Temporal Precision of Spike Trains in Extrastriate Cortex of the Behaving Macaque Monkey

How reliably do action potentials in cortical neurons encode information about a visual stimulus? Most physiological studies do not weigh the occurrences of particular action potentials as significant but treat them only as reflections of average neuronal excitation. We report that single neurons recorded in a previous study by Newsome et al. (1989; see also Britten et al. 1992) from cortical area MT in the behaving monkey respond to dynamic and unpredictable motion stimuli with a markedly reproducible temporal modulation that is precise to a few milliseconds. This temporal modulation is stimulus dependent, being present for highly dynamic random motion but absent when the stimulus translates rigidly.

[1]  K. H. Britten,et al.  Neuronal correlates of a perceptual decision , 1989, Nature.

[2]  B. B. Lee,et al.  Sensitivity of macaque retinal ganglion cells and human observers to combined luminance and chromatic temporal modulation. , 1992, Journal of the Optical Society of America. A, Optics and image science.

[3]  Bernard L. Strehler,et al.  Time structure and stimulus dependence of precisely replicating patterns present in monkey cortical neuronal spike trains , 1987, Brain Research.

[4]  William H. Press,et al.  Numerical recipes , 1990 .

[5]  K. H. Britten,et al.  Responses of neurons in macaque MT to stochastic motion signals , 1993, Visual Neuroscience.

[6]  P Andersen,et al.  Synaptic integration in hippocampal CA1 pyramids. , 1990, Progress in brain research.

[7]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[8]  D. Whitteridge,et al.  Innervation of cat visual areas 17 and 18 by physiologically identified X‐ and Y‐ type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements , 1985, The Journal of comparative neurology.

[9]  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.

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

[11]  D. Pollen,et al.  Spatial and temporal frequency selectivity of neurones in visual cortical areas V1 and V2 of the macaque monkey. , 1985, The Journal of physiology.

[12]  Curtis L. Baker,et al.  Eccentricity-dependent scaling of the limits for short-range apparent motion perception , 1985, Vision Research.

[13]  J. B. Levitt,et al.  Receptive fields and functional architecture of macaque V2. , 1994, Journal of neurophysiology.

[14]  Martin Egelhaaf,et al.  How Reliably Does a Neuron in the Visual Motion Pathway of fhe Fly Encode Behaviourally Relevant Information? , 1997, The European journal of neuroscience.

[15]  D C Van Essen,et al.  Neural activity in areas V1, V2 and V4 during free viewing of natural scenes compared to controlled viewing , 1998, Neuroreport.

[16]  P. O. Bishop,et al.  Orientation specificity and response variability of cells in the striate cortex. , 1973, Vision research.

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

[18]  U. Eysel,et al.  Fluorescent tube light evokes flicker responses in visual neurons , 1984, Vision Research.

[19]  N. Tamamaki,et al.  Hippocampal pyramidal cells excite inhibitory neurons through a single release site , 1993, Nature.

[20]  C. Stevens,et al.  Input synchrony and the irregular firing of cortical neurons , 1998, Nature Neuroscience.

[21]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[22]  Terence D. Sanger,et al.  Probability Density Methods for Smooth Function Approximation and Learning in Populations of Tuned Spiking Neurons , 1998, Neural Computation.

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

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

[25]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate primary visual cortex. I. Stimulus-response relations. , 1990, Journal of neurophysiology.

[26]  J. Movshon,et al.  The statistical reliability of signals in single neurons in cat and monkey visual cortex , 1983, Vision Research.

[27]  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.

[28]  William H. Press,et al.  The Art of Scientific Computing Second Edition , 1998 .

[29]  A. Hill The Basis of Sensation: the Action of the Sense Organs , 1929, Nature.

[30]  Wyeth Bair Analysis of temporal structure in spike trains of visual cortical area MT , 1996 .

[31]  deCharms Rc,et al.  Information coding in the cortex by independent or coordinated populations. , 1998 .

[32]  C. Stevens,et al.  An evaluation of causes for unreliability of synaptic transmission. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Alexandre Pouget,et al.  Probabilistic Interpretation of Population Codes , 1996, Neural Computation.

[34]  K. H. Britten,et al.  Power spectrum analysis of bursting cells in area MT in the behaving monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  W. Pitts,et al.  What the Frog's Eye Tells the Frog's Brain , 1959, Proceedings of the IRE.

[36]  B. B. Lee,et al.  Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker. , 1989, The Journal of physiology.

[37]  J. Kretzberg,et al.  Temporal precision of the encoding of motion information by visual interneurons , 1998, Current Biology.

[38]  Joel L. Davis,et al.  Large-Scale Neuronal Theories of the Brain , 1994 .

[39]  J. Deuchars,et al.  Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. , 1993, Journal of neurophysiology.

[40]  B. Finlay,et al.  Short-term response variability of monkey striate neurons , 1976, Brain Research.

[41]  John H. R. Maunsell,et al.  Visual response latencies in striate cortex of the macaque monkey. , 1992, Journal of neurophysiology.

[42]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  G. J. Tomko,et al.  Neuronal variability: non-stationary responses to identical visual stimuli. , 1974, Brain research.

[44]  Haim Sompolinsky,et al.  Chaotic Balanced State in a Model of Cortical Circuits , 1998, Neural Computation.

[45]  O. Prospero-Garcia,et al.  Reliability of Spike Timing in Neocortical Neurons , 1995 .

[46]  A. Sestokas,et al.  Visual response latency of X- and Y-cells in the dorsal lateral geniculate nucleus of the cat , 1986, Vision Research.

[47]  H B Barlow,et al.  Single units and sensation: a neuron doctrine for perceptual psychology? , 1972, Perception.

[48]  William H. Press,et al.  Numerical Recipes in FORTRAN - The Art of Scientific Computing, 2nd Edition , 1987 .

[49]  John H. R. Maunsell,et al.  On the relationship between synaptic input and spike output jitter in individual neurons. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Fred Rieke,et al.  Coding Efficiency and Information Rates in Sensory Neurons , 1993 .

[51]  G. Orban,et al.  The suppressive influence of moving textured backgrounds on responses of cat striate neurons to moving bars. , 1987, Journal of neurophysiology.

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

[53]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[54]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. , 1987, Journal of neurophysiology.

[55]  Idan Segev,et al.  Ion Channel Stochasticity May Be Critical in Determining the Reliability and Precision of Spike Timing , 1998, Neural Computation.

[56]  Adrian edgar douglas The basis of sensation: the action of the sense organs. , 1964 .

[57]  L. Palmer,et al.  Contribution of linear spatiotemporal receptive field structure to velocity selectivity of simple cells in area 17 of cat , 1989, Vision Research.

[58]  V. Mountcastle,et al.  THE VARIABILITY OF CENTRAL NEURAL ACTIVITY IN A SENSORY SYSTEM, AND ITS IMPLICATIONS FOR THE CENTRAL REFLECTION OF SENSORY EVENTS. , 1963, Journal of neurophysiology.

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