Stop-event-related potentials from intracranial electrodes reveal a key role of premotor and motor cortices in stopping ongoing movements

Abstract

In humans, the ability to withhold manual motor responses seems to rely on a right-lateralized frontal–basal ganglia–thalamic network, including the pre-supplementary motor area and the inferior frontal gyrus (IFG). These areas should drive subthalamic nuclei to implement movement inhibition via the hyperdirect pathway. The output of this network is expected to influence those cortical areas underlying limb movement preparation and initiation, i.e., premotor (PMA) and primary motor (M1) cortices. Electroencephalographic (EEG) studies have shown an enhancement of the N200/P300 complex in the event-related potentials (ERPs) when a planned reaching movement is successfully stopped after the presentation of an infrequent stop-signal. PMA and M1 have been suggested as possible neural sources of this ERP complex but, due to the limited spatial resolution of scalp EEG, it is not yet clear which cortical areas contribute to its generation. To elucidate the role of motor cortices, we recorded epicortical ERPs from the lateral surface of the fronto-temporal lobes of five pharmacoresistant epileptic patients performing a reaching version of the countermanding task while undergoing presurgical monitoring. We consistently found a stereotyped ERP complex on a single-trial level when a movement was successfully cancelled. These ERPs were selectively expressed in M1, PMA, and Brodmann's area (BA) 9 and their onsets preceded the end of the stop process, suggesting a causal involvement in this executive function. Such ERPs also occurred in unsuccessful-stop (US) trials, that is, when subjects moved despite the occurrence of a stop-signal, mostly when they had long reaction times (RTs). These findings support the hypothesis that motor cortices are the final target of the inhibitory command elaborated by the frontal–basal ganglia–thalamic network.

Self-Paced Reaching after Stroke: A Quantitative Assessment of Longitudinal and Directional Sensitivity Using the H-Man Planar Robot for Upper Limb Neurorehabilitation

“…To date, research into the volitional inhibitory control of manual motor actions and the ability to choose between alternative actions to achieve an identified goal have been mostly neglected by scientists working either on rehabilitation and on BCI (Mirabella, 2012). This is unfortunate given that volitional inhibition is a fundamental function of behavioral flexibility that allows us to quickly adapt behavior to unattended changes either in our thoughts or in the external environment (Mirabella, 2014), and involved both the pre-motor and the primary motor cortices (Mirabella et al, 2011; Mattia et al, 2012, 2013). …”

Correction and suppression of reaching movements in the cerebral cortex: Physiological and neuropsychological aspects

“…Thus the TMS studies do not provide strong support for a right ventrolateral prefrontal localization of a Stop unit process. Mattia et al (2012) recorded ERPs from the lateral surface of the frontal cortex in five epileptic patients. A steoreotyped ERP complex was found when successful countermanding occurred in the Stop task.…”

A common control signal and a ballistic stage can explain the control of coordinated eye-hand movements

“…Performance is typically modeled as an independent stochastic race between processes that initiate and inhibit the old motor plan (Hanes and Carpenter 1999;Lappin and Eriksen 1966;Logan 1982;Ramakrishnan et al 2010). The corresponding neurophysiological basis for implementing such a race has also accumulated over the years (Hanes et al 1998;Mattia et al 2012;Mirabella et al 2011;Murthy et al 2007;Paré and Hanes 2003;Schmidt et al 2013). This notwithstanding, little is known about the mechanisms that instantiate control when multiple effectors encompass an action.…”