Between-hand coupling during response inhibition

Abstract

Response inhibition reflects the process of terminating inappropriate preplanned or ongoing movements. When one hand is cued to stop after preparing a bimanual response (Partial trial), there is a substantial delay on the responding side. This delay is termed the interference effect and identifies a constraint that limits selective response inhibition. γ-Aminobutyric acid (GABA)-mediated networks within primary motor cortex (M1) may have distinct roles during response inhibition. In this study we examined whether the interference effect is the consequence of between-hand “coupling” into a unitary response and whether this is reflected in GABAergic intracortical inhibition within M1. Eighteen healthy right-handed participants performed a bimanual synchronous and asynchronous anticipatory response inhibition task. Electromyographic recordings were obtained from the first dorsal interosseous muscle bilaterally. Motor evoked potentials were elicited by single- and paired-pulse transcranial magnetic stimulation over right M1. As expected, Go trial performance was better with the synchronous compared with the asynchronous version of the task. Paradoxically, response delays during Partial trials were longer with the synchronous compared with the asynchronous task. Although task difficulty did not modulate GABAergic intracortical inhibition, there was a trend for between-hand coupling on asynchronous trials to be associated with greater GABAB receptor-mediated inhibition and lesser recruitment of GABAA receptor-mediated inhibition. The novel findings indicate that the interference effect is in part a consequence of between-hand coupling into a unitary response during movement preparation. The ability to respond independently with the two hands may rely on modulation of distinct inhibitory processes. NEW & NOTEWORTHY The temporal dynamics of an anticipated response task were manipulated to effect the difficulty of behavioral stopping and the underlying effects on motor neurophysiology. There were large response delays during trials where a subcomponent of an upcoming bimanual response was cued to stop in conditions where the anticipated action of the hands were synchronous, but not when asynchronous. Response delays reflected the integration of actions of both hands into a unitary response.

A Single Mechanism for Global and Selective Response Inhibition under the Influence of Motor Preparation

“…Despite the prevalent interference in the EMG at the group level, the single-trial ∆peak indicated large variability, including trials with no interference. This is in line with previous findings showing that interference can be eliminated under specific conditions (Xu et al, 2015) or when a small delay is required between the bimanual left and right hand responses (in contrast to simultaneous ones), which necessitates a decoupling of the bimanual response (Wadsley et al, 2019). These results highlight that the stop-restart behavior in the bimanual stop signal task is not mandatory, but a preferred option when selectivity is not incentivized by the task requirements.…”

Exploring Stop Signal Reaction Time Over Two Sessions of the Anticipatory Response Inhibition Task

“…This difference is not necessarily surprising as SSRT in Partial Stop trials is more than a measure of pure (or global; i.e stop everything) inhibitory network activity. The stop cue on these trials triggers a sequential non-selective stop, response uncouple, reprogram, then selective go process(Coxon et al, 2007; MacDonald et al, 2012; MacDonald et al, 2014; Cowie et al, 2016; Wadsley et al, 2019; MacDonald et al, 2021) which leads to the delayed RT. Partial RI SSRT therefore reflects a complex series of neural processes which are triggered by the partial stop cue and involve interactions between facilitatory and inhibitory prefrontal-basal ganglia networks (Coxon et al, 2009; Coxon et al, 2012).…”

“…This may be because some, or all, of the sequential process captured by the SSRT (stop, uncouple, reprogram, then go) occurred over a shorter time scale in session two. The overall time required for this process can be reduced on Partial Stop trials of both the ARIT (Wadsley et al, 2019) and SST (Xu et al, 2014) through manipulations to overall task design. Wadsley and colleagues (2019) increased the asynchrony between left and right-side components of the default response, thereby reducing the amount of time needed for response uncoupling during partial RI and reducing the stopping interference effect.…”

“…The overall time required for this process can be reduced on Partial Stop trials of both the ARIT (Wadsley et al, 2019) and SST (Xu et al, 2014) through manipulations to overall task design. Wadsley and colleagues (2019) increased the asynchrony between left and right-side components of the default response, thereby reducing the amount of time needed for response uncoupling during partial RI and reducing the stopping interference effect. Xu and colleagues (2015) also decreased the interference effect by targeting the Go process in partial RI, with specific training to shorten reaction times, although this came at a cost of incredibly short SSDs (averaging 98ms) which likely fundamentally changed partial RI behaviour.…”

“…During the more challenging Partial Stop trials, participants are required to keep only one key depressed when the corresponding bar does not reach the target and release the alternative key at the target line. The response of the continuing hand is invariably delayed, which is termed the stopping interference effect (Aron and Verbruggen, 2008; Ko and Miller, 2011; Wadsley et al, 2019). SSRTs are also calculated on these trials but are thought to reflect a more complex series of neural processes triggered by the stop signal; a sequential non-selective stop, uncouple and reprogram, then selective go process (Coxon et al, 2009; MacDonald et al, 2012; MacDonald et al, 2014; Wadsley et al, 2019; MacDonald et al, 2021).…”