The dorsal medial frontal cortex mediates automatic motor inhibition in uncertain contexts: Evidence from combined fMRI and EEG studies

Abstract

Response inhibition is commonly thought to rely on voluntary, reactive, selective, and relatively slow prefrontal mechanisms. In contrast, we suggest here that response inhibition is achieved automatically, nonselectively, within very short delays in uncertain environments. We modified a classical go/nogo protocol to probe context-dependent inhibitory mechanisms. Because no single neuroimaging method can definitely disentangle neural excitation and inhibition, we combined fMRI and EEG recordings in healthy humans. Any stimulus (go or nogo) presented in an uncertain context requiring action restraint was found to evoke activity changes in the supplementary motor complex (SMC) with respect to a control condition in which no response inhibition was required. These changes included: (1) An increase in event-related BOLD activity, (2) an attenuation of the early (170 ms) event related potential generated by a single, consistent source isolated by advanced blind source separation, and (3) an increase in the evoked-EEG Alpha power of this source. Considered together, these results suggest that the BOLD signal evoked by any stimulus in the SMC when the situation is unpredictable can be driven by automatic, nonselective, context-dependent inhibitory activities. This finding reveals the paradoxical mechanisms by which voluntary control of action may be achieved. The ability to provide controlled responses in unpredictable environments would require setting-up the automatic self-inhibitory circuitry within the SMC. Conversely, enabling automatic behavior when the environment becomes predictable would require top-down control to deactivate anticipatorily and temporarily the inhibitory set.

Contribution of the supplementary motor area and the cerebellum to the anticipatory postural adjustments and execution phases of human gait initiation

“…This effect could result from disruption of sensory perception of self-generated actions (Haggard and Whitford 2004), in addition to changes in perception threshold (Legon et al 2013), leading to decreased effort perception (Zenon et al 2015) with, in consequence, an increased force production and increased muscle activity (our results). Another explanation would be that SMA disruption interferes with the automatic inhibitory control of motor responses (Albares et al 2014). The finding that SMA disruption significantly improves akinesia (Eggers et al 2015) and decreases abnormally prolonged APAs phase durations prior to gait initiation (Jacobs et al 2009a) in PD patients, is also in line with our results.…”

Cerebral blood flow modulations during antisaccade preparation in chronic hypotension

“…Regarding the experimental task, it should be noted that it only allowed for manipulation of proactive control via inclusion of two task conditions differing in difficulty and executive function load (i.e., precued prosaccades and antisaccades). While the preparation of an antisaccade response in our precued task can be argued to involve proactive control (Talanow et al., ), the inclusion of a condition with high probability (but not certainty) of having to inhibit a saccadic response would have been informative, in line with previous literature on proactive inhibition (Albares et al, ; Chikazoe et al, ; Jaffard, Benraiss, Longcamp, Velay, & Boulinguez, ; Zandbelt, Bloemendaal, Neggers, Kahn, & Vink, ).…”

Inhibitory control and the structural parcellation of the right inferior frontal gyrus

“…However, the interpretation of goRTs produced under the SST as task-general marker of motor preparation has been challenged. For instance, SST goRTs have been found to slow down with increasing probability of a stop signal (Zandbelt & Vink, 2010), which has been taken as evidence for a braking mechanism that proactively restrains responses (proactive inhibitory control) (Albares et al, 2014;Zandbelt & Vink, 2010). Thus, motor initiation in the SST seems to be influenced by other cognitive mechanisms, such as strategic slowing in order to balance performance speed and accuracy (Leotti & Wager, 2010).…”