Stimulation of the Dorsal Premotor Cortex, But Not of the Supplementary Motor Area Proper, Impairs the Stop Function in a STOP Signal Task

Abstract

Being able to inhibit an impending movement in response to a contextual change is a distinctive feature of action control. Such inhibitory control relies on a complex cortical-subcortical network, including posterior prefrontal regions such as caudal inferior frontal gyrus and pre-supplementary motor area. According to hierarchical models of action control, both areas represent the intermediate level between prefrontodependent and motor-related cortices. Going at a lower level, accumulating evidence speaks for an involvement of the primary motor cortex (M1) to dorsal premotor cortex (PMCd) or supplementary motor area proper (SMAproper) pathways in producing inhibitory control. However, the clear-cut evidence for this conjecture is still missing. The aim of the present paper was to start filling this gap, investigating this lowest level of inhibitory control. We stimulated PMCd in a group of healthy volunteers with transcranial magnetic stimulation (TMS) or sham TMS during the response phase of a STOP-signal task performed with the lips. In a separate experimental group, we applied effective TMS/ sham TMS to SMA-proper during the same task. We found that effective TMS over PMCd increased false-start errors in STOP trials (p = 0.0005), but had no effect on GO trial performance (p = 0.85). Effective TMS on SMAproper produced no effect on STOP trials' performance (p = 0.31) nor in the GO trial performance (p = 0.56). Our data show that there is at least a portion of PMCd playing a distinctive role in the control of mouth-related M1 during instructed visuomotor inhibitory behavior. This region could therefore represent a low-level hierarchical node for externally cued action inhibition. 2018 IBRO. Published by Elsevier Ltd. All rights reserved.

Stimulation of Different Sectors of the Human Dorsal Premotor Cortex Induces a Shift from Reactive to Predictive Action Strategies and Changes in Motor Inhibition: A Dense Transcranial Magnetic Stimulation (TMS) Mapping Study

“…This hypothesis is supported by several data in the literature that indicate a hierarchical caudal-rostral specialization gradient in the primate dPM, in which the caudal part (F2 sector or dPM-proper codes conditional sensorimotor associations and has direct connections to M1—see [ 61 , 66 ] for a review) and the rostral part have higher-order functions, not related to direct action execution [ 67 , 68 , 69 ]. The latter, caudal portion is likely to be corresponding to the dPM region involved in the direct inhibitory control described in our previous works [ 13 , 41 , 42 ]. Although they do not assess proactive inhibitory control, some human’s invasive data could also suggest this specialization gradient.…”

“…This modulation suggests that inhibitory processes occur in parallel with the activation mechanisms and indicates that optimal time preparation is accompanied by a suppression in activity of the cortico-spinal tract. Some lines of research support the idea that inhibitory processes in dPM are recruited in parallel with facilitating preparatory activity [ 2 ], generating inhibitory information targeting the M1, to prevent premature movements [ 42 , 65 ].…”

“…All participants were required to hold a wood stick with their lips devoted to collect the motor responses, as reported in our previous works [ 13 , 41 , 42 ]. At the end of the stick there was a 15 g weight, with the aim to stabilize the apparatus and make the return to the starting point easier ( Figure 2 ).…”

“…In a subsequent experiment, we showed that such inhibitory connections between dPM and M1 are task specific and are prominent in the middle portion of the SET-period [ 13 ]. In a last experiment [ 42 ], we demonstrated that dPM stimulation during a GO-NOGO task selectively impaired the capacity to withhold the motor response in NOGO trials. Taken together, our previous results indicated that a specific direct connection between the dPM and M1 mediate the capacity not to move during the set-period when this is required for successful behavior.…”

Neuronal population dynamics during motor plan cancellation in non-human primates

“…Superior Colliculus (SC) reaches a fixed threshold, while the activity of fixation neurons decreases (Hanes et al, 1998;Paré and Hanes, 2003). However, the control of arm movement tested in equivalent countermanding tasks does not elicit a similar neuronal correlate, especially when tested at the single cell level (Mirabella et al, 2011;Stuphorn, 2015;Pani et al, 2013), and different cortical areas like motor and premotor cortices (especially dorsal premotor cortex, PMd) have been suggested to have a key role in movement inhibition (Mirabella et al, 2011;Mattia et al, 2012;Pani et al 2014;Pani et al 2018;Duque et al, 2012;Duque et al, 2017;Parmigiani and Cattaneo, 2018).…”