Multiscale functional imaging in V1 and cortical correlates of apparent motion

In vivo intracellular electrophysiology offers the unique possibility of listening to the “synaptic rumor” of the cortical network captured by the recording electrode in a single V1 cell. The analysis of synaptic echoes evoked during sensory processing is used to reconstruct the distribution of input sources in visual space and time. It allows us to infer, in the cortical space, the dynamics of the effective input network afferent to the recorded cell. We have applied this method to demonstrate the propagation of visually evoked activity through lateral (and possibly feedback) connectivity in the primary cortex of higher mammals. This approach, based on functional synaptic imaging, is compared here with a real-time functional network imaging technique, based on the use of voltage-sensitive fluorescent dyes. The former method gives access to microscopic convergence processes during synaptic integration in a single neuron, while the latter describes the macroscopic divergence process at the neuronal map level. The joint application of the two techniques, which address two different scales of integration, is used to elucidate the cortical origin of low-level (non-attentive) binding processes participating in the emergence of illusory motion percepts predicted by the psychological Gestalt theory.

[1]  G. Rees,et al.  Neuroimaging: Decoding mental states from brain activity in humans , 2006, Nature Reviews Neuroscience.

[2]  P. Roland,et al.  Cortical feedback depolarization waves: A mechanism of top-down influence on early visual areas , 2006, Proceedings of the National Academy of Sciences.

[3]  Y. Frégnac,et al.  The “silent” surround of V1 receptive fields: theory and experiments , 2003, Journal of Physiology-Paris.

[4]  R. Frostig,et al.  Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  J. B. Levitt,et al.  Contrast dependence of contextual effects in primate visual cortex , 1997, nature.

[6]  Jean-Baptiste Poline,et al.  Inverse retinotopy: Inferring the visual content of images from brain activation patterns , 2006, NeuroImage.

[7]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[8]  M. Shiffrar,et al.  Perceived speed of moving lines depends on orientation, length, speed and luminance , 1993, Vision Research.

[9]  U. Polat,et al.  Lateral interactions between spatial channels: Suppression and facilitation revealed by lateral masking experiments , 1993, Vision Research.

[10]  U. Polat,et al.  Collinear stimuli regulate visual responses depending on cell's contrast threshold , 1998, Nature.

[11]  Jean Lorenceau,et al.  Orientation dependent modulation of apparent speed: psychophysical evidence , 2002, Vision Research.

[12]  Jian-Young Wu,et al.  Compression and Reflection of Visually Evoked Cortical Waves , 2007, Neuron.

[13]  Michael P. Stryker,et al.  New Paradigm for Optical Imaging Temporally Encoded Maps of Intrinsic Signal , 2003, Neuron.

[14]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[15]  Mark W. Cannon,et al.  Spatial interactions in apparent contrast: Individual differences in enhancement and suppression effects , 1993, Vision Research.

[16]  David J. Field,et al.  Contour integration by the human visual system: Evidence for a local “association field” , 1993, Vision Research.

[17]  M. Tanifuji,et al.  Horizontal Propagation of Excitation in Rat Visual Cortical Slices Revealed by Optical Imaging , 1994 .

[18]  C. Gilbert,et al.  Synaptic physiology of horizontal connections in the cat's visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Amiram Grinvald,et al.  VSDI: a new era in functional imaging of cortical dynamics , 2004, Nature Reviews Neuroscience.

[20]  M. Carandini,et al.  Stimulus contrast modulates functional connectivity in visual cortex , 2009, Nature Neuroscience.

[21]  V. Bringuier,et al.  The visual cortical association field: A Gestalt concept or a psychophysiological entity? , 2000, Journal of Physiology-Paris.

[22]  Frans A. J. Verstraten,et al.  The motion aftereffect , 1998, Trends in Cognitive Sciences.

[23]  Amiram Grinvald,et al.  Imaging Cortical Dynamics at High Neurotechnique Spatial and Temporal Resolution with Novel Blue Voltage-Sensitive Dyes , 1999 .

[24]  Y. Frégnac,et al.  Orientation dependent modulation of apparent speed: a model based on the dynamics of feed-forward and horizontal connectivity in V1 cortex , 2002, Vision Research.

[25]  Leonard E. White,et al.  Mapping multiple features in the population response of visual cortex , 2003, Nature.

[26]  Robert A. Frazor,et al.  Standing Waves and Traveling Waves Distinguish Two Circuits in Visual Cortex , 2007, Neuron.

[27]  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.

[28]  Akitoshi Hanazawa,et al.  Cortical Dynamics Subserving Visual Apparent Motion , 2008, Cerebral cortex.

[29]  Chantal Delon-Martin,et al.  fMRI Retinotopic Mapping—Step by Step , 2002, NeuroImage.

[30]  N. Kanwisher,et al.  Feedback of pVisual Object Information to Foveal Retinotopic Cortex , 2008, Nature Neuroscience.

[31]  David Alais,et al.  The mechanisms of collinear integration. , 2006, Journal of vision.

[32]  J. Daugman Uncertainty relation for resolution in space, spatial frequency, and orientation optimized by two-dimensional visual cortical filters. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[33]  G. Mitchison,et al.  Long axons within the striate cortex: their distribution, orientation, and patterns of connection. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[34]  E. Switkes,et al.  Deoxyglucose analysis of retinotopic organization in primate striate cortex. , 1982, Science.

[35]  Y. Frégnac,et al.  Visual input evokes transient and strong shunting inhibition in visual cortical neurons , 1998, Nature.

[36]  R. Douglas,et al.  A Quantitative Map of the Circuit of Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[37]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[38]  S. Nelson,et al.  Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. , 1998, Journal of neurophysiology.

[39]  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.

[40]  Jean Bullier,et al.  The Timing of Information Transfer in the Visual System , 1997 .

[41]  H. K. Hartline,et al.  THE RESPONSE OF SINGLE OPTIC NERVE FIBERS OF THE VERTEBRATE EYE TO ILLUMINATION OF THE RETINA , 1938 .

[42]  Randolph Blake,et al.  Hierarchy of cortical responses underlying binocular rivalry , 2007, Nature Neuroscience.

[43]  F. Chavane,et al.  Imaging cortical correlates of illusion in early visual cortex , 2004, Nature.

[44]  J. Stone,et al.  Conduction velocity of afferents to cat visual cortex: a correlation with cortical receptive field properties. , 1971, Brain research.

[45]  D. Coulter,et al.  In vitro functional imaging in brain slices using fast voltage-sensitive dye imaging combined with whole-cell patch recording , 2008, Nature Protocols.

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

[47]  Per E. Roland,et al.  Dynamic depolarization fields in the cerebral cortex , 2002, Trends in Neurosciences.

[48]  V. Bringuier,et al.  Spatio-temporal dynamics of synaptic integration in cat visual cortical receptive fields , 1996 .

[49]  O. Hikosaka,et al.  Focal visual attention produces illusory temporal order and motion sensation , 1993, Vision Research.