Behavioral context determines network state and variability dynamics in monkey motor cortex

Abstract

Keywordsmonkey motor cortex, spike time irregularity, spike count variability, behavioral context, renewal processes not peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was . http://dx.doi.org/10.1101/233684 doi: bioRxiv preprint first posted online Dec. 14, 2017;Context-related variability in spiking activity Riehle et al. 2 AbstractVariability of spiking activity is ubiquitous throughout the brain but little is known about its contextual dependence. Trial-to-trial spike count variability, estimated by the Fano Factor (FF), and within-trial spike time irregularity, quantified by the local coefficient of variation (CV2), reflect variability on long and short time scales, respectively. We co-analyzed FF and CV2 in monkey motor cortex comparing two behavioral contexts, movement preparation (wait) and execution (movement). We find that FF significantly decreases from wait to movement, while CV2 increases. The more regular firing (low CV2) during wait is related to an increased power of local field potential beta oscillations and phase locking of spikes to these oscillations. In renewal processes, a widely used model for spiking activity under stationary input conditions, both measures are related as FF≈CV². This expectation was met during movement, but not during wait where FF>>CV2². We conclude that during movement preparation, ongoing brain processes result in changing network states and thus in high trial-to-trial variability (high FF). During movement execution, the network is recruited for performing the stereotyped motor task, resulting in reliable single neuron output. We discuss our results in the light of recent computational models that generate non-stationary network conditions. not peer-reviewed)

Spiking attractor model of motor cortex explains modulation of neural and behavioral variability by prior target information

“…1a). This behavior of FF has been observed previously in other cortical areas and different experimental tasks (Rickert et al, 2009;Churchland et al, 2010;Riehle et al, 2018). The irregularity of inter-spike intervals, CV 2 , on the other hand, is fairly constant over time (black curve in Fig.…”

Is there an intrinsic relationship between LFP beta oscillation amplitude and firing rate of individual neurons in monkey motor cortex?

“…The lack of an intrinsic relationship between LFP beta amplitude and neuronal activation level (rate) does not exclude other relationships between beta oscillations and neuronal spiking activity. Indeed, as we demonstrate in this dataset, confirming several previous studies (Murthy and Fetz 1996;Donoghue et al 1998;Baker et al 1999;Denker et al 2011;Canolty et al 2012;Engelhard et al 2013;Riehle et al 2018) there is significant locking of spike times to LFP beta oscillation phase in many neurons in motor cortex. Such phase locking may result in rhythmic synchronization among populations of neurons thereby increasing their concerted impact on post-synaptic targets without necessary increasing their spike rates (Destexhe and Paré 1999;Azouz and Gray 2000;Rudolph and Destexhe 2003).…”

“…Furthermore, several studies addressed the relationship between motor cortical LFP beta oscillations and the local spiking activity (e.g. Murthy and Fetz 1996;Donoghue et al 1998;Baker et al 1999;Denker et al 2011;Canolty et al 2012;Engelhard et al 2013;Rule et al 2017Rule et al , 2018Best et al 2017;Riehle et al 2018).…”

On the Complexity of Resting State Spiking Activity in Monkey Motor Cortex

“…On a SU level, direction-specific neuronal subpopulations encode the movement direction by firing rate (FR) modulations ( Georgopoulos et al 1986 ; Rickert et al 2009 ). These and other studies also investigated the spike time irregularity and the spike count variability in monkey motor cortex during various behavioral epochs: movements have been related to a lower spike count variability across trials ( Rickert et al 2009 ; Churchland et al 2010 ; Riehle et al 2018 ) and to a higher spike time irregularity ( Davies et al 2006 ; Riehle et al 2018 ) compared with wait or preparatory behavior without movements. However, the resting state we analyze in this study is conceptually distinct from waiting or preparatory epochs: there is no task to prepare for and no signal to be anticipated.…”

“…Spiking activity in monkey motor cortex has been studied extensively during arm movements, which give rise to an increased average neuronal firing compared with wait ( Nawrot et al 2008 ; Rickert et al 2009 ; Riehle et al 2018 ). On a SU level, direction-specific neuronal subpopulations encode the movement direction by firing rate (FR) modulations ( Georgopoulos et al 1986 ; Rickert et al 2009 ).…”