Local and Global Correlations between Neurons in the Middle Temporal Area of Primate Visual Cortex.

In humans and other primates, the analysis of visual motion includes populations of neurons in the middle-temporal (MT) area of visual cortex. Motion analysis will be constrained by the structure of neural correlations in these populations. Here, we use multi-electrode arrays to measure correlations in anesthetized marmoset, a New World monkey where area MT lies exposed on the cortical surface. We measured correlations in the spike count between pairs of neurons and within populations of neurons, for moving dot fields and moving gratings. Correlations were weaker in area MT than in area V1. The magnitude of correlations in area MT diminished with distance between receptive fields, and difference in preferred direction. Correlations during presentation of moving gratings were stronger than those during presentation of moving dot fields, extended further across cortex, and were less dependent on the functional properties of neurons. Analysis of the timescales of correlation suggests presence of 2 mechanisms. A local mechanism, associated with near-synchronous spiking activity, is strongest in nearby neurons with similar direction preference and is independent of visual stimulus. A global mechanism, operating over larger spatial scales and longer timescales, is independent of direction preference and is modulated by the type of visual stimulus presented.

[1]  J. Bullier,et al.  Cross-correlation study of the temporal interactions between areas V1 and V2 of the macaque monkey. , 1999, Journal of neurophysiology.

[2]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.

[3]  G. Elston,et al.  Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex , 2000, The Journal of Neuroscience.

[4]  Lawrence C. Sincich,et al.  Bypassing V1: a direct geniculate input to area MT , 2004, Nature Neuroscience.

[5]  M. Rosa,et al.  Chemoarchitecture of the middle temporal visual area in the marmoset monkey (Callithrix jacchus): Laminar distribution of calcium‐binding proteins (calbindin, parvalbumin) and nonphosphorylated neurofilament , 2007, The Journal of comparative neurology.

[6]  P. Lennie,et al.  Information Conveyed by Onset Transients in Responses of Striate Cortical Neurons , 2001, The Journal of Neuroscience.

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

[8]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[9]  F. Mechler,et al.  Independent and Redundant Information in Nearby Cortical Neurons , 2001, Science.

[10]  Pascal Mamassian,et al.  More is not always better: adaptive gain control explains dissociation between perception and action , 2012, Nature Neuroscience.

[11]  R. Normann,et al.  A method for pneumatically inserting an array of penetrating electrodes into cortical tissue , 2006, Annals of Biomedical Engineering.

[12]  Marcello G P Rosa,et al.  Quantitative analysis of the corticocortical projections to the middle temporal area in the marmoset monkey: evolutionary and functional implications. , 2006, Cerebral cortex.

[13]  W. Newsome,et al.  Estimates of the Contribution of Single Neurons to Perception Depend on Timescale and Noise Correlation , 2009, The Journal of Neuroscience.

[14]  Nicholas J. Priebe,et al.  Estimating Target Speed from the Population Response in Visual Area MT , 2004, The Journal of Neuroscience.

[15]  Valentin Dragoi,et al.  Adaptive coding of visual information in neural populations , 2008, Nature.

[16]  J Allman,et al.  Direction- and Velocity-Specific Responses from beyond the Classical Receptive Field in the Middle Temporal Visual Area (MT) , 1985, Perception.

[17]  A. B. Bonds,et al.  Burst firing and modulation of functional connectivity in cat striate cortex. , 1998, Journal of neurophysiology.

[18]  M. A. Smith,et al.  Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque , 2005, The Journal of Neuroscience.

[19]  Lyle J. Graham,et al.  Orientation and Direction Selectivity of Synaptic Inputs in Visual Cortical Neurons A Diversity of Combinations Produces Spike Tuning , 2003, Neuron.

[20]  Edward M. Callaway,et al.  A Disynaptic Relay from Superior Colliculus to Dorsal Stream Visual Cortex in Macaque Monkey , 2010, Neuron.

[21]  Eero P. Simoncelli,et al.  Natural signal statistics and sensory gain control , 2001, Nature Neuroscience.

[22]  Asohan Amarasingham,et al.  Conditional modeling and the jitter method of spike resampling. , 2012, Journal of neurophysiology.

[23]  Eero P. Simoncelli,et al.  A model of neuronal responses in visual area MT , 1998, Vision Research.

[24]  Nicholas J. Priebe,et al.  The Emergence of Contrast-Invariant Orientation Tuning in Simple Cells of Cat Visual Cortex , 2007, Neuron.

[25]  M. A. Smith,et al.  Correlations and brain states: from electrophysiology to functional imaging , 2009, Current Opinion in Neurobiology.

[26]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  P. L. V. Kan,et al.  Response covariance in cat visual cortex , 2004, Experimental Brain Research.

[28]  E. Seidemann,et al.  Optimal decoding of correlated neural population responses in the primate visual cortex , 2006, Nature Neuroscience.

[29]  Marc A Sommer,et al.  Spatial and Temporal Scales of Neuronal Correlation in Visual Area V4 , 2013, The Journal of Neuroscience.

[30]  Eero P. Simoncelli,et al.  How MT cells analyze the motion of visual patterns , 2006, Nature Neuroscience.

[31]  G. Elston,et al.  Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): Middle temporal area, middle temporal crescent, and surrounding cortex , 1998, The Journal of comparative neurology.

[32]  M. A. Smith,et al.  Stimulus Selectivity and Spatial Coherence of Gamma Components of the Local Field Potential , 2011, The Journal of Neuroscience.

[33]  S. Solomon,et al.  Spatial properties of koniocellular cells in the lateral geniculate nucleus of the marmoset Callithrix jacchus , 2001, The Journal of physiology.

[34]  Craig T. Nordhausen,et al.  Single unit recording capabilities of a 100 microelectrode array , 1996, Brain Research.

[35]  Michael Graupner,et al.  Synaptic Input Correlations Leading to Membrane Potential Decorrelation of Spontaneous Activity in Cortex , 2013, The Journal of Neuroscience.

[36]  R. Born,et al.  Stimulus-Dependent Modulation of Suppressive Influences in MT , 2011, The Journal of Neuroscience.

[37]  M. Cohen,et al.  Measuring and interpreting neuronal correlations , 2011, Nature Neuroscience.

[38]  Selina S. Solomon,et al.  Integration and segregation of multiple motion signals by neurons in area MT of primate. , 2014, Journal of neurophysiology.

[39]  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.

[40]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[41]  F. Attneave.  Some informational aspects of visual perception. , 1954, Psychological review.

[42]  K. Hoffmann,et al.  Synchronization of Neuronal Activity during Stimulus Expectation in a Direction Discrimination Task , 1997, The Journal of Neuroscience.

[43]  Nikos K Logothetis,et al.  Statistical comparison of spike responses to natural stimuli in monkey area V1 with simulated responses of a detailed laminar network model for a patch of V1. , 2011, Journal of neurophysiology.

[44]  W. Bair,et al.  Correlated Firing in Macaque Visual Area MT: Time Scales and Relationship to Behavior , 2001, The Journal of Neuroscience.

[45]  Adam Kohn,et al.  Laminar dependence of neuronal correlations in visual cortex. , 2013, Journal of neurophysiology.

[46]  J. Bullier,et al.  Structural basis of cortical synchronization. I. Three types of interhemispheric coupling. , 1995, Journal of neurophysiology.

[47]  Paul R. Martin,et al.  Cortical-Like Receptive Fields in the Lateral Geniculate Nucleus of Marmoset Monkeys , 2013, The Journal of Neuroscience.

[48]  E. Seidemann,et al.  Optimal temporal decoding of neural population responses in a reaction-time visual detection task. , 2008, Journal of neurophysiology.

[49]  Pieter R. Roelfsema,et al.  Noise Correlations Have Little Influence on the Coding of Selective Attention in Area V1 , 2008, Cerebral cortex.

[50]  Leo L. Lui,et al.  Spatial summation, end inhibition and side inhibition in the middle temporal visual area (MT). , 2007, Journal of neurophysiology.

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

[52]  Paul R. Martin,et al.  Slow intrinsic rhythm in the koniocellular visual pathway , 2011, Proceedings of the National Academy of Sciences.

[53]  J.P. Donoghue,et al.  Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[54]  R E Weller,et al.  Cortical connections of the middle temporal visual area (MT) and the superior temporal cortex in owl monkeys , 1984, The Journal of comparative neurology.

[55]  Yong Gu,et al.  Perceptual Learning Reduces Interneuronal Correlations in Macaque Visual Cortex , 2011, Neuron.

[56]  D. Bradley,et al.  Structure and function of visual area MT. , 2005, Annual review of neuroscience.

[57]  Leo L. Lui,et al.  Spatial and temporal frequency tuning in striate cortex: functional uniformity and specializations related to receptive field eccentricity , 2010, The European journal of neuroscience.

[58]  G. P. Moore,et al.  Statistical signs of synaptic interaction in neurons. , 1970, Biophysical journal.

[59]  R A Andersen,et al.  The response of area MT and V1 neurons to transparent motion , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  Xin Huang,et al.  Noise correlations in cortical area MT and their potential impact on trial-by-trial variation in the direction and speed of smooth-pursuit eye movements. , 2009, Journal of neurophysiology.

[61]  Valentin Dragoi,et al.  Correlated Variability in Laminar Cortical Circuits , 2012, Neuron.

[62]  Yong Gu,et al.  Choice-related activity and correlated noise in subcortical vestibular neurons , 2012, Nature Neuroscience.

[63]  P A Salin,et al.  Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. , 1992, Journal of neurophysiology.

[64]  Tai Sing Lee,et al.  Cooperative and Competitive Interactions Facilitate Stereo Computations in Macaque Primary Visual Cortex , 2009, The Journal of Neuroscience.

[65]  E. Callaway,et al.  The Parvocellular LGN Provides a Robust Disynaptic Input to the Visual Motion Area MT , 2006, Neuron.

[66]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  Paul Antoine Salin,et al.  Spatial and temporal coherence in cortico-cortical connections: a cross-correlation study in areas 17 and 18 in the cat. , 1992, Visual neuroscience.

[68]  S. Laughlin,et al.  Predictive coding: a fresh view of inhibition in the retina , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[69]  Louise S. Delicato,et al.  Stimulus-induced dissociation of neuronal firing rates and local field potential gamma power and its relationship to the blood oxygen level-dependent signal in macaque primary visual cortex , 2011, The European journal of neuroscience.

[70]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[71]  J. Anthony Movshon,et al.  Comparison of Recordings from Microelectrode Arrays and Single Electrodes in the Visual Cortex , 2007, The Journal of Neuroscience.

[72]  J. Bourne,et al.  Retinal Afferents Synapse with Relay Cells Targeting the Middle Temporal Area in the Pulvinar and Lateral Geniculate Nuclei , 2009, Front. Neuroanat..

[73]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[74]  Dora E Angelaki,et al.  Functional Specializations of the Ventral Intraparietal Area for Multisensory Heading Discrimination , 2013, The Journal of Neuroscience.

[75]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[76]  Chris Tailby,et al.  Visual motion integration by neurons in the middle temporal area of a New World monkey, the marmoset , 2011, The Journal of physiology.

[77]  Paul R. Martin,et al.  Extraclassical Receptive Field Properties of Parvocellular, Magnocellular, and Koniocellular Cells in the Primate Lateral Geniculate Nucleus , 2002, The Journal of Neuroscience.

[78]  H. Tamura,et al.  Horizontal interactions between visual cortical neurones studied by cross‐correlation analysis in the cat. , 1991, The Journal of physiology.

[79]  Alexander S. Ecker,et al.  The effect of noise correlations in populations of diversely tuned neurons , 2011 .

[80]  H. B. Barlow,et al.  Possible Principles Underlying the Transformations of Sensory Messages , 2012 .

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