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How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition

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A special issue of Brain Sciences (ISSN 2076-3425). This special issue belongs to the section "Sensory and Motor Neuroscience".

Deadline for manuscript submissions: closed (31 March 2021) | Viewed by 43292

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Dr. Giovanni Mirabella

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1. Department of Clinical and Experimental Sciences, University of Brescia, 25123 Brescia, Italy
2. IRCCS Neuromed, 86077 Pozzilli, Italy
Interests: cognitive neuroscience; motor cognition; motor learning and motor; Parkinson's disease; inhibitory control; emotion

Special Issue Information

Dear Colleagues,

Inhibitory control is a multifaceted executive function that encompasses different types of processes. Motor inhibition is one distinct type of inhibition, which refers to the ability to inhibit prepotent motor responses, and it is usually measured via the go/no-go task or the stop-signal task. At its turn, motor inhibition has two separable neuropsychological domains, i.e., reactive inhibition, (the ability to stop a response outright when a stop instruction is presented), and proactive inhibition, (the ability to shape the motor strategy according to the context in which a subject is embedded). Even though it has been shown that they share partially overlapping neural substrates, there is no doubt that these two components have complementary functions and can be selectively impaired in diseases in which impulses are poorly controlled. Most of the previous works have focused on reactive inhibition, and only recently, proactive mechanisms have attracted attention. However, there is still sparse evidence of the way these two components interact with each other.

This Special Issue of Brain Sciences is an attempt to understand better the interplay between reactive and proactive inhibition in generating motor inhibitory control both in the healthy people and in the pathophysiology of diseases characterized by poor control of urges (e.g., Parkinson’s disease, Obsessive-compulsive disorder; Attention Deficit Hyperactivity Disorder; Motor Stereotypies; Autism spectrum disorder).

Prof. Giovanni Mirabella

Guest Editor

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Keywords

Reactive inhbition
Proactive inhibition
Inhibitory control
Motor inhibition
Interference inhibition

Published Papers (14 papers)

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Editorial

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6 pages, 217 KiB

Open AccessEditorial

Beyond Reactive Inhibition: Unpacking the Multifaceted Nature of Motor Inhibition

by Giovanni Mirabella

Brain Sci. 2023, 13(5), 804; https://doi.org/10.3390/brainsci13050804 - 16 May 2023

Cited by 3 | Viewed by 887

Abstract

Inhibition is a pillar of cognitive control, i [...] Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

Research

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31 pages, 6884 KiB

Open AccessArticle

Altered Effective Connectivity within an Oculomotor Control Network in Unaffected Relatives of Individuals with Schizophrenia

by Matthew Lehet, Ivy F. Tso, Sohee Park, Sebastiaan F. W. Neggers, Ilse A. Thompson, Rene S. Kahn and Katharine N. Thakkar

Brain Sci. 2021, 11(9), 1228; https://doi.org/10.3390/brainsci11091228 - 17 Sep 2021

Cited by 1 | Viewed by 2031

Abstract

The ability to rapidly stop or change a planned action is a critical cognitive process that is impaired in schizophrenia. The current study aimed to examine whether this impairment reflects familial vulnerability to schizophrenia across two experiments comparing unaffected first-degree relatives to healthy controls. First, we examined performance on a saccadic stop-signal task that required rapid inhibition of an eye movement. Then, in a different sample, we investigated behavioral and neural responses (using fMRI) during a stop-signal task variant that required rapid modification of a prepared eye movement. Here, we examined differences between relatives and healthy controls in terms of activation and effective connectivity within an oculomotor control network during task performance. Like individuals with schizophrenia, the unaffected relatives showed behavioral evidence for more inefficient inhibitory processes. Unlike previous findings in individuals with schizophrenia, however, the relatives showed evidence for a compensatory waiting strategy. Behavioral differences were accompanied by more activation among the relatives in task-relevant regions across conditions and group differences in effective connectivity across the task that were modulated differently by the instruction to exert control over a planned saccade. Effective connectivity parameters were related to behavioral measures of inhibition efficiency. The results suggest that individuals at familial risk for schizophrenia were engaging an oculomotor control network differently than controls and in a way that compromises inhibition efficiency. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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27 pages, 4189 KiB

Open AccessArticle

Cognitive Control of Working Memory: A Model-Based Approach

by Russell J. Boag, Niek Stevenson, Roel van Dooren, Anne C. Trutti, Zsuzsika Sjoerds and Birte U. Forstmann

Brain Sci. 2021, 11(6), 721; https://doi.org/10.3390/brainsci11060721 - 28 May 2021

Cited by 6 | Viewed by 3416

Abstract

Working memory (WM)-based decision making depends on a number of cognitive control processes that control the flow of information into and out of WM and ensure that only relevant information is held active in WM’s limited-capacity store. Although necessary for successful decision making, recent work has shown that these control processes impose performance costs on both the speed and accuracy of WM-based decisions. Using the reference-back task as a benchmark measure of WM control, we conducted evidence accumulation modeling to test several competing explanations for six benchmark empirical performance costs. Costs were driven by a combination of processes running outside of the decision stage (longer non-decision time) and inhibition of the prepotent response (lower drift rates) in trials requiring WM control. Individuals also set more cautious response thresholds when expecting to update WM with new information versus maintain existing information. We discuss the promise of this approach for understanding cognitive control in WM-based decision making. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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19 pages, 1984 KiB

Open AccessArticle

Preparing to React: A Behavioral Study on the Interplay between Proactive and Reactive Action Inhibition

by Stefania C. Ficarella, Andrea Desantis, Alexandre Zénon and Boris Burle

Brain Sci. 2021, 11(6), 680; https://doi.org/10.3390/brainsci11060680 - 22 May 2021

Cited by 3 | Viewed by 2156

Abstract

Motor preparation, based on one’s goals and expectations, allows for prompt reactions to stimulations from the environment. Proactive and reactive inhibitory mechanisms modulate this preparation and interact to allow a flexible control of responses. In this study, we investigate these two control mechanisms with an ad hoc cued Go/NoGo Simon paradigm in a within-subjects design, and by measuring subliminal motor activities through electromyographic recordings. Go cues instructed participants to prepare a response and wait for target onset to execute it (Go target) or inhibit it (NoGo target). Proactive inhibition keeps the prepared response in check, hence preventing false alarms. Preparing the cue-coherent effector in advance speeded up responses, even when it turned out to be the incorrect effector and reactive inhibition was needed to perform the action with the contralateral one. These results suggest that informative cues allow for the investigation of the interaction between proactive and reactive action inhibition. Partial errors’ analysis suggests that their appearance in compatible conflict-free trials depends on cue type and prior preparatory motor activity. Motor preparation plays a key role in determining whether proactive inhibition is needed to flexibly control behavior, and it should be considered when investigating proactive/reactive inhibition. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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17 pages, 12174 KiB

Open AccessArticle

The Human Basal Ganglia Mediate the Interplay between Reactive and Proactive Control of Response through Both Motor Inhibition and Sensory Modulation

by Marion Criaud, Jean-Luc Anton, Bruno Nazarian, Marieke Longcamp, Elise Metereau, Philippe Boulinguez and Bénédicte Ballanger

Brain Sci. 2021, 11(5), 560; https://doi.org/10.3390/brainsci11050560 - 28 Apr 2021

Cited by 10 | Viewed by 6730

Abstract

The basal ganglia (BG) have long been known for contributing to the regulation of motor behaviour by means of a complex interplay between tonic and phasic inhibitory mechanisms. However, after having focused for a long time on phasic reactive mechanisms, it is only recently that psychological research in healthy humans has modelled tonic proactive mechanisms of control. Mutual calibration between anatomo-functional and psychological models is still needed to better understand the unclear role of the BG in the interplay between proactive and reactive mechanisms of control. Here, we implemented an event-related fMRI design allowing proper analysis of both the brain activity preceding the target-stimulus and the brain activity induced by the target-stimulus during a simple go/nogo task, with a particular interest in the ambiguous role of the basal ganglia. Post-stimulus activity was evoked in the left dorsal striatum, the subthalamus nucleus and internal globus pallidus by any stimulus when the situation was unpredictable, pinpointing its involvement in reactive, non-selective inhibitory mechanisms when action restraint is required. Pre-stimulus activity was detected in the ventral, not the dorsal, striatum, when the situation was unpredictable, and was associated with changes in functional connectivity with the early visual, not the motor, cortex. This suggests that the ventral striatum supports modulatory influence over sensory processing during proactive control. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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16 pages, 1947 KiB

Open AccessArticle

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

by Luigi Cattaneo and Sara Parmigiani

Brain Sci. 2021, 11(5), 534; https://doi.org/10.3390/brainsci11050534 - 24 Apr 2021

Cited by 6 | Viewed by 2642

Abstract

Delayed motor tasks require timely interaction between immobility and action. The neural substrates of these processes probably reside in the premotor and motor circuits; however, fine-grained anatomical/functional information is still lacking. Participants performed a delayed simple reaction task, structured as a ready-set-go sequence, with a fixed, predictable, SET-period. Responses were given with lip movements. During the SET-period, we performed a systematic dense-mapping of the bilateral dorsal premotor region (dPM) by means of single transcranial magnetic stimulation (TMS) pulses on an 18-spot mapping grid, interleaved with sham TMS which served as a baseline. Reaction times (RTs) in TMS trials over each grid spot were compared to RTs in sham trials to build a statistical parametric z-map. The results reveal a rostro-caudal functional gradient in the dPM. TMS of the rostral dPM induced a shift from reactive towards predictive response strategies. TMS of the caudal dPM interfered with the SET-period duration. By means of dense TMS mapping, we have drawn a putative functional map of the role of the dPM during the SET-period. A higher-order rostral component is involved in setting action strategies and a caudal, lower-order, part is probably involved in the inhibitory control of motor output. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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10 pages, 1292 KiB

Open AccessArticle

Inhibitory Control on a Stop Signal Task in Tourette Syndrome before and after Deep Brain Stimulation of the Internal Segment of the Globus Pallidus

by Francesca Morreale, Zinovia Kefalopoulou, Ludvic Zrinzo, Patricia Limousin, Eileen Joyce, Tom Foltynie and Marjan Jahanshahi

Brain Sci. 2021, 11(4), 461; https://doi.org/10.3390/brainsci11040461 - 05 Apr 2021

Cited by 4 | Viewed by 2132

Abstract

As part of the first randomized double-blind trial of deep brain stimulation (DBS) of the globus pallidus (GPi) in Tourette syndrome, we examined the effect of stimulation on response initiation and inhibition. A total of 14 patients with severe Tourette syndrome were recruited and tested on the stop signal task prior to and after GPi-DBS surgery and compared to eight age-matched healthy controls. Tics were significantly improved following GPi-DBS. The main measure of reactive inhibition, the stop signal reaction time did not change from before to after surgery and did not differ from that of healthy controls either before or after GPi-DBS surgery. This suggests that patients with Tourette syndrome have normal reactive inhibition which is not significantly altered by GPi-DBS. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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17 pages, 4745 KiB

Open AccessArticle

by Sien Hu and Chiang-shan R. Li

Brain Sci. 2020, 10(12), 1013; https://doi.org/10.3390/brainsci10121013 - 19 Dec 2020

Cited by 6 | Viewed by 2739

Abstract

Aging is associated with structural and functional changes in the hippocampus, and hippocampal dysfunction represents a risk marker of Alzheimer’s disease. Previously, we demonstrated age-related changes in reactive and proactive control in the stop signal task, each quantified by the stop signal reaction time (SSRT) and sequential effect computed as the correlation between the estimated stop signal probability and go trial reaction time. Age was positively correlated with the SSRT, but not with the sequential effect. Here, we explored hippocampal gray matter volume (GMV) and activation to response inhibition and to p(Stop) in healthy adults 18 to 72 years of age. The results showed age-related reduction of right anterior hippocampal activation during stop success vs. go trials, and the hippocampal activities correlated negatively with the SSRT. In contrast, the right posterior hippocampus showed higher age-related responses to p(Stop), but the activities did not correlate with the sequential effect. Further, we observed diminished GMVs of the anterior and posterior hippocampus. However, the GMVs were not related to behavioral performance or regional activities. Together, these findings suggest that hippocampal GMVs and regional activities represent distinct neural markers of cognitive aging, and distinguish the roles of the anterior and posterior hippocampus in age-related changes in cognitive control. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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18 pages, 1012 KiB

Open AccessArticle

A Time Series-Based Point Estimation of Stop Signal Reaction Times: More Evidence on the Role of Reactive Inhibition-Proactive Inhibition Interplay on the SSRT Estimations

by Mohsen Soltanifar, Keith Knight, Annie Dupuis, Russell Schachar and Michael Escobar

Brain Sci. 2020, 10(9), 598; https://doi.org/10.3390/brainsci10090598 - 29 Aug 2020

Cited by 7 | Viewed by 3444

Abstract

The Stop Signal Reaction Time (SSRT) is a latency measurement for the unobservable human brain stopping process, and was formulated by Logan (1994) without consideration of the nature (go/stop) of trials that precede the stop trials. Two asymptotically equivalent and larger indices of mixture SSRT and weighted SSRT were proposed in 2017 to address this issue from time in task longitudinal perspective, but estimation based on the time series perspective has still been missing in the literature. A time series-based state space estimation of SSRT was presented and it was compared with Logan 1994 SSRT over two samples of real Stop Signal Task (SST) data and the simulated SST data. The results showed that time series-based SSRT is significantly larger than Logan’s 1994 SSRT consistent with former Longitudinal-based findings. As a conclusion, SSRT indices considering the after effects of inhibition in their estimation process are larger yielding to hypothesize a larger estimates of SSRT using information on the reactive inhibition, proactive inhibition and their interplay in the SST data. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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15 pages, 1725 KiB

Open AccessArticle

Mouse Tracking to Explore Motor Inhibition Processes in Go/No-Go and Stop Signal Tasks

by Viola Benedetti, Gioele Gavazzi, Fabio Giovannelli, Riccardo Bravi, Fiorenza Giganti, Diego Minciacchi, Mario Mascalchi, Massimo Cincotta and Maria Pia Viggiano

Brain Sci. 2020, 10(7), 464; https://doi.org/10.3390/brainsci10070464 - 20 Jul 2020

Cited by 13 | Viewed by 4598

Abstract

Response inhibition relies on both proactive and reactive mechanisms that exert a synergic control on goal-directed actions. It is typically evaluated by the go/no-go (GNG) and the stop signal task (SST) with response recording based on the key-press method. However, the analysis of discrete variables (i.e., present or absent responses) registered by key-press could be insufficient to capture dynamic aspects of inhibitory control. Trying to overcome this limitation, in the present study we used a mouse tracking procedure to characterize movement profiles related to proactive and reactive inhibition. A total of fifty-three participants performed a cued GNG and an SST. The cued GNG mainly involves proactive control whereas the reactive component is mainly engaged in the SST. We evaluated the velocity profile from mouse trajectories both for responses obtained in the Go conditions and for inhibitory failures. Movements were classified as one-shot when no corrections were observed. Multi-peaked velocity profiles were classified as non-one-shot. A higher proportion of one-shot movements was found in the SST compared to the cued GNG when subjects failed to inhibit responses. This result suggests that proactive control may be responsible for unsmooth profiles in inhibition failures, supporting a differentiation between these tasks. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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Review

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15 pages, 993 KiB

Open AccessReview

Towards Conceptual Clarification of Proactive Inhibitory Control: A Review

by Wery P. M. van den Wildenberg, K. Richard Ridderinkhof and Scott A. Wylie

Brain Sci. 2022, 12(12), 1638; https://doi.org/10.3390/brainsci12121638 - 29 Nov 2022

Cited by 4 | Viewed by 2044

Abstract

The aim of this selective review paper is to clarify potential confusion when referring to the term proactive inhibitory control. Illustrated by a concise overview of the literature, we propose defining reactive inhibition as the mechanism underlying stopping an action. On a stop trial, the stop signal initiates the stopping process that races against the ongoing action-related process that is triggered by the go signal. Whichever processes finishes first determines the behavioral outcome of the race. That is, stopping is either successful or unsuccessful in that trial. Conversely, we propose using the term proactive inhibition to explicitly indicate preparatory processes engaged to bias the outcome of the race between stopping and going. More specifically, these proactive processes include either pre-amping the reactive inhibition system (biasing the efficiency of the stopping process) or presetting the action system (biasing the efficiency of the go process). We believe that this distinction helps meaningful comparisons between various outcome measures of proactive inhibitory control that are reported in the literature and extends to experimental research paradigms other than the stop task. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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13 pages, 253 KiB

Open AccessReview

Stopping a Response When You Really Care about the Action: Considerations from a Clinical Perspective

by Sharon Morein-Zamir and Gideon Anholt

Brain Sci. 2021, 11(8), 979; https://doi.org/10.3390/brainsci11080979 - 23 Jul 2021

Cited by 1 | Viewed by 2826

Abstract

Response inhibition, whether reactive or proactive, is mostly investigated in a narrow cognitive framework. We argue that it be viewed within a broader frame than the action being inhibited, i.e., in the context of emotion and motivation of the individual at large. This is particularly important in the clinical domain, where the motivational strength of an action can be driven by threat avoidance or reward seeking. The cognitive response inhibition literature has focused on stopping reactively with responses in anticipation of clearly delineated external signals, or proactively in limited contexts, largely independent of clinical phenomena. Moreover, the focus has often been on stopping efficiency and its correlates rather than on inhibition failures. Currently, the cognitive and clinical perspectives are incommensurable. A broader context may explain the apparent paradox where individuals with disorders characterised by maladaptive action control have difficulty inhibiting their actions only in specific circumstances. Using Obsessive Compulsive Disorder as a case study, clinical theorising has focused largely on compulsions as failures of inhibition in relation to specific internal or external triggers. We propose that the concept of action tendencies may constitute a useful common denominator bridging research into motor, emotional, motivational, and contextual aspects of action control failure. The success of action control may depend on the interaction between the strength of action tendencies, the ability to withhold urges, and contextual factors. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

24 pages, 3568 KiB

Open AccessReview

Reactive and Proactive Adaptation of Cognitive and Motor Neural Signals during Performance of a Stop-Change Task

by Adam T. Brockett and Matthew R. Roesch

Brain Sci. 2021, 11(5), 617; https://doi.org/10.3390/brainsci11050617 - 11 May 2021

Cited by 4 | Viewed by 3007

Abstract

The ability to inhibit or suppress unwanted or inappropriate actions, is an essential component of executive function and cognitive health. The immense selective pressure placed on maintaining inhibitory control processes is exemplified by the relatively small number of instances in which these systems completely fail in the average person’s daily life. Although mistakes and errors do inevitably occur, inhibitory control systems not only ensure that this number is low, but have also adapted behavioral strategies to minimize future failures. The ability of our brains to adapt our behavior and appropriately engage proper motor responses is traditionally depicted as the primary domain of frontal brain areas, despite evidence to the fact that numerous other brain areas contribute. Using the stop-signal task as a common ground for comparison, we review a large body of literature investigating inhibitory control processes across frontal, temporal, and midbrain structures, focusing on our recent work in rodents, in an effort to understand how the brain biases action selection and adapts to the experience of conflict. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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17 pages, 6359 KiB

Open AccessReview

Computational Mechanisms Mediating Inhibitory Control of Coordinated Eye-Hand Movements

by Sumitash Jana, Atul Gopal and Aditya Murthy

Brain Sci. 2021, 11(5), 607; https://doi.org/10.3390/brainsci11050607 - 10 May 2021

Cited by 2 | Viewed by 2634

Abstract

Significant progress has been made in understanding the computational and neural mechanisms that mediate eye and hand movements made in isolation. However, less is known about the mechanisms that control these movements when they are coordinated. Here, we outline our computational approaches using accumulation-to-threshold and race-to-threshold models to elucidate the mechanisms that initiate and inhibit these movements. We suggest that, depending on the behavioral context, the initiation and inhibition of coordinated eye-hand movements can operate in two modes—coupled and decoupled. The coupled mode operates when the task context requires a tight coupling between the effectors; a common command initiates both effectors, and a unitary inhibitory process is responsible for stopping them. Conversely, the decoupled mode operates when the task context demands weaker coupling between the effectors; separate commands initiate the eye and hand, and separate inhibitory processes are responsible for stopping them. We hypothesize that the higher-order control processes assess the behavioral context and choose the most appropriate mode. This computational mechanism can explain the heterogeneous results observed across many studies that have investigated the control of coordinated eye-hand movements and may also serve as a general framework to understand the control of complex multi-effector movements. Full article

(This article belongs to the Special Issue How Does Motor Inhibitory Control Emerge from the Interplay between Reactive and Proactive Inhibition)

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