Task context determines whether common or separate inhibitory signals underlie the control of eye-hand movements

Abstract

Whereas inhibitory control of single effector movements has been widely studied, the control of coordinated eye-hand movements has received less attention. Nevertheless, previous studies have contradictorily suggested that either a common or separate signal/s is/are responsible for inhibition of coordinated eye-hand movements. In continuation of our previous study, we varied behavioral contexts and used a stochastic accumulation-to-threshold model, which predicts a scaling of the mean reaction time distribution with its variance, to study the inhibitory control of eye-hand movements. Participants performed eye-hand movements in different task conditions, and in each condition they had to redirect movements in a fraction of trials. Task contexts where the behavior could be best explained by a common initiation signal had similar error responses for eye and hand, despite having different mean reaction times, indicating a common inhibitory signal. In contrast, behavior that could be best explained by separate initiation signals had dissimilar error responses for eye and hand indicating separate inhibitory signals. These behavioral responses were further validated using electromyography and computational models having either a common or separate inhibitory control signal/s. Interestingly, in a particular context, whereas in majority trials a common initiation and inhibitory signal could explain the behavior, in a subset of trials separate initiation and inhibitory signals predicted the behavior better. This highlights the flexibility that exists in the brain and in effect reconciles the heterogeneous results reported by previous studies. NEW & NOTEWORTHY Prior studies have contradictorily suggested either a single or separate inhibitory signal/s underlying inhibition of coordinated eye-hand movements. With the use of different tasks, we observed that when eye-hand movements were initiated by a common signal, they were controlled by a common inhibitory signal. However, when the two effectors were initiated by separate signals, they were controlled by separate inhibitory signals. This highlights the flexible control of eye-hand movements and reconciles the heterogeneous results previously reported in the literature.

Temporal cascade of frontal, motor and muscle processes underlying human action-stopping

“…However, we note a striking convergence of timings across the current experiments and in other studies, e.g. CancelTime (Hannah et al, 2019;Raud et al, 2019;Raud and Huster, 2017), time of MEP suppression (Coxon et al, 2006; van den Wildenberg et al, 2010), corticomotor conduction time (Groppa et al, 2012;Hamada et al, 2013), BurstTimes (Hannah et al, 2019), and the ballistic stage (Gopal and Murthy, 2016;Jana and Murthy, 2018). Together, these all provide support for our model.…”

“…Logan, 2009). [The duration of such ballistic stages has been estimated to be ~15 ms in saccades in non-human primates (Boucher et al, 2007;Kornylo et al, 2003;Purcell et al, 2010) and ~50 ms for reaching movements (Gopal and Murthy, 2016;Jana and Murthy, 2018)]. In other words, the time of EMG cancellation on partial trials reflects a time just before the point-of-no-return, whereby if EMG activity is allowed to continue develop beyond this point it will exceed a critical threshold such that a button press necessarily ensues (we presume this threshold reflects the point at which the inertia of the finger is overcome).…”

“…The difference between SSRT Beh and the time of EMG cancellation (CancelTime) might be attributed to an inherent "ballistic stage" in movements, and once the muscle activity crosses the point-of-no-return they can no longer be stopped, making the movement inevitable (De Jong et al, 1990;Mirabella et al, 2006;Osman et al, 1986;Verbruggen and Logan, 2009). The duration of such ballistic stages has been estimated to be 10-25 ms in saccades in non-human primates (Boucher et al, 2007;Kornylo et al, 2003;Purcell et al, 2010) and 40-50 ms for reaching movements in humans (Gopal and Murthy, 2016;Jana and Murthy, 2018). In other words, the time of EMG cancellation on partial EMG trials reflects a time just before the pointof-no-return, whereby if EMG activity is allowed to continue develop beyond this point it will exceed a critical threshold such that a button press necessarily ensues (we presume this threshold reflects the point at which the inertia of the finger is overcome).…”

“…To check this, we used a model previously used to study stopping of reaching movements in the context of coordinated eye-hand movements (Gopal and Murthy, 2016;Jana and Murthy, 2018). Here, the Go process comprises an accumulation phase, and once the accumulator hits the threshold, EMG responses can be observed, and then following a peripheral delay, the EMG builds up enough (i.e.…”

Temporal cascade of frontal, motor and muscle processes underlying human action-stopping

“…Thus, SSRT Beh could be an over-estimation of the duration of the Stop process in the brain. This extra time in SSRT Beh probably reflects a ‘ballistic stage’ in generation of the button press 40,41 . We suggest that the maximum CancelTime reflects the last point at which a Stop process can intervene to prevent responses.…”