The Effect of Middle Temporal Spike Phase on Sensory Encoding and Correlates with Behavior during a Motion-Detection Task

Previous studies have shown that sensory neurons that are the most informative of the stimulus tend to be the best correlated with the subject's perceptual decision. We wanted to know whether this relationship might also apply to short time segments of a neuron's response. We asked whether spikes that conveyed more information about a motion stimulus were also more tightly linked to the perceptual behavior. We examined single-neuron activity in middle temporal (MT) area while monkeys performed a motion-detection task. Because of a slow stimulus update (every 27 ms), activity in many MT neurons was entrained and phase-locked to the stimulus. These stimulus-entrained neuronal oscillations allowed us to separate spikes based on phase. We observed a large amount of variability in how spikes at different phases of the oscillation encoded the stimulus, as revealed by the spike-triggered average of the motion. Spikes during certain phases of the cycle were much more informative about the presence of coherent motion than others. Importantly, we found that the phases that were the most informative about the motion stimulus were also more correlated with the behavioral performance and reaction time of the animal. Our results suggest that the relationship between a neuron's spikes, the stimulus, and behavior can vary on a time scale of tens of milliseconds.

[1]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

[2]  Gary J. Rose,et al.  Roles for short-term synaptic plasticity in behavior , 2002, Journal of Physiology-Paris.

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

[4]  Pieter R. Roelfsema,et al.  Different Processing Phases for Features, Figures, and Selective Attention in the Primary Visual Cortex , 2007, Neuron.

[5]  Troy W. Margrie,et al.  Neuronal Oscillations Enhance Stimulus Discrimination by Ensuring Action Potential Precision , 2006, PLoS Biology.

[6]  Eric S Fortune,et al.  The decoding of electrosensory systems , 2006, Current Opinion in Neurobiology.

[7]  S. Wang,et al.  Coincidence detection in single dendritic spines mediated by calcium release , 2000, Nature Neuroscience.

[8]  G. DeAngelis,et al.  Contribution of Area MT to Stereoscopic Depth Perception Choice-Related Response Modulations Reflect Task Strategy , 2004, Neuron.

[9]  Rufin van Rullen,et al.  Neurons Tune to the Earliest Spikes Through STDP , 2005, Neural Computation.

[10]  H. Wässle,et al.  Response latency of brisk‐sustained (X) and brisk‐transient (Y) cells in the cat retina , 1982, The Journal of physiology.

[11]  W. Singer,et al.  Stimulus‐Dependent Neuronal Oscillations in Cat Visual Cortex: Inter‐Columnar Interaction as Determined by Cross‐Correlation Analysis , 1990, The European journal of neuroscience.

[12]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

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

[14]  M. R. Mehta,et al.  Role of experience and oscillations in transforming a rate code into a temporal code , 2002, Nature.

[15]  B. Cumming,et al.  Macaque V2 Neurons, But Not V1 Neurons, Show Choice-Related Activity , 2006, The Journal of Neuroscience.

[16]  G. Orban,et al.  Responses of macaque STS neurons to optic flow components: a comparison of areas MT and MST. , 1994, Journal of neurophysiology.

[17]  J. Maunsell,et al.  Attentional Modulation of Behavioral Performance and Neuronal Responses in Middle Temporal and Ventral Intraparietal Areas of Macaque Monkey , 2002, The Journal of Neuroscience.

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

[19]  Pieter R. Roelfsema,et al.  How Precise is Neuronal Synchronization? , 1995, Neural Computation.

[20]  M. Häusser,et al.  Dendritic coincidence detection of EPSPs and action potentials , 2001, Nature Neuroscience.

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

[22]  M. Shadlen,et al.  Neural Activity in Macaque Parietal Cortex Reflects Temporal Integration of Visual Motion Signals during Perceptual Decision Making , 2005, The Journal of Neuroscience.

[23]  M. Chacron,et al.  Neural Variability, Detection Thresholds, and Information Transmission in the Vestibular System , 2007, Journal of Neuroscience.

[24]  S. Thorpe,et al.  Dynamics of orientation coding in area V1 of the awake primate , 1993, Visual Neuroscience.

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

[26]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[27]  Maninder K. Kahlon,et al.  Visual Motion Analysis for Pursuit Eye Movements in Area MT of Macaque Monkeys , 1999, The Journal of Neuroscience.

[28]  J. Maunsell,et al.  Sensory modality specificity of neural activity related to memory in visual cortex. , 1997, Journal of neurophysiology.

[29]  D. Bradley,et al.  Neural population code for fine perceptual decisions in area MT , 2005, Nature Neuroscience.

[30]  H Barlow,et al.  Correspondence Noise and Signal Pooling in the Detection of Coherent Visual Motion , 1997, The Journal of Neuroscience.

[31]  A. Parker,et al.  Perceptually Bistable Three-Dimensional Figures Evoke High Choice Probabilities in Cortical Area MT , 2001, The Journal of Neuroscience.

[32]  S G Lisberger,et al.  Shifts in the Population Response in the Middle Temporal Visual Area Parallel Perceptual and Motor Illusions Produced by Apparent Motion , 2001, The Journal of Neuroscience.

[33]  Daeyeol Lee,et al.  Coding and transmission of information by neural ensembles , 2004, Trends in Neurosciences.

[34]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[35]  R. Romo,et al.  Neuronal correlates of subjective sensory experience , 2005, Nature Neuroscience.

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

[37]  Glenn C. Turner,et al.  Oscillations and Sparsening of Odor Representations in the Mushroom Body , 2002, Science.

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

[39]  J. Hegdé,et al.  Temporal dynamics of shape analysis in macaque visual area V2. , 2004, Journal of neurophysiology.

[40]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[41]  J. Maunsell,et al.  Attentional Modulation of Motion Integration of Individual Neurons in the Middle Temporal Visual Area , 2004, The Journal of Neuroscience.

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

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

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

[45]  André Longtin,et al.  Noise shaping by interval correlations increases information transfer. , 2004, Physical review letters.

[46]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[47]  Maurice J Chacron,et al.  Electroreceptor neuron dynamics shape information transmission , 2005, Nature Neuroscience.

[48]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[49]  M. Shadlen,et al.  A role for neural integrators in perceptual decision making. , 2003, Cerebral cortex.

[50]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

[51]  F Mechler,et al.  Robust Temporal Coding of Contrast by V1 Neurons for Transient But Not for Steady-State Stimuli , 1998, The Journal of Neuroscience.

[52]  Xiaoqin Wang,et al.  Temporal and rate representations of time-varying signals in the auditory cortex of awake primates , 2001, Nature Neuroscience.

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

[54]  R. Romo,et al.  Touch and go: decision-making mechanisms in somatosensation. , 2001, Annual review of neuroscience.

[55]  J. Donoghue,et al.  Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. , 1998, Journal of neurophysiology.

[56]  William R. Softky,et al.  Sub-millisecond coincidence detection in active dendritic trees , 1994, Neuroscience.

[57]  I. Lampl,et al.  Subthreshold oscillations of the membrane potential: a functional synchronizing and timing device. , 1993, Journal of neurophysiology.

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

[59]  John H. R. Maunsell,et al.  Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys , 1999, Visual Neuroscience.

[60]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[61]  Christopher C. Pack,et al.  Temporal dynamics of a neural solution to the aperture problem in visual area MT of macaque brain , 2001, Nature.

[62]  W. Singer,et al.  Rapid feature selective neuronal synchronization through correlated latency shifting , 2001, Nature Neuroscience.

[63]  M. Konishi,et al.  A circuit for detection of interaural time differences in the brain stem of the barn owl , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  G. Laurent,et al.  Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. , 2001, Science.

[65]  W. Newsome,et al.  Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  John H. R. Maunsell,et al.  Dynamics of neuronal responses in macaque MT and VIP during motion detection , 2002, Nature Neuroscience.

[67]  G. DeAngelis,et al.  A Logarithmic, Scale-Invariant Representation of Speed in Macaque Middle Temporal Area Accounts for Speed Discrimination Performance , 2005, The Journal of Neuroscience.

[68]  A. Parker,et al.  Neuronal activity and its links with the perception of multi-stable figures. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[70]  Victor A. F. Lamme The neurophysiology of figure-ground segregation in primary visual cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[71]  T. Sejnowski,et al.  Network Oscillations: Emerging Computational Principles , 2006, The Journal of Neuroscience.

[72]  G. Laurent,et al.  Multiplexing using synchrony in the zebrafish olfactory bulb , 2004, Nature Neuroscience.

[73]  Eero P. Simoncelli,et al.  Maximum Likelihood Estimation of a Stochastic Integrate-and-Fire Neural Encoding Model , 2004, Neural Computation.

[74]  Andreas T. Schaefer,et al.  Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. , 2003, Journal of neurophysiology.

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

[76]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[77]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[78]  J. Movshon,et al.  The Timing of Response Onset and Offset in Macaque Visual Neurons , 2002, The Journal of Neuroscience.

[79]  D. Contreras,et al.  Spatiotemporal Analysis of Local Field Potentials and Unit Discharges in Cat Cerebral Cortex during Natural Wake and Sleep States , 1999, The Journal of Neuroscience.

[80]  R. Shapley,et al.  Dynamics of Orientation Selectivity in the Primary Visual Cortex and the Importance of Cortical Inhibition , 2003, Neuron.