Adjustments to Proactive Motor Inhibition without Effector-Specific Foreknowledge Are Reflected in a Bilateral Upregulation of Sensorimotor β-Burst Rates

2021 ◽  
Vol 33 (5) ◽  
pp. 784-798 ◽  
Author(s):  
Cheol Soh ◽  
Megan Hynd ◽  
Benjamin O. Rangel ◽  
Jan R. Wessel

Abstract Classic work using the stop-signal task has shown that humans can use inhibitory control to cancel already initiated movements. Subsequent work revealed that inhibitory control can be proactively recruited in anticipation of a potential stop-signal, thereby increasing the likelihood of successful movement cancellation. However, the exact neurophysiological effects of proactive inhibitory control on the motor system are still unclear. On the basis of classic views of sensorimotor β-band activity, as well as recent findings demonstrating the burst-like nature of this signal, we recently proposed that proactive inhibitory control is implemented by influencing the rate of sensorimotor β-bursts during movement initiation. Here, we directly tested this hypothesis using scalp EEG recordings of β-band activity in 41 healthy human adults during a bimanual RT task. By comparing motor responses made in two different contexts—during blocks with or without stop-signals—we found that premovement β-burst rates over both contralateral and ipsilateral sensorimotor areas were increased in stop-signal blocks compared to pure-go blocks. Moreover, the degree of this burst rate difference indexed the behavioral implementation of proactive inhibition (i.e., the degree of anticipatory response slowing in the stop-signal blocks). Finally, exploratory analyses showed that these condition differences were explained by a significant increase in β bursting that was already present during baseline period before the movement initiation signal. Together, this suggests that the strategic deployment of proactive inhibitory motor control is implemented by upregulating the tonic inhibition of the motor system, signified by increased sensorimotor β-bursting both before and after signals to initiate a movement.

2019 ◽  
Author(s):  
Jan R. Wessel

AbstractThe neurophysiological basis of motor processes and their control is of tremendous interest to basic researchers and clinicians alike. Notably, both movement initiation and cancellation are accompanied by prominent field potential changes in the β-frequency band (15-29Hz). In trial-averages, movement initiation is indexed by β-band desynchronization over sensorimotor sites, while movement cancellation is signified by β-power increases over (pre)frontal areas. However, averaging misrepresents the true nature of the β-signal. As recent work has highlighted, raw β-band activity is characterized by short-lasting, burst-like events, rather than by steady modulations. To investigate how such β-bursts relate to movement initiation and cancellation in humans, we investigated scalp-recorded β-band activity in 234 healthy subjects performing the Stop-signal task. Four observations were made: First, both movement initiation and cancellation were indexed by systematic, localized changes in β-bursting. While β-bursting at bilateral sensorimotor sites steadily declined during movement initiation, β-bursting increased at fronto-central sites when Stop-signals instructed movement cancellation. Second, the amount of fronto-central β-bursting clearly distinguished successful from unsuccessful movement cancellation. Third, the emergence of fronto-central β-bursting coincided with the latency of the movement cancellation process, indexed by Stop-signal reaction time. Fourth, individual fronto-central β-bursts during movement cancellation were followed by a low-latency re-instantiation of bilateral sensorimotor β-bursting. These findings suggest that β-bursting is a fundamental signature of the motor system, reflecting a steady inhibition of motor cortex that is suppressed during movement initiation, and can be rapidly re-instantiated by frontal areas when movements have to be rapidly cancelled.Significance StatementMovement-related β-frequency (15-29Hz) changes are among the most prominent features of neural recordings across species, scales, and methods. However, standard averaging-based methods obscure the true dynamics of β-band activity, which is dominated by short-lived, burst-like events. Here, we demonstrate that both movement-initiation and cancellation in humans are characterized by unique trial-to-trial patterns of β-bursting. Movement initiation is characterized by steady reductions of β-bursting over bilateral sensorimotor sites. In contrast, during rapid movement cancellation, β–bursts first emerge over fronto-central sites typically associated with motor control, after which sensorimotor β–bursting re-initiates. These findings suggest a fundamentally novel, non-invasive measure of the neural interaction underlying movement-initiation and –cancellation, opening new avenues for the study of motor control in health and disease.


Author(s):  
Graciela C. Alatorre-Cruz ◽  
Heather Downs ◽  
Darcy Hagood ◽  
Seth T. Sorensen ◽  
D. Keith Williams ◽  
...  

2020 ◽  
Vol 46 (Supplement_1) ◽  
pp. S63-S63
Author(s):  
Ya Wang ◽  
Lu-xia Jia ◽  
Xiao-jing Qin ◽  
Jun-yan Ye ◽  
Raymond Chan

Abstract Background Schizotypy, a subclinical group at risk for schizophrenia, have been found to show impairments in response inhibition. Recent studies differentiated proactive inhibition (a preparatory process before the stimuli appears) and reactive inhibition (the inhibition of a pre-potent or already initiated response). However, it remains unclear whether both proactive and reactive inhibition are impaired in schizotypy and what are the neural mechanisms. The present event-related potential study used an adapted stop-signal task to examine the two inhibition processes and the underlying neural mechanisms in schizotypy compared to healthy controls (HC). Methods A total of 21 individuals with schizotypy and 25 matched HC participated in this study. To explore different degrees of proactive inhibition, we set three conditions: a “certain” go condition which no stop signal occurred, a “17% no go” condition in which stop signal would appear in 17% of trials, and a “33% no go” condition in which stop signal would appear in 33% of trials. All participants completed all the conditions, and EEG was recorded when participants completed the task. Results Behavioral results showed that in both schizotypy and HC, the reaction times (RT) of go trials were significantly prolonged as the no go percentage increased, and HC showed significantly longer go RT compared with schizotypy in both “17% no go” and “33% no go” conditions, suggesting greater proactive inhibition in HC. Stop signal reaction times (SSRTs) in “33% no go” condition was shorter than “17% no go” condition in both groups. Schizotypy showed significantly longer SSRTs in both “17% no go” and “33% no go” conditions than HC, indicating schizotypy relied more on reactive inhibition. ERP results showed that schizotypy showed larger overall N1 for go trials than HC irrespective of condition, which may indicate a compensation process in schizotypy. Schizotypy showed smaller N2 on both successful and unsuccessful stop trials in “17% no go” conditions than HC, while no group difference was found in “33% no go” conditions for stop trials, which may indicate impaired error processing. Discussion These results suggested that schizotypy tended to be impaired in both proactive control and reactive control processes.


2014 ◽  
Vol 26 (8) ◽  
pp. 1601-1614 ◽  
Author(s):  
Corey N. White ◽  
Eliza Congdon ◽  
Jeanette A. Mumford ◽  
Katherine H. Karlsgodt ◽  
Fred W. Sabb ◽  
...  

The stop-signal task, in which participants must inhibit prepotent responses, has been used to identify neural systems that vary with individual differences in inhibitory control. To explore how these differences relate to other aspects of decision making, a drift-diffusion model of simple decisions was fitted to stop-signal task data from go trials to extract measures of caution, motor execution time, and stimulus processing speed for each of 123 participants. These values were used to probe fMRI data to explore individual differences in neural activation. Faster processing of the go stimulus correlated with greater activation in the right frontal pole for both go and stop trials. On stop trials, stimulus processing speed also correlated with regions implicated in inhibitory control, including the right inferior frontal gyrus, medial frontal gyrus, and BG. Individual differences in motor execution time correlated with activation of the right parietal cortex. These findings suggest a robust relationship between the speed of stimulus processing and inhibitory processing at the neural level. This model-based approach provides novel insight into the interrelationships among decision components involved in inhibitory control and raises interesting questions about strategic adjustments in performance and inhibitory deficits associated with psychopathology.


2013 ◽  
Vol 25 (2) ◽  
pp. 157-174 ◽  
Author(s):  
Bram B. Zandbelt ◽  
Mirjam Bloemendaal ◽  
Janna Marie Hoogendam ◽  
René S. Kahn ◽  
Matthijs Vink

Stopping an action requires suppression of the primary motor cortex (M1). Inhibitory control over M1 relies on a network including the right inferior frontal cortex (rIFC) and the supplementary motor complex (SMC), but how these regions interact to exert inhibitory control over M1 is unknown. Specifically, the hierarchical position of the rIFC and SMC with respect to each other, the routes by which these regions control M1, and the causal involvement of these regions in proactive and reactive inhibition remain unclear. We used off-line repetitive TMS to perturb neural activity in the rIFC and SMC followed by fMRI to examine effects on activation in the networks involved in proactive and reactive inhibition, as assessed with a modified stop-signal task. We found repetitive TMS effects on reactive inhibition only. rIFC and SMC stimulation shortened the stop-signal RT (SSRT) and a shorter SSRT was associated with increased M1 deactivation. Furthermore, rIFC and SMC stimulation increased right striatal activation, implicating frontostriatal pathways in reactive inhibition. Finally, rIFC stimulation altered SMC activation, but SMC stimulation did not alter rIFC activation, indicating that rIFC lies upstream from SMC. These findings extend our knowledge about the functional organization of inhibitory control, an important component of executive functioning, showing that rIFC exerts reactive control over M1 via SMC and right striatum.


2012 ◽  
Vol 107 (1) ◽  
pp. 384-392 ◽  
Author(s):  
Ian Greenhouse ◽  
Caitlin L. Oldenkamp ◽  
Adam R. Aron

Much research has focused on how people stop initiated response tendencies when instructed by a signal. Stopping of this kind appears to have global effects on the motor system. For example, by delivering transcranial magnetic stimulation (TMS) over the leg area of the primary motor cortex, it is possible to detect suppression in the leg when the hand is being stopped (Badry R et al. Suppression of human cortico-motoneuronal excitability during the stop-signal task. Clin Neurophysiol 120: 1717–1723, 2009). Here, we asked if such “global suppression” can be observed proactively, i.e., when people anticipate they might have to stop. We used a conditional stop signal task, which allows the measurement of both an “anticipation phase” (i.e., where proactive control is applied) and a “stopping” phase. TMS was delivered during the anticipation phase ( experiment 1) and also during the stopping phase ( experiments 1 and 2) to measure leg excitability. During the anticipation phase, we did not observe leg suppression, but we did during the stopping phase, consistent with Badry et al. (2009) . Moreover, when we split the subject groups into those who slowed down behaviorally (i.e., exercised proactive control) and those who did not, we found that subjects who slowed did not show leg suppression when they stopped, whereas those who did not slow did show leg suppression when they stopped. These results suggest that if subjects prepare to stop, then they do so without global effects on the motor system. Thus, preparation allows them to stop more selectively.


Neuroscience ◽  
2010 ◽  
Vol 167 (3) ◽  
pp. 709-715 ◽  
Author(s):  
L.S. Colzato ◽  
G. Hertsig ◽  
W.P.M. van den Wildenberg ◽  
B. Hommel

2019 ◽  
Author(s):  
Andre Chevrier ◽  
Russell J. Schachar

AbstractBackgroundAltered brain activity that has been observed in attention deficit hyperactivity disorder (ADHD) while performing cognitive control tasks like the stop signal task (SST), has generally been interpreted as reflecting either weak (under-active) or compensatory (over-active) versions of the same functions as in healthy controls. If so, then regional activities that correlate with the efficiency of inhibitory control (i.e. stop signal reaction time, SSRT) in healthy subjects should also correlate with SSRT in ADHD. Here we test the alternate hypothesis that BOLD differences might instead reflect the redirection of neural processing resources normally used for task-directed inhibitory control, toward actively managing symptomatic behavior. If so, then activities that correlate with SSRT in TD should instead correlate with inattentive and hyperactive symptoms in ADHD.MethodsWe used fMRI in 14 typically developing (TD) and 14 ADHD adolescents performing the SST, and in a replication sample of 14 healthy adults. First we identified significant group BOLD differences during all phases of activity in the SST (i.e. warning, response, reactive inhibition, error detection and post-error slowing). Next, we correlated these phases of activity with SSRT in TD, and with SSRT, inattentive and hyperactive symptom scores in ADHD. We then identified whole brain significant correlations in regions of significant group difference in activity.ResultsOnly three regions of significant group difference were correlated with SSRT in TD and replication groups (left and right inferior frontal gyri (IFG) during error detection, and hypothalamus during post-error slowing). Consistent with regions of altered activity managing symptomatic behavior instead of task-directed behavior, left IFG correlated with greater inattentive score, right IFG correlated with lower hyperactive score, and hypothalamus correlated with greater inattentive score and oppositely correlated with SSRT compared to TD.ConclusionsResults are consistent with stimuli that elicit task-directed integration of neural processing in healthy subjects, instead directing integrated function towards managing symptomatic behavior in ADHD. The ability of the current approach to determine whether altered neural activities reflect comparable functions in ADHD and control groups has broad implications for the development and monitoring of therapeutic interventions.


Symmetry ◽  
2021 ◽  
Vol 13 (9) ◽  
pp. 1602
Author(s):  
Christian Mancini ◽  
Giovanni Mirabella

The relationship between handedness, laterality, and inhibitory control is a valuable benchmark for testing the hypothesis of the right-hemispheric specialization of inhibition. According to this theory, and given that to stop a limb movement, it is sufficient to alter the activity of the contralateral hemisphere, then suppressing a left arm movement should be faster than suppressing a right-arm movement. This is because, in the latter case, inhibitory commands produced in the right hemisphere should be sent to the other hemisphere. Further, as lateralization of cognitive functions in left-handers is less pronounced than in right-handers, in the former, the inhibitory control should rely on both hemispheres. We tested these predictions on a medium-large sample of left- and right-handers (n = 52). Each participant completed two sessions of the reaching versions of the stop-signal task, one using the right arm and one using the left arm. We found that reactive and proactive inhibition do not differ according to handedness. However, we found a significant advantage of the right versus the left arm in canceling movements outright. By contrast, there were no differences in proactive inhibition. As we also found that participants performed movements faster with the right than with the left arm, we interpret our results in light of the dominant role of the left hemisphere in some aspects of motor control.


2018 ◽  
Author(s):  
Kenneth Javad Dale Allen ◽  
D.Phil. Jill Miranda Hooley

Negative urgency, the self-reported tendency to act impulsively when distressed, increases risk for nonsuicidal self-injury (NSSI). Prior research also suggests that NSSI is associated with impaired negative emotional response inhibition (NERI), a cognitive process theoretically related to negative urgency. Specifically, individuals with a history of NSSI had difficulty inhibiting behavioral responses to negative affective images in an Emotional Stop-Signal Task, but not to those depicting positive or neutral content. The present study sought to replicate this finding, determine whether this deficit extends to an earlier stage of NERI, and explore whether impairment in these two stages of emotional inhibitory control helps explain the relationship between negative urgency and NSSI. To address these aims, 88 adults with NSSI histories (n = 45) and healthy control participants (n = 43) without NSSI history or psychopathology completed a clinical interview, symptom inventories, an impulsivity questionnaire, and behavioral impulsivity tasks measuring early and late emotional response inhibition. The NSSI group had worse late NERI than the control group on the Emotional Stop-Signal Task, but no group differences were observed in early NERI on an Emotional Go/no-go task. However, both early and late stages of NERI accounted for independent variance in negative urgency. We additionally found that late NERI explained variance in the association between negative urgency and NSSI. These results suggest that impulsive behavior in NSSI may involve specifically impaired inhibitory control over negative emotional impulses during late response inhibition, and that this cognitive deficit might reflect one mechanism or pathway to elevated negative urgency among people who self-injure.


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