.

[20]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[21]  D. Hubel,et al.  Binocular interaction in striate cortex of kittens reared with artificial squint. , 1965, Journal of neurophysiology.

[22]  M. Kilgard,et al.  Distributed representation of spectral and temporal information in rat primary auditory cortex , 1999, Hearing Research.

[23]  Edward F Chang,et al.  Progressive Degradation and Subsequent Refinement of Acoustic Representations in the Adult Auditory Cortex , 2003, The Journal of Neuroscience.

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

[25]  F. Ebner,et al.  An innocuous bias in whisker use in adult rats modifies receptive fields of barrel cortex neurons , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  G. Eschweiler,et al.  Temporal Integration in Visual Cortex of Cats with Surgically Induced Strabismus , 1993, The European journal of neuroscience.

[27]  G. Stent A physiological mechanism for Hebb's postulate of learning. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[28]  L. Abbott,et al.  Cortical Development and Remapping through Spike Timing-Dependent Plasticity , 2001, Neuron.

[29]  Y. Dan,et al.  Spike-timing-dependent synaptic modification induced by natural spike trains , 2002, Nature.

[30]  E. Kandel The Molecular Biology of Memory Storage: A Dialogue Between Genes and Synapses , 2001, Science.

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

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

[33]  Xiaoqin Wang,et al.  Remodelling of hand representation in adult cortex determined by timing of tactile stimulation , 1995, Nature.

[34]  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.

[35]  R. Dykes,et al.  Long-term enhancement of evoked potentials in cat somatosensory cortex produced by co-activation of the basal forebrain and cutaneous receptors , 2004, Experimental Brain Research.

[36]  M. Merzenich,et al.  Receptive fields in the body-surface map in adult cortex defined by temporally correlated inputs , 1988, Nature.

[37]  G. Bi,et al.  Distributed synaptic modification in neural networks induced by patterned stimulation , 1999, Nature.

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

[39]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

[40]  M. Gluck,et al.  Basal forebrain stimulation changes cortical sensitivities to complex sound , 2001, Neuroreport.

[41]  M. Tuszynski,et al.  Lesions of the Basal Forebrain Cholinergic System Impair Task Acquisition and Abolish Cortical Plasticity Associated with Motor Skill Learning , 2003, Neuron.

[42]  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.

[43]  M. Kilgard,et al.  Environmental enrichment improves response strength, threshold, selectivity, and latency of auditory cortex neurons. , 2004, Journal of neurophysiology.

[44]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[45]  A L Humphrey,et al.  Strobe rearing prevents the convergence of inputs with different response timings onto area 17 simple cells. , 1998, Journal of neurophysiology.

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

[47]  M. Kilgard,et al.  Background sounds contribute to spectrotemporal plasticity in primary auditory cortex , 2005, Experimental Brain Research.

[48]  Y. Chino,et al.  Effects of convergent strabismus on spatio-temporal response properties of neurons in cat area 18 , 2004, Experimental Brain Research.

[49]  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.

[50]  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.