Mechanisms for Phase Shifting in Cortical Networks and their Role in Communication through Coherence.

Paul H Tiesinga,Terrence J Sejnowski

doi:10.3389/fnhum.2010.00196

Abstract

In the primate visual cortex, the phase of spikes relative to oscillations in the local field potential (LFP) in the gamma frequency range (30–80 Hz) can be shifted by stimulus features such as orientation and thus the phase may carry information about stimulus identity. According to the principle of communication through coherence (CTC), the relative LFP phase between the LFPs in the sending and receiving circuits affects the effectiveness of the transmission. CTC predicts that phase shifting can be used for stimulus selection. We review and investigate phase shifting in models of periodically driven single neurons and compare it with phase shifting in models of cortical networks. In a single neuron, as the driving current is increased, the spike phase varies systematically while the firing rate remains constant. In a network model of reciprocally connected excitatory (E) and inhibitory (I) cells phase shifting occurs in response to both injection of constant depolarizing currents and to brief pulses to I cells. These simple models provide an account for phase-shifting observed experimentally and suggest a mechanism for implementing CTC. We discuss how this hypothesis can be tested experimentally using optogenetic techniques.

Highlights

The firing rates of many neurons in the visual cortex are sensitive to the orientation of stimuli in their receptive field (Hubel and Wiesel, 1968; Ferster and Miller, 2000), but this response can be modulated by changes in brain state, such as those induced by selective attention (Desimone and Duncan, 1995)
We proposed a mechanism for selective attention (Tiesinga et al, 2004, 2008) based on the synchrony of inhibitory networks and found the conditions under which this mechanism could account for the experimentally observed multiplicative gain of orientation tuning curves (McAdams and Maunsell, 1999), increased local field potential (LFP) power in the gamma frequency range (Fries et al, 2001, 2008), and increased phase locking of spikes to the gamma oscillations in the LFP (Fries et al, 2001, 2008)
Modulation of single neuron activity by the relative phase between periodic excitatory and inhibitory inputs Consider two local circuits, both projecting to a third circuit (Figure 1A), each comprised of E and I cells, with at least a projection from the local I cells to the E cells

Summary

Introduction

The firing rates of many neurons in the visual cortex are sensitive to the orientation of stimuli in their receptive field (Hubel and Wiesel, 1968; Ferster and Miller, 2000), but this response can be modulated by changes in brain state, such as those induced by selective attention (Desimone and Duncan, 1995). If the subject is interested in only one of the two stimuli, the impact of the other stimulus should be reduced and/or the response to the attended stimulus should be strengthened This can be achieved by increasing/reducing the activity in the corresponding upstream area of the cells responding to the attended/ignored stimulus, respectively, or by making the projection more or less effective. It is likely that a combination of the two processes is responsible for stimulus selection, we focus here on the latter

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