The Gamma Slideshow: Object-Based Perceptual Cycles in a Model of the Visual Cortex

While recent studies have shed light on the mechanisms that generate gamma (>40 Hz) oscillations, the functional role of these oscillations is still debated. Here we suggest that the purported mechanism of gamma oscillations (feedback inhibition from local interneurons), coupled with lateral connections implementing “Gestalt” principles of object integration, naturally leads to a decomposition of the visual input into object-based “perceptual cycles,” in which neuron populations representing different objects within the scene will tend to fire at successive cycles of the local gamma oscillation. We describe a simple model of V1 in which such perceptual cycles emerge automatically from the interaction between lateral excitatory connections (linking oriented cells falling along a continuous contour) and fast feedback inhibition (implementing competitive firing and gamma oscillations). Despite its extreme simplicity, the model spontaneously gives rise to perceptual cycles even when faced with natural images. The robustness of the system to parameter variation and to image complexity, together with the paucity of assumptions built in the model, support the hypothesis that perceptual cycles occur in natural vision.

[1]  R. von der Heydt,et al.  Synchrony and the binding problem in macaque visual cortex. , 2008, Journal of vision.

[2]  J. Lisman The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme , 2005, Hippocampus.

[3]  Victor A. F. Lamme,et al.  Synchrony and covariation of firing rates in the primary visual cortex during contour grouping , 2004, Nature Neuroscience.

[4]  Marco Idiart,et al.  A Second Function of Gamma Frequency Oscillations: An E%-Max Winner-Take-All Mechanism Selects Which Cells Fire , 2009, The Journal of Neuroscience.

[5]  S. Thorpe,et al.  Spike times make sense , 2005, Trends in Neurosciences.

[6]  T. Sejnowski,et al.  Cortical Enlightenment: Are Attentional Gamma Oscillations Driven by ING or PING? , 2009, Neuron.

[7]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[8]  B. C. Motter Central V4 Receptive Fields Are Scaled by the V1 Cortical Magnification and Correspond to a Constant-Sized Sampling of the V1 Surface , 2009, The Journal of Neuroscience.

[9]  Adriano B. L. Tort,et al.  Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons , 2009, Proceedings of the National Academy of Sciences.

[10]  U. Eysel,et al.  Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat. , 1997, Cerebral cortex.

[11]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[12]  R. von der Heydt,et al.  Illusory contours and cortical neuron responses. , 1984, Science.

[13]  Arnaud Delorme,et al.  Feed-forward contour integration in primary visual cortex based on asynchronous spike propagation , 2001, Neurocomputing.

[14]  A. Thiele,et al.  Neuronal synchrony does not correlate with motion coherence in cortical area MT , 2003, Nature.

[15]  R. VanRullen,et al.  The Phase of Ongoing EEG Oscillations Predicts Visual Perception , 2009, The Journal of Neuroscience.

[16]  C. Koch,et al.  Is perception discrete or continuous? , 2003, Trends in Cognitive Sciences.

[17]  R. F Hess,et al.  Contour integration and cortical processing , 2003, Journal of Physiology-Paris.

[18]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[19]  Xin Wang,et al.  Retinal Oscillations Carry Visual Information to Cortex , 2008, Front. Syst. Neurosci..

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

[21]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

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

[23]  Zhaoping Li,et al.  A Neural Model of Contour Integration in the Primary Visual Cortex , 1998, Neural Computation.

[24]  Risto Miikkulainen,et al.  Self-organization and segmentation in a laterally connected orientation map of spiking neurons , 1998, Neurocomputing.

[25]  Reinhard Eckhorn,et al.  Neural mechanisms of visual associative processing. , 2004, Acta neurobiologiae experimentalis.

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

[27]  Melanie R. Bernard,et al.  Abbreviated Title: , 2017 .

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

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

[30]  C T White,et al.  Intermittency in reaction time and perception, and evoked response correlates of image quality. , 1969, Acta psychologica.

[31]  R. Eckhorn,et al.  Contour decouples gamma activity across texture representation in monkey striate cortex. , 2000, Cerebral cortex.

[32]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

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

[34]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[35]  J. O’Neill,et al.  Gamma Oscillatory Firing Reveals Distinct Populations of Pyramidal Cells in the CA1 Region of the Hippocampus , 2008, The Journal of Neuroscience.

[36]  Stanislas Dehaene,et al.  Temporal Oscillations in Human Perception , 1993 .

[37]  Stephen Grossberg,et al.  Running as fast as it can: How spiking dynamics form object groupings in the laminar circuits of visual cortex , 2010, Journal of Computational Neuroscience.

[38]  Reinhard Eckhorn,et al.  A neural network for scene segmentation by temporal coding , 1996, Neurocomputing.

[39]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[40]  Walter J Freeman,et al.  A cinematographic hypothesis of cortical dynamics in perception. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  Markus Siegel,et al.  Phase-dependent neuronal coding of objects in short-term memory , 2009, Proceedings of the National Academy of Sciences.

[42]  C. Koch,et al.  Attention-driven discrete sampling of motion perception. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[43]  D. McCormick,et al.  Inhibitory Postsynaptic Potentials Carry Synchronized Frequency Information in Active Cortical Networks , 2005, Neuron.

[44]  H. Robinson,et al.  Recurrent Synaptic Input and the Timing of Gamma-Frequency-Modulated Firing of Pyramidal Cells during Neocortical “UP” States , 2008, The Journal of Neuroscience.

[45]  J E Lisman,et al.  Storage of 7 +/- 2 short-term memories in oscillatory subcycles , 1995, Science.

[46]  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.

[47]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[48]  C. Koch,et al.  An oscillation-based model for the neuronal basis of attention , 1993, Vision Research.

[49]  C. Gross,et al.  Representation of visual stimuli in inferior temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[50]  P L Latour,et al.  Evidence of internal clocks in the human operator. , 1967, Acta psychologica.