Spike coding from the perspective of a neurone

In this paper, we compare existing methods for quantifying the coding capacity of a spike train, and review recent developments in the application of information theory to neural coding. We present novel methods for characterising single-unit activity based on the perspective of a downstream neurone and propose a simple yet universally applicable framework to characterise the order of complexity of neural coding by single units. We establish four orders of complexity in the capacity for neural coding. First-order coding, quantified by firing rates, is conveyed by frequencies and is thus entirely described by first moment processes. Second-order coding, represented by the variability of interspike intervals, is quantified by the log interval entropy. Third-order coding is the result of spike motifs that associate adjacent inter-spike intervals beyond chance levels; it is described by the joint interval histogram, and is measured by the mutual information between adjacent log intervals. Finally, nonstationarities in activity represent coding of the fourth-order that arise from the effects of a known or unknown stimulus.

[1]  William Bialek,et al.  Adaptive Rescaling Maximizes Information Transmission , 2000, Neuron.

[2]  S M Pincus,et al.  Approximate entropy as a measure of system complexity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[3]  E. Adrian,et al.  The impulses produced by sensory nerve‐endings , 1926 .

[4]  D. Poulain,et al.  Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin , 1982, Neuroscience.

[5]  B. Mandelbrot,et al.  RANDOM WALK MODELS FOR THE SPIKE ACTIVITY OF A SINGLE NEURON. , 1964, Biophysical journal.

[6]  E. Vaadia,et al.  Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. , 1993, Journal of neurophysiology.

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

[8]  Neal Madras Lectures on Monte Carlo Methods , 2002 .

[9]  James A. Simmons,et al.  A possible neuronal basis for representation of acoustic scenes in auditory cortex of the big brown bat , 1993, Nature.

[10]  J. Victor Binless strategies for estimation of information from neural data. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  H. Tuckwell Linear cable theory and dendritic structure , 1988 .

[12]  Jeff Gill,et al.  What are Bayesian Methods , 2008 .

[13]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[14]  G L GERSTEIN,et al.  An approach to the quantitative analysis of electrophysiological data from single neurons. , 1960, Biophysical journal.

[15]  R N Lemon,et al.  Precise spatiotemporal repeating patterns in monkey primary and supplementary motor areas occur at chance levels. , 2000, Journal of neurophysiology.

[16]  E D Adrian The impulses produced by sensory nerve‐endings , 1926, The Journal of physiology.

[17]  Harrison M. Wadsworth Handbook of Statistical Methods for Engineers and Scientists , 1990 .

[18]  N. Singpurwalla,et al.  Methods for Statistical Analysis of Reliability and Life Data. , 1975 .

[19]  Bartlett W. Mel,et al.  Impact of Active Dendrites and Structural Plasticity on the Memory Capacity of Neural Tissue , 2001, Neuron.

[20]  Sanbing Shen,et al.  The mouse VPAC2 receptor confers suprachiasmatic nuclei cellular rhythmicity and responsiveness to vasoactive intestinal polypeptide in vitro , 2003, The European journal of neuroscience.

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

[22]  C J Sherry,et al.  Serial ordering in spike trains: what's it "trying to tell us"? , 1981, The International journal of neuroscience.

[23]  J. Aitchison,et al.  The Lognormal Distribution. , 1958 .

[24]  M. V. Rossum,et al.  In Neural Computation , 2022 .

[25]  Y. Dan,et al.  Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus , 1998, Nature Neuroscience.

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

[27]  D. V. van Essen,et al.  Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. , 1992, Journal of neurophysiology.

[28]  H. Tuckwell Introduction to Theoretical Neurobiology: Linear Cable Theory and Dendritic Structure , 1988 .

[29]  J. Simmons A view of the world through the bat's ear: The formation of acoustic images in echolocation , 1989, Cognition.

[30]  K. Türker,et al.  Tendon tap induces a single long-lasting excitatory reflex in the motoneurons of human soleus muscle , 1997, Experimental Brain Research.

[31]  Te-Won Lee Independent Component Analysis , 1998, Springer US.

[32]  P. Matthews Relationship of firing intervals of human motor units to the trajectory of post‐spike after‐hyperpolarization and synaptic noise. , 1996, The Journal of physiology.

[33]  E. Kay,et al.  Methods for statistical analysis of reliability and life data , 1974 .

[34]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[35]  F. Awiszus,et al.  Continuous functions determined by spike trains of a neuron subject to stimulation , 1988, Biological Cybernetics.

[36]  G. Poggio,et al.  TIME SERIES ANALYSIS OF IMPULSE SEQUENCES OF THALAMIC SOMATIC SENSORY NEURONS. , 1964, Journal of neurophysiology.

[37]  Gary S Bhumbra,et al.  Rhythmic changes in spike coding in the rat suprachiasmatic nucleus , 2005, The Journal of physiology.

[38]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

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

[40]  David J. C. MacKay,et al.  Information Theory, Inference, and Learning Algorithms , 2004, IEEE Transactions on Information Theory.

[41]  I. Miller Probability, Random Variables, and Stochastic Processes , 1966 .

[42]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[44]  W. Armstrong,et al.  Electrophysiological and morphological characteristics of neurons in perinuclear zone of supraoptic nucleus. , 1997, Journal of neurophysiology.

[45]  G. Laurent,et al.  Relationship between Afferent and Central Temporal Patterns in the Locust Olfactory System , 1999, The Journal of Neuroscience.

[46]  Sheila Nirenberg,et al.  Decoding neuronal spike trains: How important are correlations? , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Gareth Leng,et al.  Phasic spike patterning in rat supraoptic neurones in vivo and in vitro , 2004, The Journal of physiology.

[48]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[49]  E. Adrian,et al.  The impulses produced by sensory nerve endings , 1926, The Journal of physiology.

[50]  John Skilling,et al.  Data analysis : a Bayesian tutorial , 1996 .

[51]  R. Baierlein Probability Theory: The Logic of Science , 2004 .

[52]  Antoni Emil Karbowiak Theory of communication , 1969 .

[53]  W. Schultz,et al.  Dopamine responses comply with basic assumptions of formal learning theory , 2001, Nature.

[54]  Allan D. Coop,et al.  Estimating the Temporal Interval Entropy of Neuronal Discharge , 2004, Neural Computation.

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

[56]  Marius Usher,et al.  Network Amplification of Local Fluctuations Causes High Spike Rate Variability, Fractal Firing Patterns and Oscillatory Local Field Potentials , 1994, Neural Computation.

[57]  Adrienne L. Fairhall,et al.  Efficiency and ambiguity in an adaptive neural code , 2001, Nature.

[58]  E. Jaynes Information Theory and Statistical Mechanics , 1957 .

[59]  Richard M. Everson,et al.  Independent Component Analysis: Principles and Practice , 2001 .

[60]  Gary S Bhumbra,et al.  Measuring spike coding in the rat supraoptic nucleus , 2004, The Journal of physiology.

[61]  F. Dudek,et al.  Electrophysiological properties of neurones in the region of the paraventricular nucleus in slices of rat hypothalamus. , 1991, The Journal of physiology.

[62]  R. Reid,et al.  Synchronous activity in the visual system. , 1999, Annual review of physiology.

[63]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[64]  Robert B. Ash,et al.  Information Theory , 2020, The SAGE International Encyclopedia of Mass Media and Society.

[65]  R. Powers,et al.  Effects of large excitatory and inhibitory inputs on motoneuron discharge rate and probability. , 1999, Journal of neurophysiology.

[66]  M. Abeles Role of the cortical neuron: integrator or coincidence detector? , 1982, Israel journal of medical sciences.

[67]  K. Türker,et al.  Motor-unit firing frequency can be used for the estimation of synaptic potentials in human motoneurones , 1994, Journal of Neuroscience Methods.

[68]  R. Stein A THEORETICAL ANALYSIS OF NEURONAL VARIABILITY. , 1965, Biophysical journal.

[69]  H. Haken Principles of brain functioning , 1995 .

[70]  T. Collett,et al.  Chasing behaviour of houseflies (Fannia canicularis) , 1974, Journal of comparative physiology.

[71]  Jianfeng Feng,et al.  Responses of Magnocellular Neurons to Osmotic Stimulation Involves Coactivation of Excitatory and Inhibitory Input: An Experimental and Theoretical Analysis , 2001, The Journal of Neuroscience.

[72]  Rajesh P. N. Rao,et al.  Probabilistic Models of the Brain , 2002 .

[73]  D Ferster,et al.  Cracking the Neuronal Code , 1995, Science.

[74]  L. Maler,et al.  Negative Interspike Interval Correlations Increase the Neuronal Capacity for Encoding Time-Dependent Stimuli , 2001, The Journal of Neuroscience.

[75]  P H Ellaway,et al.  Cumulative sum technique and its application to the analysis of peristimulus time histograms. , 1978, Electroencephalography and clinical neurophysiology.

[76]  Gary S Bhumbra,et al.  Assessment of Spike Activity in the Supraoptic Nucleus , 2004, Journal of neuroendocrinology.

[77]  S. Stevenson,et al.  Discrimination of jittered sonar echoes by the echolocating bat, Eptesicus fuscus: The shape of target images in echolocation , 1990, Journal of Comparative Physiology A.

[78]  Masakazu Konishi,et al.  Mechanisms of sound localization in the barn owl (Tyto alba) , 1979, Journal of comparative physiology.

[79]  G. Laurent,et al.  Who reads temporal information contained across synchronized and oscillatory spike trains? , 1998, Nature.

[80]  John G. Proakis,et al.  Probability, random variables and stochastic processes , 1985, IEEE Trans. Acoust. Speech Signal Process..

[81]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[82]  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.

[83]  W. R. Klemm,et al.  What is the meaningful measure of neuronal spike train activity? , 1984, Journal of Neuroscience Methods.

[84]  William H. Press,et al.  Numerical recipes in C , 2002 .

[85]  B. Katz,et al.  Spontaneous subthreshold activity at motor nerve endings , 1952, The Journal of physiology.

[86]  F. Ruddle,et al.  The gene encoding peripheral myelin protein zero is located on mouse chromosome 1 , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

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

[89]  F. Awiszus,et al.  On a method to detect long-latency excitations and inhibitions of single hand muscle motoneurons in man , 2004, Experimental Brain Research.

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

[91]  G. Laurent,et al.  Impaired odour discrimination on desynchronization of odour-encoding neural assemblies , 1997, Nature.

[92]  G Leng,et al.  Regulation of the milk ejection reflex in the rat. , 1986, The Journal of physiology.

[93]  R. Dyball,et al.  Defined Cell Groups in the Rat Suprachiasmatic Nucleus Have Different Day/Night Rhythms of Single-Unit Activity In Vivo , 2003, Journal of biological rhythms.

[94]  J A Simmons,et al.  Perception of echo phase information in bat sonar. , 1979, Science.

[95]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[96]  R W RODIECK,et al.  Some quantitative methods for the study of spontaneous activity of single neurons. , 1962, Biophysical journal.

[97]  Grace L. Yang,et al.  On statistical methods in neuronal spike-train analysis , 1978 .

[98]  Eric R. Ziegel,et al.  The Elements of Statistical Learning , 2003, Technometrics.

[99]  William Bialek,et al.  Entropy and Information in Neural Spike Trains , 1996, cond-mat/9603127.

[100]  George L. Gerstein,et al.  Improvements to the Sensitivity of Gravitational Clustering for Multiple Neuron Recordings , 2000, Neural Computation.

[101]  T. Sejnowski,et al.  Comparison of current-driven and conductance-driven neocortical model neurons with Hodgkin-Huxley voltage-gated channels. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[102]  R. Shapley,et al.  Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. , 1991, Journal of neurophysiology.

[103]  A. C. Webb,et al.  The spontaneous activity of neurones in the cat’s cerebral cortex , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[104]  Peter F. Heil,et al.  Survival Distributions: Reliability Applications in the Biomedical Sciences , 1976 .

[105]  G. Ermentrout Principles of brain functioning: A synergetic approach to brain activity, behavior, and cognition , 1997 .

[106]  Y. Laporte,et al.  A method of analysing the responses of spindle primary endings to fusimotor stimulation , 1968, The Journal of physiology.

[107]  G L Gerstein,et al.  Detecting spatiotemporal firing patterns among simultaneously recorded single neurons. , 1988, Journal of neurophysiology.

[108]  B J Richmond,et al.  Stochastic nature of precisely timed spike patterns in visual system neuronal responses. , 1999, Journal of neurophysiology.

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

[110]  C. Gray The Temporal Correlation Hypothesis of Visual Feature Integration Still Alive and Well , 1999, Neuron.

[111]  J. H. Sheesley Methods for Statistical Analysis of Reliability and Life Data , 1977 .

[112]  L. M. M.-T. Theory of Probability , 1929, Nature.

[113]  H. Nakahama,et al.  Statistical dependency between interspike intervals of spontaneous activity in thalamic lemniscal neurons. , 1966, Journal of neurophysiology.

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

[115]  John Harris,et al.  Handbook of mathematics and computational science , 1998 .

[116]  G L Gerstein,et al.  Favored patterns in spike trains. II. Application. , 1983, Journal of neurophysiology.

[117]  A. Aertsen,et al.  Response synchronization in the visual cortex , 1993, Current Opinion in Neurobiology.

[118]  G Deco,et al.  The coding of information by spiking neurons: an analytical study. , 1998, Network.

[119]  William R. Softky,et al.  Simple codes versus efficient codes , 1995, Current Opinion in Neurobiology.

[120]  Walter Heiligenberg,et al.  Temporal hyperacuity in the electric sense of fish , 1985, Nature.

[121]  C J Sherry,et al.  Entropy as an index of the informational state of neurons. , 1981, The International journal of neuroscience.

[122]  D. Wetmore,et al.  Post‐spike distance‐to‐threshold trajectories of neurones in monkey motor cortex , 2004, The Journal of physiology.

[123]  William H. Press,et al.  Numerical recipes in C. The art of scientific computing , 1987 .