On the complexity of resting state spiking activity in monkey motor cortex

Resting state has been established as a classical paradigm of brain activity studies, mostly based on large scale measurements such as fMRI or M/EEG. This term typically refers to a behavioral state characterized by the absence of any task or stimuli. The corresponding neuronal activity is often called idle or ongoing. Numerous modeling studies on spiking neural networks claim to mimic such idle states, but compare their results to task- or stimulus-driven experiments, which might lead to misleading conclusions. To provide a proper basis for comparing physiological and simulated network dynamics, we characterize simultaneously recorded single neurons’ spiking activity in monkey motor cortex and show the differences from spontaneous and task-induced movement conditions. The resting state shows a higher dimensionality, reduced firing rates and less balance between population level excitation and inhibition than behavior-related states. Additionally, our results stress the importance of distinguishing between rest with eyes open and closed.

Conservation of preparatory neural events in monkey motor cortex regardless of how movement is initiated

A time-consuming preparatory stage is hypothesized to precede voluntary movement. A putative neural substrate of motor preparation occurs when a delay separates instruction and execution cues. When readiness is sustained during the delay, sustained neural activity is observed in motor and premotor areas. Yet whether delay-period activity reflects an essential preparatory stage is controversial. In particular, it has remained ambiguous whether delay-period-like activity appears before non-delayed movements. To overcome that ambiguity, we leveraged a recently developed analysis method that parses population responses into putatively preparatory and movement-related components. We examined cortical responses when reaches were initiated after an imposed delay, at a self-chosen time, or reactively with low latency and no delay. Putatively preparatory events were conserved across all contexts. Our findings support the hypothesis that an appropriate preparatory state is consistently achieved before movement onset. However, our results reveal that this process can consume surprisingly little time.

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

Variability 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.