Proactive inhibition is marked by differences in the pattern of motor cortex activity during movement preparation and execution

Abstract

Successful human behaviour relies on the ability to flexibly alter movements depending on the context in which they are made. One such context-dependent modulation is proactive inhibition, a type of behavioural inhibition used when anticipating the need to stop or change movements. We investigated how the motor cortex might prepare and execute movements made under different contexts. We used transcranial magnetic stimulation (TMS) in different coil orientations (PA: postero-anterior and AP: antero-posterior flowing currents) and pulse widths (120 µs and 30 µs) to probe the excitability of different inputs to corticospinal neurons whilst participants performed two reaction time tasks: a simple reaction time task and a stop-signal task requiring proactive inhibition. We took inspiration from state space models to assess whether the pattern of motor cortex activity changed due to proactive inhibition (PA and AP neuronal circuits represent the x and y axes of a state space upon which motor cortex activity unfolds during motor preparation and execution). We found that the rise in motor cortex excitability was delayed when proactive inhibition was required. State space visualisations showed altered patterns of motor cortex activity (combined PA120 and AP30 activity) during proactive inhibition, despite adjusting for reaction time. Overall, we show that the pattern of neural activity generated by the motor cortex during movement preparation and execution is dependent upon the context under which the movement is to be made.

The Effect of Coil Orientation on the Stimulation of the Pre–Supplementary Motor Area: A Combined TMS and EEG Study

“…Besides coil orientation (CO), this differential activation also depends on the stimulation intensity (SI) used, i.e., a low SI is more selective in activating subsets of inputs to corticospinal neurons [ 5 ]. Even more importantly, this specific activation seems to be behaviourally relevant: it has been suggested that the suppression of a set of motor cortical neurons, obtained by a specific current direction of TMS, may have an impact on movement preparation [ 8 , 9 ].…”

Comparing the speed of action initiation and action inhibition

“…Likewise, in the context of stopping behaviors considered here, participants may make the decision to respond quite quickly after seeing the go cue (i.e., whether to act), but may delay initiation of their response to avoid the risk of initiating a movement that should instead be canceled. Indeed, reaction times in previous stop-signal tasks are often prolonged (e.g., Leunissen et al, 2017) and accompanied by delayed motor cortex excitability (Rawji et al, 2022), suggesting that participants deliberately delay their responses so as to allow time for the movement to be aborted if needed (Gulberti et al, 2014; Özyurt et al, 2003) and can even flexibly adjust their reaction speed to shift the balance in favor of responding or stopping behavior (Corneil et al, 2013; Leotti and Wager, 2010).…”

“…However, slowing of responses has been widely observed in previous stop-signal tasks over and above that imposed by task design (e.g., Corneil et al, 2013; Gulberti et al, 2014; Lappin and Eriksen, 1966; Leotti and Wager, 2010; Özyurt et al, 2003; Verbruggen and Logan, 2008). As a result, response times in stop-signal tasks are typically prolonged (e.g., Leunissen et al, 2017) and are accompanied by delayed motor cortex excitability (Rawji et al, 2022). Intriguingly, it has been found that participants often delayed the response by an amount slightly greater (~ 5 to 20 ms) than the time lag between the primary go and stop signals (Lappin and Eriksen, 1966), which is just enough to allow them to stop a response (it also suggests that inhibition is as fast as initiation).…”

The role of PMd in voluntary motor control: insights from TMS research.

“…Despite some inconsistencies, as we have outlined above, reconsidering results from TMS studies that use single and double stimulation methods to index changes in intercortical circuits as movements are prepared in the context of the emerging theories in the single-neuron recording literature may provide a fruitful avenue for explaining the available data and planning future investigations. Indeed, a series of recent TMS studies investigating fluctuations in corticospinal excitability during motor preparation explicitly designed in response to these emergent theories have yielded interesting results that may push the field in productive new directions [64][65][66] .…”