MINI REVIEW

published: 12 August 2020

doi: 10.3389/fpsyg.2020.01991

Arousal and Executive Alterations in

Attention Deficit Hyperactivity
Disorder (ADHD)
Diana Martella
1*, Nerea Aldunate , 2Luis J. Fuentes and3 Noelia Sánchez-Pérez 4*
1
Facultad de Ciencias Sociales y Humanidades, Instituto de Estudios Sociales y Humanísticos, Universidad Autónoma
de Chile, Santiago, Chile, 2 Escuela de Psicología, Pontificia Universidad Católica de Chile, Santiago, Chile, 3 Departamento
de Psicología Básica y Metodología, Facultad de Psicología, Universidad de Murcia, Murcia, Spain, 4 Departamento
de Psicología y Sociología, Facultad de Ciencias Sociales y Humanas, Universidad de Zaragoza, Teruel, Spain

Attention deficit hyperactivity disorder (ADHD) is the most common neurobehavioral

disorder in childhood and can significantly affect a child’s personal and social
development and academic achievement. Taking into account the model of
Edited by: attentional networks proposed by Posner et al., the aim of the present study was to
Roumen Kirov,
review the literature regarding two main explicative models of ADHD, i.e., the
Institute of Neurobiology (BAS),
Bulgaria inhibition model and the cognitive-energetic model, by discussing behavioral and
Reviewed by: neurological evidence of both models and the limitations of each model. The review
Serge Brand,
University Psychiatric Clinics Basel,
highlights evidence that favors the energetic model and points to an unstable arousal
Switzerland as a potential pathogenetic factor in ADHD.
Alexander Prehn-Kristensen,
Center for Integrative Psychiatry (ZIP), Keywords: attention deficit hyperactivity disorder, arousal, executive functions, inhibition, cognitive-energetic
Germany model
*Correspondence:
Diana Martella
[email protected]
Noelia Sánchez-Pérez
INTRODUCTION
[email protected] Attention deficit hyperactivity disorder (ADHD) is one of the most prevalent psychiatric disorders
(Polanczyk et al., 2014). ADHD is mainly characterized by varying degrees of inattention,
hyperactivity, and impulsivity (American Psychiatric Association, 2013) as critical features of the
Specialty section: disorder, which are usually accompanied by other concomitant deficits, such as lower
This article was submitted to emotional/motivational management, impaired fine motor coordination, low management of time,
Psychopathology, more frequent disruptive behavior, unstable sleep habits, academic achievement lower than their
a section of the journal possible intellectual abilities, and impaired quality of life (Fenollar-Cortés and Fuentes, 2016). These
Frontiers in Psychology
symptoms appear at early stages of children’s development before the age of 12 (American
Received: 05 March 2020 Psychiatric Association, 2013) and may change over time (American Psychiatric Association, 2013),
Accepted: 17 July 2020
such as decrease in hyperactivity–impulsivity symptoms with age (Döpfner et al., 2015). However,
Published: 12 August 2020
the disorder has been found to be relatively stable and persistent from childhood to adulthood
Citation:
(Barkley, 2000), and it can become a chronic condition that requires social and financial support
Martella D, Aldunate N,
Fuentes LJ and Sánchez-Pérez N
(Pelham et al., 2020). Many studies have consistently reported the negative impact of ADHD
(2020) Arousal and Executive symptoms on children’s academic achievement and socioemotional development. For instance,
Alterations in Attention Deficit children with ADHD exhibit impairments in acquiring mathematical and language skills compared to
Hyperactivity Disorder (ADHD). their peers with typical development (Kim and Kaiser, 2000; Bruce et al., 2006; McConaughy et al.,
Front. Psychol. 11:1991. 2011), problems in their interpersonal relationships with both teachers and
doi: 10.3389/fpsyg.2020.01991

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Martella et al. Arousal and Executive Models of ADHD

peers (Becker et al., 2006; Coghill et al., 2006; Nijmeijer et al., particular theoretical approach may help with the diagnosis and
2008), and difficulties in social cognition (Uekermann et al., therapeutic strategies to tackle some core deficits related to the
2010). Additionally, children with ADHD are more likely to report disease. In doing so, here we adopt the cognitive neuroscience
depression and anxiety symptoms (Meinzer et al., 2014; Sciberras approach as a theoretical umbrella to examine two more standard
et al., 2014). models that come from a clinical neuropsychological tradition: one
Although the first case description of ADHD was reported in 1902 model emphasizes executive function deficits in ADHD that are
(Still, 1902), the etiology, diagnosis, and treatment of ADHD are mainly related to a failure in inhibition, and the other model
still unclear. Concerning diagnosis, the symptoms of ADHD lack emphasizes a deficit of energetic factors among ADHD patients,
significant specificity, making it difficult to detect the disease at leading to both inattention and hyperactivity symptoms.
an early stage, and the diagnosis is still mainly based on
observation and informant reports (Drechsler et al., 2020). A lack
of specificity in the diagnosis increases the possibility that THEORETICAL MODELS OF ATTENTION
patients may not be correctly diagnosed (Levelink et al., 2020). In DEFICIT HYPERACTIVITY DISORDER
addition, manifestations of ADHD seem to be very heterogeneous,
and it is difficult to understand both the neurological and cognitive As mentioned previously, there are several theories to explain the
mechanisms underlying ADHD- related deficits (Drechsler et al., ADHD symptoms, but so far, two models have been dominant in
2020; Sutcubasi et al., 2020). In a recent systematic review, ADHD research: (1) the inhibition model (Barkley, 1997), which
Bellato et al. (2020) suggest a possible link between a suggests that the core deficit in individuals with ADHD is poor
dysregulation of arousal (related to the autonomic nervous behavioral inhibition associated with the executive network of the
system) and a deficit in attentional and executive functions as the attention system and (2) the cognitive-energetic model (CEM;
core problem associated with ADHD. In this line, the attentional Sergeant, 2000), which proposes that the core problem in ADHD
network model proposed by Posner et al. (2019) can be deemed symptoms is a deficit in the energetic maintenance related to the
as an appropriate theoretical framework to account for ADHD alerting network. In this article, we aim to review some relevant
dysfunctions (Berger and Posner, 2000; Posner et al., 2019). From evidence related to the two aforementioned ADHD models, and
a cognitive neuroscience approach, the model proposes that we use the Posner’s cognitive neuroscience framework of
attention is an organic system that comprises a variety of neural attention to discuss empirical support for and the limitations of
processes (Posner and Petersen, 1990; Fan et al., 2005). each model. A summary of evidence favoring each model is
According to Posner and Petersen (1990), three specialized presented in Supplementary Table 1.
attentional neural networks are strictly linked with the activity of The Inhibition Model of Attention Deficit
specific neuromodulator systems subtending three different
Hyperactivity Disorder
attentional functions: (1) alerting – defined as achieving (phasic
alerting) and maintaining (tonic alerting or vigilance) a general
state of activation (or arousal) of the cognitive system, (2) Barkley’s model (Barkley, 1997) proposes that the central deficit
orienting – defined as selectively allocating the attentional focus in ADHD is poor response inhibition, which involves three
to potentially relevant locations/objects in the visual field, and (3) interrelated processes: (1) to inhibit the initial prepotent response
executive control – defined as the ability to control our own to an event; (2) to stop an ongoing response, allowing a delay in
behavior to achieve intended goals, resolve conflict among the decision to reply; and (3) to control interference from
alternative responses, and inhibit impulsive responses. distracting information (to preserve a period of delay from
distracting stimuli). The dysfunction in inhibition would lead to
The alerting network has been associated with the right frontal consequences on the efficient performance of the
and parietal lobe, and the locus coeruleus, which provides the neuropsychological abilities named executive functions (EFs) [e.g.,
system with norepinephrine (NE) (Cohen et al., 1987; Berger and non-verbal working memory (WM), self-regulation of affect,
Posner, 2000; Sturm and Willmes, 2001). The orienting network motivation, arousal, internalization speech or verbal WM, and
is thought to be mediated by a lateralized network located in reconstitution], which in turn might affect motor control. Although
the right superior parietal cortex and in the right inferior frontal
the definition of EF varies, most of the abilities included by Barkley
gyrus (Corbetta and Shulman, 2002), and it is modulated by the have been conceptualized as part of the executive attentional
cholinergic system (Berger and Posner, 2000; Thiel et al., 2004). network (Berger and Posner, 2000). Following this approach, if
Finally, the executive network is associated with the anterior behavioral inhibition is the core deficit in ADHD, we would expect
cingulate cortex, the basal ganglia, and the lateral prefrontal children with ADHD to perform poorly on inhibition and EF tasks
cortex (Berger and Posner, 2000), and this network is modulated compared to typically developed peers; we would also expect
by the neurotransmitter dopamine (DA). Although deficits in the abnormalities in the structure and function of brain areas involved
executive network have been associated with ADHD symptoms, in the executive attentional network, i.e., the anterior cingulate
there is also empirical evidence of ADHD patients having cortex and the prefrontal cortex modulated by DA.
difficulties in controlling their level of arousal depending on the Behavioral Evidence
alerting network (Sergeant, 2005; Bellato et al., 2020). Given the
relevance of the attentional networks functioning to characterize
attention-dependent deficits in ADHD, in this review, we want to According to Barkley’s (1997) model, previous behavioral studies
go further and present recent evidence that highlights how this have shown that children with ADHD symptoms show some

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Martella et al. Arousal and Executive Models of ADHD

deficits in inhibition (Berlin et al., 2004; Geurts et al., 2005; Wodka (Ellison-Wright
et al., 2007; Schoemaker
et al., 2008;
et al.,Nakao
2012; see et al.,
also 2011;
the following
Frodl and
meta-analyses: Oosterlaan et al., 1998; Willcutt et al., 2005; Wright Skokauskas,
et al., 2014),
2012),
verbal
although
WM (Berlin
the effect
et al.,was
2004;
attenuated
Brocki etover
al., time
2008; Kasper et al., 2012; Martinussen et al., 2005), non-verbal WMand (Berlin
wasetnoal.,
longer
2004;detectable
Westerberg inetadulthood
al., 2004;(Nakao
Martinussen
et al.,et2011;
al., 2005; Re et al., 2010; Sowerby et al., 2011; Kasper et al., 2012), Frodl
self-regulation
and Skokauskas,
(Braaten2012).
and Rosén,
Furthermore,
2000; Berlin
someetmeta-
al., 2004;
analyses
Crundwell, 2005), and reconstitution (Berlin et al., 2004; Harrier have and DeOrnellas,
shown hypoactivation
2005). These
in frontostriatal
findings might regions
indicate
(rightthat
inferior
behavioral inhibition is the dysfunction underlying the ADHD symptoms. frontalHowever,
cortex,notstriatum,
all the evidence
and supplemental
has been consistent.
motor For cortex)
instance, there are also studies that have failed to find significant differences
(Hartetal.,2013)andfrontoparietalareas(dorsolateral
in non-verbal WM (Berlin et al., 2004; Geurts prefrontal,
et al.,
2005; Brocki et al., 2008; Schoemaker et al., 2012), verbal WM (Sowerby anterior etcingulate,
al., 2011;
andPineau
inferior
et parietal
al., 2019),cortices)
self-regulation
in children of with
arousal (Stevens et al., 2002), and reconstitution (Geurts et al., 2005)ADHDbetween compared
ADHD children to and controls.
controls In those during
cases, the
researchers have stressed the importance of taking into account the performanceofinhibitiontasks(Corteseetal.,2012).According
ADHD subtype (individuals with the prevalent inattentive to
subtype might exhibit impairments in processing speed and focused this attention
view, rather
an ample
thanmedical
behavioral
treatment
inhibition used
andwith individuals with
working memory deficits; Barkley, 1997) and the developmental ADHD involves Thestimulant
Cognitive-Energetic
drugs targetedModel of
to counteract a
changes in EF (younger ADHD children, but not older children, Attention
hypodopaminergic state (Arnsten,Deficit 2006).Hyperactivity
Interestingly, the
serendipitous discovery that amphetamines make children calmer
Disorder and more focused (Glaser and Gerhardt, 2012) has strongly
supported the hypodopaminergic ADHD hypothesis. In addition,
whereas the prevalence of DA in the nucleus accumbens may
explain the ADHD alterations in reward sensitivity, the low levels
of DA in the striatum may justify ADHD hyperactivity, and the
presence of DA in the frontal cortex may support the decreased
inhibitory control in ADHD (BerridgeandDevilbiss,2011).

were found to have deficits in verbal WM) to explain the The CEM focuses on energetic factors as the most critical
inconsistentresults. explanationofADHD,proposingthatthedeficitofthesefactors
In addition to the incongruent results in EF, there are also leads to both inattention and hyperactivity symptoms. This
studies that have failed to find significant group differences in model claims that the overall efficiency of information processing
inhibition (Westerberg et al., 2004; Shaw et al., 2005; Brocki et al., is determined by the interplay among three mechanisms at
2008; Bioulac et al., 2014), which is especially critical because this different levels, with top-down and bottom-up streams among
mechanism has been proposed by Barkley to be the core failure them (Sergeant, 2000). The lower level includes four general
in ADHD. To account for failures to find inhibition deficits in stages of computational mechanisms of attention: encoding,
ADHD, some authors have examined the reliability of certain search, decision, and motor organization. The middle level
inhibition tasks, as some measures have been deemed insensitive comprises the energetic pools: arousal, effort, and activation.
to assess interference control in individuals with ADHD (Brocki The arousal pool is defined as a phasic response that is time-
et al., 2008). In contrast, other researchers have claimed that the locked to stimulus processing and is typically influenced by
reason for the non-significant results might be the underaroused signal intensity and novelty, and it is behaviorally indexed by
state of individuals with ADHD. Similarly, Shaw et al. (2005) sleep–wake patterns. The effort pool is characterized by the
argued that the non-significant differences in inhibition skills energy necessary to meet with task demands, is located within
between individuals with ADHD and controls, measured by the hippocampus, and seems to function by both exciting and
computerized tasks, might be due to the greater motivation, inhibiting the other two energetic pools (arousal and activation).
effort, and arousal evoked by computer games than the effort The activation pool is defined as the tonic physiological readiness
induced by traditional laboratory-based tasks. Consequently, the to respond. Finally, the upper level refers to the executive control
primary deficit might not be based on response inhibition but on system and is associated with planning, response inhibition, error
the difficulty experienced by individuals with ADHD in reaching detection and correction responses, WM, and flexibility, among
anoptimallevelofactivation. otherabilities.
Neurological Evidence Behavioral Evidence

Regarding neurological evidence, we would expect individuals Following this approach, impairments observed in individuals with
with ADHD to show abnormalities in the structure and function of ADHD are expected at the three levels of the CEM. For instance,
brain areas involved in the executive attentional network (anterior motor difficulties have been reported in children with ADHD
cingulate, prefrontal cortex, and basal ganglia) as well as in the (Goulardins et al., 2013; Kaiser et al., 2015; Rosa Neto et al.,
dopaminergic system compared to typically developed peers. In a 2015; Fenollar-Cortés and Fuentes, 2016; Fenollar- Cortés et al.,
recent review published by Gallo and Posner (2016), the authors 2017), which might reflect dysfunction at the lower level.
describe the volumetric reduction found in the basal ganglia in Moreover, children with ADHD generally exhibit a dysfunction in
individuals with ADHD compared to controls their response inhibition (upper level), as we

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Martella et al. Arousal and Executive Models of ADHD

mentioned previously. However, this dysfunction is not specific to The alerting system proposed by Posner and Petersen (1990) has
ADHD, as this deficit is also common to other disorders, such as been related to the noradrenergic system and may modulate
conduct disorder and autism spectrum disorders (Oosterlaan et attention and arousal. Many studies have shown different
al., 1998; Geurts et al., 2014). In fact, evidence suggests that neurotransmitters implied in ADHD, with NE being the most
inhibition deficits associated with ADHD may, at least in part, be important neurotransmitter, and increasing evidence has shown
due to energetic dysfunction (Sergeant et al., 1999). Although less NE in ADHD patients than in controls (i.e., Biederman and
there are few specific tests to directly measure the energetic pool, Spencer, 1999). Since ADHD symptoms involve both attentional
some studies show that the event rate, that is, the speed with and arousal deficits, it is plausible that dysregulation of the NE
which stimuli are presented, affects the energetic state, and that system may be involved in the pathophysiology of ADHD
the event rate is an important determinant of performance (Biederman and Spencer, 1999; Park et al., 2012). Furthermore,
(Sergeant, 2005). A slow event rate would induce a rather the atomoxetine, a drug effectively used for ADHD treatment, acts
underarousal/underactivation state, with slow and inaccurate as an inhibitor highly selective of noradrenergic reuptake (Arnsten,
responses, whereas a fast event rate would lead to a rather 2006), which strongly supports a relationship between NE and
overarousal/overactivation state, resulting in fast and inaccurate ADHD. Finally, the depletion of NE results in increased
responses. In fact, some behavioral studies indicate that distractibility and motor hyperactivity, both typically ADHD
individuals with ADHD perform more poorly in tasks involving slow symptoms. In contrast, stimulation of the NE system is associated
event rates, with a significant slowing in reaction times (Meere et with a decrease in distractibility and an improvement of cognitive
al., 1992; Wiersema et al., 2005, 2006; for a review, see Metin et functions (Sengupta et al., 2012).
al., 2012), although the results are not consistent (e.g.,
Raymaekers et al., 2007).
Neurological Evidence
The conception of ADHD as a result of a hypoaroused brain state CONCLUSION
has been supported by electrophysiological studies. Previous
electroencephalographic (EEG) studies among children with ADHD The exact etiopathogenesis of ADHD is still unclear. In this review,
have reported an increase in low-frequency power (predominantly we discuss the behavioral and neurological previsions and
in the theta band) and a decrease in high- frequency power (alpha evidence of two well-known models: the inhibition model,
and beta bands) (Kuperman et al., 1996; Clarke et al., 2001, 2002; proposed by Barkley (1997), and the cognitive-energetic model,
Markovska-Simoska and Pop- Jordanova, 2017; Clarke et al., introduced by Sergeant (2000). On the one hand, the hypothesis
2019). Specifically, the theta band has been related to low of a dysfunction of the DA system and the related Barkley’s model
activation, such as in drowsiness states and relaxed wakefulness do not seem to explain all the characteristic symptoms of ADHD.
(Scher, 2017; Mari-Acevedo et al., 2019), whereas alpha and beta Inconsistent results (e.g., Brocki et al., 2008; Bioulac et al., 2014;
bands have been associated with goal- directed activities, Pineau et al., 2019) highlight the relevance of considering other
sustained attention, and higher task-related attention (Laufs et al., factors, such as the ADHD subtype, as well as the maturation of
2006; Dockree et al., 2007). A greater ratio of the theta power executive functions throughout life. On the other hand, many
band to the beta band (increased theta/beta ratio index) may results (e.g., Metin et al., 2012; Clarke et al., 2019; Bellato et al.,
reflect a reduced cortical control function, resulting in 2020) seem to support the hypothesis of dysfunction of the locus
motivational imbalances (Schutter and Van Honk, 2005). coeruleus-norepinephrine (LC-NE) system and therefore to
Moreover, this index has been found to be strongly associated sustain the hypoarousal and the RH hypothesis in addition to
with ADHD symptoms (Barry et al., 2003; Jarrett et al., 2017; Sergeant’s energetic model. In line with this, it has recently been
Markovska-Simoska and Pop-Jordanova, 2017). In addition, proposed that the core problem in ADHD is an unstable arousal
evidence suggests that this difference in theta/beta ratio (Hegerl and Hensch, 2014), and numerous findings seem to
decreases across years (Arns et al., 2013; Markovska- Simoska support this hypothesis (e.g., Strauß et al., 2018; Bellato et al.,
and Pop-Jordanova, 2017). This hypoaroused cortical state has 2020). From this point of view, hyperactivity and sensation
been mainly localized in the frontal and posterior areas (Clarke et seeking are considered an organism’s regulatory response to an
al., 2002), the same brain regions that have been identified as the unstable level of cortical arousal. The model provides an
neuroanatomical substrates of the attentional network (Posner, explanation for the attentional deficits, especially related to
2012). Since the right hemisphere (RH) plays a crucial role in sustained attention and vigilance, and for the ADHD subtypes
maintaining and controlling both arousal and the intensity aspects (Hegerl and Hensch, 2014). Furthermore, sleep problems and
of attention (Sturm and Willmes, 2001), if the pathophysiology of circadian alterations are very common in ADHD patients, and
ADHD was a deficit in the arousal system, we would expect people many studies (e.g., Yoon et al., 2012; Bioulac et al., 2020) have
with ADHD to show RH dysfunction. In fact, several studies have indicated that all factors inducing sleep deficits and dysregulation
highlighted an impairment in both anterior and posterior RH areas of arousal can impair ADHD symptoms. Finally, drug stimulants
related to the attentional system in ADHD (Stefanatos and are known to reduce slow wave activity, attention deficits, and
Wasserstein, 2006). These dysfunctions are further supported by hyperactivity through the regularization of the arousal level. All of
both behavioral and neuroimaging data (van Ewijk et al., 2012). this evidence points to the dysregulation of arousal as a biomarker
of ADHD, a relevant factor that should be considered in diagnostic
processes and intervention programs.

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Martella et al. Arousal and Executive Models of ADHD

AUTHOR CONTRIBUTIONS of Chile, project PSI2017-84556-P granted by the Spanish

NA and DM conceived this manuscript. NA and DM reviewed the Ministry of Science, Innovation and Universities (FEDER funds),
literature. NS-P and DM wrote the first draft of the manuscript. and project 21172/IV/19 granted by Fundacion Seneca-Agencia
DM, NA, and LF edited and provided intellectual input to the de Ciencia y Tecnología de la Región de Murcia (Spain).
manuscript. All authors approved the final version of the
manuscript for submission.

SUPPLEMENTARY MATERIAL
FUNDING The Supplementary Material for this article can be found online at:
This work was supported by FONDECYT 1181472 of the National https://www.frontiersin.org/articles/10.3389/fpsyg.
Commission for Scientific and Technological Research 2020.01991/full#supplementary- material

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Still, G. (1902). Some abnormal psychical conditions in children: the goulstonian absence of any commercial or financial relationships that could be construed as a
lectures. Lancet 10, 126–136. doi: 10.1177/1087054706288114 potential conflict of interest.
Strauß, M., Ulke, C., Paucke, M., Huang, J., Mauche, N., Sander, C., et al. (2018).
Brain arousal regulation in adults with attention-deficit/hiperactivity disorder Copyright © 2020 Martella, Aldunate, Fuentes and Sánchez-Pérez. This is an open-
(ADHD). Psychiatry Res. 261, 102–108. doi: 10.1016/j.psychres.2017. 12.043 access article distributed under the terms of the Creative Commons Attribution
License (CC BY). The use, distribution or reproduction in other forums is permitted,
Sturm, W., and Willmes, K. (2001). On the functional neuroanatomy of intrinsic provided the original author(s) and the copyright owner(s) are credited and that the
and phasic alertness. Neuroimage 14, S76–S84. original publication in this journal is cited, in accordance with accepted academic
Sutcubasi, B., Metin, B., Kurban, M. K., Metin, Z. E., Beser, B., and practice. No use, distribution or reproduction is permitted which does not comply
Sonuga-Barke, E. (2020). Resting-state network dysconnectivity in ADHD: a with these terms.

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