Processing of Sounds by Population Spikes in a Model of Primary Auditory Cortex

We propose a model of the primary auditory cortex (A1), in which each iso-frequency column is represented by a recurrent neural network with short-term synaptic depression. Such networks can emit Population Spikes, in which most of the neurons fire synchronously for a short time period. Different columns are interconnected in a way that reflects the tonotopic map in A1, and population spikes can propagate along the map from one column to the next, in a temporally precise manner that depends on the specific input presented to the network. The network, therefore, processes incoming sounds by precise sequences of population spikes that are embedded in a continuous asynchronous activity, with both of these response components carrying information about the inputs and interacting with each other. With these basic characteristics, the model can account for a wide range of experimental findings. We reproduce neuronal frequency tuning curves, whose width depends on the strength of the intracortical inhibitory and excitatory connections. Non-simultaneous two-tone stimuli show forward masking depending on their temporal separation, as well as on the duration of the first stimulus. The model also exhibits non-linear suppressive interactions between sub-threshold tones and broad-band noise inputs, similar to the hypersensitive locking suppression recently demonstrated in auditory cortex. We derive several predictions from the model. In particular, we predict that spontaneous activity in primary auditory cortex gates the temporally locked responses of A1 neurons to auditory stimuli. Spontaneous activity could, therefore, be a mechanism for rapid and reversible modulation of cortical processing.

[1]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[2]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[3]  B. Clopton,et al.  Unit responses in the inferior colliculus of rat to temporal auditory patterns of tone sweeps and noise bursts. , 1974, Experimental neurology.

[4]  M M Merzenich,et al.  Representation of cochlea within primary auditory cortex in the cat. , 1975, Journal of neurophysiology.

[5]  R. Britt,et al.  Synaptic events and discharge patterns of cochlear nucleus cells. II. Frequency-modulated tones. , 1976, Journal of neurophysiology.

[6]  D. P. Phillips,et al.  Separate mechanisms control spike numbers and inter-spike intervals in transient responses of cat auditory cortex neurons , 1991, Hearing Research.

[7]  D. Irvine,et al.  Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. I: Effects of variation of stimulus parameters , 1992, Hearing Research.

[8]  J. Fritz,et al.  Tonotopic and functional organization in the auditory cortex of the big brown bat, Eptesicus fuscus. , 1993, Journal of neurophysiology.

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

[10]  A. Treves.  Mean-field analysis of neuronal spike dynamics , 1993 .

[11]  J. Deuchars,et al.  Temporal and spatial properties of local circuits in neocortex , 1994, Trends in Neurosciences.

[12]  Michael B. Calford,et al.  Monaural inhibition in cat auditory cortex. , 1995, Journal of neurophysiology.

[13]  Jos J. Eggermont,et al.  Burst‐firing sharpens frequency‐tuning in primary auditory cortex , 1996, Neuroreport.

[14]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[15]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[16]  C. Schreiner,et al.  Time course of forward masking tuning curves in cat primary auditory cortex. , 1997, Journal of neurophysiology.

[17]  P. Heil,et al.  Auditory cortical onset responses revisited. I. First-spike timing. , 1997, Journal of neurophysiology.

[18]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[19]  Israel Nelken,et al.  Responses of auditory-cortex neurons to structural features of natural sounds , 1999, Nature.

[20]  J J Eggermont,et al.  The Magnitude and Phase of Temporal Modulation Transfer Functions in Cat Auditory Cortex , 1999, The Journal of Neuroscience.

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

[22]  H. Markram,et al.  t Synchrony Generation in Recurrent Networks with Frequency-Dependent Synapses , 2000, The Journal of Neuroscience.

[23]  C. Schreiner,et al.  Modular organization of frequency integration in primary auditory cortex. , 2000, Annual review of neuroscience.

[24]  P. Jen,et al.  Bicuculline application affects discharge patterns, rate–intensity functions, and frequency tuning characteristics of bat auditory cortical neurons , 2000, Hearing Research.

[25]  I. Nelken,et al.  Responses to linear and logarithmic frequency‐modulated sweeps in ferret primary auditory cortex , 2000, The European journal of neuroscience.

[26]  Susan L. Denham,et al.  CORTICAL SYNAPTIC DEPRESSION AND AUDITORY PERCEPTION , 2000 .

[27]  Israel Nelken,et al.  Relating cluster and population responses to natural sounds and tonal stimuli in cat primary auditory cortex , 2001, Hearing Research.

[28]  M. Atzori,et al.  Differential synaptic processing separates stationary from transient inputs to the auditory cortex , 2001, Nature Neuroscience.

[29]  Xiaoqin Wang,et al.  Temporal and rate representations of time-varying signals in the auditory cortex of awake primates , 2001, Nature Neuroscience.

[30]  Jian Wang,et al.  Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons , 2002, Brain Research.

[31]  I. Nelken,et al.  Responses of Neurons in Cat Primary Auditory Cortex to Bird Chirps: Effects of Temporal and Spectral Context , 2002, The Journal of Neuroscience.

[32]  Tonal response patterns of primary auditory cortex neurons in alert cats , 2002, Brain Research.

[33]  Li I. Zhang,et al.  Topography and synaptic shaping of direction selectivity in primary auditory cortex , 2003, Nature.

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

[35]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

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

[37]  M. DeWeese,et al.  Binary Spiking in Auditory Cortex , 2003, The Journal of Neuroscience.

[38]  Alon Fishbach,et al.  Neural model for physiological responses to frequency and amplitude transitions uncovers topographical order in the auditory cortex. , 2003, Journal of neurophysiology.

[39]  C. Schreiner,et al.  Thalamocortical transformation of responses to complex auditory stimuli , 2004, Experimental Brain Research.

[40]  I. Nelken.  Processing of complex stimuli and natural scenes in the auditory cortex , 2004, Current Opinion in Neurobiology.

[41]  T. Bliss,et al.  Unit analysis of hippocampal population spikes , 2004, Experimental Brain Research.

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

[43]  J. Fritz,et al.  Dynamics of Precise Spike Timing in Primary Auditory Cortex , 2004, The Journal of Neuroscience.

[44]  Misha Tsodyks,et al.  Computation by Ensemble Synchronization in Recurrent Networks with Synaptic Depression , 2002, Journal of Computational Neuroscience.

[45]  Christian K. Machens,et al.  Linearity of Cortical Receptive Fields Measured with Natural Sounds , 2004, The Journal of Neuroscience.

[46]  A. Palmer,et al.  Representation of the purr call in the guinea pig primary auditory cortex , 2005, Hearing Research.

[47]  T. Hromádka,et al.  Reliability and Representational Bandwidth in the Auditory Cortex , 2005, Neuron.

[48]  A. Zador,et al.  Synaptic Mechanisms of Forward Suppression in Rat Auditory Cortex , 2005, Neuron.

[49]  I. Nelken,et al.  Representation of Tone in Fluctuating Maskers in the Ascending Auditory System , 2005, The Journal of Neuroscience.

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

[51]  D. Bendor,et al.  The neuronal representation of pitch in primate auditory cortex , 2005, Nature.

[52]  Nancy Kopell,et al.  Network architecture, receptive fields, and neuromodulation: computational and functional implications of cholinergic modulation in primary auditory cortex. , 2006, Journal of neurophysiology.

[53]  M. DeWeese,et al.  Non-Gaussian Membrane Potential Dynamics Imply Sparse, Synchronous Activity in Auditory Cortex , 2006, The Journal of Neuroscience.

[54]  I. Nelken,et al.  Responses of neurons in primary auditory cortex (A1) to pure tones in the halothane-anesthetized cat. , 2006, Journal of neurophysiology.