Abstract

Visually induced neuronal activity in V1 displays a marked gamma-band component which is modulated by stimulus properties. It has been argued that synchronized oscillations contribute to these gamma-band activity. However, analysis of Local Field Potentials (LFPs) across different experiments reveals considerable diversity in the degree of oscillatory behavior of this induced activity. Contrast-dependent power enhancements can indeed occur over a broad band in the gamma frequency range and spectral peaks may not arise at all. Furthermore, even when oscillations are observed, they undergo temporal decorrelation over very few cycles. This is not easily accounted for in previous network modeling of gamma oscillations. We argue here that interactions between cortical layers can be responsible for this fast decorrelation. We study a model of a V1 hypercolumn, embedding a simplified description of the multi-layered structure of the cortex. When the stimulus contrast is low, the induced activity is only weakly synchronous and the network resonates transiently without developing collective oscillations. When the contrast is high, on the other hand, the induced activity undergoes synchronous oscillations with an irregular spatiotemporal structure expressing a synchronous chaotic state. As a consequence the population activity undergoes fast temporal decorrelation, with concomitant rapid damping of the oscillations in LFPs autocorrelograms and peak broadening in LFPs power spectra. We show that the strength of the inter-layer coupling crucially affects this spatiotemporal structure. We predict that layer VI inactivation should induce global changes in the spectral properties of induced LFPs, reflecting their slower temporal decorrelation in the absence of inter-layer feedback. Finally, we argue that the mechanism underlying the emergence of synchronous chaos in our model is in fact very general. It stems from the fact that gamma oscillations induced by local delayed inhibition tend to develop chaos when coupled by sufficiently strong excitation.

Highlights

  • An increase of activity in the gamma band (30–100 Hz) is observed in Local Field Potential (LFP) and Multi-Unit Activity (MUA) recordings [1,2,3,4,5,6,7,8,9,10,11,12,13,14], as well as in EEG and Electrocorticogram studies [15,16] in primary visual cortex (V1) upon visual stimulation

  • Delayed inhibition, without need of an active involvement of excitatory populations, is capable inducing collective synchronous oscillations in neuronal activity. The frequency of these oscillations falls in the gamma band if the synaptic time constant of the inhibition is in an appropriate range

  • Relying on extensive numerical simulations, we show that our model displays broad-band gamma modulations of the spectra of LFPs upon stimulation of the network at low as well as at high contrast

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Summary

Introduction

An increase of activity in the gamma band (30–100 Hz) is observed in Local Field Potential (LFP) and Multi-Unit Activity (MUA) recordings [1,2,3,4,5,6,7,8,9,10,11,12,13,14], as well as in EEG and Electrocorticogram studies [15,16] in primary visual cortex (V1) upon visual stimulation. In one possible scenario, the dynamics of the inhibitory postsynaptic currents is non-instantaneous (due to axonal delays, and to finite synaptic time-constants). Delayed inhibition, without need of an active involvement of excitatory populations, is capable inducing collective synchronous oscillations in neuronal activity The frequency of these oscillations falls in the gamma band if the synaptic time constant of the inhibition is in an appropriate range. In addition to the LGN input, excitatory and inhibitory cells are driven by an untuned noisy input, representing the background firing of other cortical areas This input is modeled by a single AMPA-type synapse per cell, with peak conductance gbg activated by Ornstein-Uhlenbeck processes [61]. Following [108], the numerical integration of the membrane potential V of a given neuron is stopped as soon as V reaches a gbg

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