Resting heart rate variability, emotion regulation, psychological wellbeing and autism symptomatology in adults with and without autism☆
Introduction
Anxiety disorders and depression are the most prevalent mental health conditions (Kessler et al., 2005), affecting 14.5% to 33.7% and 8% to 12% of the general population, respectively (Andrade et al., 2003; Bandelow and Michaelis, 2015). In addition to their high prevalence, both disorders have significant negative impact on physical and somatic health (Bhattacharya et al., 2014; Murray and Lopez, 1997; Patten et al., 2008; Scott et al., 2007; Vogelzangs et al., 2010). For example, depression has been projected as one of the top contributors to disease burden in 2020, second to coronary artery disease (Murray and Lopez, 1997), and anxiety disorders increase the risk of coronary heart disease by almost 3-fold and comorbid anxiety/depression by 3.6 fold (Vogelzangs et al., 2010).
Anxiety and depression are particularly prevalent in individuals diagnosed with autism spectrum disorder (ASD), irrespective of their age, with up to 70% of individuals experiencing clinically significant levels of anxiety and up to 84% with depression (Croen et al., 2015; Kim et al., 2000; Lainhart, 1999; Lugnegård et al., 2011; Hofvander et al., 2009; Mazzone et al., 2012; Muris et al., 1998). As in other populations, anxiety and depression symptoms have a major negative impact on the health of individuals with ASD, as evidenced by the associations with greater loneliness, behavioural problems, lower quality of life, sleep problems and suicidal ideation (Farrugia and Hudson, 2006; Hedley et al., 2017; Richdale and Baglin, 2015; Stewart et al., 2006; White and Roberson-Nay, 2009).
One of the key risk factors linked to the development and maintenance of affective and behavioural problems in the general population (Aldao et al., 2010; Gross and Jazaieri, 2014; McLaughlin et al., 2011), and more recently in ASD (Mazefsky et al., 2013; Weiss et al., 2014; White et al., 2014), is deficits in the ability to regulate emotions. Emotion regulation (ER) is the goal-directed process of modifying and responding to emotions that are experienced in everyday life (Eisenberg and Spinrad, 2004; Thompson, 1991). There is a repertoire of ER strategies that can be chosen and implemented (Bonanno and Burton, 2013), and individuals vary in their capacity to regulate emotions and their strategy preferences (Gross and John, 2003; Sheppes et al., 2014). Two strategies for regulating emotions that have been most robustly studied are cognitive reappraisal, which involves re-interpreting a situation to change the way one feels about it (Lazarus and Alfert, 1964), and expressive suppression, which involves inhibiting the expression of emotions (Gross and Levenson, 1993). Extensive research has been conducted to examine the consequences of both strategies and, overall, it has been concluded that reappraisal is a more adaptive strategy for regulating emotions than suppression (Butler et al., 2003; Campbell-Sills et al., 2006; Ehring et al., 2010; Garnefski et al., 2002; Gross and John, 2003; Gross, 1998; Gross and Levenson, 1993; Gross and Levenson, 1997; Mauss et al., 2007; Richards and Gross, 1999; Richards and Gross, 2000; Richards et al., 2003; Wenzlaff and Luxton, 2003).
One common factor that connects anxiety and depression with emotion dysregulation is heart rate variability (HRV), a reliable marker of autonomic activity (Malik, 1996). The next section provides a brief overview of the literature on HRV in the general population and its relationship with psychological health. The association between HRV and ER in predicting mental health is also discussed, highlighting its relevance for understanding the frequency and severity of anxiety and depression reported in ASD.
HRV represents the variation in the interval between consecutive heartbeats and is most commonly measured via short- or long-term electrocardiogram (ECG) recordings. Cardiac vagal control can be measured via respiratory sinus arrhythmia (RSA), the high frequency heart rate variability associated with the respiratory cycle (Berntson et al., 1997). High HRV represents a sign of autonomic flexibility, and has been shown to protect against future cardiac events (e.g., Tsuji et al., 1996). In contrast, low HRV predicts both risk of coronary heart disease (e.g., Dekker et al., 2000) and risk of mortality (e.g., La Rovere et al., 2003).
Extensive research demonstrates the connections between low HRV and concomitant psychological disorders, particularly anxiety and depression. There are three comprehensive meta-analyses of the relationship between HRV and anxiety (Chalmers et al., 2014) and depression (Kemp et al., 2010; Rottenberg, 2007) in physically healthy individuals. The findings indicate that lower resting RSA is associated with increased symptoms of depression (Rottenberg, 2007), and lower resting HRV is associated with both depression (Kemp et al., 2010) and anxiety (Chalmers et al., 2014). Extending findings beyond anxiety and depression, a recent meta-analysis by Alvares et al. (2016) demonstrated reduced HRV in patients with a wide range of mental health conditions (mood, anxiety, psychosis and substance dependent disorders) relative to controls.
Psychotropic medications have been shown to impact on the cardiovascular system. There is ample evidence from both empirical studies and reviews to conclude that the use of tricyclic antidepressants is associated with lower HRV (e.g., Alvares et al., 2016; Kemp et al., 2010; Lehofer et al., 1997). However, the impact of other antidepressants is currently inconclusive, for example, there was an active debate on the effects of selective serotonin reuptake inhibitors (SSRIs). In their meta-analytical review, Kemp et al. (2010) found that SSRIs are associated with benign cardiac effects whereas in a longitudinal study, Licht et al. (2010) concluded that tricyclic antidepressants, SSRIs and noradrenergic and specific serotonergic antidepressants (NaSSAs) decreased RSA. Kemp et al. (2011) suggested several reasons for Licht et al.'s findings including the analytical approach used and methodological issues. Furthermore, van Zyl et al. (2008) found that SSRIs increased one HRV measure in studies with short recording intervals. Finally, certain antipsychotic medications such as clozapine also have varying effects on HRV (e.g., Alvares et al., 2016; Silke et al., 2002).
According to the Polyvagal Theory of emotions (Porges, 1997), cardiovascular control is associated with emotion regulatory capacity and in turn determines socio-communicative behaviours. Thus, researchers have suggested that HRV is a physiological indicator of the capacity to regulate emotions (Appelhans and Luecken, 2006; Thayer and Lane, 2000). Several empirical studies have demonstrated that higher resting HRV or RSA are associated with better emotion regulation and use of more constructive coping strategies (Fabes and Eisenberg, 1997; O'Connor et al., 2002) and lower resting HRV is associated with use of less constructive strategies (Fuller, 1992; Pauls and Stemmler, 2003; Sgoifo et al., 2003).
Only two studies, both with female samples, have examined the relationships between HRV and the use of reappraisal and suppression. Butler et al. (2006) found that women who were asked to either suppress or reappraise their emotions during face-to-face interactions showed a greater increase in RSA than women who were not prompted to use specific ER strategies. In the second study where female undergraduate students viewed an anger-inducing video, participants who were instructed to reappraise prior to watching the video showed increased HRV whereas those who were asked to either suppress or simply watch the video showed no such HRV increases (Denson et al., 2011). The authors concluded that the use of reappraisal might result in greater autonomic flexibility in situations that trigger anger. These two studies measured participant HRV before and after exposure to the experimental stimuli under specific conditions (i.e., suppress, reappraise, or no ER prompt). In light of these findings, it seems relevant to characterise the relationships of the habitual use of reappraisal and suppression with resting HRV. However, to our knowledge, no research to date has addressed this in either the general or ASD populations.
Findings on the associations between ASD symptom severity and resting HRV have largely depended on the sample used in studies. For example, using a combined sample of children with and without ASD, Neuhaus et al. (2014) found that parent-reported ASD symptomatology was moderately associated with children's baseline RSA. In contrast, Klusek et al. (2013) examined the relationship between autism severity and baseline RSA in their ASD and control groups separately, and only found a significant association in the TD group. Research comparing resting HRV (and RSA) in individuals with and without ASD has yielded mixed results. Some studies report reduced resting levels in ASD (e.g., Guy et al., 2014; Mathewson et al., 2011), while others have found similar resting levels in the two groups (e.g., Levine et al., 2012; Sheinkopf et al., 2013; Toichi and Kamio, 2003).
Research has also demonstrated a relationship between resting RSA and psychological wellbeing in combined samples of children with and without ASD. Guy et al. (2014) showed higher parent-reported anxiety symptoms were correlated significantly with lower baseline RSA. Similarly, Neuhaus et al. (2014) also found baseline RSA to be correlated significantly with internalising and externalising symptoms (including measures of anxiety and depression) reported by parents. However, the relationship between resting HRV and psychological wellbeing has not been examined in adult samples.
In addition to the high prevalence of anxiety and depression in ASD (American Psychiatric Association, 2013; Croen et al., 2015; Totsika et al., 2011), individuals with ASD also experience more ER difficulties, and either self-report or demonstrate a less adaptive pattern of ER strategy use (e.g., Bruggink et al., 2016; Samson et al., 2012). Based on a review of empirical work in ER, the higher prevalence of internalising symptoms in ASD appears linked to the habitual use of adaptive or/and maladaptive ER strategies (Cai et al., 2018). Based on the research summarised, it is possible that either AS symptom severity, psychological wellbeing, emotion regulation strategy use, or a combination of these are related to resting HRV, however these constructs have never been examined together.
Given their dimensional nature, it is increasingly recognised that in order to understand processes and mechanisms underlying specific mental health symptoms it is necessary to explore shared biological, cognitive, neural and behavioural elements across both normative and clinical populations (Insel et al., 2010). Autonomic nervous system dysfunction is suggested to be a marker for both psychological and physiological disorders (Alvares et al., 2016; Appelhans and Luecken, 2006). In addition, emotion dysregulation has been shown to be a trans-diagnostic process associated with a range of mental health disorders (Aldao et al., 2016; Gross and John, 2003). Importantly, variations across both autonomic nervous system function and ER are observed in the general population. Therefore in the current study we adopted a dimensional approach to examine these constructs in a sample of adults with and without ASD. A similar approach has been used in other HRV (and RSA) research in autism (e.g., Neuhaus et al., 2014).
The aim in the current study was to examine the relationships between ASD symptomatology, ER (reappraisal and suppression), resting HRV and psychological wellbeing (anxiety, depression and positive wellbeing) in a combined sample of adults with and without ASD. Based on existing findings, we hypothesised that lower ASD symptomatology, psychological wellbeing, specifically higher positive aspects of psychological wellbeing and lower symptoms of anxiety and depression, and greater use of reappraisal and/or lower use of suppression would be associated with higher resting HRV. We were also interested to discover which of these variables predicted resting HRV.
Section snippets
Participants
Twenty-four individuals with ASD and twenty control individuals with intelligence quotients (IQ) > 80 participated in this study (see Table 1 for demographic information). All participants in the ASD group self-reported an ASD clinical diagnosis. The existence of an ASD diagnosis was an exclusionary criterion for the control group. Participants with mental health conditions were not excluded from this study, given that the scope of the study included examining individual differences in
ASD symptomatology
All individuals with ASD met criteria for ASD on one or both ADOS-2 (Lord et al., 2012) and the AQ-short (Hoekstra et al., 2011). Four individuals with ASD (16.7%) fell within the non-spectrum category based on their ADOS-2 Module 4 severity score, but they all scored >65 (range 76–92) on the AQ-Short, and two participants who met ADOS-2 criteria for ASD had an AQ-short score ≤ 65 (i.e., 61 and 62). Five individuals in the control group (25%) scored >65 on the AQ-Short (i.e., 66, 67, 71, 76,
Discussion
The aim of the current study was to characterise the relationships between resting HRV, ASD symptom severity, ER strategy use, and positive and negative aspects of psychological wellbeing in a sample of adults with and without ASD. We adopted a dimensional approach by using the combined sample to examine whether or not these variables of interest were correlated, and which variables impacted HRV. These preliminary results indicate that cognitive reappraisal predicts resting HRV above and beyond
Acknowledgement
Ru Ying Cai acknowledges the financial support of the Cooperative Research Centre for Living with Autism (Autism CRC), established and supported under the Australian Government's Cooperative Research Centers Program. We would like to thank all those who participated in Ru's PhD study. We would also like to thank Dr. Emma Baker for coding the ADOS-2 videos as well as Dr. James Heathers and Dr. Mika Tarvainen on their advice on HRV and Kubios, respectively.
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2021, Research in Developmental DisabilitiesCitation Excerpt :Beyond comparison of HRV between individuals with and without ASD, past investigations reported a controversial association between a resting autonomic modulation impairment and the gravity of ASD symptoms. Cai, Richdale, Dissanayake, and Uljarević (2018)) reported a significant correlation between HRV linear indices and ASD symptoms, otherwise, Lory, Kadlaskar, Keehn, Francis, and Keehn (2020)) reported no significant correlation between those two variables. These results doubt the real relationship between resting HRV and symptoms severity in ASD.
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2021, Neuroscience and Biobehavioral ReviewsCitation Excerpt :This is important to consider in a population where autistic individuals’ emotional experiences can sometimes be hard for parents to observe. On the other hand, four studies did not find any links between symptoms of anxiety and HRV (Cai et al., 2019; Edmiston et al., 2016; Klusek et al., 2013; Mathewson et al., 2011). Edmiston et al. (2016) reported that reduced RSA was associated with higher symptoms of depression in their autistic group; and similarly, Neuhaus et al. (2014) found a relationship between higher baseline RSA and lower internalizing symptoms.
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2020, International Journal of PsychophysiologyCitation Excerpt :Many studies have found that children with ASD show reduced RSA compared to their typically-developing (TD) peers (e.g., Bal et al., 2010; Ming et al., 2005; Neuhaus et al., 2014), and in ASD, greater RSA at baseline is associated with better emotion recognition (Bal et al., 2010), as well as better social skills (Van Hecke et al., 2009). Van Hecke et al. (2009) and Neuhaus et al. (2014) both found associations between RSA and social skills when looking at combined samples of children with and without ASD as well, and similarly, Cai et al. (2019) showed that higher baseline RSA was associated with fewer autistic traits in a combined sample of adults with and without ASD. In contrast, work with children by Klusek et al. (2013) found that higher RSA was related to lower autism symptom severity in the TD group only, with no relation found in the ASD group.
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Declarations of interest: none.
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.