Current Psychiatry Reports (2019) 21:17

https://doi.org/10.1007/s11920-019-1003-6

ATTENTION-DEFICIT DISORDER (A ROSTAIN, SECTION EDITOR)

Attention-Deficit/Hyperactivity Disorder (ADHD)

and Emotion Regulation Over the Life Span
Hanna Christiansen 1 & Oliver Hirsch 2 & Björn Albrecht 3 & Mira-Lynn Chavanon 1

# Springer Science+Business Media, LLC, part of Springer Nature 2019

Abstract
Purpose of Review Emotional symptoms are common and persistent in youth and adults with attention-deficit/hyperactivity
disorder (ADHD) and cause clinically significant impairments. We review recent neuropsychological, neurophysiological, and
peripheral psychophysiological evidence for emotion and emotion regulation deficits in ADHD across youth and adults.
Recent Findings Central and autonomous nervous system correlates argue in favor of more general self-regulation deficits and
also specific emotional deficits in ADHD. These include general performance deficits in executive functions, and structural as
well as functional impairments in neuronal networks associated with top-down self-regulation. Specific deficits with bottom-up
emotional activation in the amygdala and emotion evaluation associated with the orbitofrontal cortex have also been described.
Furthermore, vagally mediated, high-frequency heart rate variability is associated with emotional self-regulation deficits through-
out the life span. The current evidence is based on multilevel studies that assess associations of emotion regulation. However,
further studies that adequately consider the processual recursive character of emotion generation and regulation may give
important new insights into emotional regulation of ADHD.
Summary Emotion regulation deficits in ADHD are associated with specific as well as general self-regulation deficits traceable
on the level of neuropsychological, neurophysiological, and psychophysiological assessments. The temporal dynamics of the
interplay of those different systems need further study in order to optimize and personalize treatment of emotion regulation
difficulties, including emotional reactivity, in patients with ADHD.

Keywords Attention-deficit/hyperactivity disorder (ADHD) . Emotion regulation . Children . Adults . Neuropsychology .

Neurophysiology (fMRI EEG) . Peripheral psychophysiology (heart rate variability)

Introduction cross-situational (i.e., at home as well as at school or work).

Originally conceptualized as a disorder of childhood, longitu-
Attention-deficit/hyperactivity disorder (ADHD) has an onset dinal studies demonstrate persistence rates of the disorder of
in childhood (before the age of 7 according to ICD-10 [1] and about 20–80% [3]. According to prevalence studies, about 5%
before the age of 12 years according to DSM-5 [2]) with of youths [4, 5] and 2.5% of adults are affected [6], making
impairing and age-inadequate levels of the three core symp- ADHD one of the most prevalent disorders in childhood and
toms (inattention, hyperactivity, and impulsivity) that present adolescence and a still very prevalent disorder during adult-
hood [7, 8].
This article is part of the Topical Collection on Attention-Deficit Disorder As the core symptoms do not sufficiently explain either the
severity of the disorder nor functional impairments over the
* Hanna Christiansen life span [9–11], emotion regulation deficits (ERDs) have
christih@staff.uni-marburg.de been considered a translational factor relevant for ADHD
[12–14, 15••], as ERDs are often observed in patients [9,
1
Department of Psychology, Clinical Child and Adolescent 16–18, 19•, 20••, 21••], and are associated with significant
Psychology, Philipps-University Marburg, Gutenbergstr. 18, functional impairments [22–24]. With high affect lability
35037 Marburg, Germany and emotional reactivity as well as reduced affect control,
2
FOM University of Applied Sciences, Siegen, Germany the ERD concept is already present in the Wender Utah criteria
3
Department of Child and Adolescent Psychiatry, University Medical of adult ADHD [25], even though those are not explicitly
Center Göttingen, Göttingen, Germany considered in DSM-5 or ICD-10. A major inconsistency in
 17 Page 2 of 11 Curr Psychiatry Rep (2019) 21:17

the literature on emotion regulation (ER) is the large variety of expressive suppression; see Fig. 1). The strategies also differ
terms used to describe those deficits in patients with ADHD in their effectiveness to modify emotional outcomes as indexed
(for instance, “emotional dysregulation” [25], “emotional im- by experiential, behavioral, and physiological measures [33].
pulsiveness” [26], and “emotional lability” [27]). Despite the For example, active thinking about a positive event that is un-
expansion of empirical work in the field of emotion and ER, related to the evocative situation is an effective distraction strat-
the field still lacks a consensual definition that describes ER egy across all response levels. Cognitive change strategies such
with clarity, precision, and differentiation among constructs. as perspective taking are effective in modifying experiential
To address this, we first give a short overview about emotions and behavioral outcomes, and response modulation may
and their regulation and then review recent evidence of the change behavior in the intended direction, while physiological
association between ER, ADHD, and associated neuropsy- states are not necessarily related to such strategies.
chological and physiological characteristics that may be com- However, temporal dynamics have been spotlighted in re-
promised in ADHD. cent theoretical debates. According to the extended model of
emotion regulation by Gross [31••] (see Fig. 1 for details),
more dynamic processes or regulatory stages have been intro-
Emotions and ER duced. To gain control of emotions, we enter a cyclical process
whereby we identify the emotion needing to be regulated
Emotions are temporally limited, qualitative states that are as- (identification), select (selection), and then execute an ER
sociated with changes of feelings, expression, and physiology strategy (implementation). Finally, we monitor the regulatory
[28]. They differ from stress responses and mood in several effects so as to decide whether regulation was sufficient or not
ways, but the most prominent difference is that emotions are (stopping or maintaining regulatory engagement) or whether
elicited by specific internal or external activating events. we should switch to another strategy (monitoring). For more
Emotions require that we direct our attention (consciously or details, see Sheppes et al. [34].
preconsciously) to this activating event, and that we value or
appraise it with regard to our goals. Finally, emotions promote
relevant action urges (approach vs. withdrawal), physiological ADHD and ER
activation (central and peripheral), and expressive behaviors
[29]. Thus, emotions unfold over time and are helpful when Elevated ERD is a rather consistent observation in ADHD
they appropriately guide sensory processing, enhance decision across the life span. A recent meta-analysis (k = 77) reported
making, or provide information regarding the best course of that ADHD is strongly associated with both emotion reactivity
action. Emotions are potentially harmful when they are of in- (d = .95) and ERD (d = .80) [20••]. Prevalence studies on chil-
appropriate intensity, duration, frequency, or type for a partic- dren, adolescents, and adults with ADHD show that a consid-
ular situation [29]. The fact that emotions unfold over time also erable portion of them present with elevated ERD. For the
implies that each emotion is characterized by dynamic features, youngest group of patients, a population-based study by
such as latency of onset, rise gradient, maximal intensity of the Overgaard and colleagues [35] reported that about 25% of
response, duration or persistence of an emotion, and slope of preschoolers with ADHD show signs of emotional dysregula-
recovery. Across response levels, those temporal features may tion, significantly more frequent than in control children. In a
differ, and they may also differ among emotions [30•]. large community-based population sample, parents reported
When seeking a definition of emotion regulation, it is more emotional lability for 6% of the children overall, whereas chil-
or less consensual that ER refers to all efforts to influence the dren with ADHD were found to have greater than a 12-fold
emotions we have, when we have them, and how we experi- increase in the odds ratio observed [36]. Other studies on
ence and express them [29]. As emotions have a strong tem- youth with ADHD and ER report rates ranging from 21%
poral dimension, regulatory dynamic processes—no matter [37] to 66% [38], with roughly similar rates observed for
whether automatic or voluntarily used [31••]—interact to in- adults with ADHD [17, 24].
fluence our emotional states flexibly so as to promote adap- Given that ERDs are present in a variety of mental disor-
tive, goal-oriented behaviors [32]. ders, from both the externalizing and internalizing spectrum
ER strategies vary greatly (e.g., putting on a poker face, [36], it is important to note that ERD in ADHD is not simply
applying mediative breathing, taking a shower, trying to think explained by comorbidity [17, 18, 24]. It is also observed in
differently about a situation), and they are traditionally classi- non-comorbid ADHD cases [10, 19•]. A longitudinal study by
fied into those that occur prior to the emotional response (ante- Biederman and colleagues [39] found that ER problems are
cedent-focused regulation; e.g., situation selection, situation highly persistent within individuals. In their sample, 57% of
modification, attentional deployment, and cognitive change) youth with childhood ERD still had ERD 4 years later. ERDs
and regulation strategies that occur after the emotional response in childhood were also positively related to the persistence of
is already triggered (response-focused regulation; e.g., ADHD symptoms 4 years later. About 50% of youth with
Curr Psychiatry Rep (2019) 21:17 Page 3 of 11 17

Fig. 1 Modified ER model based on Gross [31••]

persistent ADHD had ERD compared to none in the group of flexibility, and (iv) action planning [24]. Model 2 perceives
the non-persisters. This finding is corroborated by a recent ADHD with ERD as qualitatively different from pure ADHD.
longitudinal study showing an association of childhood ERD A basis for this model is genetic studies that demonstrate the co-
with the high persistent pattern of ADHD, but not with the occurrence of ADHD and ERD in families [16, 18]. This model
ameliorating symptom trajectory [40]. Another recent pro- thus implies a distinct etiological entity as well as a distinct
spective longitudinal study, in which a sample of 5-year-old course of ADHD + ERD. Model 3 postulates ADHD and
children was followed up to age 13 [41•], found that poor ER ERD as correlated, with overlapping circuits, but distinct
and particularly poor positive ER were predictive of an in- neurocognitive deficits. Proof comes from studies with moder-
crease in inattention symptoms, whereas good ER predicted ate correlations between ADHD symptoms and ERD [43].
a decrease of inattention symptoms across time [41•].
In sum, those findings underscore the importance of ERD in
the diagnosis and treatment of ADHD. A recent comprehensive Neurocognitive Correlates of ER in ADHD
review concludes that emotional symptoms of ADHD are not
simply epiphenomena of comorbidity, as they are common and ERD in ADHD is often hypothesized to result from the same
persistent in youth and adults with ADHD, are present in non- or at least overlapping neurocognitive deficits in inhibition,
comorbid cases, and are sufficiently specific for ADHD to func- working memory, and executive functions as core symptoms
tion as diagnostic criteria [21••]. Nevertheless, the definition of do (see models 1 and 3 of Shaw et al. [43]).
the constructs presently used under the umbrella term of ER
needs more precision, as does the association of the nature and Children and Adolescents
pathophysiological mechanisms of the ER-ADHD association.
With respect to the latter, Shaw et al. [15••] suggest three models In a seminal study by Walcott and Landau [44], boys aged
to explain the overlap between ADHD and ER. According to 6 years to 11 years who participated in a frustrating peer com-
model 1, ERDs are a core symptom of ADHD due to joint petition, inhibitory control in a stop-signal task were predicted
neurocognitive deficits in self-regulation that underlie cognitive to have successful ER. Another large study of 424 children
and ER systems [42]. This joint deficit could be a common with ADHD (6–18 years of age) and their 564 healthy siblings
consequence of (i) the regulation of physiological arousal, (ii) assessed ER using aggregated parent and teacher ratings along
inhibition deficits, (iii) attention regulation and cognitive neuropsychological functioning tests of inhibition, working
 17 Page 4 of 11 Curr Psychiatry Rep (2019) 21:17

memory, and delay aversion [45]. Results suggest that a range individuals newly diagnosed with adult ADHD who were all
of neuropsychological variables predicted ERD, but this asso- medication-naive. A seven-factor confirmatory model was
ciation was completely mediated by severity of ADHD symp- supported by our data leading to the conclusion that deficits
toms. Conversely, the association of ADHD symptom severity in ER are an integral part of adult ADHD. Our study contrib-
with neuropsychological variables was not mediated by ERD. utes to a deeper understanding of the impairments related to
This finding is supported by another study of ADHD children adult ADHD and can be used for further differentiation of
demonstrating that emotional cues did not impair interference subgroups within this population. This was examined in more
control in an inhibition task [46], (but see, e.g., [47] for di- detail in a follow-up study applying a cluster analytic ap-
verging results). proach to subtype patients on the relative presence or absence
A neuroimaging study demonstrated a double dissociation of ERD [53]. We found two clusters, with cluster 2 in contrast
between two neural circuits engaged in executive attention to cluster 1 showing high deficits in ER that were associated
and control vs. ER [48]. Medication-naïve children with with higher impairments in most clinical areas: ADHD core
ADHD (n = 22) showed reduced connectivity in the executive symptoms, depression, additional clinical symptoms, and
attention circuit (major seed dorsolateral prefrontal cortex symptoms of personality disorders. Women were overrepre-
(PFC); connectivity with caudate, anterior cingulate) com- sented in this cluster. There were also higher rates of comor-
pared to controls (n = 20). This deviation was correlated with bidity in this cluster, such as somatoform disorders that were
executive attention deficits, but not with emotional lability. By associated with deficits in ER. Of note, the presence of comor-
contrast, reduced connectivity in the ER circuit (major hub bidity did not significantly account for ERD in this sample.
ventral striatum, connectivity among others with the Neuropsychological variables like the Quantified Behavior
orbitofrontal cortex (OFC) and amygdala) correlated with Test Plus (Ob+) [54] also did not contribute significantly to
emotional lability, but not with executive attention deficits. cluster formation.
As those studies rely on self-reports and parent/observer
Adults reports and their associations with other variables, we now
review experimental tasks using central and autonomous ner-
One of the first studies on ADHD and ER in adults compared vous system activity to follow up emotion and ER processes.
male and female patients (n = 39) with gender- and IQ-
matched control subjects (n = 40) on an emotional working
memory task [49]. Compared to control subjects, patients with Neurophysiology and ER in ADHD
ADHD showed both a general working memory deficit and
enhanced distractibility (lower performance accuracy). A brief review of underlying brain activity may be useful to
Controls showed impaired working memory performance differentiate emotion generation (bottom-up processes arising
for highly arousing negative background pictures, while pa- from related brain areas as amygdala, ventral striatum, and
tients with ADHD demonstrated decreased attention and a somatosensory areas) from emotion regulation (top-down pro-
comparable decrement with low arousing pictures [49]. A cesses associated with neuronal activity in executive neural
large study on 325 adults with and without ADHD and with networks including the central role of the prefrontal cortex).
and without ER deficits revealed no differences in executive
functions for the two groups with ADHD (that is ADHD + ER Bottom-Up Emotion Generation
and ADHD only). Compared to adults without ADHD, both
groups with ADHD demonstrated lower scores across several Two different paradigms in neuroscience are regularly used to
measures of executive function, suggesting that deficits in ER study emotion generation: (1) functional MRI that confronts
are independent of neuropsychological impairments [50]. patients with affectively charged stimuli and (2) associations
In two studies by our group, we were able to demonstrate of structural MRI or resting state connectivity with trait mea-
that ERDs are a core component in adult ADHD and that sures of emotional reactivity. A representative example of the
neuropsychological measures do not contribute significantly former is the work by Posner et al. [55]. They assessed emo-
to subgroup formation in adults with ADHD and ERD. In our tional reactivity to subliminally presented fearful faces and
first study, apart from ADHD symptoms assessed with the detected abnormally high activity in the amygdala and stron-
Conners Adult ADHD Rating Scales (CAARS) [51], we sep- ger connectivity in the lateral prefrontal cortex in children with
arately assessed negative and positive affective states and ER ADHD. Both these responses were attenuated with stimulant
skills in adults with ADHD to test a model that distinguished medication. Yu et al. [56] detected elevated emotional lability
positive and negative affect, problems with self-concept, and based on Conners’ parent ratings in medication-naïve boys
ER skills as factors that were distinct, but most likely corre- with ADHD as well as an association with reduced resting
lated with the symptom domains of inattention, hyperactivity, state functional connectivity among the bilateral superficial
and impulsivity [52•]. Our sample consisted of 213 amygdala, the dorsolateral prefrontal, and the inferior parietal
Curr Psychiatry Rep (2019) 21:17 Page 5 of 11 17

areas. Superficial amygdala regions are connected to the OFC Interestingly, there is some evidence that performance in
areas associated with emotional outcome evaluation. These cognitive tasks and associated brain activity impairments may
detected circuits may form the core of an emotion network be ameliorated by either immediate rewards or ADHD medi-
that is dysregulated in ADHD. The amygdala may also mod- cation [69–71]. Thus, it seems plausible to assume that even
ulate the processing of fearful compared to neutral and joyful the “cold” self-regulation and action regulation systems are
stimuli and may initiate visual attention orientation when pro- modulated by emotional bottom-up input. From an experi-
cessing fearful ones by establishing functional connectivity mental psychology point of view, it seems indispensable to
between the superficial amygdala, the visual cortex, and the distinguish those emotionally colored cognitive control and
superior parietal cortex [57]. Further, abnormally increased action control processes from emotion regulation processes.
amygdala activity (and hypo-responsiveness in the ventral
striatum) was evoked when anticipated reward was delayed,
in a study with adults with ADHD [58]. As such, activity in Core Systems of Emotion Regulation
the amygdala may serve as an important bottom-up processing
hub that is probably impaired in ADHD. There are few studies that address ER and ERD in patients
with ADHD using emotional stimulation. Most of them rely
implicitly on Shaw et al.’s model 1, namely that ER and cog-
Top-Down Regulation
nitive deficits may be common consequences of a core deficit
in self-regulation. The current evidence suggests that a lack of
A recent meta-analysis on human neuroimaging studies [42]
cognitive control in emotionally stimulating situations may
divides top-down processes into three parts: (1) a common
lead to increased distraction and thus impaired ER in patients
core system for self-regulation, encompassing the inferior
with ADHD. In line with this proposed general lack of cogni-
frontal gyrus, the medial frontal cortex (MFC) with the ante-
tive control (see above), there is evidence from a study of boys
rior cingulate cortex (ACC), the supplementary motor area
with ADHD that revealed emotional distractors caused dimin-
(SMA), and the right temporoparietal junction (TPJ); (2) a
ished performance in a digit categorization task. For boys with
specific action regulation or response inhibition system (e.g.,
ADHD, this was accompanied by larger N2 amplitudes to
dorsal premotor cortices, intra-parietal sulci, thalamus); and
emotional as compared to neutral distractors, indicating that
(3) an ER system (e.g., more posterior parts of the TPJ and
these emotional stimuli may induce a larger conflict in patients
MFC) [42]. A number of studies revealed difficulties in pa-
with ADHD than in healthy controls [72]. On the other hand,
tients with ADHD within the former two regulation systems;
another study with a Go/NoGo paradigm incorporating back-
however, there are very few studies that elucidate emotional
ground affective pictures revealed enhanced NoGo-P3 ampli-
regulatory processes specifically.
tude and concurrent activity in the OFC sensitive to emotional
context similar to that of controls (a potential compensatory
Core Systems for General Self-Regulation and Action increment of neuronal processing) [73].
Regulation There is also some evidence regarding the impact of ER
strategies while processing affective pictures. Compared to
It is well known that patients with ADHD show deficits in controls, adult patients with ADHD showed increased late
cognitive control, an important aspect of executive functions frontal positive potentials that in a subgroup of medication-
[59–62]. Such deficits have been demonstrated with a wide naïve patients also extended towards centro-parietal locations.
range of tasks such as tapping interference control (Stroop This is generally associated with conscious processing of
tests) or inhibition of (prepotent) responses (Go/NoGo and stimulus’ emotional intensity [69]. In a study by Shushakova
Stop tasks) [63–66]. Deficits typically appear as slower and et al. [74•], late frontal potentials were associated with ADHD
more error-prone responses and as abnormal activity in brain symptom severity. Analyses of the visual N2pc to cues related
regions associated with cognitive control. Patients with to selective attention revealed an abnormal bias towards neg-
ADHD showed diminished brain activity during cognitive ative emotional background stimuli in patients with ADHD
control in the dorsolateral prefrontal cortex (DLPFC), the that was also related to diminished self-reported ER abilities
ACC, and (pre-)SMA in studies using functional magnetic [75].
resonance imaging (fMRI) and in others using brain electrical Another study found diminished activity in the OFC during
activity. Moreover, error processing seems to be blunted in processing of an oddball task incorporating emotional facial
ADHD. For example, early error negativity assumed to indi- expressions in children with ADHD [76]. This is in line with
cate response conflict between required response and rein- the finding of diminished OFC activity as reflected in lower
forcement learning mechanism (main sources: ACC, error positivity amplitude, particularly in tasks where errors
DLPFC) is less pronounced in ADHD compared to healthy are rare and salient. Taken together, these findings of abnor-
controls [67, 68]. mal activity in the OFC may indicate difficulties with the
 17 Page 6 of 11 Curr Psychiatry Rep (2019) 21:17

emotional evaluation of stimuli along with impaired response groups using different paradigms such as social exclusion
outcomes in ADHD. [98].
The most recent study from this lab [80•] studied emotion
systems coherence in 100 children aged 7–11 years. Children
Psychophysiology and ER in ADHD watched the same emotion evocative film clip as in the study
of Musser et al. [78], and facial emotion display across both
Along with the central nervous system (CNS), the autonomic negative and positive emotion induction was coded in addition
nervous system (ANS) is highly relevant for emotions and to HF-HRV and PEP, in order to examine time-linked coher-
their regulation [77]. While emotion reactivity has been asso- ence of facial display, autonomic reactivity, and regulation.
ciated with sympathetic alterations, ER seems to be more Children with ADHD showed weaker coherence among auto-
closely related to parasympathetic regulation [78, 79, 80•]. nomic activation and negative facial affect behavior during the
As hypothesized by the neurovisceral integration theory induction of both negative and positive emotions when com-
[81], accumulating evidence suggests that measures of vagally pared to typically developing children.
mediated heart rate variability reflect PFC function and hence Taken together, studies on children and adolescents dem-
CNS substrates of ER [82–85]. This is corroborated by evi- onstrate specific physiological regulation patterns of ADHD
dence demonstrating that resting state vagal tone, indexed by and ER in certain contexts (i.e., social vs. cognitive tasks with
high-frequency heart rate variability (HF-HRV), predicts frustration; positive vs. negative valence). Overall, the studies
sustained attention, task engagement, and ER over the life are indicative of an altered vagal regulation pattern—
span [86–89]. A recent meta-analysis reports a small, but rel- presumably reflecting PFC dysfunctions.
evant association between markers of self-control in laborato-
ry tasks and vagally mediated resting state heart rate (r = .15) Adults
[90]. Finally, greater task-induced withdrawal in vagal tone
has been associated with better attention [86, 91], social be- We are only aware of two studies on adult ADHD, ER, and
havior [92, 93], impulse control [77, 94, 95], and fewer exter- physiological arousal [99, 100]. A study on stress reactivity
nalizing and internalizing problems among children (see [96] [99] used the Trier social stress test—a standardized
for a review). cognitive-psychosocial stressor, simulating a job interview in
conjunction with mental arithmetics in front of an audience
Children and Adolescents [101]. Subjective stress levels were higher in patients with
ADHD compared to healthy controls, but HF-HRV did not
Among children and adolescents, several studies have inves- differ between groups. Comparable results were obtained in a
tigated ADHD, ER, and autonomic parasympathetic/vagal study with young adults with and without ADHD symptoms
markers such as HF-HRV, as well as markers related to sym- on a frustrating driving simulation [100]. Participants with
pathetic activity such as the pre-ejection period (PEP) [78, 79, high ADHD symptoms reported more anger and frustration,
94, 97, 98]. Most evidence comes from a number of consec- but differences for HF-HRV were not significant. The study
utive investigations from Musser et al. [78, 97], Karalunas by Lackschewitz and colleagues [99] followed a high diag-
et al. [79], and Musser and Nigg [80•] with overlapping sam- nostic standard, but both studies lack power due to small sam-
ples. In their studies, boys and girls with ADHD watched ple sizes (n < 25). Thus, evidence for pathophysiologic differ-
emotional evocative film clips (positive and negative) and ences in ADHD adults is currently very sparse, and interpre-
were instructed to empathize with the main character. They tations and implications are consequently limited.
either had to mimic (induction task) or to suppress (suppres-
sion task) emotions. In their first study, the researchers did not
find any group differences for resting state HF-HRV. Conclusions and Future Research
However, across emotion tasks, healthy controls showed a
systematic variation in HF-HRV depending on valence (re- ADHD is often considered a neurocognitive disorder, al-
duced for positive emotion, increased for negative emotion) though emotional symptoms are highly prevalent and as-
and task demand (suppression needed more activation than sociated with higher impairment and undesired negative
induction). Children with ADHD were observed to have var- outcomes across life span. We know from the literature that
iable HF-HRV in response to the emotional tasks overall, but emotional symptoms are only partially responsive to treat-
without any significant modulation [78]. In later studies, the ment [102]; thus, it is necessary to understand the associ-
authors demonstrated that there are subsamples of patients ation of ER and ERD in ADHD. This review demonstrates
with ADHD who have altered sympathetic-based emotion re- that current translational research suffers from major limi-
activity as well as regulatory differences in parasympathetic tations resulting from a lack of conceptual clarity regarding
HF-HRV [97]. These results have been confirmed by other ER and ERD in ADHD. The extant research summarized
Curr Psychiatry Rep (2019) 21:17 Page 7 of 11 17

clearly points to the relevance of ER and ERD in ADHD, Compliance with Ethical Standards
but it ignores related processes such as the unfolding of
emotions over time, and the time variation for different Conflict of Interest The authors declare that they have no conflict of
interest.
components of emotion such as subjective feelings, moti-
vation, cognition, action tendencies, expressive behavior,
Human and Animal Rights and Informed Consent This article does not
and neuropsychophysiology [28]. To improve our under- contain any studies with human or animal subjects performed by any of
standing of ER and ERD in ADHD, the time dimension the authors.
seems to be highly salient, and there is growing consensus
that processual characteristics should be incorporated in Publisher’s Note Springer Nature remains neutral with regard to juris-
dictional claims in published maps and institutional affiliations.
studies of emotion and ER [21••, 30•]. This consensus also
calls, at least partially, for a paradigmatic shift in research,
as neuroscience methods such as fMRI have merits in test-
ing structural assumptions but are less suited to investigate References
the time dimension compared to other techniques such as
EEG, MEG, and peripheral psychophysiology. The re- Papers of particular interest, published recently, have been
search reviewed in the present article illustrates the current highlighted as:
pitfalls and benefits of ERD in ADHD. An important pend- • Of importance
ing research question in the field of emotion is whether, •• Of major importance
and if so, how, emotions can be induced in our labs to
ensure research that is internally and externally valid and 1. ICD-10: international statistical classification of diseases and re-
that is informative for the delineation of treatment options. lated health problems: tenth revision. 2nd ed. Geneva: WHO;
2004.
However, the aforementioned extended process-
2. American Psychiatric Association. Diagnostic and statistical man-
oriented framework by Gross [31••] specifies iterative ual of mental disorders: American Psychiatric Association; 2013.
regulatory stages, regulatory decisions, and potential fail- 3. Fischer M, Barkley R. The persistence of ADHD into adulthood:
ure points related to (1) whether or not to regulate (iden- (once again) it depends on whom you ask. ADHD Report.
tification), (2) when to select a regulatory category and 2007;15:7–16.
specific regulation tactic to use, (3) then how to execute 4. Polanczyk G, de Lima MS, Horta BL, Biederman J, Rohde LA.
The worldwide prevalence of ADHD: a systematic review and
this strategy with the aim of changing the emotion or its metaregression analysis. Am J Psychiatry. 2007;164:942–8.
generation, and (4) how to monitor the regulatory effects https://doi.org/10.1176/ajp.2007.164.6.942.
that tell us whether ER is sufficient or not (stopping or 5. Polanczyk GV, Willcutt EG, Salum GA, Kieling C, Rohde LA.
maintaining regulatory engagement) or whether we should ADHD prevalence estimates across three decades: an updated
systematic review and meta-regression analysis. Int J Epidemiol.
switch to another strategy. Those challenges and potential 2014;43:434–42. https://doi.org/10.1093/ije/dyt261.
points of failure might differ among individual patients 6. Fayyad J, Sampson NA, Hwang I, Adamowski T, Aguilar-Gaxiola
with ADHD and may suggest specific alternative treat- S, Al-Hamzawi A, et al. The descriptive epidemiology of DSM-IV
ments for different subgroups. Such disparities may ex- adult ADHD in the World Health Organization World Mental
Health Surveys. Atten Defic Hyperact Disord. 2017;9:47–65.
plain why one treatment, e.g., pharmacological interven-
https://doi.org/10.1007/s12402-016-0208-3.
tions, has limited effects on specific emotional symptoms. 7. Simon V, Czobor P, Bálint S, Mészáros A, Bitter I. Prevalence and
In sum, the process model allows for studying ER in correlates of adult attention-deficit hyperactivity disorder: meta-
real time, to specifically track emotions and the associa- analysis. Br J Psychiatry. 2009;194:204–11. https://doi.org/10.
tions among emotions, ER, and psychopathology. Beyond 1192/bjp.bp.107.048827.
8. Kessler R. The prevalence and correlates of adult ADHD in the
general self-regulation problems, ERDs are thus viewed
United States: results from the National Comorbidity Survey
as specific difficulties or configurations of difficulties Replication. Am J Psychiatry. 2006;163:716. https://doi.org/10.
arising from separate levels of emotion processing (e.g., 1176/appi.ajp.163.4.716.
difficulties due to a deficient set of strategies, rigidity in 9. Anastopoulos AD, Smith TF, Garrett ME, Morrissey-Kane E,
using only a small set of strategies, identification prob- Schatz NK, Sommer JL, et al. Self-regulation of emotion, func-
tional impairment, and comorbidity among children with AD/HD.
lems (when to regulate which emotion in a specific con- J Atten Disord. 2011;15:583–92. https://doi.org/10.1177/
text), problems with implementing the strategy). This 1087054710370567.
could reveal valuable information about treatment options 10. Skirrow C, Asherson P. Emotional lability, comorbidity and im-
in order to tailor personalized strategies to improve ER. pairment in adults with attention-deficit hyperactivity disorder. J
Affect Disord. 2013;147:80–6. https://doi.org/10.1016/j.jad.2012.
However, to this end, we need more sophisticated exper-
10.011.
iments and research targeting the temporal dynamics of 11. Szuromi B, Bitter I, Czobor P. Functional impairment in adults
emotion and ER using multilevel approaches and tech- positively screened for attention-deficit hyperactivity disorder:
niques with high temporal resolution. the role of symptom presentation and executive functioning.
17 Page 8 of 11 Curr Psychiatry Rep (2019) 21:17

Compr Psychiatry. 2013;54:974–81. https://doi.org/10.1016/j. 23. Stringaris A, Maughan B, Goodman R. What’s in a disruptive
comppsych.2013.04.002. disorder? Temperamental antecedents of oppositional defiant dis-
12. Barkley RA. Deficient emotional self-regulation is a core compo- order: findings from the Avon longitudinal study. J Am Acad
nent of ADHD. J ADHD Relat Disord. 2010:5–37. Child Adolesc Psychiatry. 2010;49:474–83.
13. Reimherr FW, Marchant BK, Strong RE, Hedges DW, Adler L, 24. Barkley RA, Fischer M. The unique contribution of emotional
Spencer TJ, et al. Emotional dysregulation in adult ADHD and impulsiveness to impairment in major life activities in hyperactive
response to atomoxetine. Biol Psychiatry. 2005;58:125–31. children as adults. J Am Acad Child Adolesc Psychiatry. 2010;49:
https://doi.org/10.1016/j.biopsych.2005.04.040. 503–13. https://doi.org/10.1016/j.jaac.2010.01.019.
14. Corbisiero S, Stieglitz R-D, Retz W, Rösler M. Is emotional dys- 25. Wender PH. Attention-deficit hyperactivity disorder in adults.
regulation part of the psychopathology of ADHD in adults? Atten New York: Oxford University Press; 1995.
Defic Hyperact Disord. 2013;5:83–92. https://doi.org/10.1007/ 26. Barkley RA. Attention-deficit hyperactivity disorder: a handbook
s12402-012-0097-z. for diagnosis and treatment. 4th ed. New York: Guilford; 2018.
15.•• Shaw P, Stringaris A, Nigg J, Leibenluft E. Emotion dysregulation 27. Conners CK, Erhardt D, Epstein JN, Parker JDA, Sitarenios G,
in attention deficit hyperactivity disorder. Am J Psychiatry. Sparrow E. Self-ratings of ADHD symptoms in adults I: factor
2014;171:276–93. https://doi.org/10.1176/appi.ajp.2013. structure and normative data. J Atten Disord. 1999;3:141–51.
13070966 Comprehensive review on emotion regulation in 28. Schmidt-Atzert L, Peper M, Stemmler G. Emotionspsychologie:
ADHD from a multilevel perspective. The authors finally Ein Lehrbuch. 2nd ed. Stuttgart: Kohlhammer; 2014.
suggest three conceptual models to explain the overlap 29. Gross JJ, Jazaieri H. Emotion, emotion regulation, and psychopa-
between emotion regulation and ADHD. thology: an affective science perspective. Clin Psychol Sci.
16. Biederman J, Spencer T, Lomedico A, Day H, Petty CR, Faraone 2014;2:387–401.
SV. Deficient emotional self-regulation and pediatric attention def- 30.• Waugh CE, Shing EZ, Avery BM. Temporal dynamics of emo-
icit hyperactivity disorder: a family risk analysis. Psychol Med. tional processing in the brain. Emot Rev. 2015;7:323–9. https://
2012;42:639–46. https://doi.org/10.1017/S0033291711001644. doi.org/10.1177/1754073915590615 This recent review on
17. Sobanski E, Banaschewski T, Asherson P, Buitelaar J, Chen W, affective neuroscience highlights the importance of
Franke B, et al. Emotional lability in children and adolescents with examining neural temporal dynamics of emotions to better
attention deficit/hyperactivity disorder (ADHD): clinical corre- understand emotional phenomena.
lates and familial prevalence. J Child Psychol Psychiatry. 31.•• Gross JJ. Emotion regulation: current status and future prospects.
2010;51:915–23. https://doi.org/10.1111/j.1469-7610.2010. Psychol Inq. 2015;26:1–26. https://doi.org/10.1080/1047840X.
02217.x. 2014.940781 This target article by Gross and its discussion
18. Surman CBH, Biederman J, Spencer T, Yorks D, Miller CA, Petty in the same issue is an inspiring and valuable contribution to
CR, et al. Deficient emotional self-regulation and adult attention the theoretical and empirical challenges within the field of
deficit hyperactivity disorder: a family risk analysis. Am J emotion regulation.
Psychiatry. 2011;168:617–23. https://doi.org/10.1176/appi.ajp. 32. Thompson RA. Emotion regulation: a theme in search of defini-
2010.10081172. tion. Monogr Soc Res Child Dev. 1994;59:25–52.
19.• Skirrow C, Ebner-Priemer U, Reinhard I, Malliaris Y, Kuntsi J, 33. Webb TL, Miles E, Sheeran P. Dealing with feeling: a meta-
Asherson P. Everyday emotional experience of adults with atten- analysis of the effectiveness of strategies derived from the process
tion deficit hyperactivity disorder: evidence for reactive and en- model of emotion regulation. Psychol Bull. 2012;138:775–808.
dogenous emotional lability. Psychol Med. 2014;44:3571–83. https://doi.org/10.1037/a0027600.
https://doi.org/10.1017/S0033291714001032 This study used 34. Sheppes G, Suri G, Gross JJ. Emotion regulation and psychopa-
real-time ambulatory assessment in a sample of individuals thology. Annu Rev Clin Psychol. 2015;11:379–405. https://doi.
with ADHD without comorbidity and healthy controls. The org/10.1146/annurev-clinpsy-032814-112739.
authors showed that adults with ADHD reported heightened 35. Overgaard KR, Aase H, Torgersen S, Reichborn-Kjennerud T,
intensity and instability of negative emotions in daily life. Oerbeck B, Myhre A, et al. Continuity in features of anxiety and
20.•• Graziano PA, Garcia A. Attention-deficit hyperactivity disorder attention deficit/hyperactivity disorder in young preschool chil-
and children’s emotion dysregulation: a meta-analysis. Clin dren. Eur Child Adolesc Psychiatry. 2014;23:743–52. https://doi.
Psychol Rev. 2016;46:106–23. https://doi.org/10.1016/j.cpr. org/10.1007/s00787-014-0538-7.
2016.04.011 Most recent meta-analysis on emotion regulation 36. Stringaris A, Goodman R. Mood lability and psychopathology in
in children with ADHD. youth. Psychol Med. 2009;39:1237–45. https://doi.org/10.1017/
21.•• Faraone SV, Rostain AL, Blader J, Busch B, Childress AC, S0033291708004662.
Connor DF, et al. Practitioner review: Emotional dysregulation 37. Ambrosini PJ, Bennett DS, Elia J. Attention deficit hyperactivity
in attention-deficit/hyperactivity disorder—implications for clini- disorder characteristics: II. Clinical correlates of irritable mood. J
cal recognition and intervention. J Child Psychol Psychiatry. Affect Disord. 2013;145:70–6. https://doi.org/10.1016/j.jad.2012.
2018. https://doi.org/10.1111/jcpp.12899 This review addresses 07.014.
important issues regarding emotion regulation in ADHD 38. Sjöwall D, Roth L, Lindqvist S, Thorell LB. Multiple deficits in
(conceptual clarifications, similarities, and differences ADHD: executive dysfunction, delay aversion, reaction time var-
between emotion regulation deficits in ADHD and other iability, and emotional deficits. J Child Psychol Psychiatry.
disorders, ERD treatment responses). They provide a 2013;54:619–27. https://doi.org/10.1111/jcpp.12006.
temporal model of emotion-processing impairments in 39. Biederman J, Spencer TJ, Petty C, Hyder LL, O’Connor KB,
ADHD, separating emotional reactivity from emotion regula- Surman CB, et al. Longitudinal course of deficient emotional
tion components. self-regulation CBCL profile in youth with ADHD: prospective
22. Stringaris A, Goodman R. Longitudinal outcome of youth controlled study. Neuropsychiatr Dis Treat. 2012;8:267–76.
oppositionality: irritable, headstrong, and hurtful behaviors have https://doi.org/10.2147/NDT.S29670.
distinctive predictions. J Am Acad Child Adolesc Psychiatry. 40. Sasser TR, Kalvin CB, Bierman KL. Developmental trajectories
2009;48:404–12. https://doi.org/10.1097/CHI. of clinically significant attention-deficit/hyperactivity disorder
0b013e3181984f30. (ADHD) symptoms from grade 3 through 12 in a high-risk
Curr Psychiatry Rep (2019) 21:17 Page 9 of 11 17

sample: predictors and outcomes. J Abnorm Psychol. 2016;125: emotion regulation skills as distinct but correlating factors
207–19. https://doi.org/10.1037/abn0000112. with the symptom domains of inattention, hyperactivity, and
41.• Brocki KC, Forslund T, Frick M, Bohlin G. Do individual differ- impulsivity.
ences in early affective and cognitive self-regulation predict de- 53. Hirsch O, Chavanon ML, Christiansen H. Emotional dysregula-
velopmental change in ADHD symptoms from preschool to ado- tion subgroups in patients with adult attention-deficit/hyperactiv-
lescence? J Atten Disord. 2017:1087054717693372. https://doi. ity disorder (ADHD): a cluster analytic approach. Sci Rep. under
org/10.1177/1087054717693372 A longitudinal study that review after revision.
emphasizes the importance of distinguishing between 54. Hirsch O, Christiansen H. Factorial structure and validity of the
cognitive and affective self-regulation in relation to inattention quantified behavior test plus (Qb+©). Assessment. 2017;24:
and hyperactivity/impulsivity over time. 1037–49. https://doi.org/10.1177/1073191116638426.
42. Langner R, Leiberg S, Hoffstaedter F, Eickhoff SB. Towards a 55. Posner J, Nagel BJ, Maia TV, Mechling A, Oh M, Wang Z, et al.
human self-regulation system: common and distinct neural signa- Abnormal amygdalar activation and connectivity in adolescents
tures of emotional and behavioral control. Neurosci Biobehav with attention-deficit/hyperactivity disorder. J Am Acad Child
Rev. 2018;90:400–10. https://doi.org/10.1016/j.neubiorev.2018. Adolesc Psychiatry. 2011;50:828–37.e3. https://doi.org/10.1016/
04.022. j.jaac.2011.05.010.
43. Shaw P, Sudre G, Wharton A, Weingart D, Sharp W, Sarlls J. 56. Yu X, Liu L, Chen W, Cao Q, Zepf FD, Ji G, et al. Integrity of
White matter microstructure and the variable adult outcome of amygdala subregion-based functional networks and emotional la-
c h i l d h o o d a t t e n t i o n d e f i c i t h y p e r a c t i v i t y d i s o rd e r. bility in drug-naïve boys with ADHD. J Atten Disord. 2016:
Neuropsychopharmacology. 2015;40:746–54. https://doi.org/10. 108705471666141. https://doi.org/10.1177/1087054716661419.
1038/npp.2014.241. 57. Koelsch S, Skouras S, Fritz T, Herrera P, Bonhage C, Küssner
44. Walcott CM, Landau S. The relation between disinhibition and MB, et al. The roles of superficial amygdala and auditory cortex
emotion regulation in boys with attention deficit hyperactivity in music-evoked fear and joy. NeuroImage. 2013;81:49–60.
disorder. J Clin Child Adolesc Psychol. 2004;33:772–82. https:// https://doi.org/10.1016/j.neuroimage.2013.05.008.
doi.org/10.1207/s15374424jccp3304_12. 58. Plichta MM, Vasic N, Wolf RC, Lesch K-P, Brummer D, Jacob C,
45. Banaschewski T, Jennen-Steinmetz C, Brandeis D, Buitelaar JK, et al. Neural hyporesponsiveness and hyperresponsiveness during
Kuntsi J, Poustka L, et al. Neuropsychological correlates of emo- immediate and delayed reward processing in adult attention-defi-
tional lability in children with ADHD. J Child Psychol Psychiatry. cit/hyperactivity disorder. Biol Psychiatry. 2009;65:7–14. https://
2012;53:1139–48. https://doi.org/10.1111/j.1469-7610.2012. doi.org/10.1016/j.biopsych.2008.07.008.
02596.x.
59. Albrecht B, Uebel-von Sandersleben H, Gevensleben H,
46. van Cauwenberge V, Sonuga-Barke EJS, Hoppenbrouwers K, van
Rothenberger A. Pathophysiology of ADHD and associated
Leeuwen K, Wiersema JR. "turning down the heat": is poor per-
problems-starting points for NF interventions? Front Hum
formance of children with ADHD on tasks tapping "hot" emotion-
Neurosci. 2015;9:359. https://doi.org/10.3389/fnhum.2015.
al regulation caused by deficits in "cool" executive functions? Res
00359.
Dev Disabil. 2015;47:199–207. https://doi.org/10.1016/j.ridd.
60. Johnstone SJ, Barry RJ, Clarke AR. Ten years on: a follow-up
2015.09.012.
review of ERP research in attention-deficit/hyperactivity disorder.
47. Villemonteix T, Marx I, Septier M, Berger C, Hacker T, Bahadori
Clin Neurophysiol. 2013;124:644–57. https://doi.org/10.1016/j.
S, et al. Attentional control of emotional interference in children
clinph.2012.09.006.
with ADHD and typically developing children: an emotional N-
back study. Psychiatry Res. 2017;254:1–7. https://doi.org/10. 61. Shiels K, Hawk LW. Self-regulation in ADHD: the role of error
1016/j.psychres.2017.04.027. processing. Clin Psychol Rev. 2010;30:951–61. https://doi.org/10.
48. Posner J, Rauh V, Gruber A, Gat I, Wang Z, Peterson BS. 1016/j.cpr.2010.06.010.
Dissociable attentional and affective circuits in medication-naïve 62. Downes M, Bathelt J, de Haan M. Event-related potential mea-
children with attention-deficit/hyperactivity disorder. Psychiatry sures of executive functioning from preschool to adolescence. Dev
Res. 2013;213:24–30. https://doi.org/10.1016/j.pscychresns. Med Child Neurol. 2017;59:581–90. https://doi.org/10.1111/
2013.01.004. dmcn.13395.
49. Marx I, Domes G, Havenstein C, Berger C, Schulze L, Herpertz 63. Lansbergen MM, Kenemans JL, van Engeland H. Stroop interfer-
SC. Enhanced emotional interference on working memory perfor- ence and attention-deficit/hyperactivity disorder: a review and me-
mance in adults with ADHD. World J Biol Psychiatry. ta-analysis. Neuropsychology. 2007;21:251–62. https://doi.org/
2011;12(Suppl 1):70–5. https://doi.org/10.3109/15622975.2011. 10.1037/0894-4105.21.2.251.
599213. 64. Alderson RM, Rapport MD, Kofler MJ. Attention-deficit/hyper-
50. Surman CBH, Biederman J, Spencer T, Miller CA, McDermott activity disorder and behavioral inhibition: a meta-analytic review
KM, Faraone SV. Understanding deficient emotional self- of the stop-signal paradigm. J Abnorm Child Psychol. 2007;35:
regulation in adults with attention deficit hyperactivity disorder: 745–58. https://doi.org/10.1007/s10802-007-9131-6.
a controlled study. Atten Defic Hyperact Disord. 2013;5:273–81. 65. Mullane JC, Corkum PV, Klein RM, McLaughlin E.
https://doi.org/10.1007/s12402-012-0100-8. Interference control in children with and without ADHD: a
51. Christiansen H, Hirsch O, Philipsen A, Oades RD, Matthies S, systematic review of flanker and Simon task performance.
Hebebrand J, et al. German validation of the conners adult Child Neuropsychol. 2009;15:321–42. https://doi.org/10.
ADHD rating scale-self-report: confirmation of factor structure 1080/09297040802348028.
in a large sample of participants with ADHD. J Atten Disord. 66. Huang-Pollock CL, Karalunas SL, Tam H, Moore AN. Evaluating
2013;17:690–8. https://doi.org/10.1177/1087054711435680. vigilance deficits in ADHD: a meta-analysis of CPT performance.
52.• Hirsch O, Chavanon M, Riechmann E, Christiansen H. Emotional J Abnorm Psychol. 2012;121:360–71. https://doi.org/10.1037/
dysregulation is a primary symptom in adult attention-deficit/hy- a0027205.
peractivity disorder (ADHD). J Affect Disord. 2018;232:41–7. 67. Albrecht B, Brandeis D, Uebel H, Heinrich H, Mueller UC,
https://doi.org/10.1016/j.jad.2018.02.007 Recent study of our Hasselhorn M, et al. Action monitoring in boys with attention-
group that probed a model that explicitly distinguished deficit/hyperactivity disorder, their nonaffected siblings, and nor-
positive and negative affect, problems with self-concept and mal control subjects: evidence for an endophenotype. Biol
17 Page 10 of 11 Curr Psychiatry Rep (2019) 21:17

Psychiatry. 2008;64:615–25. https://doi.org/10.1016/j.biopsych. youth with ADHD, emotion systems were more poorly
2007.12.016. coordinated.
68. McLoughlin G, Albrecht B, Banaschewski T, Rothenberger A, 81. Thayer JF, Hansen AL, Saus-Rose E, Johnsen BH. Heart rate
Brandeis D, Asherson P, et al. Performance monitoring is altered variability, prefrontal neural function, and cognitive performance:
in adult ADHD: a familial event-related potential investigation. the neurovisceral integration perspective on self-regulation, adap-
Neuropsychologia. 2009;47:3134–42. https://doi.org/10.1016/j. tation, and health. Ann Behav Med. 2009;37:141–53. https://doi.
neuropsychologia.2009.07.013. org/10.1007/s12160-009-9101-z.
69. Hajcak G, MacNamara A, Olvet DM. Event-related potentials, 82. Thayer JF, Ahs F, Fredrikson M, Sollers JJ, Wager TD. A meta-
emotion, and emotion regulation: an integrative review. Dev analysis of heart rate variability and neuroimaging studies: impli-
Neuropsychol. 2010;35:129–55. https://doi.org/10.1080/ cations for heart rate variability as a marker of stress and health.
87565640903526504. Neurosci Biobehav Rev. 2012;36:747–56. https://doi.org/10.
70. Rosch KS, Hawk LW. The effects of performance-based rewards 1016/j.neubiorev.2011.11.009.
on neurophysiological correlates of stimulus, error, and feedback 83. Jennings JR, Sheu LK, Kuan DC-H, Manuck SB, Gianaros PJ.
processing in children with ADHD. Psychophysiology. 2013;50: Resting state connectivity of the medial prefrontal cortex covaries
1157–73. https://doi.org/10.1111/psyp.12127. with individual differences in high-frequency heart rate variability.
71. Uebel H, Albrecht B, Asherson P, Börger NA, Butler L, Chen W, Psychophysiology. 2016;53:444–54. https://doi.org/10.1111/
et al. Performance variability, impulsivity errors and the impact of psyp.12586.
incentives as gender-independent endophenotypes for ADHD. J 84. Beauchaine TP, Thayer JF. Heart rate variability as a
Child Psychol Psychiatry. 2010;51:210–8. https://doi.org/10.1111/ transdiagnostic biomarker of psychopathology. Int J
j.1469-7610.2009.02139.x. Psychophysiol. 2015;98:338–50. https://doi.org/10.1016/j.
72. López-Martín S, Albert J, Fernández-Jaén A, Carretié L. ijpsycho.2015.08.004.
Emotional distraction in boys with ADHD: neural and behavioral 85. Lane RD, McRae K, Reiman EM, Chen K, Ahern GL, Thayer JF.
correlates. Brain Cogn. 2013;83:10–20. https://doi.org/10.1016/j. Neural correlates of heart rate variability during emotion.
bandc.2013.06.004. NeuroImage. 2009;44:213–22. https://doi.org/10.1016/j.
neuroimage.2008.07.056.
73. López-Martín S, Albert J, Fernández-Jaén A, Carretié L.
86. Duschek S, Muckenthaler M, Werner N, del Paso GAR.
Emotional response inhibition in children with attention-def-
Relationships between features of autonomic cardiovascular con-
icit/hyperactivity disorder: neural and behavioral data.
trol and cognitive performance. Biol Psychol. 2009;81:110–7.
Psychol Med. 2015;45:2057–71. https://doi.org/10.1017/
https://doi.org/10.1016/j.biopsycho.2009.03.003.
S0033291714003195.
87. Gentzler AL, Santucci AK, Kovacs M, Fox NA. Respiratory sinus
74.• Shushakova A, Ohrmann P, Pedersen A. Exploring deficient emo-
arrhythmia reactivity predicts emotion regulation and depressive
tion regulation in adult ADHD: electrophysiological evidence.
symptoms in at-risk and control children. Biol Psychol. 2009;82:
Eur Arch Psychiatry Clin Neurosci. 2018;268:359–71. https://
156–63. https://doi.org/10.1016/j.biopsycho.2009.07.002.
doi.org/10.1007/s00406-017-0826-6 This study suggests that
88. Hansen AL, Johnsen BH, Thayer JF. Vagal influence on working
the processing of aversive stimuli as well as emotion
memory and attention. Int J Psychophysiol. 2003;48:263–74.
regulation is associated with greater cognitive effort in
https://doi.org/10.1016/S0167-8760(03)00073-4.
patients with ADHD than in healthy controls. The latter also
89. Pu J, Schmeichel BJ, Demaree HA. Cardiac vagal control predicts
suggests difficulties during the implementation of emotion
spontaneous regulation of negative emotional expression and sub-
regulation strategies.
sequent cognitive performance. Biol Psychol. 2010;84:531–40.
75. Shushakova A, Wiesner CD, Ohrmann P, Pedersen A. https://doi.org/10.1016/j.biopsycho.2009.07.006.
Electrophysiological evidence of an attentional bias towards ap- 90. Zahn D, Adams J, Krohn J, Wenzel M, Mann CG, Gomille LK,
petitive and aversive words in adults with attention-deficit/hyper- et al. Heart rate variability and self-control—a meta-analysis. Biol
activity disorder. Clin Neurophysiol. 2018;129:1937–46. https:// Psychol. 2016;115:9–26. https://doi.org/10.1016/j.biopsycho.
doi.org/10.1016/j.clinph.2018.06.019. 2015.12.007.
76. Perlman SB, Hein TC, Stepp SD. Emotional reactivity and its 91. Suess PE, Porges SW, Plude DJ. Cardiac vagal tone and sustained
impact on neural circuitry for attention-emotion interaction in attention in school-age children. Psychophysiology. 1994;31:17–
childhood and adolescence. Dev Cogn Neurosci. 2014;8:100–9. 22.
https://doi.org/10.1016/j.dcn.2013.08.005. 92. Calkins SD, Graziano PA, Keane SP. Cardiac vagal regulation
77. Porges SW. The polyvagal perspective. Biol Psychol. 2007;74: differentiates among children at risk for behavior problems. Biol
116–43. https://doi.org/10.1016/j.biopsycho.2006.06.009. Psychol. 2007;74:144–53. https://doi.org/10.1016/j.biopsycho.
78. Musser ED, Backs RW, Schmitt CF, Ablow JC, Measelle JR, Nigg 2006.09.005.
JT. Emotion regulation via the autonomic nervous system in chil- 93. Geisler FCM, Kubiak T, Siewert K, Weber H. Cardiac vagal tone
dren with attention-deficit/hyperactivity disorder (ADHD). J is associated with social engagement and self-regulation. Biol
Abnorm Child Psychol. 2011;39:841–52. https://doi.org/10. Psychol. 2013;93:279–86. https://doi.org/10.1016/j.biopsycho.
1007/s10802-011-9499-1. 2013.02.013.
79. Karalunas SL, Fair D, Musser ED, Aykes K, Iyer SP, Nigg JT. 94. Beauchaine TP, Katkin ES, Strassberg Z, Snarr J.
Subtyping attention-deficit/hyperactivity disorder using tempera- Disinhibitory psychopathology in male adolescents: discrim-
ment dimensions: toward biologically based nosologic criteria. inating conduct disorder from attention-deficit/hyperactivity
JAMA Psychiatry. 2014;71:1015–24. https://doi.org/10.1001/ disorder through concurrent assessment of multiple auto-
jamapsychiatry.2014.763. nomic states. J Abnorm Psychol. 2001;110:610–24. https://
80.• Musser ED, Nigg JT. Emotion dysregulation across emotion sys- doi.org/10.1037/0021-843X.110.4.610.
tems in attention deficit/hyperactivity disorder. J Clin Child 95. Utendale WT, Nuselovici J, Saint-Pierre AB, Hubert M, Chochol
Adolesc Psychol. 2017:1–13. https://doi.org/10.1080/15374416. C, Hastings PD. Associations between inhibitory control, respira-
2016.1270828 This is the first study that examined the tory sinus arrhythmia, and externalizing problems in early child-
coherence of emotion systems in children with and without hood. Dev Psychobiol. 2014;56:686–99. https://doi.org/10.1002/
ADHD. The authors demonstrated in a large sample that in dev.21136.
Curr Psychiatry Rep (2019) 21:17 Page 11 of 11 17

96. Graziano P, Derefinko K. Cardiac vagal control and children’s 2008;33:612–24. https://doi.org/10.1016/j.psyneuen.2008.01.
adaptive functioning: a meta-analysis. Biol Psychol. 2013;94: 016.
22–37. https://doi.org/10.1016/j.biopsycho.2013.04.011. 100. Oliver ML, Nigg JT, Cassavaugh ND, Backs RW. Behavioral and
97. Musser ED, Galloway-Long HS, Frick PJ, Nigg JT. Emotion reg- cardiovascular responses to frustration during simulated driving
ulation and heterogeneity in attention-deficit/hyperactivity disor- tasks in young adults with and without attention disorder symp-
der. J Am Acad Child Adolesc Psychiatry. 2013;52:163–171.e2. toms. J Atten Disord. 2012;16:478–90. https://doi.org/10.1177/
https://doi.org/10.1016/j.jaac.2012.11.009. 1087054710397132.
98. McQuade JD, Breaux RP. Are elevations in ADHD symptoms 101. Kirschbaum C, Pirke KM, Hellhammer DH. The ‘Trier social
associated with physiological reactivity and emotion dysregula- stress test’—a tool for investigating psychobiological stress
tion in children? J Abnorm Child Psychol. 2017;45:1091–103. responses in a laboratory setting. Neuropsychobiology.
https://doi.org/10.1007/s10802-016-0227-8. 1993;28:76–81. https://doi.org/10.1159/000119004.
99. Lackschewitz H, Hüther G, Kröner-Herwig B. Physiological and 102. Posner J, Kass E, Hulvershorn L. Using stimulants to treat ADHD-
psychological stress responses in adults with attention-deficit/hy- related emotional lability. Curr Psychiatry Rep. 2014;16:478.
peractivity disorder (ADHD). Psychoneuroendocrinology. https://doi.org/10.1007/s11920-014-0478-4.