Movement-related coupling of human subthalamic nucleus spikes to cortical gamma.

Petra Fischer,Wolf-Julian Neumann,Witold J Lipski,Peter Brown,Robert S Turner,Pascal Fries,R Mark Richardson

doi:10.7554/elife.51956

Abstract

Cortico-basal ganglia interactions continuously shape the way we move. Ideas about how this circuit works are based largely on models those consider only firing rate as the mechanism of information transfer. A distinct feature of neural activity accompanying movement, however, is increased motor cortical and basal ganglia gamma synchrony. To investigate the relationship between neuronal firing in the basal ganglia and cortical gamma activity during movement, we analysed human ECoG and subthalamic nucleus (STN) unit activity during hand gripping. We found that fast reaction times were preceded by enhanced STN spike-to-cortical gamma phase coupling, indicating a role in motor preparation. Importantly, increased gamma phase coupling occurred independent of changes in mean STN firing rates, and the relative timing of STN spikes was offset by half a gamma cycle for ipsilateral vs. contralateral movements, indicating that relative spike timing is as relevant as firing rate for understanding cortico-basal ganglia information transfer.

Highlights

Oscillations in extracellular field potential recordings reflect the synchronous rhythmic activation of thousands of nearby neurons capturing a mixture of sub- and suprathreshold activity (Buzsaki et al, 2012)
The mean variability (SD) of RTs within each patient was 0.19 ± 0.09 s and 0.23 ± 0.12 s. This variability in RTs allowed us to compare the extent of spike-to-gamma phase coupling between trials with fast and slow RTs by grouping trials with RTs below the median and trials with RTs above the median
We found that enhanced subthalamic nucleus (STN) spike-to-cortical gamma phase coupling preceded faster RTs already at the time of the Go cue, suggesting a role for subcortico-cortical coupling in preparing movement

Summary

Introduction

Oscillations in extracellular field potential recordings reflect the synchronous rhythmic activation of thousands of nearby neurons capturing a mixture of sub- and suprathreshold activity (Buzsaki et al, 2012). At the onset of contralateral movements, relatively narrow gamma-band oscillations (~60–90 Hz) appear in the human basal ganglia, thalamus and motor cortex (Brucke et al, 2008; Brucke et al, 2012; Brucke et al, 2013; Muthukumaraswamy, 2010; Jenkinson et al, 2013). The potential significance of these oscillations is illustrated by the fact that neural activity synchronizes strongly only when movements are actively initiated, but not during similar passive displacements (Liu et al, 2008; Muthukumaraswamy, 2010; Brucke et al, 2012).

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