Abstract

A central problem in cortical processing including sensory binding and attentional gating is how neurons can synchronize their responses with zero or near-zero time lag. For a spontaneously firing neuron, an input from another neuron can delay or advance the next spike by different amounts depending upon the timing of the input relative to the previous spike. This information constitutes the phase response curve (PRC). We present a simple graphical method for determining the effect of PRC shape on synchronization tendencies and illustrate it using type 1 PRCs, which consist entirely of advances (delays) in response to excitation (inhibition). We obtained the following generic solutions for type 1 PRCs, which include the pulse-coupled leaky integrate and fire model. For pairs with mutual excitation, exact synchrony can be stable for strong coupling because of the stabilizing effect of the causal limit region of the PRC in which an input triggers a spike immediately upon arrival. However, synchrony is unstable for short delays, because delayed inputs arrive during a refractory period and cannot trigger an immediate spike. Right skew destabilizes antiphase and enables modes with time lags that grow as the conduction delay is increased. Therefore, right skew favors near synchrony at short conduction delays and a gradual transition between synchrony and antiphase for pairs coupled by mutual excitation. For pairs with mutual inhibition, zero time lag synchrony is stable for conduction delays ranging from zero to a substantial fraction of the period for pairs. However, for right skew there is a preferred antiphase mode at short delays. In contrast to mutual excitation, left skew destabilizes antiphase for mutual inhibition so that synchrony dominates at short delays as well. These pairwise synchronization tendencies constrain the synchronization properties of neurons embedded in larger networks.

Highlights

  • A role has been proposed for synchronous oscillations in binding of sensory experiences (Singer, 1993) and attention (Fries et al, 2001)

  • SUMMARY The major result of this paper is to understand how the shape of the phase response curve (PRC) determines the generic modes that are observed in pairs of neurons with no delays, and how conduction delays affect the tendency of pairs of neurons to synchronize

  • A gradual transition from synchrony to antiphase with increasing conduction delay exists only if the center of the two branches lies to the right of the invariant line whose intersection with the PRC determines the intrinsic phase at which each neuron receives an input in the antiphase mode with no delay

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Summary

Introduction

A role has been proposed for synchronous oscillations in binding of sensory experiences (Singer, 1993) and attention (Fries et al, 2001). Synchronization that occurs between distal brain regions is almost always associated with oscillatory activity (Konig et al, 1995). This synchrony is achieved rapidly (Singer, 1999) and persists only transiently. The role of reciprocal coupling in synchronizing neural oscillators is supported by the observation that strong inter-hemispheric phase locking in the gamma frequency band with zero phase lag occurred in cat visual cortex could be disrupted by severing the corpus callosum (Engel et al, 1991). Type 1 PRCs (Hansel et al, 1995) are comprised of either all advances (for excitation) or all delays (for inhibition), whereas type 2 PRCs exhibit both advances and delays

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