Emotion dysregulation in adults with ADHD: The role of cognitive reappraisal and expressive suppression

Attention-deficit/hyperactivity disorder (ADHD) is a common neurodevelopmental disorder, characterized by inattention, hyperactivity, and impulsivity with related functional impairments (American Psychiatric Association, 2013). In recent years, a substantial body of research has highlighted the frequent co-occurrence and importance of emotion dysregulation (ED) symptoms in both children and adults with ADHD, with some authors advocating for ED to be considered as a fourth dimension of the disorder (e.g., Barkley, 2010; Faraone et al., 2019).

ED may arise from either excessive bottom-up subcortical emotional reactivity, or deficient subcortical regulation or deficient top-down cortical control, or all three (Gross and Jazaieri, 2014). Symptomatic descriptions may emphasize either excessive emotional reactivity (i.e., rapid mood changes and rapid generation of high intensity emotion, disproportionate to the trigger or context) or deficits in emotion regulation (i.e., an inability to control these emotional responses by applying appropriate emotion regulation strategies) (Shaw et al., 2014). Yet, the psychopathogenic processes involved in ED of ADHD are not well understood. A key aim of this study is therefore to elucidate these mechanisms using both behavioral and neuroimaging data, within an established theoretical model.

Our conceptual framework is Gross's (2015) process model of emotion regulation, which represents the most widely used model of emotion regulation in the affective science field. The process model posits five families of regulation strategies, including (i) situation selection, (ii) situation modification, (iii) attentional deployment, (iv) cognitive change, and (v) response modification (Gross, 2015). The process model specifies that, all else being equal, strategies activated earlier in the emotion generation process (i.e., antecedent-based strategies, activated before the emotion is fully formed) are likely to be more effective than those implemented later (i.e., response-focused strategies, activated once the emotion is fully formed).

This prediction has so far been born out in the wider mental health literature, with two particular strategies often used as exemplars of these emotion regulation categories: cognitive reappraisal (CR) and expressive suppression (ES). CR is an antecedent-focused (cognitive change) strategy that involves cognitively re-interpreting or intentionally changing the meaning of an emotional stimulus or event (e.g., reframing things in a more balanced or positive light). ES, in contrast, is a response-focused (response modulation) strategy that involves suppressing the behavioral expression (i.e. inhibit the acting out) of an emotion at the final stage of emotion regulation process (Gross, 1998; Gross, 2015).

CR is widely regarded as a generally effective strategy in the emotion regulation field. Regular use of CR has been associated with a wide range of desirable long-term outcomes (e.g., strong social functioning and well-being) (Goldin et al., 2008), whereas high use of ES is typically associated with poor functioning (e.g., poorer social functioning and well-being) (Schäfer et al., 2017; Sloan et al., 2017; Kivity and Huppert, 2018). Indeed, a variety of categories of psychopathology are characterized by low use of CR and high use of ES, such as depression and social anxiety disorder (Lincoln et al., 2022; Kivity and Huppert, 2018; Preece et al., 2020). Thus, low CR use and high ES use may be characteristic of ED problems. Emerging data suggest that such patterns may also be present for ADHD (e.g., Materna et al., 2019), though the impact of these emotion regulation strategy patterns in ADHD has not yet been explored in depth - in particular, the neural substrates involved in ED in adults with ADHD are poorly understood.

In general, at the neurobiological level, the amygdala and its connectivity play critical roles in the subcortical level of emotion generation and regulation. In contrast, the orbitofrontal cortex, medial prefrontal cortex, and fronto-parietal networks are mainly involved in the cortical level of top-down emotional processing and regulation (Shaw et al., 2014). ED in clinical populations has been studied in relation to these three broad neurobiological domains: subcortical emotion generation, subcortical (implicit) emotion regulation, and cortical (explicit) emotion control.

At the psychological level, ED can also be examined as arising from deficits in, or misapplication of, emotion regulation strategies, such as CR and ES (with corresponding neural circuitry correlates). There are three broad groups of studies on the neural correlates of emotion processing relevant to this study. The first group of studies focus on comparing ADHD participants with and without ED. The second group of studies focus on the neural correlates of CR and ES in non-clinical populations. The third group focuses on clinical populations performing CR or ES tasks (mostly in samples with depression or anxiety, and only one sample with ADHD).

In the first group of studies, a limited number of task-fMRI studies (based on emotion perception and visual emotion stimulus processing tasks) have revealed that participants with ADHD exhibited abnormal patterns in amygdala activation and in functional connectivity of amygdala-prefrontal areas during emotion processing (Posner et al., 2011; Viering et al., 2021a). Resting-state fMRI (rs-fMRI) research has found altered connectivity in amygdala-based circuits (including rostral anterior cingulate cortex, bilateral insula, superior temporal gyrus, dorsolateral prefrontal cortex, and inferior parietal lobe) to be associated with ED in children with ADHD (Hulvershorn et al., 2014; Yu et al., 2020).

In the second group of studies, neuroimaging evidence from healthy individuals has suggested that CR activates cognitive control areas within the brain, including the prefrontal cortex (PFC), posterior parietal cortex, as well as lateral temporal lobe, and decreases the activity the bilateral amygdala (Buhle et al., 2014; Poon et al., 2022). In contrast, ES has been found to increase activation of the dorsolateral/lateral PFC, the right inferior frontal gyrus, bilateral putamen, pre-supplementary motor area, and right supramarginal gyrus (Vanderhasselt et al., 2013a; Vrticka et al., 2013). Moreover, ES has been reported to be negatively associated with the global efficiency of the fronto-parietal network and default-mode network (Pan et al., 2018). Considering the subcortical regions, some findings suggested that ES was related to higher activation of the amygdala (Goldin et al., 2008; Vanderhasselt et al., 2013b), and ventral striatum (Petrican et al., 2015).

The third group of studies involve patients with mood disorders, anxiety disorders, addiction disorders, schizophrenia, or personality disorders; and found consistent reduced activation of the ventrolateral prefrontal cortex and dorsolateral prefrontal cortex during emotion regulation tasks using CR in clinical samples (Zilverstand et al., 2017). Furthermore, in individuals with mood disorders or anxiety disorders, ED has been correlated with enhanced amygdala activation and reduced activation in the dorsal anterior cingulate cortex and inferior/superior parietal cortex (Zilverstand et al., 2017). However, in these studies, ES has not been investigated. With respect to ADHD, only one study has been reported in the literature to our knowledge; it found that the anterior cingulate cortex (ACC) activations when viewing negative pictures were significantly positively correlated with self-reported CR in adults with ADHD, whereas this correlation was not detected in healthy controls. Meanwhile, no ES-related brain functional alteration was identified (Materna et al., 2019). Overall, the potential roles of CR- and/or ES-related brain functional abnormalities in ADHD have not been examined fully by previous studies.

To address these gaps in the literature, we sought to evaluate the roles of emotion regulation strategy use in ED expression in adults with ADHD, using both behavioral and neuroimaging measures. First, we explored the association of CR and ES use with ED expression using psychometric-based behavioral data. Based on the existing evidence for the differential effectiveness of CR and ES in emotion regulation, we hypothesized that adults with ADHD would utilize less CR and more ES compared to a healthy control (HC) sample. Second, we examined functional connections of the bilateral amygdala, to elucidate potential functional alterations related to emotion regulation and subsequent ED manifestations. Third, to further probe the nature of observed relationships, we tested whether detected neural correlates may mediate the association between emotion regulation strategy use and behavioral manifestations of ED.

Based on the existing literature on the neural correlates of CR and ES (Buhle et al., 2014; Vanderhasselt et al., 2013b), we hypothesized that impairments in regulation strategy usage may be related to atypical functional connectivities between bilateral amygdala and cognitive control areas (like PFC, ACC) in ADHD. These, in turn, may ultimately contribute to the ED manifestations in adult ADHD.

Participants

Adults with ADHD were recruited from the outpatient clinic of Peking University Sixth Hospital, China. Healthy controls (HCs) were recruited through advertisements to communities in China. The inclusion criteria of the ADHD group were as follows: (1) met the diagnostic criteria for ADHD according to the fourth edition of the American Diagnostic and Statistical Manual of Mental Disorders (DSM-IV; American Psychiatric Association [APA], 1994); (2) 18 years old or older; (3) ADHD medication-naïve

Comparisons of emotion dysregulation between the ADHD and HC groups

Clinical and demographic characteristics of the ADHD and HC groups are shown in Table 1. Participants with ADHD self-reported a higher EC score than HCs (p = 4.52E-77, η² _partial = 0.434), indicating impaired emotion regulation (i.e. ↑EC = ↑ED). Given a significant difference in ED expression was detected between male and female participants (p < 0.001), stratified analyses by sex were conducted with age and IQ as covariates. Differences between cases and controls were detected in both males

Discussion

Our aim in this study was to examine the role of emotion regulation in adult ADHD, and to assess its impact on overall ED levels. Overall, we found that the characteristic ED in ADHD was associated principally with less use of CR. However, in the ADHD group only, higher ES use was negatively correlated with ED, suggesting ES as a potential compensatory strategy. Furthermore, imaging analyses indicated that ADHD participants potentially showed an abnormal CR associated FC pattern of the right

Conclusions

To our knowledge, this is the first comprehensive study to examine CR, ES, and their neural substrates as part of the ED presentation of adult ADHD. Our findings indicate that compared to HCs, participants with adult ADHD were more likely to use ES rather than CR to regulate their emotions; and the less frequent use of CR might help to account for their elevated ED symptoms. The increased use of ES might play a potential compensatory role in the emotion regulation process. Our results have also

Funding

This work was supported by the National Natural Science Foundation of China (81873802; 81641163; 81571340), the Capital's Funds for Health Improvement and Research (CFH: 2022-2-4114; CFH: 2020-2-4112), Beijing Natural Science Foundation (7172245).

CRediT authorship contribution statement

Lu Liu, Qiujin Qian, and Wai Chen contributed conception and design of the study; Qianrong Liu, Defeng Xu, Guanghui Fu, and Haimei Li organized the database; Qianrong Liu, Lu Liu, and Wai Chen designed the statistical analysis; Qianrong Liu performed the statistical analysis. Qianrong Liu, Lu Liu, Wai Chen, David A. Preece, Ningning Liu, Yufeng Wang, Qiujin Qian, and James J. Gross interpreted the results and wrote sections of the manuscript. All authors contributed to manuscript revision and

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgements

We would like to thank all subjects who participated in this study.