Contextual modulation of synchronization to random dots in the cat visual cortex

Synchronization of neuronal activity has been proposed as a binding mechanism for integration of image properties into one coherent percept. In the present study, we investigated the contextual modulation of synchronization to random dot patterns. Coherent motion of random dots evoked well synchronized responses in area 17 of anaesthetized cats when the stimulus was presented in the compound receptive field of recorded sites. Gradually changing the directional coherence of random dots in the surround while maintaining fully coherent motion of the stimulus in the receptive field significantly suppressed synchronization of neuronal activity for some stimulus conditions. However, usually one or two peaks of increased synchronization were found in the surround coherence tuning curves with low (8–12%) and/or moderate (25–50%) coherence in the surround. At the population level, synchronization was significantly depressed with incoherent motion in the receptive field and when both the surround and the receptive field were jointly stimulated with 0% coherence. The intriguing finding was the discovery of two distinct groups of cells with opposite synchronization changes dependent on the presence or absence of significant synchronization in their spontaneous activity. The latter group of neurons showed peaks of increased synchronization with lower surround coherence, thus probably being more sensitive to the direction of the surround motion. Overall, our findings support the notion that binding of stimulus properties can be achieved by synchronized activity of cortical cells. However, our findings go further than the original hypothesis of feature binding by synchrony to show that synchronization of cortical activity may be directly related to the decision making processes, which in turn are related to the threshold of perception of coherent motion.

[1]  J. Movshon,et al.  Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[2]  P. H. Schiller,et al.  Neural responses to relative speed in the primary visual cortex of rhesus monkey , 2003, Visual Neuroscience.

[3]  A. Destexhe,et al.  Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. , 2000, Journal of neurophysiology.

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

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

[6]  Heribert J. P. Reitboeck,et al.  A 19-channel matrix drive with individually controllable fiber microelectrodes for neurophysiological applications , 1983, IEEE Transactions on Systems, Man, and Cybernetics.

[7]  S. Molotchnikoff,et al.  Relationships between image structure and gamma oscillations and synchronization in visual cortex of cats , 2000, The European journal of neuroscience.

[8]  J. Nelson,et al.  Orientation-selective inhibition from beyond the classic visual receptive field , 1978, Brain Research.

[9]  O. Creutzfeldt,et al.  An intracellular analysis of visual cortical neurones to moving stimuli: Responses in a co-operative neuronal network , 2004, Experimental Brain Research.

[10]  J. Csicsvari,et al.  Intracellular features predicted by extracellular recordings in the hippocampus in vivo. , 2000, Journal of neurophysiology.

[11]  Yumiko Yoshimura,et al.  Suppressive effects of receptive field surround on neuronal activity in the cat primary visual cortex , 2002, Neuroscience Research.

[12]  Christoph von der Malsburg,et al.  The Correlation Theory of Brain Function , 1994 .

[13]  Kazuyuki Aihara,et al.  Dynamical Cell Assembly Hypothesis -- Theoretical Possibility of Spatio-temporal Coding in the Cortex , 1996, Neural Networks.

[14]  Andrea Hasenstaub,et al.  Barrages of Synaptic Activity Control the Gain and Sensitivity of Cortical Neurons , 2003, The Journal of Neuroscience.

[15]  B. McNaughton,et al.  Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex , 1995, Journal of Neuroscience Methods.

[16]  W. J. Melssen,et al.  Detection and estimation of neural connectivity based on crosscorrelation analysis , 1987, Biological Cybernetics.

[17]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[18]  F. Wörgötter,et al.  Context, state and the receptive fields of striatal cortex cells , 2000, Trends in Neurosciences.

[19]  D. Mackay,et al.  Modulatory influences of moving textured backgrounds on responsiveness of simple cells in feline striate cortex , 1981, The Journal of physiology.

[20]  R. L. de Valois,et al.  Responses of simple and complex cells to random dot patterns: a quantitative comparison. , 1988, Journal of neurophysiology.

[21]  S. Kastner,et al.  Neuronal Correlates of Pop-out in Cat Striate Cortex , 1997, Vision Research.

[22]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

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

[24]  Andrew T. Smith,et al.  Is global motion really based on spatial integration of local motion signals? , 1994, Vision Research.

[25]  J J Eggermont,et al.  Neural interaction in cat primary auditory cortex. Dependence on recording depth, electrode separation, and age. , 1992, Journal of neurophysiology.

[26]  Stimuli outside the classical receptive field modulate the synchronization of action potentials between cells in visual cortex of cats , 2000, Neuroreport.

[27]  P König,et al.  Direct physiological evidence for scene segmentation by temporal coding. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[28]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[29]  O. Braddick,et al.  What is Noise for the Motion System? , 1996, Vision Research.

[30]  Chris J. Tinsley,et al.  Gain control from beyond the classical receptive field in primate primary visual cortex , 2003, Visual Neuroscience.

[31]  W. Singer,et al.  Temporal coding in the visual cortex: new vistas on integration in the nervous system , 1992, Trends in Neurosciences.

[32]  D. V. van Essen,et al.  Response modulation by texture surround in primate area V1: Correlates of “popout” under anesthesia , 1999, Visual Neuroscience.

[33]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[34]  K. Albus,et al.  Effects of interacting visual patterns on single cell responses in cat's striate cortex , 1977, Vision Research.

[35]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[36]  C. Gray,et al.  Dynamics of striate cortical activity in the alert macaque: II. Fast time scale synchronization. , 2000, Cerebral cortex.

[37]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[38]  J S Lappin,et al.  The perceptual coherence of moving visual patterns. , 1981, Acta psychologica.

[39]  S Molotchnikoff,et al.  Modulation of the synchronization between cells in visual cortex by contextual targets , 2001, The European journal of neuroscience.

[40]  W Singer,et al.  Role of the temporal domain for response selection and perceptual binding. , 1997, Cerebral cortex.

[41]  Roman Bauer,et al.  Different rules of spatial summation from beyond the receptive field for spike rates and oscillation amplitudes in cat visual cortex , 1995, Brain Research.

[42]  M. Livingstone,et al.  Mechanisms of Direction Selectivity in Macaque V1 , 1998, Neuron.

[43]  L. Palmer,et al.  Effects of surround motion on receptive-field gain and structure in area 17 of the cat , 2002, Visual Neuroscience.

[44]  H. Vaughan,et al.  Averaged multiple unit activity as an estimate of phasic changes in local neuronal activity: effects of volume-conducted potentials , 1980, Journal of Neuroscience Methods.

[45]  Salvatore Squatrito,et al.  Influences of uniform and textured backgrounds on the impulse activity of neurons in area V1 of the alert macaque , 1990, Brain Research.

[46]  F. Grover,et al.  Correlation of cell size with amplitude of background fast activity in specific brain nuclei. , 1970, Journal of neurophysiology.

[47]  W. Singer,et al.  In search of common foundations for cortical computation , 1997, Behavioral and Brain Sciences.

[48]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[49]  R. Eckhorn,et al.  Oscillatory and non-oscillatory synchronizations in the visual cortex and their possible roles in associations of visual features. , 1994, Progress in brain research.

[50]  S Molotchnikoff,et al.  Comparative computations of spike synchronization in visual cortex of cats. , 2001, Brain research. Brain research protocols.

[51]  R. S. J. Frackowiak,et al.  Activity in human areas V1/V2, V3 and V5 during the perception of coherent and incoherent motion , 1996, NeuroImage.

[52]  K. Albus A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat , 1975, Experimental brain research.

[53]  H. Jones,et al.  Context-dependent interactions and visual processing in V1 , 1996, Journal of Physiology-Paris.

[54]  G. Orban,et al.  Human velocity and direction discrimination measured with random dot patterns , 1988, Vision Research.

[55]  R. Eckhorn,et al.  A Model of Figure/Ground Separation Based on Correlated Neural Activity in the Visual System , 1987 .

[56]  C. Malsburg Nervous Structures with Dynamical Links , 1985 .

[57]  A. Sillito,et al.  Surround suppression in primate V1. , 2001, Journal of neurophysiology.

[58]  P. Milner A model for visual shape recognition. , 1974, Psychological review.

[59]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[60]  A. Aertsen,et al.  Evaluation of neuronal connectivity: Sensitivity of cross-correlation , 1985, Brain Research.

[61]  Simone Cardoso Synchronization of Neuronal Activity during Stimulus Expectation in a Direction Discrimination Task , 1997 .

[62]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[63]  D. Fitzpatrick Seeing beyond the receptive field in primary visual cortex , 2000, Current Opinion in Neurobiology.