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DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY INVITED REVIEW

Inhibitory control and impulsive responses in neurodevelopmental


disorders
GIOVANNI MIRABELLA 1,2

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

Plain language summary: https://onlinelibrary.wiley.com/doi/10.1111/dmcn.15451

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)

520 DOI: 10.1111/dmcn.14778 © 2020 Mac Keith Press


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
while the latter measures the ability to inhibit an action What this paper adds
that has already been initiated (action cancellation). • The mechanisms underlying the inability to control urges in neurodevelop-
In contrast, interference inhibition assesses the ability to mental disorders are heterogeneous.
resolve response conflict due to irrelevant but incompati- • Inhibition impairments cannot generally explain all neurodevelopmental dis-
ble, and therefore interfering, stimulus characteristics that orders characterized by poor urge control.
must be inhibited to avoid erroneous responses. This type
feel less self-confident and more anxious.1,18 As discussed
of inhibitory control is usually studied with the Simon,11
in the next section, the cognitive mechanisms subserving
Eriksen flanker,12 and Stroop13 tasks. The response-related
reactive and proactive control can be affected selectively,
interference in the Simon and Eriksen flanker tasks is the
thereby determining the emergence of the phenotypes of
consequence of the simultaneous activation of two poten-
different disorders.
tial responses. What the Stroop task really assesses is a
Therefore, when assessing motor inhibition, it is crucial
matter of debate. It has been suggested that it involves a
to employ a paradigm that allows the measurement of both
different type of response-related interference than the
reactive and proactive inhibition. The stop-signal task, but
other two tasks because response-related interference in
not the go/no-go task, has this potential. In the stop-signal
the Stroop task is due to the involuntary activation of a
task, reactive inhibition is always quantified by measuring
prepotent response, for example, the automatic tendency to
the time it takes to inhibit an action when the stop-signal
read a word.14
is presented, that is, the stop-signal reaction time.10 By
There are also other types of cognitive inhibition, such
contrast, how to estimate proactive control is more contro-
as inhibition of memory retrieval, which can be assessed
versial.
using the think/no-think task,15 or verbal inhibition, which
On the one hand, some researchers have modified the
can be assessed using the Hayling task.16
stop-signal task by introducing cues that inform the partic-
Even though all these tasks share the requirement to
ipant about the probability of an upcoming stop-signal as
suppress the processing of a prepotent, bottom-up-gener-
in the conditional stop-signal (Fig. 1)19 or stop-signal
ated inappropriate response, it is possible that the cognitive
anticipation tasks (Fig. 1).20 In the conditional stop-task,
abilities required for a given type of inhibition could be
all trials begin with a cue circle’s appearance, with the left
differently affected in different disorders. In particular,
half of one colour and the right half of another colour
given that people with poor impulse control are likely to
(Fig. 1). The cue instructs the participants that one direc-
perform out-of-context movements, it seems reasonable to
tion is ‘critical’ (e.g., black), and the other is ‘non-critical’
suppose that motor inhibition could be the most affected
(e.g., grey). Then, an arrow appears within the circle. If
component of inhibitory control. Thus, the present review
the arrow points to the critical direction, the participants
focuses only on this domain.
have to press the right key as soon as possible (no-stop tri-
als, 66% of total trials) unless a tone occurs after a delay
THE COMPLEXITY OF MOTOR INHIBITION (stop-signal delay). In this instance, the participants have
Motor inhibition is defined as the ability to suppress a pre-
to withhold the response (stop trials, 34% of total trials).
potent motor response. This inhibition domain is no less
However, if the arrow points to the non-critical direction
complex than other, sometimes defined as more cognitive,
(towards the left side in Fig. 1), the participants have to
forms of inhibitory control (e.g. interference inhibition).
press the left key irrespective of whether a tone occurs
Suppressing an action that is about to be generated implies
(no-stop trials type 1, 66% of total trials) or whether it
the evaluation of the pros and cons of several dimensions
occurs (no-stop trials type 2, 34% of total trials). Thus, in
that are part of the decision-making process.17 Action
the non-critical direction, participants must ignore the stop
withholding involves the retrieval of past experiences,
signals. In the stop-anticipation task, most trials are no-
exploitation of task instructions, evaluation of the current
stop trials. A bar moves at a constant speed from the bot-
context, and internal states.
tom up in those trials, reaching the black line (the target)
Of relevance, motor inhibition is not a unitary construct;
in 800ms (Fig. 1). Participants have to stop the bar as close
at least two neuropsychological domains have been distin-
to the black line as possible by pressing a button with the
guished: (1) reactive inhibition, that is, the ability to stop a
right index finger. In fewer trials (stop trials), the bar stops
response immediately when a stop instruction is presented;
before reaching the target line, and participants are
and (2) proactive inhibition, that is, the ability to adapt the
instructed to withhold pressing the key. The probability of
motor strategy according to the context where an individ-
stop-signal occurrence changed across trials (0%, 27.5%,
ual is embedded. Both components probably play a role in
32.5%, 37.5%) and is indicated by the characteristics of
diseases characterized by poor urge control. Deficits in
the target line (in Fig. 1, indicated by the different line
reactive inhibition are likely to be directly linked to the
hatchings). These two tasks are cognitively very demanding
inability to suppress unwanted actions. In contrast, since
since participants must remember the meaning of cues and
proactive control strategies are tightly linked to one’s
task instructions. Under these conditions, it is likely that
short-, medium-, and long-term goals, which are retrieved
the load on attentional and working memory is high.
from stored memories according to the current context,
Therefore, outcome measures cannot be easily ascribed to
impairment of this component could lead the individual to

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%)

Reaction time Reaction time

STOP TRIAL (34%) NO-STOP TRIAL: TYPE 2 (34%)

SSD SSD

STOP-SIGNAL ANTICIPATION TASK


(b) NO-STOP TRIAL STOP TRIAL STOP-SIGNAL PROBABILITY

0% 27.5% 32.5% 37.5%


Time (ms) Time (ms)

ARM REACHING STOP-SIGNAL TASK

(c) GO-ONLY TASK STOP-SIGNAL TASK


NO-STOP TRIAL (66%)
Go-signal Success

STOP TRIAL (34%)


Go-signal Success Go-signal Stop-signal Success
SSD

MASKED PRIMING TASK


(d) PRIME MASK TARGET CORRECT RESPONSE
Press right
COMPATIBLE

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

522 Developmental Medicine & Child Neurology 2021, 63: 520–526


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
consists only of go-only trials, while the stop-signal task previous stimulus (the prime) unconscious. Finally, a
consists of a pseudorandom mix of no-stop (66%) and stop supraliminal arrow target is shown. Participants have to
trials (34%). All trials begin with the appearance of a cen- press the right key if the supraliminal arrow target points
tral stimulus; participants have to reach the stimulus and to the right and the left key if it points to the left. When
hold it for a variable period (500–800ms). Then, a periph- the prime arrow points in the same direction as the arrow
eral target appears (go-signal). In the go-only and no-stop target, the trial is defined as compatible; otherwise, it is
trials, participants have to reach and hold the target for defined as incompatible (Fig. 1). When the delay between
300 to 400ms. On the other hand, in the stop trials, before the prime and target is short, compatible priming allows
movement onset, the central stimulus (stop-signal) reap- faster and more accurate responses, whereas incompatible
pears at a variable stop-signal delay, prompting the partici- priming impairs motor performance. However, when the
pant to withhold the incipient movement. To succeed, delay between the prime and target delay is long enough,
participants must keep the index finger on the stop-signal the effect reverses, a phenomenon known as the negative
(Fig. 1). It has been shown that when participants perform compatibility effect. This phenomenon has been inter-
a no-stop trial, reaction time is lengthened, and movement preted as an effect of automatic delayed inhibition process-
time is shortened compared to when they perform a go- ing occurring in the motor system, which reverses the
only trial. This phenomenon has been named the ‘context priming-induced response activation.25
effect’ and represents an example of motor strategy opti- Given these premises, the results of studies providing
mization. In fact, during the execution of no-stop trials, measures of reactive, proactive, and automatic motor inhi-
participants tend to lengthen reaction time to increase the bition in neurodevelopmental disorders characterized by
opportunity to stop the response in case a stop-signal is poor urge control are reviewed and compared in the next
presented. At the same time, longer reaction times allow section of the review.
better coding of the target parameters and hence faster
movement times. By contrast, during the execution of go- SPECIFIC PATTERNS OF MOTOR INHIBITION
only trials, participants react very quickly to go-signals to IMPAIRMENT SHAPE THE PHENOTYPES OF
the detriment of the target parameter coding. Thus, move- NEURODEVELOPMENTAL DISORDERS WITH POOR
ment execution must be completed during the movement URGE CONTROL
phase, thereby lengthening movement times.23 The advan- To identify studies that assessed the impairment patterns
tage of this approach over the use of cues indicating the of proactive, reactive, and automatic motor inhibition in
probability of a stop-signal being presented lies in the fact neurodevelopmental disorders, two different literature
that attentional and working memory demands are kept to searches were conducted in PubMed according to the rec-
a minimum. Therefore, results can be promptly linked to ommendations described in the Preferred Reporting Items
changes in proactive strategies. for Systematic Reviews and Meta-Analysis (PRISMA)
Even though proactive mechanisms have attracted atten- guidelines.26 Two systematic searches up to September
tion only relatively recently,1 there is no doubt that this 2020 were conducted using the terms described in Figs S1
component serves a complementary function to reactive and S2 (online supporting information). The results are
inhibition and that motor inhibitory control emerges from summarized in Table 1. The five neurodevelopmental dis-
the interplay between these two domains. The different orders studied in the articles identified by these searches
phenotypes characterizing the many types of impulse disor- were: Tourette syndrome; obsessive–compulsive disorder
ders are most likely generated by combinations of impair- (OCD); attention-deficit/hyperactivity disorder (ADHD);
ments affecting reactive and proactive inhibition. primary motor stereotypies; and autism spectrum disorder
Recent work has suggested that a critical aspect of the (ASD). Motor stereotypies are repetitive, rhythmic, appar-
stop-signal task is that motor inhibition is an explicit goal; ently purposeless movements that interfere with activities
thus, it requires participants to maintain the task set while of daily living. They have a fixed pattern, are triggered by
performing the task. Under these conditions, a failure to some states of mind (e.g. stress, fatigue, boredom), and can
remember the instructions or inattention to relevant stim- be stopped by diverting attention. These are all conditions
uli may be interpreted erroneously as poor inhibitory con- where movements are not adequately controlled and per-
trol.24 To overcome these potential limitations, a type of formed despite the willingness of the individual. Even
inhibition that does not require an explicit stop-signal and though all these disorders are characterized by poor urge
the conscious awareness of participants, that is automatic control, their phenotypes are different, suggesting that they
motor inhibition, has been measured.24 Automatic inhibi- represent independent disorders arising from different
tion has been assessed using a subliminal masked priming pathophysiological mechanisms. Thus, at least when these
task (Fig. 1). In this task, all trials begin with the presenta- disorders are not comorbid with one another, the defi-
tion of a fixed dot. Then, participants are shown an arrow ciency in impulse control is likely to be generated by dif-
for the shortest possible time, that is, one refresh rate of ferent cognitive mechanisms. The identification of such
the monitor, followed by a random pattern mask (in Fig. 1, cognitive mechanisms represents a crucial step towards
this is a random mix of vertical and horizontal lines) which understanding disorder aetiology and the development of
lasts for a longer time, making the perception of the effective treatments. The generic claim that the core

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

ual incapable of resisting from moving on exogenous or


size

endogenous trigger presentation, despite the action being


inappropriate. On the other hand, a deficit in proactive

Proactive inhibition only


Reactive inhibition only
Reactive inhibition only

Reactive inhibition only


inhibitory control would affect an individual’s ability to
exploit environmental or mental cues to maintain informa-
inhibition in OCD
Deficits in motor

tion about which actions are most appropriate in a given


Reactive and

context. Finally, a possible effect of damage to the auto-


No deficits
proactive
inhibition

matic inhibition domain is that individuals cannot stop


actions triggered by object affordances when those objects
are not behaviourally relevant.24 These potential move-
ments are normally suppressed without conscious aware-
Reactive and proactive inhibition

Reactive and proactive inhibition


Reactive and proactive inhibition

Reactive and proactive inhibition

Reactive and proactive inhibition


Type of motor inhibition studied

ness. A loss of this ability would induce impulsive


behaviours that are simply triggered by the sight of objects
in the individual’s surroundings.
With this frame of reference, it is possible to interpret
Automatic inhibition

the results from Mirabella et al.21 regarding drug-na€ıve


children with primary motor stereotypies (i.e. stereotypies
not associated with other neurological conditions; primary
motor stereotypies). Mirabella et al.21 found that these
children had a marked deficit in reactive inhibition com-
pared to typically developing children. However, proactive
control was similar to the typically developing control
stop-signal task and go-only task

stop-signal task and go-only task

group. This evidence might explain the two key features of


Stop-signal and go-only tasks
Reaching arm version of the

Reaching arm version of the


Stop-signal anticipation task

the phenotype of primary motor stereotypies. On the one


hand, impairment of reactive inhibition could be the rea-
son for patients’ inability to refrain from performing
Masked priming task

stereotypic movements when triggered by excitement,


Stop-signal task

stress, boredom, or fatigue.27 On the other hand, an intact


proactive control should allow patients to be aware of the
context and thus to stop when their attention is diverted.27
Task(s)

Interestingly, the results from the study by Mirabella


et al.21 are in contrast with those of Schmitt et al.,22 who
tested a large cohort of patients with uncomplicated ASD
and Tourette syndrome + OCD

(i.e. patients with ASD without comorbid psychiatric disor-


Primary motor stereotypies

ders; Table 1), finding a deficit in proactive control strate-


Tourette syndrome, OCD,

ADHD and ASD + ADHD

gies whereas reactive inhibition was similar to that of


typically developing controls. Interestingly, impairment in
proactive control scaled with the severity of restrictive
repetitive behaviours and, in particular, with motor stereo-
Disorder(s)

typies. Schmitt et al.22 used an experimental approach sim-


ilar to that of Mirabella et al.,21 that is, in both cases, the
ADHD
ADHD
ASD
children and adolescents

version of the stop-signal paradigm was minimally


demanding in terms of attentional and working memory
van Hulst et al.20
Mirabella et al.21

requirements. Thus, apart from the fact that in the former


Schmitt et al.22
Mancini et al.6

Keute et al.24

study participants had to inhibit key-press movements,


Pani et al.31

whereas in the latter participants had to suppress arm-


Study

reaching movements, the contrasting findings are unlikely


to be explained by experimental design. A more relevant
a

524 Developmental Medicine & Child Neurology 2021, 63: 520–526


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difference lies in the age range of participants, which is Relevant to the topic of this review, it has been shown that
much wider in the Schmitt et al.22 sample than in the cognitive mechanisms underlying tic and compulsion con-
study by Mirabella et al.21 (Table 1). Since inhibitory trol are completely different. Mancini et al.6 assessed reac-
control changes over the lifespan,28 a wide age range is tive and proactive inhibitory control using a reaching arm
more likely to produce large variability. Indeed, Schmitt version of the stop-signal task in a very large cohort of
et al.22 showed that proactive control matures throughout drug-na€ıve children/adolescents affected by Tourette syn-
childhood and adolescence to early adulthood in individ- drome, OCD, and in those where the two disorders co-oc-
uals with ASD and typically developing individuals. curred (Table 1). They found that both reactive and
However, the ability to exert proactive strategies is proactive inhibition were impaired; the impairment scaled
impaired since childhood and it develops slower in indi- with the severity of OCD symptoms. By contrast, inhibi-
viduals with ASD than in typically developing individuals. tory control in patients with uncomplicated Tourette syn-
In light of these considerations, it is more likely that drome was similar to that of typically developing controls.
ASD and primary motor stereotypies might be character- The simultaneous deficit in proactive and reactive inhibi-
ized by a different pattern of inhibitory control impair- tion makes patients with OCD unable to resist performing
ment. The deficit in proactive inhibition in individuals compulsive actions triggered by their obsessive thoughts,
with ASD could clinically manifest in an inability to thereby severely decreasing their ability to learn how to
learn using contextual cues to inhibit inappropriate repet- controls urges in the same or similar situations. The
itive behaviours. A phenotypical feature of ASD is beha- awareness patients with OCD have of a less efficient cogni-
vioural inflexibility, especially in novel or unexpected tive control of motor responses in the short and long term
situations.29 Impairment of proactive control may also might play a major role in the emergence of anxiety,
reflect an intolerance to uncertainty to which patients depression, and maladaptive beliefs, such as beliefs about
with ASD respond with the execution of restrictive, threat overestimation, intolerance of uncertainty, and fear
repetitive behaviours.30 All these intriguing hypotheses of losing control over their behaviour.32 The severe dam-
need to be tested in further research. age to inhibitory control mechanisms might also explain
Another important piece of evidence about the complex- why OCD symptoms tend to persist in adulthood much
ity of the outcome of deficits in inhibitory control comes more than tic symptoms.33
from the study by van Hulst et al.,20 who showed a selec- All this evidence strongly suggests that the cognitive
tive deficit in reactive inhibition but an intact proactive mechanisms underlying impulse control are very heteroge-
control in children with ASD with comorbid ADHD and neous and that detailed measurement of inhibition may
ADHD only compared to typically developing children help to differentiate distinct disorders qualitatively. This
(Table 1). The discrepancy between these results and those evidence goes against the view suggesting that inhibitory
of Schmitt et al.22 can be explained by the fact that van impairments represent a transdiagnostic feature of neu-
Hulst et al.20 included patients with ASD showing marked rodevelopmental disorders with poor impulsivity control.34
ADHD symptoms. Thus, at least as far as inhibitory con- In other words, the findings of the current review make
trol deficits are concerned, ADHD symptomatology was implausible the notion that a common cognitive mecha-
likely to be prevalent. Selective impairment of reactive nism underlies inhibitory deficit across different disorders.
inhibition seems to be a hallmark of ADHD, as found by
Pani et al.31 using a standard key-press version of the stop- CONCLUSIONS
signal task. This feature is common to both inattention The evidence stemming from the studies reviewed is that
and hyperactivity ADHD subtypes.20,31 In addition, the correspondence between poor impulse control and a
patients with ADHD do not seem to suffer from low-level generic deficit in inhibitory control is untenable. This
automatic motor inhibition deficits.24 In principle, reactive review focused on the deficit in motor inhibitory control
inhibitory deficit may explain a number of ADHD pheno- because this is presumably the most affected domain for
type features, such as being unable to stick to tasks and people with poor impulse control. Motor inhibitory con-
constantly changing activity, being unable to wait for one’s trol is a multifaceted process with several subdomains (re-
turn, and performing actions impulsively. These beha- active, proactive, and automatic inhibition) that, when
vioural traits should not depend on stimulus affordances24 damaged, seem to produce unique disorder phenotypes.
but on environmental or internal cues that children with Thus, identifying specific inhibitory impairments in urge
ADHD cannot resist even though, given the intact proac- control disorders might be extremely important in defining
tive control, they should be aware of the inappropriateness the disorder and suggesting the most appropriate therapeu-
of their actions. In a sense, this pattern of inhibitory con- tic strategies. To conclude, the features of complex neu-
trol deficits could resemble that of primary motor stereo- rodevelopmental disorders, such as OCD and ADHD, are
typies, even though the simultaneous deficit in other unlikely to depend exclusively on the alteration of the inhi-
executive functions, mainly attention, makes the ADHD bitory function, but also on the way it interacts with the
phenotype much more complex and debilitating. other executive functions, that is, working memory and
The other two examples of syndromes characterized by selective attention. The interplay between these executive
poor urge control are Tourette syndrome and OCD. functions is what ultimately shapes the agent’s behaviour.

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:

REFERENCES
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DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY INVITED REVIEW

CONTROL INHIBITORIO Y RESPUESTAS IMPULSIVAS EN TRASTORNOS DEL NEURODESARROLLO


A menudo se asume que el deterioro del control inhibitorio es el de ficit central de varios trastornos del neurodesarrollo caracteri-
zados por un control deficiente de los impulsos. Sin embargo, ¿podrıa el mismo de ficit explicar diferentes fenotipos clınicos? La
evidencia de los estudios de comportamiento es muy variada. Esto se debe en parte a que la inhibicio  n es una funcio  n ejecutiva
muy compleja. Por lo tanto, es probable que los diferentes tipos de tareas que generalmente aprovechan el control inhibitorio pro-
porcionen diferentes resultados. Adema  s, la falta de homogeneidad de la muestra en te rminos de edad, comorbilidad y trata-
miento me dico son factores de confusio  n. Por tanto, para realizar una valoracio  n fiable del de  ficit de control inhibitorio en un
determinado trastorno, se debe emplear la misma tarea y muestras con caracterısticas similares. Este artıculo revisa y analiza estu-
dios sobre cinco trastornos del desarrollo neurolo  gico con alteracio n del control de los impulsos en los que se han utilizado estos
criterios: sındrome de Tourette; trastorno obsesivo compulsivo; deficit de atencio  n y trastorno de hiperactividad; estereotipias
motoras primarias; y trastorno del espectro autista. En general, sugieren que los mecanismos subyacentes a la incapacidad para
controlar los impulsos son extremadamente heteroge  neos y no pueden atribuirse a un deterioro general de la inhibicio  n. Estos
hallazgos no apoyan la hipo  tesis de que los de ficits inhibitorios representen una caracterıstica transdiagno  stica de los trastornos
del neurodesarrollo con control deficiente de los impulsos.


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.

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