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Develop Med Child Neuro - 2020 - Mirabella - Inhibitory Control and Impulsive Responses in Neurodevelopmental Disorders
Develop Med Child Neuro - 2020 - Mirabella - Inhibitory Control and Impulsive Responses in Neurodevelopmental Disorders
1 Department of Clinical and Experimental Sciences, University of Brescia, Brescia; 2 Istituto di Ricovero e Cura a Carattere Scientifico Neuromed, Pozzilli, Italy.
Correspondence to Giovanni Mirabella at Department of Clinical and Experimental Sciences, Brescia University, Viale Europa, 11, 25123 Brescia, Italy. E-mail: giovanni.mirabella@unibs.it
The impairment of inhibitory control is often assumed to be the core deficit of several neu-
PUBLICATION DATA rodevelopmental disorders characterized by poor impulse control. However, could the same
Accepted for publication 13th November deficit explain different clinical phenotypes? Evidence from behavioural studies is very mixed.
2020. This is partly because inhibition is a highly complex executive function. Thus, the different
Published online 19th December 2020 types of tasks that generically tap into inhibitory control are likely to provide different out-
comes. Additionally, sample inhomogeneity in terms of age, comorbidity, and medical treat-
ABBREVIATIONS ment are confounding factors. Therefore, to make a reliable assessment of the deficit of
ASD Autism spectrum disorder inhibitory control in a given disorder, the same task and samples with similar characteristics
OCD Obsessive–compulsive disorder must be employed. This article reviews and discusses studies on five neurodevelopmental
disorders with impaired impulse control where these criteria have been used: Tourette syn-
drome; obsessive–compulsive disorder; attention-deficit/hyperactivity disorder; primary motor
stereotypies; and autism spectrum disorder. Overall, they suggest that the mechanisms
underlying the inability to control urges are extremely heterogeneous and cannot be ascribed
to a general impairment of inhibition. These findings do not support the hypothesis that inhi-
bitory deficits represent a transdiagnostic feature of neurodevelopmental disorders with poor
impulse control.
The relationship between the impairment of inhibitory controlling for several confounding factors. First, the
control and neurodevelopmental disorders characterized by review focuses on one domain of inhibition, that is, motor
poor urge control is a hotly debated subject. Movement inhibition. Since people with pathological control of
inhibition allows the gating of inappropriate response ten- impulses tend to produce inappropriate movements, motor
dencies, thereby ensuring the emergence of context-appro- inhibition is likely to be the most affected domain of inhibi-
priate, goal-directed behaviours. Therefore, impairments in tory control. In line with this reasoning, only the results of
motor inhibition have often been considered the core defi- studies where the stop-signal task was employed have been
cit of neurodevelopmental disorders characterized by pre- considered. Second, only studies with participants of similar
mature, impulsive, and out-of-context motor behaviours.1–4 age (children/adolescents) have been included. Third, the
However, the picture emerging from studies that address review focuses only on behavioural studies because, despite
this issue is extremely mixed. Tourette syndrome repre- differences in task design and sample selection, they repre-
sents a paradigmatic example. In fact, while some studies sent a set of more homogeneous data than those obtained
revealed impaired inhibitory control in Tourette syndrome with other techniques (e.g. neuroimaging) where the num-
compared to typically developing controls,5 others found ber of confounding variables is higher. By applying such
no differences,6 and a few studies paradoxically found strict criteria, a clearer picture of the role of inhibitory con-
enhanced inhibitory control.7 This is partly because inhibi- trol in neurodevelopmental disorder emerges.
tory control is multifaceted and includes several domains.
Confounding factors, such as the behavioural task used THE MANY FACETS OF INHIBITORY CONTROL
and/or differences in sample characteristics (presence of Inhibitory control is not a single executive function;
comorbid disorders, age of patients, presence or absence of instead, it encompasses several different components. A
medical treatment), can explain such conflicting results. generally accepted distinction is the one between motor
Consequently, at present, it is difficult to draw any firm and interference inhibition.8 Motor inhibition refers to the
conclusions about the role of deficits in inhibitory control ability to inhibit a preplanned motor response, and it is
in disorders where patients show poor urge control. usually measured using the go/no-go9 or stop-signal
This review aims to explore whether and how inhibition tasks.10 The two tasks differ because the former measures
deficits can explain different clinical phenotypes after the ability to suppress a potential action (action restraint)
Review 521
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CONDITIONAL STOP-SIGNAL TASK
(a) CRITICAL DIRECTION (50%) NON-CRITICAL DIRECTION (50%)
NO-STOP TRIAL (66%) NO-STOP TRIAL: TYPE 1 (66%)
SSD SSD
Press left
INCOMPATIBLE
Time (ms)
Figure 1: The many facets of inhibitory control. (a) Schematic representation of the conditional stop-signal task. Adapted from Aron et al.19 with per-
mission. (b) Schematic representation of the stop-signal anticipation task. Adapted from van Hulst et al.20 with permission. (c) Schematic representation
of the reaching arm version of the go-only and stop-signal tasks. Adapted from Mancini et al.6 with permission. (d) Schematic representation of the
masked priming task. Adapted from Keute et al.24 with permission. SSD, stop-signal delay
proactive strategies because of the concurrent cognitive response; reaction time) and movement timing (i.e. the
demands on other executive functions. time to execute the motor response; movement time) of
An alternative approach is the one based on comparing no-stop trials (i.e. trials employing the stop-signal task
the behavioural parameters of the very same movements where participants have to perform a movement) with
executed in two different contexts, that is when individuals those measured during the execution of the same action in
are aware of an upcoming stop-signal versus when they the context of a simple reaction time task (go-only
know that a stop-signal is not going to be presented.6,21,22 trial6,21). In the reaching arm version of the stop-signal
Exploiting the reaching arm version of the stop-signal task task, participants are comfortably seated in front of a
(Fig. 1) has shown that proactive control can be assessed touchscreen placed within a reachable distance; visual stim-
by comparing the reaction (i.e. the time to initiate a uli are presented on the touchscreen. The go-only task
Review 523
14698749, 2021, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/dmcn.14778 by CAPES, Wiley Online Library on [31/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
feature of all these disorders lies in the impairment of
Drug-na€ıvea
Medication
Drug-na€ıve
Drug-na€ıve
Drug-na€ıve
motor inhibition1–4 is unlikely to provide an exhaustive
Table 1: Summary of the main findings from studies assessing deficits in proactive and reactive inhibitory control and/or in automatic inhibition in disorders characterized by poor impulsivity control in
Mixed
Mixed
status
explanation of the disorder.
Given this, it is crucial to establish a bridge between
inhibitory control deficits and their clinical manifestations.
range (y)
Therefore, before discussing the results of single studies,
10–17
7–15
8–12
6–10
5–28
7–10
Age
the potential effects of deficiencies in each type of inhibi-
tion on cognitive-motor processes will be described.
Drug-na€ıve patients did not receive any drugs. OCD, obsessive–compulsive disorder; ADHD, attention-deficit/hyperactivity disorder; ASD, autism spectrum disorder.
Impairment of reactive inhibition should make an individ-
16, 13, 8
39, 32
20
28
121
50
Sample
Keute et al.24
Review 525
14698749, 2021, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/dmcn.14778 by CAPES, Wiley Online Library on [31/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
A CK N O W L E D G E M E N T S Figure S1. Flow chart of the stop-signal task assessing both
The author has stated that they have no interests that might be proactive and reactive inhibition in neurodevelopmental disorders.
perceived as posing a conflict or bias.doi: 10.1111/dmcn.14778 Figure S2. Flow chart of the negative compatibility effect to
assess automatic motor inhibition in neurodevelopmental disor-
SUPPORTING INFORMATION ders.
The following additional material may be found online:
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CONTROLE INIBITORIO E RESPOSTAS IMPULSIVAS EM TRANSTORNOS NEURODESENVOLVIMENTAIS
A deficie ^ ncia do controle inibito rio e
frequentemente assumida como o de ficit central de va
rios transtornos neurodesenvolvimen-
tais caracterizados por pouco controle do impulso. No entanto, o mesmo de ficit pode explicar diferentes feno tipos clınicos?
Evide ^ncias de estudos comportamentais sa ~ o muito diversas. Isso se deve parcialmente ao fato de que a inibicßa ~o e uma funcßa ~o
executiva altamente complexa. Assim, os diferentes tipos de tarefas que genericamente abordam o controle inibito rio sa~o
prova veis de fornecer resultados diferentes. Ale m disso, a falta de homogeneidade das amostras em termos de idade, comorbida-
des, e tratamentos me dicos sa
~ o fatores de confusa ~o. Portanto, para se fazer uma avaliacßa ~ o confia
vel do deficit de controle ini-
rio em uma dada desordem, a mesma tarefa e amostras com caracterısticas similares devem ser empregadas. Este artigo
bito
revisa e discute cinco transtornos neurodesenvolvimentais com deficie ^ ncia do controle do impulso em que estes crite rios foram
empregados: sındrome de Tourette; transtorno obsessivo compulsivo; estereotipias motoras prima rias; e transtorno do espectro
autista. Em geral, eles sugerem que os mecanismos subjacentes a capacidade de controlar ımpetos sa ~ o extremamente hete-
roge ^neos e na ~ o podem ser circunscritos a uma deficie ~o Estes achados na
^ncia geral de inibicßa ~o sustentam a hipo tese de que os
deficits inibito rios representam um aspecto transdiagno stico dos transtornos neurodesenvolvimentais com pouco controle dos
impulsos.