Regulation of spike timing in visual cortical circuits

A train of action potentials (a spike train) can carry information in both the average firing rate and the pattern of spikes in the train. But can such a spike-pattern code be supported by cortical circuits? Neurons in vitro produce a spike pattern in response to the injection of a fluctuating current. However, cortical neurons in vivo are modulated by local oscillatory neuronal activity and by top-down inputs. In a cortical circuit, precise spike patterns thus reflect the interaction between internally generated activity and sensory information encoded by input spike trains. We review the evidence for precise and reliable spike timing in the cortex and discuss its computational role.

[1]  H. L. Bryant,et al.  Spike initiation by transmembrane current: a white‐noise analysis. , 1976, The Journal of physiology.

[2]  James C. Bezdek,et al.  Pattern Recognition with Fuzzy Objective Function Algorithms , 1981, Advanced Applications in Pattern Recognition.

[3]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  R. Malinow,et al.  The probability of transmitter release at a mammalian central synapse , 1993, Nature.

[6]  C. Koch,et al.  An oscillation-based model for the neuronal basis of attention , 1993, Vision Research.

[7]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

[8]  Bartlett W. Mel Synaptic integration in an excitable dendritic tree. , 1993, Journal of neurophysiology.

[9]  J. C. Anderson,et al.  Polyneuronal innervation of spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.

[10]  M. Wong-Riley,et al.  Primate Visual Cortex , 1994 .

[11]  J Deuchars,et al.  Relationships between morphology and physiology of pyramid‐pyramid single axon connections in rat neocortex in vitro. , 1994, The Journal of physiology.

[12]  M. Hasselmo Neuromodulation and cortical function: modeling the physiological basis of behavior , 1995, Behavioural Brain Research.

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

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

[15]  M. Hasselmo,et al.  Cholinergic modulation of cortical oscillatory dynamics. , 1995, Journal of neurophysiology.

[16]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[17]  J. White,et al.  A bifurcation analysis of neuronal subthreshold oscillations. , 1995, Biophysical journal.

[18]  P. Somogyi,et al.  Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons , 1995, Nature.

[19]  K. Martin,et al.  Excitatory synaptic inputs to spiny stellate cells in cat visual cortex , 1996, Nature.

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

[21]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[22]  D. Snodderly,et al.  Response Variability of Neurons in Primary Visual Cortex (V1) of Alert Monkeys , 1997, The Journal of Neuroscience.

[23]  Maria V. Sanchez-Vives,et al.  Influence of low and high frequency inputs on spike timing in visual cortical neurons. , 1997, Cerebral cortex.

[24]  Norbert Krüger,et al.  Face recognition by elastic bunch graph matching , 1997, Proceedings of International Conference on Image Processing.

[25]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[26]  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.

[27]  Michael J. Berry,et al.  Refractoriness and Neural Precision , 1997, The Journal of Neuroscience.

[28]  T. Albright,et al.  Efficient Discrimination of Temporal Patterns by Motion-Sensitive Neurons in Primate Visual Cortex , 1998, Neuron.

[29]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[30]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

[31]  A. Zador Impact of synaptic unreliability on the information transmitted by spiking neurons. , 1998, Journal of neurophysiology.

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

[33]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[34]  Michael J. Berry,et al.  The Neural Code of the Retina , 1999, Neuron.

[35]  R. Yuste,et al.  Linear Summation of Excitatory Inputs by CA1 Pyramidal Neurons , 1999, Neuron.

[36]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

[37]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[38]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[39]  W. Bair Spike timing in the mammalian visual system , 1999, Current Opinion in Neurobiology.

[40]  B. Connors,et al.  Efficacy of Thalamocortical and Intracortical Synaptic Connections Quanta, Innervation, and Reliability , 1999, Neuron.

[41]  Y. Yarom,et al.  Resonance, oscillation and the intrinsic frequency preferences of neurons , 2000, Trends in Neurosciences.

[42]  R. Reid,et al.  Temporal Coding of Visual Information in the Thalamus , 2000, The Journal of Neuroscience.

[43]  R. Reid,et al.  Low Response Variability in Simultaneously Recorded Retinal, Thalamic, and Cortical Neurons , 2000, Neuron.

[44]  F. G. Pike,et al.  Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents , 2000, The Journal of physiology.

[45]  J. Magee Dendritic integration of excitatory synaptic input , 2000, Nature Reviews Neuroscience.

[46]  C. Gray,et al.  Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Emilio Salinas,et al.  Gain Modulation A Major Computational Principle of the Central Nervous System , 2000, Neuron.

[48]  William Bialek,et al.  Synergy in a Neural Code , 2000, Neural Computation.

[49]  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.

[50]  Robert C. Liu,et al.  Variability and information in a neural code of the cat lateral geniculate nucleus. , 2001, Journal of neurophysiology.

[51]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[52]  B. Sakmann,et al.  Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons , 2001, The Journal of physiology.

[53]  S. Raghavachari,et al.  Gating of Human Theta Oscillations by a Working Memory Task , 2001, The Journal of Neuroscience.

[54]  B Sakmann,et al.  Functionally Independent Columns of Rat Somatosensory Barrel Cortex Revealed with Voltage-Sensitive Dye Imaging , 2001, The 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]  勇一 作村,et al.  Biophysics of Computation , 2001 .

[57]  T J Sejnowski,et al.  Computational model of carbachol‐induced delta, theta, and gamma oscillations in the hippocampus , 2001, Hippocampus.

[58]  P. Alstrøm,et al.  Characterization of reliability of spike timing in spinal interneurons during oscillating inputs. , 2001, Journal of neurophysiology.

[59]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[60]  Mark C. W. van Rossum,et al.  A Novel Spike Distance , 2001, Neural Computation.

[61]  R. Reid,et al.  Predicting Every Spike A Model for the Responses of Visual Neurons , 2001, Neuron.

[62]  R. Reid,et al.  The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Robert A. Frazor,et al.  Visual cortex neurons of monkeys and cats: temporal dynamics of the contrast response function. , 2002, Journal of neurophysiology.

[64]  Paul H. E. Tiesinga,et al.  Attractor Reliability Reveals Deterministic Structure in Neuronal Spike Trains , 2002, Neural Computation.

[65]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[66]  R. Reid,et al.  Precise Firing Events Are Conserved across Neurons , 2002, The Journal of Neuroscience.

[67]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

[68]  T. Sejnowski,et al.  Information transfer in entrained cortical neurons. , 2002, Network.

[69]  P H E Tiesinga,et al.  Precision and reliability of periodically and quasiperiodically driven integrate-and-fire neurons. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[70]  J. White,et al.  Frequency selectivity of layer II stellate cells in the medial entorhinal cortex. , 2002, Journal of neurophysiology.

[71]  Luis M Martinez,et al.  Synaptic physiology of the flow of information in the cat's visual cortex in vivo , 2002, The Journal of physiology.

[72]  G. Shepherd,et al.  Emerging rules for the distributions of active dendritic conductances , 2002, Nature Reviews Neuroscience.

[73]  R. Yuste,et al.  Thalamocortical Bursts Trigger Recurrent Activity in Neocortical Networks: Layer 4 as a Frequency-Dependent Gate , 2002, The Journal of Neuroscience.

[74]  J. D. Hunter,et al.  Amplitude and frequency dependence of spike timing: implications for dynamic regulation. , 2003, Journal of neurophysiology.

[75]  Paul H. E. Tiesinga,et al.  A New Correlation-Based Measure of Spike Timing Reliability , 2002, Neurocomputing.

[76]  Moshe Abeles,et al.  On Embedding Synfire Chains in a Balanced Network , 2003, Neural Computation.

[77]  A. Reyes Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro , 2003, Nature Neuroscience.

[78]  P. Somogyi,et al.  Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo , 2003, Nature.

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

[80]  R. Yuste,et al.  Attractor dynamics of network UP states in the neocortex , 2003, Nature.

[81]  Bartlett W. Mel,et al.  Pyramidal Neuron as Two-Layer Neural Network , 2003, Neuron.

[82]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[83]  A. Thomson,et al.  Interlaminar connections in the neocortex. , 2003, Cerebral cortex.

[84]  Carlos D. Brody,et al.  Simple Networks for Spike-Timing-Based Computation, with Application to Olfactory Processing , 2003, Neuron.

[85]  R. Reid,et al.  Efficacy of Retinal Spikes in Driving Cortical Responses , 2003, The Journal of Neuroscience.

[86]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[87]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

[88]  Christof Koch,et al.  A model for the neuronal implementation of selective visual attention based on temporal correlation among neurons , 1994, Journal of Computational Neuroscience.

[89]  W. Singer,et al.  Short- and Long-Term Effects of Cholinergic Modulation on Gamma Oscillations and Response Synchronization in the Visual Cortex , 2004, The Journal of Neuroscience.

[90]  E. Chichilnisky,et al.  Precision of spike trains in primate retinal ganglion cells. , 2004, Journal of neurophysiology.

[91]  Paul H. E. Tiesinga,et al.  Rapid Temporal Modulation of Synchrony by Competition in Cortical Interneuron Networks , 2004, Neural Computation.

[92]  Paul Tiesinga,et al.  Influence of ionic conductances on spike timing reliability of cortical neurons for suprathreshold rhythmic inputs. , 2004, Journal of neurophysiology.

[93]  Jorge V. José,et al.  Inhibitory synchrony as a mechanism for attentional gain modulation , 2004, Journal of Physiology-Paris.

[94]  T. Sejnowski,et al.  Discovering Spike Patterns in Neuronal Responses , 2004, The Journal of Neuroscience.

[95]  H. Lüscher,et al.  Spatiotemporal evolution of excitation and inhibition in the rat barrel cortex investigated with multielectrode arrays. , 2004, Journal of neurophysiology.

[96]  Bartlett W. Mel,et al.  Computational subunits in thin dendrites of pyramidal cells , 2004, Nature Neuroscience.

[97]  D. Chklovskii,et al.  Neurogeometry and potential synaptic connectivity , 2005, Trends in Neurosciences.

[98]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[99]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[100]  D. McCormick,et al.  Inhibitory Postsynaptic Potentials Carry Synchronized Frequency Information in Active Cortical Networks , 2005, Neuron.

[101]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

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

[103]  E J Chichilnisky,et al.  Prediction and Decoding of Retinal Ganglion Cell Responses with a Probabilistic Spiking Model , 2005, The Journal of Neuroscience.

[104]  J. Duncan,et al.  Faculty Opinions recommendation of Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. , 2005 .

[105]  Robert Desimone,et al.  Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4 , 2005, Science.

[106]  Tim P Vogels,et al.  Signal Propagation and Logic Gating in Networks of Integrate-and-Fire Neurons , 2005, The Journal of Neuroscience.

[107]  Paul H. E. Tiesinga,et al.  The Possible Role of Spike Patterns in Cortical Information Processing , 2005, Journal of Computational Neuroscience.

[108]  Miguel A L Nicolelis,et al.  Fast modulation of prefrontal cortex activity by basal forebrain noncholinergic neuronal ensembles. , 2006, Journal of neurophysiology.

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

[110]  Terrence J. Sejnowski,et al.  Selective attention through phase relationship of excitatory and inhibitory input synchrony in a model cortical neuron , 2006, Neural Networks.

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

[112]  J. Magee,et al.  State-Dependent Dendritic Computation in Hippocampal CA1 Pyramidal Neurons , 2006, The Journal of Neuroscience.

[113]  G. Buzsáki Rhythms of the brain , 2006 .

[114]  Paul H. E. Tiesinga Stimulus competition by inhibitory interference , 2006, Neurocomputing.

[115]  Paul H. E. Tiesinga,et al.  Attentional modulation of firing rate and synchrony in a model cortical network , 2005, Journal of Computational Neuroscience.

[116]  D. Contreras,et al.  Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation , 2006, The Journal of Neuroscience.

[117]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[118]  J. Magee,et al.  Integrative Properties of Radial Oblique Dendrites in Hippocampal CA1 Pyramidal Neurons , 2006, Neuron.

[119]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[120]  Arne D. Ekstrom,et al.  Brain Oscillations Control Timing of Single-Neuron Activity in Humans , 2007, The Journal of Neuroscience.

[121]  Idan Segev,et al.  Modeling a layer 4-to-layer 2/3 module of a single column in rat neocortex: Interweaving in vitro and in vivo experimental observations , 2007, Proceedings of the National Academy of Sciences.

[122]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[123]  Wolfgang Maass,et al.  A Statistical Analysis of Information- Processing Properties of Lamina-specific Cortical Microcircuit Models , 2022 .

[124]  Pablo Fuentealba,et al.  Cell Type-Specific Tuning of Hippocampal Interneuron Firing during Gamma Oscillations In Vivo , 2007, The Journal of Neuroscience.

[125]  Ian R. Wickersham,et al.  Monosynaptic Restriction of Transsynaptic Tracing from Single, Genetically Targeted Neurons , 2007, Neuron.

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

[127]  Ohad Ben-Shahar,et al.  Stochastic Emergence of Repeating Cortical Motifs in Spontaneous Membrane Potential Fluctuations In Vivo , 2007, Neuron.

[128]  J. Lübke,et al.  Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex , 2007, Brain Structure and Function.

[129]  Yuzhuo Su,et al.  Spike Timing Amplifies the Effect of Electric Fields on Neurons: Implications for Endogenous Field Effects , 2007, The Journal of Neuroscience.

[130]  Jaime de la Rocha,et al.  Supplementary Information for the article ‘ Correlation between neural spike trains increases with firing rate ’ , 2007 .

[131]  E. Boyden,et al.  Multiple-Color Optical Activation, Silencing, and Desynchronization of Neural Activity, with Single-Spike Temporal Resolution , 2007, PloS one.

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

[133]  Feng Zhang,et al.  Multimodal fast optical interrogation of neural circuitry , 2007, Nature.

[134]  B. Sakmann,et al.  Dendritic Spikes in Apical Dendrites of Neocortical Layer 2/3 Pyramidal Neurons , 2007, The Journal of Neuroscience.

[135]  Jude F. Mitchell,et al.  Differential Attention-Dependent Response Modulation across Cell Classes in Macaque Visual Area V4 , 2007, Neuron.

[136]  Romesh D Kumbhani,et al.  Precision, reliability, and information-theoretic analysis of visual thalamocortical neurons. , 2007, Journal of neurophysiology.

[137]  C. Schroeder,et al.  Neuronal Oscillations and Multisensory Interaction in Primary Auditory Cortex , 2007, Neuron.

[138]  Alain Destexhe,et al.  Inhibition Determines Membrane Potential Dynamics and Controls Action Potential Generation in Awake and Sleeping Cat Cortex , 2007, The Journal of Neuroscience.