Cerebellar Purkinje cells control eye movements with a rapid rate code that is invariant to spike irregularity.

Hannah L Payne,Jennifer L Raymond,Ranran L French,Tiina Manninen,Christine C Guo,Td Barbara Nguyen-Vu

doi:10.7554/elife.37102

Hannah L Payne, Jennifer L Raymond + Show 4 more

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https://doi.org/10.7554/elife.37102

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Abstract

The rate and temporal pattern of neural spiking each have the potential to influence computation. In the cerebellum, it has been hypothesized that the irregularity of interspike intervals in Purkinje cells affects their ability to transmit information to downstream neurons. Accordingly, during oculomotor behavior in mice and rhesus monkeys, mean irregularity of Purkinje cell spiking varied with mean eye velocity. However, moment-to-moment variations revealed a tight correlation between eye velocity and spike rate, with no additional information conveyed by spike irregularity. Moreover, when spike rate and irregularity were independently controlled using optogenetic stimulation, the eye movements elicited were well-described by a linear population rate code with 3-5 ms temporal precision. Biophysical and random-walk models identified biologically realistic parameter ranges that determine whether spike irregularity influences responses downstream. The results demonstrate cerebellar control of movements through a remarkably rapid rate code, with no evidence for an additional contribution of spike irregularity.

Highlights

Action potentials, or spikes, are the primary language used by the nervous system
It is well established that the spike rate of a majority of Purkinje cells in this region of the cerebellum encode gaze velocity (Lisberger and Fuchs, 1974; Lisberger et al, 1994; Pastor et al, 1997; Raymond and Lisberger, 1998; Hirata and Highstein, 2000; Katoh et al, 2015)
Gaze velocity is defined as the angular velocity of the eye in world coordinates, which is equal to the sum of eye velocity in the head, plus head velocity in the world

Summary

Introduction

Spikes, are the primary language used by the nervous system. Throughout the brain, the rate at which neurons fire spikes encodes information (Adrian, 1928; Kuffler, 1951; Hubel and Wiesel, 1959; Wright et al, 1967; reviewed in Borst and Theunissen, 1999), affects the activity of downstream neurons (Tsodyks and Markram, 1997; Bagnall et al, 2008; Turecek et al, 2016), and drives motor output (Crowell et al, 1968; Evarts, 1968; Evarts, 1969; Henn and Cohen, 1976; Georgopoulos et al, 1982; Hanes and Schall, 1996; reviewed in Ebbesen and Brecht, 2017), indicating that a rate code is widely used for neural computation. The precise temporal pattern of spikes can encode information beyond that carried by spike rate, suggesting that a temporal code may contribute to information processing (O’Keefe and Recce, 1993; Theunissen and Miller, 1995; Gawne et al, 1996; de Ruyter van Steveninck et al, 1997; Stopfer et al, 1997; Victor, 1999; Stopfer and Laurent, 1999; Reich et al, 2000; Panzeri et al, 2001; Huxter et al, 2003; Butts et al, 2007; Engineer et al, 2008; Gollisch and Meister, 2008; Huxter et al, 2008).

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