Spike Timing, Spike Count, and Temporal Information for the Discrimination of Tactile Stimuli in the Rat Ventrobasal Complex

The aim of this work was to investigate the role of spike timing for the discrimination of tactile stimuli in the thalamic ventrobasal complex of the rat. We applied information-theoretic measures and computational experiments on neurophysiological data to test the ability of single-neuron responses to discriminate stimulus location and stimulus dynamics using either spike count (40 ms bin size) or spike timing (1 ms bin size). Our main finding is not only that spike timing provides additional information over spike count alone, but specifically that the temporal aspects of the code can be more informative than spike count in the rat ventrobasal complex. Virtually all temporal information—i.e., information exclusively related to when the spikes occur—is conveyed by first spikes, arising mostly from latency differences between the responses to different stimuli. Although the imprecision of first spikes (i.e., the jitter) is highly detrimental for the information conveyed by latency differences, jitter differences can contribute to temporal information, but only if latency differences are close to zero. We conclude that temporal information conveyed by spike timing can be higher than spike count information for the discrimination of somatosensory stimuli in the rat ventrobasal complex.

[1]  A. Canedo,et al.  GABAB receptor-mediated modulation of cutaneous input at the cuneate nucleus in anesthetized cats , 2006, Neuroscience.

[2]  J. Lisman The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme , 2005, Hippocampus.

[3]  R. D. Pinto,et al.  Reliability and precision of neural spike timing: simulation of spectrally broadband synaptic inputs , 2004, Neuroscience.

[4]  J. D. Hunter,et al.  Resonance effect for neural spike time reliability. , 1998, Journal of neurophysiology.

[5]  F. Ebner,et al.  Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. , 1999, Journal of neurophysiology.

[6]  Stefano Panzeri,et al.  Correcting for the sampling bias problem in spike train information measures. , 2007, Journal of neurophysiology.

[7]  Garrett B Stanley,et al.  Timing Precision in Population Coding of Natural Scenes in the Early Visual System , 2008, PLoS biology.

[8]  F N JONES Space-time relationships in somesthetic localization. , 1956, Science.

[9]  G. Pollak,et al.  Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons , 2005, The Journal of Neuroscience.

[10]  G A Cecchi,et al.  Noise in neurons is message dependent. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[11]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[12]  M. Castro-Alamancos,et al.  Spatiotemporal Gating of Sensory Inputs in Thalamus during Quiescent and Activated States , 2005, The Journal of Neuroscience.

[13]  Tim Gollisch,et al.  Rapid Neural Coding in the Retina with Relative Spike Latencies , 2008, Science.

[14]  Arnaud Delorme,et al.  Spike-based strategies for rapid processing , 2001, Neural Networks.

[15]  Miguel A L Nicolelis,et al.  Orbitofrontal ensemble activity monitors licking and distinguishes among natural rewards. , 2006, Journal of neurophysiology.

[16]  M. Laubach,et al.  Layer-Specific Somatosensory Cortical Activation During Active Tactile Discrimination , 2004, Science.

[17]  Jean-Luc Blanc,et al.  Coding processes involved in the cortical representation of complex tactile stimuli , 2007, Journal of Physiology-Paris.

[18]  Cyrus P. Billimoria,et al.  Neuromodulation of Spike-Timing Precision in Sensory Neurons , 2006, The Journal of Neuroscience.

[19]  Brian H Scott,et al.  Dynamic amplitude coding in the auditory cortex of awake rhesus macaques. , 2007, Journal of neurophysiology.

[20]  T. Sejnowski,et al.  Regulation of spike timing in visual cortical circuits , 2008, Nature Reviews Neuroscience.

[21]  M. Diamond,et al.  Population Coding of Stimulus Location in Rat Somatosensory Cortex , 2001, Neuron.

[22]  Eric D Young,et al.  Spike-Timing Codes Enhance the Representation of Multiple Simultaneous Sound-Localization Cues in the Inferior Colliculus , 2006, The Journal of Neuroscience.

[23]  W. Singer,et al.  The gamma cycle , 2007, Trends in Neurosciences.

[24]  J. Victor,et al.  Nature and precision of temporal coding in visual cortex: a metric-space analysis. , 1996, Journal of neurophysiology.

[25]  A. Treves,et al.  The representational capacity of the distributed encoding of information provided by populations of neurons in primate temporal visual cortex , 1997, Experimental Brain Research.

[26]  Jones Fn,et al.  Space-Time Relationships in Somesthetic Localization , 1956 .

[27]  M W Oram,et al.  The temporal resolution of neural codes: does response latency have a unique role? , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[29]  M A Nicolelis,et al.  Spatiotemporal properties of layer V neurons of the rat primary somatosensory cortex. , 1999, Cerebral cortex.

[30]  Lauren M Jones,et al.  Precise temporal responses in whisker trigeminal neurons. , 2004, Journal of neurophysiology.

[31]  S. Panzeri,et al.  Diverse and Temporally Precise Kinetic Feature Selectivity in the VPm Thalamic Nucleus , 2008, Neuron.

[32]  A. Nuñez,et al.  Cholinergic Modulation of Synaptic Transmission and Postsynaptic Excitability in the Rat Gracilis Dorsal Column Nucleus , 2006, The Journal of Neuroscience.

[33]  Christopher R. Stambaugh,et al.  Encoding of Tactile Stimulus Location by Somatosensory Thalamocortical Ensembles , 2000, The Journal of Neuroscience.

[34]  S. Panzeri,et al.  Role of precise spike timing in coding of dynamic vibrissa stimuli in somatosensory thalamus. , 2007, Journal of neurophysiology.

[35]  Eric E. Thomson,et al.  Encoding and Decoding Touch Location in the Leech CNS , 2006, The Journal of Neuroscience.

[36]  M. Nicolelis,et al.  Spatiotemporal structure of somatosensory responses of many-neuron ensembles in the rat ventral posterior medial nucleus of the thalamus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  J. Kaas,et al.  Magnification, receptive-field area, and "hypercolumn" size in areas 3b and 1 of somatosensory cortex in owl monkeys. , 1980, Journal of neurophysiology.

[38]  B. Sakmann,et al.  Cortex Is Driven by Weak but Synchronously Active Thalamocortical Synapses , 2006, Science.

[39]  V. Amassian Evoked single cortical unit activity in the somatic sensory areas. , 1953, Electroencephalography and clinical neurophysiology.

[40]  G D Lewen,et al.  Reproducibility and Variability in Neural Spike Trains , 1997, Science.

[41]  D J Woodward,et al.  Dynamic and distributed properties of many-neuron ensembles in the ventral posterior medial thalamus of awake rats. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[42]  G Foffani,et al.  Tactile responses of hindpaw, forepaw and whisker neurons in the thalamic ventrobasal complex of anesthetized rats , 2008, The European journal of neuroscience.

[43]  Gal Chechik,et al.  Encoding Stimulus Information by Spike Numbers and Mean Response Time in Primary Auditory Cortex , 2005, Journal of Computational Neuroscience.

[44]  N. Logothetis,et al.  Phase-of-Firing Coding of Natural Visual Stimuli in Primary Visual Cortex , 2008, Current Biology.

[45]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[46]  C. Rivadulla,et al.  New corticocuneate cellular mechanisms underlying the modulation of cutaneous ascending transmission in anesthetized cats. , 2003, Journal of neurophysiology.

[47]  Alexander Borst,et al.  Information theory and neural coding , 1999, Nature Neuroscience.

[48]  Chun-I Yeh,et al.  Temporal precision in the neural code and the timescales of natural vision , 2007, Nature.

[49]  F. Mechler,et al.  Temporal coding of contrast in primary visual cortex: when, what, and why. , 2001, Journal of neurophysiology.

[50]  Guglielmo Foffani,et al.  Computational role of large receptive fields in the primary somatosensory cortex. , 2008, Journal of neurophysiology.

[51]  Karen A Moxon,et al.  Relationship between physiological response type (RA and SA) and vibrissal receptive field of neurons within the rat trigeminal ganglion. , 2006, Journal of neurophysiology.

[52]  L. Optican,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis. , 1987, Journal of neurophysiology.

[53]  Guglielmo Foffani,et al.  Role of Spike Timing in the Forelimb Somatosensory Cortex of the Rat , 2004, The Journal of Neuroscience.

[54]  A. Nuñez,et al.  Electrophysiological Effects of Temporary Deafferentation on Two Characterized Cell Types in the Nucleus Gracilis of the Rat , 1997, The European journal of neuroscience.

[55]  Rajesh P. N. Rao,et al.  Frequency dependence of spike timing reliability in cortical pyramidal cells and interneurons. , 2001, Journal of neurophysiology.

[56]  S. Thorpe,et al.  Spike times make sense , 2005, Trends in Neurosciences.

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

[58]  J. Isaac,et al.  Rapid, Activity-Dependent Plasticity in Timing Precision in Neonatal Barrel Cortex , 2006, The Journal of Neuroscience.

[59]  Asaf Keller,et al.  Robust Temporal Coding in the Trigeminal System , 2004, Science.

[60]  Michael J. Berry,et al.  The structure and precision of retinal spike trains. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[61]  M. Diamond,et al.  Deciphering the Spike Train of a Sensory Neuron: Counts and Temporal Patterns in the Rat Whisker Pathway , 2006, The Journal of Neuroscience.

[62]  B. Richmond,et al.  Latency: another potential code for feature binding in striate cortex. , 1996, Journal of neurophysiology.

[63]  William Bialek,et al.  Neural Coding of Natural Stimuli: Information at Sub-Millisecond Resolution , 2007, BMC Neuroscience.

[64]  J J Eggermont Azimuth coding in primary auditory cortex of the cat. II. Relative latency and interspike interval representation. , 1998, Journal of neurophysiology.

[65]  Eric D Young,et al.  First-spike latency information in single neurons increases when referenced to population onset , 2007, Proceedings of the National Academy of Sciences.

[66]  R. Johansson,et al.  First spikes in ensembles of human tactile afferents code complex spatial fingertip events , 2004, Nature Neuroscience.

[67]  W. McCulloch,et al.  The limiting information capacity of a neuronal link , 1952 .

[68]  C. Petersen,et al.  Visualizing the Cortical Representation of Whisker Touch: Voltage-Sensitive Dye Imaging in Freely Moving Mice , 2006, Neuron.

[69]  Michael J. Berry,et al.  Synergy, Redundancy, and Independence in Population Codes , 2003, The Journal of Neuroscience.

[70]  R. Christopher deCharms,et al.  Primary cortical representation of sounds by the coordination of action-potential timing , 1996, Nature.

[71]  G. Orban,et al.  Response latency of macaque area MT/V5 neurons and its relationship to stimulus parameters. , 1999, Journal of neurophysiology.

[72]  M. Diamond,et al.  The Role of Spike Timing in the Coding of Stimulus Location in Rat Somatosensory Cortex , 2001, Neuron.

[73]  J. C. Middlebrooks,et al.  Cortical representation of auditory space: information-bearing features of spike patterns. , 2002, Journal of neurophysiology.

[74]  M. Deschenes,et al.  The Relay of High-Frequency Sensory Signals in the Whisker-to-Barreloid Pathway , 2003, The Journal of Neuroscience.

[75]  Tomás Gedeon,et al.  Dejittered Spike-Conditioned Stimulus Waveforms Yield Improved Estimates of Neuronal Feature Selectivity and Spike-Timing Precision of Sensory Interneurons , 2005, The Journal of Neuroscience.

[76]  G. V. Simpson,et al.  Phase Locking of Single Neuron Activity to Theta Oscillations during Working Memory in Monkey Extrastriate Visual Cortex , 2003, Neuron.

[77]  E. D. Adrian,et al.  The Basis of Sensation , 1928, The Indian Medical Gazette.

[78]  Inés Samengo,et al.  Spike-timing precision underlies the coding efficiency of auditory receptor neurons. , 2006, Journal of neurophysiology.

[79]  G. Foffani,et al.  Responses of infragranular neurons in the rat primary somatosensory cortex to forepaw and hindpaw tactile stimuli , 2008, Neuroscience.

[80]  Guglielmo Foffani,et al.  PSTH-based classification of sensory stimuli using ensembles of single neurons , 2004, Journal of Neuroscience Methods.

[81]  John O'Keefe,et al.  Independent rate and temporal coding in hippocampal pyramidal cells , 2003, Nature.

[82]  C. Rivadulla,et al.  The lemniscal–cuneate recurrent excitation is suppressed by strychnine and enhanced by GABAA antagonists in the anaesthetized cat , 2002, The European journal of neuroscience.

[83]  J. J. Hopfield,et al.  Pattern recognition computation using action potential timing for stimulus representation , 1995, Nature.

[84]  William Bialek,et al.  Reading a Neural Code , 1991, NIPS.

[85]  M. Kilgard,et al.  Cortical activity patterns predict speech discrimination ability , 2008, Nature Neuroscience.

[86]  Guglielmo Foffani,et al.  Structure of the excitatory receptive fields of infragranular forelimb neurons in the rat primary somatosensory cortex responding to touch. , 2006, Cerebral cortex.

[87]  Barry J. Richmond,et al.  Decoding cortical neuronal signals: Network models, information estimation and spatial tuning , 1994, Journal of Computational Neuroscience.