Abstract
Neuronal firing rate variability prior to movement onset contributes to trial-to-trial variability in primate behavior. However, in humans, whether similar mechanisms contribute to trial-to-trial behavioral variability remains unknown. We investigated the time-course of trial-to-trial variability in corticospinal excitability (CSE) using transcranial magnetic stimulation (TMS) during a self-paced reach-to-grasp task. We hypothesized that CSE variability will be modulated prior to the initiation of reach and that such a modulation would explain trial-to-trial behavioral variability. Able-bodied individuals were visually cued to plan their grip force before exertion of either 30% or 5% of their maximum pinch force capacity on an object. TMS was delivered at six time points (0.5, 0.75, 1, 1.1, 1.2, and 1.3 s) following a visual cue that instructed the force level. We first modeled the relation between CSE magnitude and its variability at rest (n = 12) to study the component of CSE variability pertaining to the task but not related to changes in CSE magnitude (n = 12). We found an increase in CSE variability from 1.2 to 1.3 s following the visual cue at 30% but not at 5% of force. This effect was temporally dissociated from the decrease in CSE magnitude that was observed from 0.5 to 0.75 s following the cue. Importantly, the increase in CSE variability explained at least ∼40% of inter-individual differences in trial-to-trial variability in time to peak force rate. These results were found to be repeatable across studies and robust to different analysis methods. Our findings suggest that the neural mechanisms underlying modulation in CSE variability and CSE magnitude are distinct. Notably, the extent of modulation in variability in corticospinal system prior to grasp within individuals may explain their trial-to-trial behavioral variability.
Highlights
Trial-to-trial variability is an inherent feature of motor behavior (Stein et al, 2005; Faisal et al, 2008)
We found that corticospinal excitability (CSE) variability increased beyond changes observed in CSE magnitude (i.e., CVDIFF of Motor evoked potentials (MEP)) prior to the performance of the self-paced reach-to-grasp task
The increase in CSE variability occurred after the “go” cue presentation and this effect was temporally dissociated from the decrease in CSE magnitude that occurred before the “go” cue presentation
Summary
Trial-to-trial variability is an inherent feature of motor behavior (Stein et al, 2005; Faisal et al, 2008). Variation in fMRI responses within inferior parietal lobule observed during motor execution has been shown to explain differences in intertrial variability in reach kinematics across individuals (Haar et al, 2017). The modulation in intertrial variability in CSE assessed prior to movement onset has been shown to encode value-based decision-making processes and differentiate fast versus slow reaction time responses (KleinFlugge et al, 2013). These findings suggest that the temporal unfolding of CSE variability from trial-to-trial may provide information regarding task-related central processes that may be related to and/or explain an observed behavior. We expected differences in these findings for the two force levels because the neural activity might be dependent on the magnitude of force (Dettmers et al, 1996; Ehrsson et al, 2001; Hendrix et al, 2009; Perez and Cohen, 2009; Parikh et al, 2014)
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