Abstract

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.

Highlights

  • While oscillatory activity pervades the brain, its functional implications are still a matter of intense research

  • We suggest that the purported mechanism of gamma oscillations, 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

  • A clear signature of perceptual cycles emerges, in the form of negative correlation between the firing activities of cells responding to different objects, and positive correlation for cells responding to the same object

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Summary

Introduction

While oscillatory activity pervades the brain, its functional implications are still a matter of intense research. Gammaband oscillations (>40 Hz) have attracted significant attention since their discovery in feline visual cortex two decades ago (Eckhorn et al, 1988; Gray and Singer, 1989). Several functional roles have been suggested for gamma-band oscillations, including assisting selective attention (Niebur et al, 1993; Womelsdorf and Fries, 2007), controlling transient communication between distant regions (Fries, 2005), serving as a reference frame for temporal coding (Vanrullen et al, 2005a; Fries et al, 2007), organizing discrete items in working memory (Lisman, 2005), etc. The well-known binding-by-synchrony hypothesis posits that spatially distant neurons corresponding to a common object or concept will tend to fire together, allowing for their identification as a single representation by downstream centers (von der Malsburg, 1981; Singer, 1999). Evidence for this proposal has been reported in the context of visual perception (Gray et al, 1989; Gail et al, 2000; Samonds et al, 2006), though the hypothesis is still controversial (Thiele and Stoner, 2003; Roelfsema et al, 2004; Dong et al, 2008; Leveille et al, 2010)

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