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. Author manuscript; available in PMC: 2021 Jul 1.
Published in final edited form as: J Abnorm Child Psychol. 2020 Jul;48(7):923–933. doi: 10.1007/s10802-020-00651-6

Physiological Correlates of Sluggish Cognitive Tempo in Children: Examining Autonomic Nervous System Reactivity During Social and Cognitive Stressor Tasks

Stephen P Becker 1,2, Julia D McQuade 3
PMCID: PMC7306431  NIHMSID: NIHMS1587239  PMID: 32328864

Abstract

It is important to establish correlates of sluggish cognitive tempo (SCT) across units of analysis and to better understand how SCT may be conceptualized in models of psychopathology. The current study examined SCT symptoms in relation to automatic nervous system reactivity during social and cognitive stressor tasks. Participants were 61 children ages 8–12 years with a full range of attention-deficit/hyperactivity disorder (ADHD) symptom severity. Parents provided ratings of SCT and parents and teachers completed measures that were used to create composite indices of ADHD symptoms. Children were administered standardized peer rejection and impossible puzzle tasks, during which their respiratory sinus arrhythmia (RSA) and skin conductance level (SCL) reactivity were recorded. Regression analyses indicated that SCT symptoms were unassociated with RSA reactivity to either task. Greater SCT symptoms were significantly associated with greater SCL reactivity to peer rejection. Greater SCT symptoms were not significantly associated with SCL reactivity to the impossible puzzle task. The pattern of findings was unchanged in sensitivity analyses that controlled for ADHD symptoms, internalizing symptoms, medication status, or sex. This study provides the first evidence that SCT symptoms are associated with sympathetic nervous system reactivity. These findings suggest that SCT symptoms may be associated with greater behavioral inhibition system activation, and reactivity may be especially pronounced in social challenges.

Keywords: sluggish cognitive tempo, sympathetic nervous system, electrodermal activity, parasympathetic nervous system, respiratory sinus arrhythmia, skin conductance level

A growing body of evidence supports the internal and external validity of sluggish cognitive tempo (SCT), a set of behavioral symptoms characterized by slowed behavior/thinking, mental confusion and fogginess, staring, and excessive daydreaming (Barkley, 2014; Becker, Leopold, et al., 2016; Becker, Marshall, & McBurnett, 2014). However, there is a need for research examining SCT in relation to measures across units of analysis that can help advance theoretical models of SCT (Becker & Willcutt, 2019). Studies examining physiological regulation are especially needed since they may inform conceptualizations of SCT. Indeed, SCT has sometimes been conceptualized as resulting from suboptimal arousal, and individuals high in SCT symptoms tend to be characterized by emotion dysregulation, behavioral inhibition, and social withdrawal (Barkley, 2014; Becker & Willcutt, 2019). Measures of autonomic nervous system reactivity to stress have shown promise as biological indicators of arousal, emotion regulation and reactivity (Graziano & Derefinko, 2013; McQuade & Breaux, 2017b; Ortiz & Raine, 2004). Yet no study has examined whether SCT symptoms are associated with a unique pattern of physiological reactivity to stress. Accordingly, the current study provides an initial examination of children’s SCT symptoms in relation to autonomic nervous system reactivity, including both respiratory sinus arrhythmia and skin conductance level reactivity, during standardized social and cognitive stressor tasks.

Autonomic Nervous System Reactivity and Possible Associations with SCT

The autonomic nervous system includes the sympathetic nervous system (SNS) and the parasympathetic nervous system (PNS) branches. The SNS is activated during times of stress and is involved in “fight or flight” functions, whereas the PNS maintains homeostasis and is involved in “rest and digest” functions (Porges, 2007). Typically, stressful or threatening situations lead to an increase in SNS activity and/or a decrease in PNS activity. Polyvagal theory proposes that these physiological changes facilitate the mobilization of biological resources that can support effective emotional regulation, attention, and coping with environmental demands (Porges, 2001, 2003, 2007). However, the SNS and PNS branches do not always operate in a reciprocal manner, highlighting the importance of examining reactivity in both branches of the autonomic nervous system (Berntson, Cacioppo, & Quigley, 1991). Although there are several indicators of SNS and PNS functioning, changes in respiratory sinus arrhythmia (RSA) and skin conductance level (SCL) may have particular relevance in understanding SCT.

RSA is one of the most common measures of PNS influence and is an indicator of heart rate variability that reflects vagal input on the heart. A decrease in RSA corresponds to a decrease in vagal influence and is akin to taking one’s foot off the break, resulting in an increase in heart rate and the efficient mobilization of biological resources. Thus a decrease in RSA, termed RSA withdrawal, indicates an increase in physiological arousal. There is long-standing interest in whether RSA reactivity during emotion-induction or stressor tasks is associated with symptoms of psychopathology. Among children, meta-analytic results suggest that RSA withdrawal to stress or challenge is associated with lower levels of both internalizing and externalizing problems in children (Graziano & Derefinko, 2013). In contrast, a more recent meta-analysis of adult studies found that RSA withdrawal was associated with greater externalizing behaviors but was unrelated to internalizing symptoms (Beauchaine et al., 2019). SCT symptoms are strongly associated with internalizing symptoms (Becker, Leopold, et al., 2016), and there is growing evidence that SCT may be best conceptualized within the internalizing spectrum of psychopathology (Becker & Willcutt, 2019; Lee, Burns, Beauchaine, & Becker, 2016). Accordingly, particularly among children (Graziano & Derefinko, 2013), SCT symptoms may be associated with blunted RSA withdrawal.

SCL is a common measure of SNS arousal, reflecting the activity of the sweat glands. When the SNS is activated, increases in threat or stress result in the filling of the eccrine sweat glands; thus SCL, or electrodermal activity, is often used as a method for assessing SNS activation (Fowles, 1986; Fox, Hane, & Pérez- Edgar, 2015). SCL is a particularly useful indicator of SNS arousal because electrodermal activity receives no input from the parasympathetic system (Fowles, 1980, 1986). Seminal work by Fowles (1980, 1988) used Gray’s (1970, 1976) motivational theory to propose that greater SCL reactivity reflects activation of the behavioral inhibition system (see also Beauchaine, 2001). In support of this interpretation, Fowles and colleagues (Fowles, Kochanska, & Murray, 2000) found that greater skin conductance lability was associated with both fearfulness and effortful (inhibitory) control, two dimensions of temperament that are also components of the behavioral inhibition system. In another study, typically developing children had the expected increase in SCL response to the removal of reward, suggesting behavioral inhibition system activation, whereas the absence of this response in children with ADHD indicated a weak behavioral inhibition system (Iaboni, Douglas, & Ditto, 1997). In contrast, children displaying low SCL reactivity are believed to be more fearless (Fowles et al., 2000; Ortiz & Raine, 2004), as children with externalizing behaviors (conduct problems, aggression) show decreased SCL (Herpertz et al., 2001; Posthumus, Bocker, Raaijmakers, Van Engeland, & Matthys, 2009). Given evidence that SCT symptoms are uniquely associated with lower externalizing behaviors (Becker & Barkley, 2018) and higher behavioral ratings of behavioral inhibition system sensitivity (Becker et al., 2013; Becker, Schmitt, et al., 2018), it may be expected that children higher in SCT symptoms will show exaggerated SCL reactivity in the context of stress.

No study to date has examined SCT symptoms in relation to RSA or SCL reactivity. However, Yung et al. (Yung, Lai, Chan, Ng, & Chan, 2020) used a school-based sample of 30 children (ages 6–12 years) and examined several other measures of PNS and SNS reactivity while children completed an experimental warning signal paradigm. The researchers found that SCT symptoms were not associated with their indicators of PNS reactivity but were associated specifically with a measure of SNS functioning (the standard deviation of the Poincaré plot perpendicular along the line of identity). Specifically, they found that children higher in SCT symptoms showed greater SNS reactivity to the warning signals. Although such results provide promising preliminary evidence that SCT symptoms may relate to differences in autonomic nervous system reactivity, the sample was small and comprised of children without any psychiatric diagnosis or clinical elevations, limiting conclusions that can be drawn. In addition, the meaning of SNS and PNS reactivity measures is context specific. Thus, additional studies are needed to understand whether SCT symptoms are associated with different patterns of autonomic nervous system reactivity across contexts. In the present study we examined the association between SCT symptoms and children’s autonomic nervous system reactivity to two standardized stressor tasks, one social and the other cognitive. These are domains that children high in SCT symptoms are likely to struggle in and for which understanding patterns of reactivity may be particularly illuminating.

Autonomic Nervous System Reactivity: The Importance of Context

Mounting evidence suggests that patterns of autonomic nervous system reactivity are likely to differ across situations and contexts (Fox et al., 2015; Obradović & Boyce, 2012). Indeed, a key direction for physiological research is “whether youth would show the same patterns of autonomic nervous system reactivity across different tasks” (Buss, Jaffee, Wadsworth, & Kliewer, 2018), p. 1603). In addition, tasks that are emotionally negative or challenging are especially likely to inform questions related to emotional reactivity and regulation (Porges, 2001). We therefore examined SCT symptoms in relation to two tasks that are each likely to be experienced as negative – a social stressor task (peer rejection task) and a cognitive stressor task (impossible puzzles task). Although both tasks evoked standardized negative experiences, they also are crucially distinct given their differential recruitment of processes in socially and cognitively demanding situations. This is an important consideration for SCT specifically, which has been linked to distinct correlates in both social situations (e.g., withdrawal; Becker, Garner, Tamm, Antonini, & Epstein, 2019; Willcutt et al., 2014) and academic situations (e.g., low motivation; Smith, Breaux, Green, & Langberg, 2019). Given the different demands of social and academic tasks, it is possible that SCT will also be differentially associated with autonomic nervous system reactivity across social and cognitive stressor tasks.

Current Study

This is the first study to examine SCT symptoms in relation to physiological reactivity during negatively valanced stress tasks. Specifically, we examined SCT symptoms in relation to RSA and SCL reactivity to peer rejection and impossible puzzles tasks in a sample of youth with a full range of ADHD symptomatology. Previous analyses with this sample found ADHD symptoms were associated with blunted RSA withdrawal in response to a peer rejection task, whereas internalizing symptoms were associated with greater SCL reactivity in response to the peer rejection task (McQuade & Breaux, 2017a). Thus, the present study allows us to compare how associations with SCT are similar or dissimilar to those for ADHD and internalizing symptoms. We hypothesized that SCT symptoms would be associated with blunted RSA withdrawal and higher SCL reactivity to social and cognitive stressor tasks. Finally, as a robust test of identified associations, sensitivity analyses were conducted to evaluate whether associations between SCT and physiological reactivity remained when controlling for ADHD symptoms, internalizing symptoms, medication status, or sex.

Methods

Participants

Participants were 61 children, ages 8 to 12 years (M = 10.67; SD = 1.28; 52.5% female, 47.5% male) with and without clinically significant ADHD symptoms. Participants were drawn from a larger study (N = 124) examining social functioning in youth with and without ADHD. As part of the larger study, all child participants completed an assessment of ADHD that included a structured and semi-structured clinical interview with the parent and symptom and broadband rating scales collected from parents and teachers (see McQuade, Breaux, Miller, & Mathias, 2017). To maximize the variability in ADHD symptoms, children meeting full DSM-5 criteria for ADHD, children with subthreshold clinical elevations in ADHD, and children without clinically significant ADHD were included in the larger study. Children were excluded from the larger study if parents reported on the initial phone screen or semi-structured clinical interview that the child had a history of autism spectrum disorder, bipolar disorder, or a neurologic condition; had an estimated IQ below 80 based on the Kaufman Brief Intelligence Test, Second Edition (Kaufman & Kaufman, 2004); or there was diagnostic uncertainty regarding ADHD status. Approximately one year later, a subset of these participants were invited to participate in a second study examining children’s emotion regulation capacities. Due to the primary aims of the second study (see McQuade & Breaux, 2017a), children with clinical elevations in ADHD symptoms were only re-contacted for the second study if they displayed three or more hyperactive-impulsive symptoms. In addition, only families who provided contact information for participation in future research were re-contacted and invited to participate. This resulted in 101 eligible children, with 61 participating.

Based on the initial assessment of ADHD completed one year earlier, 23 children (38%) met DSM-5 criteria for ADHD, seven children (11%) were classified as subthreshold ADHD (demonstrating at least four symptoms of inattention and/or hyperactivity-impulsivity in addition to cross-domain impairment), and 31 were classified as typically developing (51%). Among the children with ADHD, 13 met criteria for ADHD combined presentation (ten male, three female), eight met criteria for ADHD predominantly inattentive presentation (four male, four female), and two met criteria for ADHD predominantly hyperactive-impulsive presentation (one male, one female). The sample was 85% White, 5% Asian, and 7% other or multi-racial; 8% identified as Hispanic or Latinx. The median household income was $100,000, the average parent education level was 16 years (SD = 1.28), and 77% of parents were married or cohabiting. Children who participated in the second study did not significantly differ from those not included in the second study on demographic characteristics or initial SCT symptom levels.

Procedures

The study was approved by the Amherst College institutional review board; parents provided consent and children provided assent to participate. Data for the present study were collected during two laboratory visits that occurred within a one-month period (M = 4 days). At the first study visit parents completed rating scale measures of the child’s symptoms and functioning. At the second study visit children completed a cognitive and social failure task in counterbalanced order while their autonomic nervous system arousal was assessed (described below). Teachers were invited to complete ratings scales through an online survey. To minimize medication effects, participants taking stimulants (n = 10) discontinued medication on both study visit days; however, three participants taking selective serotonin reuptake inhibitors remained on their medication during the assessments. Families were compensated $100 for participation and teachers were compensated $25 for participating.

Measures

SCT symptoms.

Children’s SCT symptoms were assessed based on parent report on the SCT subscale on the Child Behavior Checklist (CBCL) (Achenbach & Rescorla, 2001). The CBCL is a broadband rating scale assessing children’s disruptive behavior, emotional problems, and competencies. Parents rated how true each item was on a 0 (not true) to 2 (very true or often true) scale. The CBCL SCT scale is a frequently-used measure of SCT (Bauermeister, Barkley, Bauermeister, Martinez, & McBurnett, 2012; Becker & Langberg, 2013; Becker, Withrow, et al., 2016; Garner et al., 2017; Ward et al., 2019), correlates strongly with longer measures of SCT (Skirbekk, Hansen, Oerbeck, & Kristensen, 2011), and demonstrates distinction from CBCL-assessed ADHD and internalizing scales (Becker, Luebbe, Fite, Stoppelbein, & Greening, 2014). As in previous studies, the SCT subscale items were: confused or seems to be in a fog, daydreams or gets lost in his/her thoughts, stares blankly, and underactive, slow moving, or lacks energy. Items were summed to create a subscale score (α = .75).

Autonomic nervous system reactivity.

Children’s RSA and SCL reactivity was assessed in response to two failure tasks completed in counterbalanced order: an impossible puzzle task and a peer rejection task. The sequence and timing of measurements is depicted in Figure 1. Prior to the introduction of each task, children were told to sit quietly and relax while waiting to start the next activity, during which time they viewed a silent video of fish swimming as a 3 min baseline was collected. After each task, participants completed post-task performance evaluation questions as a manipulation check. In order to further minimize continued physiological arousal after children completed the first stressor task, the task was followed by an additional 3 min period of rest. Children were then provided with an external excuse for why the task was challenging (i.e., due to a research assistant mistake) and then completed a 3 min distractor task. This was followed by the second baseline and then the introduction of the second failure task. The time between the completion of the first task and the second baseline was an average of 10 min. After completion of both tasks, children were debriefed with a parent present.

Figure 1.

Figure 1.

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Flow diagram of tasks completed during assessment of children’s autonomic nervous system reactivity. Peer rejection and impossible puzzle tasks were completed in counterbalanced order across participants.

The impossible puzzle task was modified from prior research (Hoza, Pelham, Waschbusch, Kipp, & Owens, 2001). Participants were presented with three letter matrix puzzles on a laptop computer, one at a time, and instructed to find three nonsense words hidden in the puzzle. However, in reality only the first word in the first puzzle was actually hidden in the word matrix; the remaining eight words were impossible to find. For each puzzle, children were given 2 min to find the words and were given verbal feedback about the number of words found at the end of the 2 min. Children’s RSA and SCL arousal were specifically measured while they attempted to solve the last two puzzles, when all words were impossible to find (4.0 min). A manipulation check indicated that on average children rated the puzzles as “quite a bit hard” and reported that they found “hardly any words.” Participants also reported significant increases in anger and sadness from pre- to post-task (see McQuade, Penzel, Silk, & Lee, 2017) for additional details regarding the task).

The peer rejection task was modified from prior research (Silk et al., 2012). In this task, children were told that they would be chatting with unknown peers through an online chat program. In reality, the chat task was programmed and the peers were fictitious. After creating a profile that included a photograph and a brief list of interests/hobbies, participants were matched with two age and gender-matched “virtual” peers. In an initial choosing round, each peer chose who they would like to chat with about 15 different topics and a large X appeared on the photograph of the peer that was not chosen. The task was programmed so that the two virtual peers made their choices first, and in each round, the participant was chosen for only 20% of the topics. Children’s RSA and SCL arousal were recorded while the virtual peers made their choices and the participant was repeatedly not chosen (4.5 min). A manipulation check indicated that children on average reported that the other peers liked them “just a little” and that they were chosen “not very often” Participants reported significant increases in anger and sadness from pre- to post-task (see McQuade, Penzel, et al., 2017) for additional details regarding the task).

Children’s RSA and SCL arousal were recorded using an ambulatory physiology system (Biolog UFI 3991). Children were instructed to remain seated with both feet on the floor and their hand resting on their lap; the research assistant remained in the room with the child and prompted them if they did not follow these instructions. RSA was assessed using an EKG (1000 Hz sampling rate) with electrodes placed on the left rib cage and sternum and a ground lead placed on the right rib cage. Interbeat intervals (IBI) between successive R waves of the electrocardiogram were measured in milliseconds. The time-domain Porges-Bohrer method was used to quantify RSA (Lewis, Furman, McCool, & Porges, 2012). To calculate RSA, IBIs were first extracted and movement or measurement artifacts were edited using CardioEdit software (Brain-Body Center, 2007). CardioBatch software (Brain-Body Center, 2007) was then used to calculate RSA using the Porges-Bohrer method (Porges, 1985). The Porges-Bohrer method has two steps. First, the method removes slow aperiodic trends in the heart rate time series using a moving polynomial filter. Functionally, this ‘pre-stations’ or makes the time series stationary to ensure that the ‘filtered’ data are not contaminated with variance from sources at frequencies slower than breathing. Since there are no sources of variance in the heart rate time series at frequencies faster than breathing, setting the highest end above actual breathing frequencies does not create a vulnerability to noise. Second, the method calculates the variance within the band of frequencies in which spontaneous breathing will occur based on knowledge of age and physical demands (e.g., greater metabolic demands will be associated with faster breathing). Given the age range and activity for these participants, a wider range of spontaneous respiration (0.12 to 1.00 Hz) was used for all data.

Amplitude of RSA was calculated based on the natural logarithm of the variances of 30-second IBI epochs, which were averaged. RSA is reported in ln(ms)2 units. The Porges-Boher method for measuring RSA is statistically equivalent to frequency domain methods (i.e., spectral analysis) when heart period data are stationary (Denver, Reed, & Porges, 2007; Porges & Byrne, 1992). SCL was measured with two Ag/AgCl electrodes attached to the palmer surface of the middle phalanges of the second and third fingers of the participant’s non-dominant hand. Prior to attaching electrodes, participants washed and dried their hands and an isotonic NaCl electrolyte gel was placed on the electrodes to increase conduction. SCL was calculated based on the average electrical conductance in microsiemens.

RSA reactivity (RSA-R) and SCL reactivity (SCL-R) during each task were calculated as the difference between child’s average baseline arousal in the baseline directly prior to the task and their average arousal during the task (reactivity = task arousal – baseline arousal). Positive RSA-R values indicate an increase in PNS activity (RSA augmentation) and negative values indicate a decrease in PNS activity (RSA withdrawal). Positive SCL-R values indicate an increase in SNS activity whereas negative values indicate a decrease in SNS activity.

ADHD symptoms.

Children’s ADHD symptoms, considered in sensitivity analyses, were assessed based on the Disruptive Behavior Disorder Rating Scale (DBD) (Pelham, Gnagy, Greenslade, & Milich, 1992). A parent and a primary teacher each rated how often the child displayed the DSM-IV symptoms of ADHD on a 0 (not at all) to 3 (very much) scale. Symptoms endorsed as pretty much (2) or very much (3) present by either the parent or teacher were counted as endorsed symptoms and a total symptom count was computed (α = .96). Ratings were based on children’s unmedicated behavior; however, teacher ratings for four children were based on medicated behavior because the teacher had not observed the child off of medication.

Internalizing symptoms.

Children’s internalizing symptoms, considered in sensitivity analyses, were assessed based on parent report on the CBCL (Achenbach & Rescorla, 2001). The internalizing problems subscale includes items describing anxious behavior, depressed mood, and somatic complaints. A raw subscale score based on a sum of 32 items was used (α = .92).

Data Analytic Plan

First, Pearson correlation analyses were conducted among the primary study variables, including biserial correlations when examining the association between a dichotomous and continuous variable (given the sample size and distribution, race was dichotomized as White and non-White). A correlation of 0.10 is considered a small effect, 0.30 is considered a medium effect, and 0.50 is considered a large effect (Cohen, Cohen, West, & Aiken, 2003). Next, regression analyses were conducted in Mplus version 8 (Muthén & Muthén, 1998–2018). Specifically, the association between SCT symptoms and each of the physiological measures was tested (RSA-R and SCL-R to the peer rejection and impossible puzzle task). Given evidence that baseline physiological arousal is systematically related to reactivity (Graziano & Derefinko, 2013), baseline arousal prior to the task was included as a covariate along with significantly correlated demographic variables. Maximum likelihood robust estimator was used to address missing data1 and variable skew. Significance was interpreted based on unstandardized coefficients, with standardized coefficients reported for interpretation. Finally, sensitivity analyses were conducted to examine if significant effects remained when including ADHD symptoms, internalizing symptoms, medication status, or sex as an additional predictor.

Results

Descriptive Statistics and Preliminary Analyses

Descriptive statistics and correlations of primary study variables are presented in Table 1. Paired t-tests indicated that on average, children demonstrated a significant decrease in RSA from baseline to task in both the peer rejection task, t(53) = 2.02, p = .049, d = .28, and the impossible puzzle task, t(54) = 5.46, p < .001, d = .75. On average, children also demonstrated a significant increase in SCL from baseline to task for both the peer rejection task, t(58) = −7.16, p < .001, d = 1.19, and the impossible puzzle task, t(58) = −7.16, p < .001, d = .93. Thus, the typical response was to show an increase in physiological arousal, reflected in PNS withdrawal and SNS activation. Paired t-tests comparing reactivity to the peer rejection and impossible puzzle task indicated that there was not a significant difference in RSA-R, t(50) = 1.46, p = 1.51, d = .20, or SCL-R, t(58) = − .06, p = .956, d = .01, across the two tasks.

Table 1.

Descriptive Statistics and Correlations among Primary Study Variables

Mean SD Min Max 2 3 4 5 6 7 8 9
1. SCT 1.36 1.72 0 7 −.01 −.11 .16 −.12 .37** .18 −.22 .07
2. Peer Rejection SCL Baseline 8.09 5.83 .13 25.96 – .00 .55*** −.01 .15 −.08 .57*** −.11
3. Peer Rejection RSA Baseline 7.46 1.20 3.49 10.41 – −.07 .85*** −.23+ −.53*** .05 −.18
4. Impossible Puzzles SCL Baseline 7.49 5.03 .48 23.63 – −.14 .63*** −.14 −.01 −.01
5. Impossible Puzzles RSA Baseline 7.49 1.02 4.46 9.18 – −.27* −.30* .12 −.39**
6. Peer Rejection SCL-R 2.42 2.03 −0.22 8.19 – −.06 −.07 −.10
7. Peer Rejection RSA-R −0.23 0.83I −2.66 1.13 – −.11 .21
8. Impossible Puzzles SCL-R 2.45 2.63 −2.36 10.96 – −.29*
9. ImpossiblePuzzles RSA-R −0.41 0.55 −1.45 1.13 –
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Note. RSA reactivity (RSA-R) and SCL reactivity (SCL-R) during each task were calculated as the difference between child’s average baseline arousal in the baseline directly prior to the task and their average arousal during the task (reactivity = task arousal – baseline arousal). SCT = sluggish cognitive tempo; SCL-R = skin conductance reactivity; RSA-R = respiratory sinus arrhythmia reactivity.

+

p < .10;

*

p < .05;

**

p < .01;

***

p < .001.

Preliminary analyses examined the correlation between dependent variables and demographic variables (child age, sex, non-White status, non-Hispanic/Latinx status, household income, and parent education). Younger child age was significantly correlated with greater SCL-R to peer rejection (r = −.36, p = .005); no other significant correlations emerged (all ps > .05). Preliminary analyses also examined whether there were systematic differences in SCT symptoms based on demographic. SCT symptoms did not significantly differ based on child age, sex, non-white status, non-Hispanic/Latinx status, household income, or parent education (all ps > .05). Stimulant medication status was significantly associated with SCT symptoms (r = .27, p = .036) and with greater RSA-R during the puzzle task only (r = .30, p = .02). SSRI medication status was significantly associated with SCT symptoms (r = .26, p = .041) but was not significantly associated with reactivity measures (all ps > .05).

Primary Analyses

As reported in Table 1, above and beyond baseline arousal and child age, greater SCT symptoms were significantly associated with greater SCL-R to peer rejection suggesting children with more SCT symptoms tended to show greater SNS activation to peer rejection. SCT symptoms explained 10% of the variability in SCL-R to peer rejection (ΔR2 = .10). In contrast, controlling for baseline arousal, SCT symptoms were not significantly associated with SCL-R during the puzzle task (ΔR2 = .05).

Controlling for baseline arousal, SCT symptoms were not significantly associated with RSA-R to peer rejection (ΔR2 = .02). Likewise, controlling for baseline arousal, SCT symptoms were not significantly associated with RSA-R during the puzzles task (ΔR2 = .00).

Sensitivity Analyses

Follow-up tests of robustness examined if significant effects remained when controlling for children’s ADHD symptoms or internalizing problems. The significant effect of SCT on SCL-R to peer rejection remained significant when controlling for ADHD symptoms, b = .43, SE = .15, p = .004, and when controlling for internalizing symptoms, b = .48, SE = .15, p = .002. Importantly, although prior analyses with this sample suggested a significant association between internalizing symptoms and greater SCL-R to peer rejection (McQuade & Breaux, 2017a), when also accounting for the effect of SCT, internalizing symptoms were no longer a significant predictor of SCL-R to peer rejection, b = −.024, SE = .04, p = .525.

Analyses also examined if significant effects remained when controlling for stimulant medication and SSRI medication use. SCT symptoms remained significantly associated with SCL-R to peer rejection when accounting for medication use, b = .46, SE = .14, p = .001.

Although there were no systematic sex differences in SCT symptoms, t(59) = −.080, p = .937 (boys M ± SD = 1.38 ± 1.99, girls M ± SD = 1.34 ± 1.47), sensitivity analyses also examined if results were consistent when child sex was included in the model. The main effect of SCT on SCL-R to peer rejection remained significant when controlling for child sex, b = .40, SE = .14, p = .004.

Discussion

This study makes an important contribution to our understanding of SCT by extending research to the physiological unit of analysis. This is, to our knowledge, the first study to examine SCT symptoms in relation to both branches of the autonomic nervous system during stressor tasks. As such, findings from this study provide a first step in understanding whether – and under what context – SCT symptoms are related to physiological reactivity.

SCT and Sympathetic Nervous System Reactivity

Growing research suggests that patterns of autonomic nervous system reactivity are context-specific (Buss et al., 2018; Fox et al., 2015; Obradović & Boyce, 2012). Results from the present study underscore the task-specificity of autonomic nervous system reactivity differences, finding different associations between SCT and SCL-R to a social and cognitive stressor task. Greater SCT symptoms were associated with increased SCL-R to the social stressor task, suggesting that children with greater SCT experience greater SNS arousal in response to novel peer rejection. Of note, the association between SCT and SCL-R in response to the peer rejection task was a medium-sized effect (r = .37) and remained significant when controlling for ADHD symptoms, internalizing symptoms, medication status, or sex. Further, the association between internalizing symptoms and SCL-R to peer rejection was no longer significant when SCT symptoms were included in the model, pointing to SCT as a key clinical correlate of SNS arousal to peer rejection. Higher SCL-R in response to social stress may reflect greater emotional reactivity to peer rejection (Hubbard et al., 2002), increased anxiety, or greater activation of the behavioral inhibition system (Beauchaine, 2001; Fowles, 1980, 1988). The latter possibility fits well with the larger literature on SCT, documenting unique associations between SCT and ratings of greater behavioral inhibition system sensitivity (Becker et al., 2013; Becker, Schmitt, et al., 2018), conflicted shyness (Sáez, Servera, Becker, & Burns, 2019), and social withdrawal (Becker et al., 2019; Becker, Burns, Leopold, Olson, & Willcutt, 2018; Marshall, Evans, Eiraldi, Becker, & Power, 2014; Willcutt et al., 2014). It has been hypothesized that children with SCT find social situations to be overwhelming (Flannery, Becker, & Luebbe, 2016; Willcutt et al., 2014), and findings from the present study provide biological support to the possibility that children with SCT have a heightened, or overreactive, response to stressful social encounters. However, it is important to note that we used one specific, computerized task of peer rejection, and future studies would benefit from a broader examination of SCT in relation to physiological reactivity to social stress (e.g., dyadic and group interactions with unfamiliar peers; Trier Social Stress Test).

In contrast to findings for the peer rejection social task, SCT symptoms were unassociated with SCL-R to the impossible puzzles task. Children with SCT are characterized by amotivation and apathy (Becker, Leopold, et al., 2016), which could be reflected in low sympathetic reactivity in certain situations. Critical differences between the peer rejection task and the impossible puzzle task might also explain the different patterns of SNS reactivity found. The peer rejection task involved negative social evaluation, which children were asked to passively observe. In contrast, the impossible puzzle task involved continued unsuccessful attempts to find hidden words, asking children to cognitively engage and devote attentional resources to searching for the words. In the context of an attentionally demanding cognitive stressor, it is possible that children with elevated SCT symptoms do not show strong sympathetic reactivity. Additional studies will be needed to better understand the interrelations of SCT, physiology, and motivation during various cognitive tasks.

The divergent relations between SCT and SCL-R in response to the social and cognitive tasks also underscore the reality that, as with other psychopathologies, any search for a simple psychophysiological biomarker of SCT is likely to be unfruitful (Buss et al., 2018; Kozak & Cuthbert, 2016). A more effective approach would be to identify endophenotypes, processes, and contexts that link the SCT phenotype to biological units of analysis. Indeed, our findings pertaining to SCT and SCL-R may at first glance seem to offer a conflicting story regarding SCT and arousal; and yet, “arousal is a dimension of sensitivity to external and internal stimuli and facilitates interaction with the environment according to context” (Kozak & Cuthbert, 2016, p. 291, italics added).

SCT and Parasympathetic Nervous System Reactivity

In turning to PNS functioning, SCT symptoms were not associated with RSA-R to either stressor task used in this study. This suggests that children with elevated SCT may not demonstrate divergent patterns of PNS reactivity to social or cognitive stressors. Of note, previous analyses with this sample have reported that ADHD symptoms were associated with blunted RSA withdrawal in response to the peer rejection task (McQuade & Breaux, 2017a). It thus appears that SCT and ADHD symptoms are differently related to parasympathetic reactivity to social stress, at least as measured during the laboratory-based social task used in this study. It is important to note that the tasks used in this study were designed to be experienced as negative and stressful. Tasks that are more ambiguous or neutral, such as meeting a new peer or completing a cognitive test, may evoke different patterns of RSA-R and may also have relevance to understanding SCT (Fox et al., 2015; Hastings et al., 2008; Ward, Alarcón, Nigg, & Musser, 2015). Future studies should aim to examine SCT and RSA reactivity across different tasks and contexts, including both stressful/threatening, ambiguous, and neutral contexts.

Limitations and Future Directions

Several limitations are important to note and point to key directions for future research. The cross-sectional design does not allow for causal or temporal conclusions. We therefore cannot identify whether SCT more clearly predicts physiological reactivity or vice versa. In addition, we used laboratory tasks that strengthened internal validity but may not accurately reflect the social and cognitive challenges encountered by children in their everyday lives. In addition, the sample size was relatively small and we could not examine other factors that may be important, including sex differences and age effects. It would also be beneficial for future studies with larger samples to examine non-linear associations, as well as how SCT relates to physiological reactivity change over time during stressful situations (e.g., growth curve trajectories; see, e.g., Lambe, Craig, & Hollenstein, 2019). There are also different approaches to quantifying RSA (e.g., time-domain methods as used in the current study or frequency-domain methods such as spectral analysis), and research is needed to directly examine if physiological correlates of SCT are consistent across measurement techniques. In addition, although movement was minimal while children completed the stress tasks, we did not directly assess, or control for, child movement in analyses. Finally, we did not recruit based on SCT symptoms and used a limited measure of SCT, as SCT-specific measures with nationally representative data have only recently been developed (Barkley, 2013; Burns & Becker, 2019). Still, the CBCL SCT scale is frequently used and captures the daydreaming and underactive facets of SCT (Becker, Leopold, et al., 2016). Considered together, these limitations point to the need for additional studies with larger samples to examine SCT and physiological reactivity across a range of tasks, ideally using longitudinal designs that are able to evaluate temporal associations.

Conclusions

The current study makes a novel contribution to the growing literature on SCT in children. By examining SCT symptoms in relation to physiological reactivity across social and cognitive stressor tasks, our findings provide key initial support for an association between higher SCT symptoms and SNS reactivity. However, the nature of the relation between SCT and SNS reactivity appears to differ between social and cognitive tasks, underscoring the importance of carefully evaluating context in future studies examining physiological and other biological correlates of SCT. Future research will further advance conceptual models of SCT, as well as whether physiological reactivity predicts the course of SCT and associated impairments.

Table 2.

Sluggish Cognitive Tempo Symptoms in Relation to Autonomic Nervous System Reactivity

SCL-R Peer Rejection RSA-R Peer Rejecticon
b SE β R2 b SE β R2
0.25 0.31
Child Age −0.50* 0.19 −0.32
Baseline arousal 0.04 0.05 0.12 −0.37*** 0.09 −0.52
SCT 0.39** 0.14 0.34 0.07 0.04 0.14
SCL-R Impossible Puzzles RSA-R Impossible Puzzles
b SE β R2 b SE β R2
0.05 0.17
Baseline arousal 0.02 0.07 0.03 −0.22** 0.08 −0.41
SCT −0.34 0.18 −0.22 0.01 0.04 0.02
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Note. SCT = sluggish cognitive tempo; SCL-R = skin conductance reactivity; RSA-R = respiratory sinus arrhythmia reactivity.

*

p < .05;

**

p < .01;

***

p < .001

Acknowledgements.

Stephen Becker is supported by award number K23MH108603 from the National Institute of Mental Health (NIMH). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIMH.

Footnotes

Publisher's Disclaimer: This Author Accepted Manuscript is a PDF file of a an unedited peer-reviewed manuscript that has been accepted for publication but has not been copyedited or corrected. The official version of record that is published in the journal is kept up to date and so may therefore differ from this version.

Conflict of interests. The authors declare no potential conflicts of interest with respect to the research, authorship, or publication of this article.

1 Reactivity data on both tasks was treated as missing for one child because of extreme non-compliance during the task. Reactivity data on the social task was treated as missing for one additional subject who failed to understand the task. Due to equipment failure, RSA data was missing for four participants on the impossible puzzle task and three participants on the peer rejection task.

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