Reading spike timing without a clock: intrinsic decoding of spike trains

The precise timing of action potentials of sensory neurons relative to the time of stimulus presentation carries substantial sensory information that is lost or degraded when these responses are summed over longer time windows. However, it is unclear whether and how downstream networks can access information in precise time-varying neural responses. Here, we review approaches to test the hypothesis that the activity of neural populations provides the temporal reference frames needed to decode temporal spike patterns. These approaches are based on comparing the single-trial stimulus discriminability obtained from neural codes defined with respect to network-intrinsic reference frames to the discriminability obtained from codes defined relative to the experimenter's computer clock. Application of this formalism to auditory, visual and somatosensory data shows that information carried by millisecond-scale spike times can be decoded robustly even with little or no independent external knowledge of stimulus time. In cortex, key components of such intrinsic temporal reference frames include dedicated neural populations that signal stimulus onset with reliable and precise latencies, and low-frequency oscillations that can serve as reference for partitioning extended neuronal responses into informative spike patterns.

[1]  Steven F. Kalik,et al.  Analysis of perisaccadic field potentials in the occipitotemporal pathway during active vision. , 2003, Journal of neurophysiology.

[2]  Jason Wolfe,et al.  Sparse temporal coding of elementary tactile features during active whisker sensation , 2009, Nature Neuroscience.

[3]  Charles H. Brown,et al.  The Influence of Natural Scene Dynamics on Auditory Cortical Activity , 2010, The Journal of Neuroscience.

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

[5]  R. Nichols,et al.  Prediction of the first year college performance of high aptitude students. , 1963, Psychological monographs.

[6]  D. Buonomano,et al.  The neural basis of temporal processing. , 2004, Annual review of neuroscience.

[7]  D. Kleinfeld,et al.  Frisking the Whiskers Patterned Sensory Input in the Rat Vibrissa System , 2004, Neuron.

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

[9]  W. Maass,et al.  State-dependent computations: spatiotemporal processing in cortical networks , 2009, Nature Reviews Neuroscience.

[10]  K. Harris Neural signatures of cell assembly organization , 2005, Nature Reviews Neuroscience.

[11]  Fred Wolf,et al.  Olfactory Coding with Patterns of Response Latencies , 2010, Neuron.

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

[13]  M. Treisman Temporal discrimination and the indifference interval. Implications for a model of the "internal clock". , 1963, Psychological monographs.

[14]  Jonathan D. Victor,et al.  How the brain uses time to represent and process visual information 1 1 Published on the World Wide Web on 16 August 2000. , 2000, Brain Research.

[15]  M E Diamond,et al.  Learning through maps: functional significance of topographic organization in primary sensory cortex. , 1999, Journal of neurobiology.

[16]  David Poeppel,et al.  Cortical oscillations and speech processing: emerging computational principles and operations , 2012, Nature Neuroscience.

[17]  Rasmus S Petersen,et al.  Comparison of latency and rate coding for the direction of whisker deflection in the subcortical somatosensory pathway. , 2012, Journal of neurophysiology.

[18]  Gal Chechik,et al.  Information theory in auditory research , 2007, Hearing Research.

[19]  Oren Shriki,et al.  Fast Coding of Orientation in Primary Visual Cortex , 2012, PLoS Comput. Biol..

[20]  N. Logothetis,et al.  Neurons with Stereotyped and Rapid Responses Provide a Reference Frame for Relative Temporal Coding in Primate Auditory Cortex , 2012, The Journal of Neuroscience.

[21]  Peter Lakatos,et al.  Dynamics of Active Sensing and perceptual selection , 2010, Current Opinion in Neurobiology.

[22]  R. Quiroga,et al.  Extracting information from neuronal populations : information theory and decoding approaches , 2022 .

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

[24]  M Abeles,et al.  Spatio-temporal firing patterns in the frontal cortex of behaving monkeys , 1996, Journal of Physiology-Paris.

[25]  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.

[26]  Anthony M Zador,et al.  Differences in Sensitivity to Neural Timing among Cortical Areas , 2012, The Journal of Neuroscience.

[27]  Gustavo Deco,et al.  Oscillations, Phase-of-Firing Coding, and Spike Timing-Dependent Plasticity: An Efficient Learning Scheme , 2009, The Journal of Neuroscience.

[28]  Tim Gollisch,et al.  Disentangling Sub-Millisecond Processes within an Auditory Transduction Chain , 2005, PLoS biology.

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

[30]  A Grinvald,et al.  Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex. , 1995, Journal of neurophysiology.

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

[32]  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.

[33]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.

[34]  S. Thorpe,et al.  Spike Timing Dependent Plasticity Finds the Start of Repeating Patterns in Continuous Spike Trains , 2008, PloS one.

[35]  Timothée Masquelier,et al.  Neural variability, or lack thereof , 2013, Front. Comput. Neurosci..

[36]  H. Sompolinsky,et al.  The tempotron: a neuron that learns spike timing–based decisions , 2006, Nature Neuroscience.

[37]  N. Logothetis,et al.  Millisecond encoding precision of auditory cortex neurons , 2010, Proceedings of the National Academy of Sciences.

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

[39]  Marcelo A. Montemurro,et al.  Spike-Phase Coding Boosts and Stabilizes Information Carried by Spatial and Temporal Spike Patterns , 2009, Neuron.

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

[41]  Idan Segev,et al.  Optimization principles of dendritic structure , 2007, Theoretical Biology and Medical Modelling.

[42]  Stefano Panzeri,et al.  Analysis of Slow (Theta) Oscillations as a Potential Temporal Reference Frame for Information Coding in Sensory Cortices , 2012, PLoS Comput. Biol..

[43]  Stefano Panzeri,et al.  Sensory Input Drives Multiple Intracellular Information Streams in Somatosensory Cortex , 2010, The Journal of Neuroscience.

[44]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[45]  Anthony M Zador,et al.  Millisecond-scale differences in neural activity in auditory cortex can drive decisions , 2008, Nature Neuroscience.

[46]  S. Shamma,et al.  Temporal coherence and attention in auditory scene analysis , 2011, Trends in Neurosciences.

[47]  Stefano Panzeri,et al.  Information Carried by Population Spike Times in the Whisker Sensory Cortex can be Decoded Without Knowledge of Stimulus Time , 2010, Front. Syn. Neurosci..

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

[49]  Stefano Panzeri,et al.  The Laminar and Temporal Structure of Stimulus Information in the Phase of Field Potentials of Auditory Cortex , 2011, The Journal of Neuroscience.

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

[51]  P. Cavanagh,et al.  Opinion TRENDS in Cognitive Sciences Vol.11 No.5 The ‘when ’ pathway of the right parietal lobe , 2022 .

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

[53]  M. Diamond,et al.  Whisker-Mediated Texture Discrimination , 2008, PLoS biology.

[54]  Nicolas Brunel,et al.  Sensory neural codes using multiplexed temporal scales , 2010, Trends in Neurosciences.

[55]  Gal Chechik,et al.  Reduction of Information Redundancy in the Ascending Auditory Pathway , 2006, Neuron.

[56]  Matthew C Smear,et al.  Precise olfactory responses tile the sniff cycle , 2011, Nature Neuroscience.

[57]  David Kleinfeld,et al.  Hierarchy of orofacial rhythms revealed through whisking and breathing , 2013, Nature.

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

[59]  D. Poeppel,et al.  Phase Patterns of Neuronal Responses Reliably Discriminate Speech in Human Auditory Cortex , 2007, Neuron.

[60]  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.

[61]  A. Aertsen,et al.  Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding , 2010, Nature Reviews Neuroscience.

[62]  M. Diamond,et al.  Neuronal Activity in Rat Barrel Cortex Underlying Texture Discrimination , 2007, PLoS biology.

[63]  Michael Okun,et al.  The Subthreshold Relation between Cortical Local Field Potential and Neuronal Firing Unveiled by Intracellular Recordings in Awake Rats , 2010, The Journal of Neuroscience.

[64]  Kerry M. M. Walker,et al.  Neural Ensemble Codes for Stimulus Periodicity in Auditory Cortex , 2010, The Journal of Neuroscience.

[65]  R. Miall,et al.  Remembering the time: a continuous clock , 2006, Trends in Cognitive Sciences.

[66]  K. Harris,et al.  Gating of Sensory Input by Spontaneous Cortical Activity , 2013, The Journal of Neuroscience.

[67]  J. C. Middlebrooks,et al.  Coding of Sound-Source Location by Ensembles of Cortical Neurons , 2000, The Journal of Neuroscience.

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

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

[70]  M. Diamond,et al.  Decoding neuronal population activity in rat somatosensory cortex: role of columnar organization. , 2003, Cerebral cortex.

[71]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[72]  Per Magne Knutsen,et al.  Orthogonal coding of object location , 2009, Trends in Neurosciences.

[73]  Ole Paulsen,et al.  Phase of Firing as a Local Window for Efficient Neuronal Computation: Tonic and Phasic Mechanisms in the Control of Theta Spike Phase , 2010, Front. Hum. Neurosci..

[74]  Maik C. Stüttgen,et al.  Integration of Vibrotactile Signals for Whisker-Related Perception in Rats Is Governed by Short Time Constants: Comparison of Neurometric and Psychometric Detection Performance , 2010, The Journal of Neuroscience.

[75]  Alan R Palmer,et al.  First Spike Latency Code for Interaural Phase Difference Discrimination in the Guinea Pig Inferior Colliculus , 2011, The Journal of Neuroscience.

[76]  A. Zador,et al.  Neural representation and the cortical code. , 2000, Annual review of neuroscience.

[77]  M. Diamond,et al.  Whisker sensory system – From receptor to decision , 2013, Progress in Neurobiology.

[78]  J. Victor,et al.  Quality Time: Representation of a Multidimensional Sensory Domain through Temporal Coding , 2009, The Journal of Neuroscience.