Firing rate-dependent phase responses of Purkinje cells support transient oscillations.

Yunliang Zang,Erik De Schutter,Sungho Hong

doi:10.7554/elife.60692

Yunliang Zang, Erik De Schutter + Show 1 more

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https://doi.org/10.7554/elife.60692

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Abstract

Both spike rate and timing can transmit information in the brain. Phase response curves (PRCs) quantify how a neuron transforms input to output by spike timing. PRCs exhibit strong firing-rate adaptation, but its mechanism and relevance for network output are poorly understood. Using our Purkinje cell (PC) model, we demonstrate that the rate adaptation is caused by rate-dependent subthreshold membrane potentials efficiently regulating the activation of Na+ channels. Then, we use a realistic PC network model to examine how rate-dependent responses synchronize spikes in the scenario of reciprocal inhibition-caused high-frequency oscillations. The changes in PRC cause oscillations and spike correlations only at high firing rates. The causal role of the PRC is confirmed using a simpler coupled oscillator network model. This mechanism enables transient oscillations between fast-spiking neurons that thereby form PC assemblies. Our work demonstrates that rate adaptation of PRCs can spatio-temporally organize the PC input to cerebellar nuclei.

Highlights

The propensity of neurons to fire synchronously depends on the interaction between cellular and network properties (Ermentrout et al, 2001)
The Phase response curves (PRCs) quantifies how a weak stimulus exerted at different phases during the interspike interval (ISI) can shift subsequent spike timing in repetitively firing neurons (Ermentrout et al, 2001; Gutkin et al, 2005) and thereby predicts how well-timed synaptic input can modify spike timing
PRCs were obtained by repeatedly exerting a weak stimulus at different phases of the ISI

Summary

Introduction

The propensity of neurons to fire synchronously depends on the interaction between cellular and network properties (Ermentrout et al, 2001). The PRC determines the potential of network synchronization (Ermentrout et al, 2001; Ermentrout et al, 2008; Gutkin et al, 2005; Smeal et al, 2010) It is not static and shows significant adaptation to firing rates. Responses in later phases become phase-dependent, with earlier onset-phases and gradually increasing peak amplitudes This PRC property has never been theoretically replicated or explained (Couto et al, 2015; Phoka et al, 2010), nor has its effect on synchronizing spike outputs been explored

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