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Gepubliceerd in: Journal of Psychopathology and Behavioral Assessment 1/2024

Open Access 15-02-2024

Interaction of Resting Heart Rate with Empathy in Predicting Externalizing Behavior

Auteurs: Sofi Oskarsson, Bridget M. Bertoldi, Anneli Andersson, Rebecca Siponen, Shichun Ling, Adrian Raine, Laura Baker, Brittany Evans, Catherine Tuvblad

Gepubliceerd in: Journal of Psychopathology and Behavioral Assessment | Uitgave 1/2024

Abstract

Biopsychosocial criminological theories suggest that it is important to consider interactions between risk factors from different domains in the prediction of externalizing behavior. Lower resting heart rate is considered the best replicated biological risk factor for externalizing behavior. The psychological construct of empathy has also shown to be predictive of such behavior, but little is known about the potential interaction between these two different risk factors in predicting externalizing behavior. We examined the moderating role of empathy on the association between resting heart rate in childhood and adolescence with externalizing behavior by young adulthood using two subsets of participants from the Longitudinal Risk Factors for Antisocial Behavior project: Subsample 1 (n = 697) at ages 9–10 and 19–20 years and Subsample 2 (n = 394) at ages 14–15 and 19–20 years. Linear and logistic regressions showed that empathy moderated the association between resting heart rate in adolescence and externalizing behavior by young adulthood. Among individuals with low but not high levels of empathy, increased resting heart rate predicted lower levels of externalizing behavior. Interventions enhancing empathic skills in individuals with psychophysiological risk profiles could be beneficial.
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Supplementary Information

The online version contains supplementary material available at https://​doi.​org/​10.​1007/​s10862-024-10123-6.

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Introduction

Lower resting heart rate (RHR) is a well-established risk factor for externalizing behavior, including but not limited to criminal offending (Latvala et al., 2015; Kendler et al., 2021), substance use (Latvala et al., 2016; Kendler et al., 2021), aggression (Raine et al., 2014), psychopathy (Kavish et al., 2017), and violent and non-violent behavior (Bertoldi, Tuvblad et al., 2022b). The association between RHR and externalizing behavior was first reported in a sample of refractory adolescent boys (Davies & Maliphant, 1971). Since then, numerous scientific articles have been published showing an association between RHR and various conceptualizations of externalizing behavior. Four separate meta-analyses have all concluded that lower RHR is associated with higher levels of externalizing behavior, with effect sizes of Cohen’s d = − 0.38 (Lorber, 2004), d = − 0.44 (Ortiz & Raine, 2004), d = − 0.20 (Portnoy & Farrington, 2015), and Hedges g = − 0.17 (de Looff et al., 2022)1. In other words, lower RHR is robustly associated with an increased risk of engaging in externalizing behavior, even after adjusting for potential confounding factors such as socioeconomic status (SES), height, weight, and physical capacity (Latvala et al., 2015; Oskarsson et al., 2021). Studies have also demonstrated that RHR is associated with internalizing behavior, where a higher RHR was associated with an increased risk of for example anxiety disorders and obsessive-compulsive disorder (Latvala et al., 2016; Kendler et al., 2021). However, there are conflicting findings in the literature where RHR was unrelated to internalizing behavior (Bertoldi et al., 2022b)2. While a higher RHR may be associated with a wide range of psychiatric disorders, a lower RHR seems to be associated specifically with externalizing behavior.
RHR is regulated by the autonomic nervous system, primarily by the parasympathetic nervous system which is dominant in resting conditions (Palma et al., 2014). Although the association between RHR and externalizing behavior is well-established, the underlying reasons for this consistent association remain largely unknown. The theoretical perspectives put forth in the literature thus far, mainly centers around fearlessness theory and stimulation-seeking theory. Fearlessness theory suggest that individuals who exhibit a low RHR also exhibit low levels of fear, as externalizing behavior may require a degree of fearlessness to execute (Raine, 2002). The resting state referred to when measuring RHR is in fact a mildly stressful situation as individuals are exposed to a novel environment during psychophysiological testing. A low RHR in this situation is therefore proposed to reflect a lack of response to stressful stimuli (i.e., fearlessness). Studies have shown that RHR is not only associated with externalizing behavior but also with unintentional injuries (Latvala et al., 2015), which may reflect a fearless and uninhibited temperament. Sensation-seeking focus on low RHR as reflecting a chronic underaroused physiological state, something that is perceived as unpleasant (Quay, 1965; Beauchaine, 2012). Individuals exhibiting lower RHR thus seek out stimulation through engaging in for example externalizing behaviors to increase their levels of arousal to a more optimal and comfortable level.
A third theoretical perspective not commonly addressed in the RHR-externalizing behavior literature, is empathy (Raine, 2013). Empathy can be defined as the “tendency to apprehend another person’s condition or state of mind” (Johnson et al., 1983, p. 1299), and is important in the development of social skills and moral judgment, aspects that help us function in a complex society (Hoffman, 2000). This definition acknowledges a cognitive (i.e., the capacity to comprehend the emotional state of another person) as well as an affective (i.e., the sharing of the emotional state of another person) component. Not only has deficient empathy been described as a precursor to externalizing behavior, and especially violent behavior (Joliffe & Farrington, 2004), but previous work has also demonstrated that individuals with lower RHR were less empathic than individuals with higher RHR (Colasante & Malti, 2017; Zahn-Waxler et al., 1995).
A meta-analysis including 35 studies showed an association between lower levels of empathy and higher levels of externalizing behavior, with a mean effect size of d = − 0.28 (Joliffe & Farrington, 2004). Subdividing empathy into cognitive and affective empathy revealed a strong association between cognitive empathy and offending d = − 0.48 and a weak association between affective empathy and offending d = − 0.11. The capacity to comprehend the emotional state of another person (i.e., cognitive empathy) thus seem to be more strongly related to externalizing behavior than the sharing of the emotional state of another person (i.e., affective empathy).
Another meta-analysis including 106 effect sizes revealed an overall weak association between empathy and aggression (Pearson correlation coefficient [r] = − 0.11; Vachon, Lynam & Johnson, 2013)3. More specifically, the mean empathy-aggression correlation using a total score on the Interpersonal Reactivity Index (IRI; a common measure of empathy; Davis, 1980, 1983) and a total aggression score, was also weak, r = − .08. Nevertheless, stronger effects were reported for the associations between specific subscales of the IRI (i.e., perspective taking and empathic concern; Davis, 1980, 1983), with verbal and physical aggression (rs ranging from − 0.13 to − 0.26). The IRI is comprised of four subscales, two of which measure cognitive empathy (perspective taking, empathic fantasy) and two of which measure affective empathy (empathic concern, personal distress; Davis, 1980; 1983). However, perspective taking and empathic concern are more commonly used to conceptualize cognitive and affective empathy than the other two subscales (Joliffe & Farrington, 2004). The “empathic fantasy” subscale is rarely used in interpersonal assessments, and the “personal distress” subscale measures responses in emergency situations (Joliffe & Farrington, 2004). Results from the meta-analysis by Vachon et al. (2013) suggest that it is two specific subscales of the IRI that may be better at capturing cognitive and affective empathy and thus relates more strongly to externalizing behavior, i.e., “perspective taking” and “empathic concern”.
Despite evidence for both RHR and empathy as being associated with externalizing behavior in isolation (Joliffe & Farrington, 2004; Latvala et al., 2015), work exploring how RHR may interact with empathy in predicting externalizing behavior is limited. One prospective study, utilizing a low-income male-only community sample of 160 individuals followed from infancy and onward, examined interactive effects between RHR and a global score of empathy (Galán et al., 2017). This study found an interaction between RHR and empathy such that lower empathy predicted an increased risk for violent behavior among individuals with lower but not higher RHR. Another cross-sectional study employed a sample of 110 boys and girls to examine whether the negative association between RHR and externalizing behavior was offset by high guilt and sympathy, elements that relate to empathy (Colasante & Malti, 2017). Lower RHR was associated with higher physical aggression in children who reported low ratings of guilt and sympathy, suggesting that social emotions in children with low RHR may influence their conflict management skills.
Findings from these aforementioned studies are in line with the biosocial model of externalizing behavior (Barnes et al., 2022) or the interaction hypothesis (Raine, 2013), which suggest that when a biological risk factor is paired with a psychological or social risk factor, the risk of externalizing behavior emerge. There are several empirical examples of the biosocial model or the interaction hypothesis for externalizing behavior in the literature. For example, findings suggest that low RHR combined with a low socioeconomic status (Bertoldi et al., 2022b; Barnes et al., 2022), parental separation, low nonverbal IQ (Farrington, 1997; Barnes et al., 2022), harsh parental discipline, a depressed mother (Farrington, 2020) high troublesomeness and high dishonesty (Barnes et al., 2022), increased the risk of externalizing behavior. The interpretation from such studies suggests that externalizing behaviors are exhibited by individuals who have a combination of a biological risk factor together with a psychological or a social risk factor. Thus, it may be that all individuals with low RHR are not at risk of externalizing behavior unless this biological risk is paired with an additional psychological or social risk. This further suggest that psychological and social factors may have the potential to buffer against a biological risk factor to reduce the risk of externalizing behavior. No single risk factor can fully account for the occurrence of externalizing behavior (Barnes et al., 2016; Focquaert, 2019); rather, it is likely that a combination of multiple risk factors will interact to increase the risk for externalizing behavior (Farrington, 2020).While there is some evidence that empathy moderates the association between RHR and externalizing behavior (Galán et al., 2017; Colasante & Malti, 2017), more studies confirming this interaction are needed.
Although earlier studies have made significant contributions to the research field, further efforts are required to address methodological limitations such as small sample sizes, cross-sectional study designs, the operationalization of empathy, greater racial-ethnical diversity, and longitudinal data. Thus, the current study sought to expand upon previous findings and address some of the methodological shortcomings observed in prior research by using a sizable longitudinal sample consisting of boys and girls with psychophysiological data measured at two different time points. Our primary objective was to investigate the moderating role of empathy in the relationship between RHR in childhood and adolescence, and externalizing behavior by young adulthood. The goal of the study was to gain a better understanding of how a complex construct like empathy may intersect with the well-established association between RHR and externalizing behavior.

Methods

Participants

We utilized data from the University of Southern California (USC) Risk Factors for Antisocial Behavior (RFAB) Project (base sample N = 1,673, 51.4% female), described elsewhere (Baker et al., 2013). For the current study, we utilized two different subsamples which were based on when psychophysiological data was obtained. The first subsample (W1 subsample; n = 697, 56% female) was comprised of participants for whom RHR data was obtained during the first wave of data collection (i.e., W1) when participants were 9–10 years old. The second subsample (W3 subsample; n = 394, 59% female) was comprised of participants for whom RHR data was obtained during the third wave of data collection (i.e., W3) when participants were 13–14 years old. Studies have shown that the parasympathetic nervous system, which is responsible for regulating RHR, has a complex maturational pattern which may be attributed to hormonal changes (Harteveld et al., 2021). Thus, it may be that the measure of RHR is different during childhood as opposed to adolescence. As such, we utilized two different samples rather than combining measures of RHR over the waves, to isolate potential maturational effects. Both subsamples included the same predictor variables, covariates, and outcome variables. For a description of when data was collected for each subsample, see Table 1.
Table 1
Subsample description
  
Wave when measure obtained
  
Subsample W1
Subsample W3
Predictors
RHR
W1
W3
 
Empathy
W5
W5
Covariates
Race/ethnicity
W1
W1
 
BMI
W1
W3
Outcome
Externalizing behavior
W5
W5
 
Trouble with the police
W5
W5
Informed Consent
was obtained from the caregivers of all participants in the RFAB project at W1 and from the participants themselves at W5. The Institutional Review Board at USC approved of the project (Baker et al., 2013).

Measures

Resting Heart Rate

Resting heart rate (RHR) was collected during W1 and W3 using a 38-channel Isolated Bioelectric Amplifier manufactured by the James Long Company (1999; Caroga Lake, New York) that recorded cardiac activity onto a data acquisition computer. Disposable electrodes were attached to the participants’ ribs after cleaning the skin with alcohol wipes. Before the collection of RHR, an interviewer conversed with the participant to help the participant relax. The interviewer remained in the room with the participant for approximately 10–20 min before leaving the room to start data collection (Baker et al., 2009). The participant was instructed to relax, remain seated, and be quiet. Baseline recordings of RHR was obtained for 3 min. Data were further analyzed using the Interbeat Interval Analysis Software program (James Long Company; see Tuvblad et al., 2010 for more information). RHR was defined as beats per minute averaged across a resting period of 3 min. Participants with less than 1 min of usable data were excluded from analyses (n = 25). For a more detailed description of data cleaning and analysis, please refer to Bertoldi et al., (2022b).

Empathy

We used data from the Interpersonal Reactivity Index (IRI; Davis, 1980, 1983) collected at W5. The IRI comprises four subscales; however, considering previous research indicating associations with externalizing behavior for only two of these subscales (Vachon et al., 2013), we focused our analyses on data from these specific subscales: “perspective taking” (W1 subsample α = 0.77, W3 subsample α = 0.77) which measure cognitive empathy and “empathic concern” (W1 subsample α = 0.75, W3 subsample α = 0.76) which measure affective empathy. Davis (1983) refers to “perspective taking” as the extent to which an individual can adopt the point of view of another person and understand their thoughts and feelings, whereas “empathic concern” reflects the individual’s ability to experience feelings of compassion and concern for others who are expressing distress.
Empathy was quantified in terms of scores on these two separate scales rather than as a single omnibus score, given earlier findings suggesting that the total score may not be appropriate (Wang et al., 2020). We also did not compile subscales to form two factors: cognitive and affective empathy, as the original study did (Davis, 1980, 1983), given that later research supported a four-factor model (Chrysikou & Thompson, 2016). All items use a five-point Likert scale: Never (0), Rarely (1), Sometimes (2), Often (3), and Always (4), with a higher score indicating higher levels of empathy (Davis, 1980).

Outcome

Externalizing Behavior

Adult Self-Report
During W5, participants were administered the Adult Self-Report provided by the ASEBA, a widely used system enabling to assess problems from different domains (i.e., emotional, social, and behavioral; Achenbach & Rescorla, 2003). The high reliability and validity of the ASR has been reported elsewhere (Achenbach, 2009). Following guidelines from the ASEBA adult forms manual, each item was coded and scored on a 3-point scale (0 = not true; 1 = sometimes true; 2 = very true/often true) and summarized as a continuous score. As a next step, an externalizing behavior scale (W1 subsample α = 0.89; W3 subsample α = 0.89) was conceptualized as the sum score of the subscales: “aggressive behavior” (W1 subsample α = 0.83; W3 subsample α = 0.82), “rule-breaking behavior” (W1 subsample α = 0.82; W3 subsample α = 0.81), and “intrusive behavior” (W1 subsample α = 0.71; W3 subsample α = 0.72).
Trouble with the Police
At W5, participants completed a questionnaire focused on antisocial behavior, specifically developed for the RFAB-study. To provide an additional measure of externalizing behavior, we included a specific question regarding the participants lifetime personal history of legal issues. Participants were asked: “Have you ever been in trouble with the police?” If participants had any previous trouble with the police, this item was coded as “1”. Conversely, if they had never experienced any trouble with the police, it was coded as “0”.

Covariates

We included a measure of body mass index (BMI) as a covariate because of its potential association with RHR and ASB (Beckley et al., 2014). BMI was measured at both W1 and W3, and the measure from W1 was therefore used in the W1 subsample whereas the measure from W3 was used in the W3 subsample. Further, because Black and Hispanic individuals tend to be overpoliced compared to White individuals in the United States (Gaston, 2019), as well as previous findings suggesting that the association between RHR and externalizing behavior is racially variant (Portnoy et al., 2020), we used race/ethnicity measured at W1 as a covariate4.

Statistical Analyses

Data management and analyses were performed using R Studio version 2022.12.0 (R Studio Development Core Team, 2022). As a first step, zero-order associations were examined between RHR, the subscales of IRI, BMI, race/ethnicity, and the externalizing behavior measures. As a second step, linear regressions were used to estimate associations and 95% confidence intervals (CIs) for the continuous outcome. In each linear regression model, we entered RHR, one of the subscales from the IRI, the interaction term between RHR and the IRI subscale as predictors of the continuous measure of externalizing behavior. BMI and race/ethnicity were included as covariates in the models. This resulted in two separate models for each subsample. As a third step, logistic regressions were implemented to estimate odds ratios (ORs) and 95% confidence intervals (CIs) for the binary outcome. In each logistic regression model, we entered: RHR, one of the subscales of the IRI, and the interaction term between RHR and the same IRI-subscale as predictors of ASB. BMI and race/ethnicity were included as covariates in the models. This resulted in two separate models for each subsample. All models accounted for the independency between twins and triplets by considering the correlation between observations within clusters using a cluster robust sandwich estimator. It should be noted that associations between RHR and trouble with the police have been published earlier using a slightly different subsample from the RFAB (Bertoldi et al., 2022a). However, given analyses of moderation, the main effects could not be omitted from the results.

Results

Baseline characteristics of the two subsamples are shown in Table 2.
Table 2
Descriptive information for the W1 and the W3 subsamples
 
W1a (n = 697)
W3b (n = 394)
 
M (SD)
Min
Max
M (SD)
Min
Max
Resting heart rate
86.6 (11.0)
55.1
125.0
76.0 (11.8)
49.5
147.8
Body mass index
18.6 (3.9)
12.2
49.6
22.5 (5.2)
13.6
50.7
Interpersonal Reactivity Index (Wave 5)
      
Perspective taking
17.9 (4.4)
4.0
28.0
17.9 (4.4)
4.0
28.0
Empathic concern
20.1 (4.1)
4.0
28.0
20.4 (4.1)
4.0
28.0
Adult Self-Report
(Wave 5)
      
Externalizing behavior
10.0 (8.3)
0.0
70.0
10.4 (8.3)
0.0
42.0
Trouble with the police (Wave 5)
      
Yes
130 (19)
  
67 (17)
  
No
567 (81)
  
327 (83)
  
a Participants were aged 9–10 years at W1
b Participants were aged 13–14 years at W3
Table 3 displays zero-order associations for the W1 subsample between RHR, BMI, the two subscales of IRI, and externalizing behavior measures. RHR was negatively related to the outcome measures: externalizing behavior scale, r = − .10, p < .01 and ever having been in trouble with the police, r = − .15, p < .001. RHR was positively associated with perspective taking, r = .09, p < .05 and empathic concern, r = .11, p < .05. Perspective taking was negatively associated with the externalizing behavior scale, r = − .22, p < .001, and ever having been in trouble with the police, r = − .12, p < .01. Empathic concern was negatively associated with the externalizing behavior scale, r = − .14, p < .001 and ever having been in trouble with the police, r = − .10, p < .01.
Table 3
Zero-order associations between predictors, covariates, and outcomes for the W1 subsample (n = 697)
 
RHR
BMI
IRI PT
IRI EC
Ext
TWP
RHR
-
     
BMI
0.01
-
    
IRI PT
0.09*
− 0.02
-
   
IRI EC
0.11**
− 0.02
0.57***
-
  
Ext
− 0.10**
− 0.08*
− 0.22***
− 0.14***
-
 
TWP
− 0.15***
0.08
− 0.12**
− 0.10**
0.28***
-
Abbreviations Resting heart rate (RHR), body mass index (BMI), Interpersonal Reactivity Index Perspective Taking (IRI PT), Interpersonal Reactivity Index Empathic Concern (IRI EC), Externalizing Behavior (Ext), Trouble with the Police (TWP)
* 0.05, ** 0.01, *** 0.001
Table 4 displays zero-order associations for the W3 subsample between RHR, BMI, the two subscales of IRI, and externalizing behavior measures. RHR was negatively related to the outcome measures: externalizing behavior and trouble with the police, although the associations did not reach statistical significance (r = − .09 & − 0.07, ps = ns). RHR was positively associated with perspective taking and empathic concern, although associations did not reach statistical significance (r = .01 & 0.03, ps = ns). Perspective taking was negatively associated with the externalizing behavior scale, r = − .20, p < .001, and ever having been in trouble with the police, although this association was not statistically significant (r = − .07, p = ns). Empathic concern was negatively associated with both the externalizing behavior scale, r = − .15, p < .001, and with ever having been in trouble with the police, r = − .11, p < .05.
Table 4
Zero-order associations between predictors, covariates, and outcomes for the W3 subsample (n = 394)
 
RHR
BMI
IRI PT
IRI EC
Ext
TWP
RHR
-
     
BMI
0.01
-
    
IRI PT
0.01
− 0.01
-
   
IRI EC
0.03
− 0.01
0.60***
-
  
Ext
− 0.09
0.15**
− 0.20***
− 0.15***
-
 
TWP
− 0.07
0.04
− 0.07
− 0.11*
0.25***
-
Abbreviations Resting heart rate (RHR), body mass index (BMI), Interpersonal Reactivity Index Perspective Taking (IRI PT), Interpersonal Reactivity Index Empathic Concern (IRI EC), Externalizing Behavior (Ext), Trouble with the Police (TWP)
* 0.05, ** 0.01, *** 0.001

Interaction of RHR and Empathy in Predicting the Externalizing Behavior Scale

W1 Subsample

All models tested for interactive effects of RHR and the two subscales of IRI in the prediction of externalizing behavior measured with ASR while adjusting for race/ethnicity and BMI (see Table 5). No interaction effects were evident between any of the two IRI subscales and RHR in the prediction of externalizing behavior, ps < 0.05. Several main effects were evident. All models showed that a RHR was negatively associated with externalizing behavior (e.g., Est. = − 0.12, 95% CI = − 0.27, − 0.07, p < .05, all estimates are reported in Table 5), such that higher RHR predicted lower levels of externalizing behavior. A main effect was also evident for perspective taking (Est. = − 0.28, 95% CI = − 0.38, − 0.18, p < .001), such that higher levels of perspective taking predicted lower levels of externalizing behavior. Lastly, a main effect was also evident for empathic concern (Est. = − 0.17, 95% CI = − 0.27, − 0.07, p < .001), such that higher levels of perspective taking predicted lower levels of externalizing behavior.
Table 5
Linear regression results for the W1 subsample: RHR and empathy interaction with ASR Externalizing behavior as the outcome
Outcome
Predictors
Estimate
SE
95% CI
p-value
Externalizing behavior
RHR * IRI PT
− 0.01
0.05
− 0.11, 0.09
0.817
 
RHR
− 0.11
0.05
− 0.21, − 0.02
0.023
 
IRI PT
− 0.28
0.05
− 0.38, − 0.18
< 0.001
 
RHR * IRI EC
0.04
0.05
− 0.07, 0.14
0.467
 
RHR
− 0.12
0.05
− 0.22, − 0.02
0.018
 
IRI EC
− 0.17
0.05
− 0.27. − 0.07
< 0.001
Note n = 697, bold values are significant at an alpha level of .05
Abbreviations Resting heart rate (RHR), body mass index (BMI), Interpersonal Reactivity Index Perspective Taking (IRI PT), Interpersonal Reactivity Index Empathic Concern (IRI EC), Adult Self-Report (ASR), Wave 1 (W1)
* Estimates were adjusted for BMI, race/ethnicity, and sex

W3 Subsample

All models tested for interactive effects of RHR and the two subscales of IRI in the prediction of externalizing behavior measured with ASR while adjusting for race/ethnicity and BMI (see Table 6). In the model testing for interactive effects between the perspective taking subscale of IRI and RHR in predicting externalizing behavior, we found a moderating effect of perspective taking. To characterize the nature of the interaction effect, we probed the association between RHR and externalizing behavior at low (− 1SD) and high (+ 1 SD) perspective taking. Whereas no significant effect of RHR was observed at 1 SD above the mean of perspective taking (Est. = 0.10, 95% CI = − 0.11, 0.31, p = ns), a significant effect of RHR was evident at 1 SD below the mean of perspective taking (Est. = − 0.31, 95% CI = − 0.49, − 0.13, p < .001). Thus, at low levels of perspective taking, a 1 SD increase in RHR predicted a 0.31 unit decrease in externalizing behavior, see Fig. 1.
Table 6
Logistic regression results for the W1 subsample: RHR and empathy interaction with trouble with the police as the outcome
Outcome
Predictors
Adj OR*
95% CI
p-value
Trouble with the police
RHR* IRI PT
0.97
0.78, 1.19
0.752
 
RHR
0.66
0.53, 0.81
< 0.001
 
IRI PT
0.76
0.62, 0.93
0.009
 
RHR * IRI EC
0.90
0.72, 1.12
0.360
 
RHR
0.65
0.52, 0.80
< 0.001
 
IRI EC
0.79
0.64, 0.97
0.025
Note n = 697, bold values are significant at an alpha level of .05
Abbreviations Resting heart rate (RHR), body mass index (BMI), Interpersonal Reactivity Index Perspective Taking (IRI PT), Interpersonal Reactivity Index Empathic Concern (IRI EC), Wave 1 (W1)
* ORs were adjusted for BMI, race/ethnicity, and sex
A main effect was evident for RHR (Est. = − 0.14, 95% CI = − 0.271, − 0.001 p < .05), such that higher levels of RHR predicted lower levels of externalizing behavior. A main effect was also evident for perspective taking (Est. = − 0.28, 95% CI = − 0.41, − 0.15, p < .001), such that higher levels of perspective taking predicted lower levels of externalizing behavior.
No interaction was observed between RHR and empathic concern. A main effect was however evident for empathic concern (Est. = − 0.21, 95% CI = − 0.34, − 0.08, p < .01), such that higher levels of empathic concern predicted lower levels of externalizing behavior.

Interaction of RHR and Empathy in Predicting Trouble with the Police

W1 Subsample

All models tested for interactive effects of RHR and the two subscales of IRI in the prediction of externalizing behavior measured as ever having been in trouble with the police, while adjusting for race/ethnicity and BMI (see Table 7). No interaction effects were evident, ps = ns. Several main effects were evident. Both models showed that RHR was negatively associated with ever having been in trouble with the police (e.g., OR = 0.66, 95% CI = 0.53, 0.81, p < .001, all estimates are reported in Table 7), such that a one unit increase in RHR was associated with a 34% decreased risk of ever having been in trouble with the police. A main effect was also evident for perspective taking (OR = 0.76, 95% CI = 0.62, 0.93, p < .01), such that a one unit increase in perspective taking was associated with a 24% decreased risk of ever having been in trouble with the police. Lastly, a main effect was evident for empathic concern (OR = 0.79, 95% CI = 0.64, 0.97, p < .05), such that a one unit increase in perspective taking was associated with a 21% decreased risk of ever having been in trouble with the police.
Table 7
Linear regression results for the W3 subsample: RHR and empathy interaction with ASR Externalizing behavior as the outcome
Outcome
Predictors
Estimate
SE
95% CI
p-value
Externalizing behavior
RHR * IRI PT
0.21
0.07
0.07, 0.35
0.004
 
RHR
− 0.14
0.07
− 0.27, − 0.00
0.048
 
IRI PT
− 0.28
0.07
− 0.41, − 0.15
< 0.001
 
RHR * IRI EC
0.14
0.07
− 0.01, 0.29
0.062
 
RHR
− 0.13
0.07
− 0.26, 0.00
0.057
 
IRI EC
− 0.21
0.07
− 0.34, − 0.08
0.002
Note n = 394, bold values are significant at an alpha level of .05
Abbreviations Resting heart rate (RHR), body mass index (BMI), Interpersonal Reactivity Index Perspective Taking (IRI PT), Interpersonal Reactivity Index Empathic Concern (IRI EC), Adult Self-Report (ASR), Wave 3 (W3)
* Estimates were adjusted for BMI, race/ethnicity, and sex

W3 Subsample

All models tested for interactive effects of RHR and the two subscales of IRI in the prediction of externalizing behavior measured as ever having been in trouble with the police, while adjusting for race/ethnicity and BMI (see Table 8). In the model testing for interactive effects between perspective taking and RHR in predicting ever having been in trouble with the police, we found a moderating effect of perspective taking. To characterize the nature of the interaction effect, we probed the association between RHR and ever having been in trouble with the police at low (-1 SD) and high (+ 1 SD) perspective taking. Whereas no significant effect of RHR was observed at 1 SD above the mean of perspective taking (OR = 1.32, 95% CI = 0.83, 2.06, p = ns), a significant effect of RHR was evident at 1 SD below the mean of perspective taking (OR = 0.57, 95% CI = 0.37, 0.83, p < .01). Thus, at low levels of perspective taking, a 1 SD increase in RHR was associated with a 43% decreased risk of ever having been in trouble with the police, see Fig. 2. No main effects were evident for either RHR or perspective taking (ps = ns).
Table 8
Logistic regression results for the W3 subsample: RHR and empathy interaction with trouble with the police as the outcome
Outcome
Predictors
Adj OR*
95% CI
p-value
Trouble with the police
RHR* IRI PT
1.53
1.13, 2.07
0.006
 
RHR
0.80
0.59, 1.05
0.123
 
IRI PT
0.84
0.64, 1.09
0.196
 
RHR * IRI EC
1.39
1.02, 1.91
0.039
 
RHR
0.80
0.60, 1.06
0.131
 
IRI EC
0.80
0.59, 1.00
0.053
Note n = 394, bold values are significant at an alpha level of .05
Abbreviations Resting heart rate (RHR), body mass index (BMI), Interpersonal Reactivity Index Perspective Taking (IRI PT), Interpersonal Reactivity Index Empathic Concern (IRI EC), Wave 3 (W3)
* ORs were adjusted for W3 BMI and W1 race/ethnicity
In the model testing for interactive effects between RHR and empathic concern in predicting ever having been in trouble with the police, we found a moderating effect of empathic concern. To characterize the nature of the interaction effect, we probed the association between RHR and ever having been in trouble with the police at low (-1 SD) and high (+ 1 SD) empathic concern. Whereas no significant effect of RHR was observed at 1 SD above the mean of empathic concern (OR = 1.18, 95% CI: 0.74, 1.86, p = ns), a significant effect of RHR was evident at 1 SD below the mean of empathic concern (OR = 0.61, 95% CI: 0.40, 0.90, p < .05). Thus, at low levels of empathic concern, a one SD increase in RHR was associated with a 39% decreased risk of getting in trouble with the police, see Fig. 3. No main effects were evident for either RHR or the empathic concern subscale of IRI (ps = ns).

Discussion

Externalizing behavior is multifactorial and highly complex (Focquaert, 2019); therefore, the importance of considering risk factors from multiple domains, including biology, psychology, and sociology, is paramount to better clarify our understanding of such behavior (Barnes et al., 2022). The present study examined the moderating effects of empathy on the association between RHR in childhood and adolescence with externalizing behavior by young adulthood. Our results corroborate earlier findings of RHR as a predictor of externalizing behavior (de Looff et al., 2022; Latvala et al., 2015), as well as an interaction between RHR in adolescence and empathy in young adulthood in predicting externalizing behavior in young adulthood (Galán et al., 2017). Thus, the current study contributes to the biopsychosocial criminological literature by providing evidence for a moderating role of a psychological construct (empathy) on the association between RHR and externalizing behavior, using a relatively large, longitudinal sample spanning from childhood to young adulthood.
Earlier studies have consistently reported that RHR and empathy are independently negatively associated with externalizing behavior, indicating that both lower levels of RHR and lower levels of empathy are associated with an increased risk of externalizing behavior (de Looff et al., 2022; Joliffe & Farrington, 2004; Latvala et al., 2015). In the current study, we utilized two subsamples from the Risk Factors for Antisocial Behavior (RFAB) project, one with RHR data from the first wave of data collection (W1) during childhood, and one from the third wave of data collection (W3) during adolescence. We found three interaction effects where the subscale “perspective taking” moderated the association between RHR and the externalizing behavior scale as well as the association between RHR and ever having been in trouble with the police. The subscale “empathic concern” was found to moderate the association between RHR and ever having been in trouble with the police. When we probed the associations, we found that among individuals with lower perspective taking and among individuals with lower empathic concern, a higher RHR decreased the risk of externalizing behavior by young adulthood. These findings corroborate those of Galán and colleagues (2017) who reported that among men with lower but not higher levels of RHR, a lower level of empathy predicted an increased risk of violent behavior by late adolescence/young adulthood. As such, Galán and colleagues (2017) found that RHR moderated the association between empathy and ASB. We add to the existing literature where earlier work has demonstrated a moderating effect of RHR on the association between empathy and ASB, by showing that empathy has a moderating effect on the association between RHR and ASB. Our findings along with results from Galán and colleagues (2017) demonstrate the complex interplay between RHR, empathy and ASB.
Although previous work has shown that cognitive empathy is more strongly related to ASB than affective empathy (Joliffe & Farrington, 2004), our findings showed relatively similar estimates for “perspective taking” (cognitive empathy) as well as for “empathic concern” (affective empathy). Results from the present study suggest that as RHR increase, individuals were more attuned to others’ emotions and thoughts (cognitive empathy), as well as more likely to share in their emotional experiences (affective empathy).
Perspective taking and empathic concern are the subscales from the IRI that are most used to conceptualize cognitive and affective empathy respectively. The “empathic fantasy” subscale of the IRI is rarely used in interpersonal assessments, and the “personal distress” subscale of the IRI measures responses in emergency situations, rather than empathy (Joliffe & Farrington, 2004). Previous work has reported that frequent violent offending was associated with a lower level of empathy on all subscales of the IRI, except for “personal distress” (Lauterbach & Hosser, 2007). The same study also showed that only the subscale “perspective taking” was associated with an increased risk of violent reoffending. Other studies have shown that among young adult offenders, the subscales “perspective taking”, “empathic fantasy”, and “personal distress” were associated with an increased risk of violent reoffending, whereas only “empathic fantasy” and “empathic concern” were associated with an increased risk of non-violent reoffending (Bock & Hosser, 2014). Our findings align with previous findings suggesting that “perspective taking” and “empathic concern” capture aspects of empathy that relate to externalizing behavior.
The findings of the current study are in line with previous work that has integrated lower levels of empathy into theoretical explanations of the association between RHR and externalizing behavior (Raine, 2013). Earlier studies reported that individuals with lower RHR were less empathic than individuals with higher RHR (Zahn-Waxler et al., 1995), and empathy has been considered a precursor to externalizing behavior (Joliffe & Farrington, 2004). This theoretical reasoning suggests that RHR and empathy may interact to predict externalizing behavior. Lower RHR has been postulated to contribute to reduced sensitivity to social cues, including the emotions and perspectives of others (Raine, 2013). This diminished sensitivity can make it challenging for individuals with lower RHR to comprehend and empathize with others, potentially elevating their susceptibility to engaging in externalizing behavior. Our results support that lower RHR is a risk factor for externalizing behavior, but only for individuals who also exhibit low levels of empathy. Thus, a high level of empathy may buffer against a biological risk factor such as lower RHR. Despite the potential externalizing behavior-reducing properties of empathy (Malti & Krettenauer, 2013), little attention has been paid to the potential interaction between RHR and empathy in predicting externalizing behavior. Our results show that an increase in RHR was only predictive of a lower level of externalizing behavior among individuals who exhibited low levels of empathy, suggesting that high empathy may buffer against the biological risk of a lower RHR.
In line with Galán et al. (2017) who also measured RHR in early adolescence, we found no strong main effects for RHR or empathy in our W3 subsample when predicting externalizing behavior. While the p-value for the main effect of RHR in predicting the externalizing behavior scale was less than 0.05 and thus indicate significance, the confidence interval was close to 0 which warrants careful interpretation. We also found no interactive effects between RHR and empathy in our W1 subsample, independent of what measure of externalizing behavior we used. Despite these findings, RHR, perspective taking, and empathic concern were individually associated with the two externalizing behavior measures in the W1 subsample which supports RHR in childhood and specific facets of empathy in young adulthood as independent predictors of externalizing behavior by young adulthood. We also observed associations between perspective taking and empathic concern with the two measures of externalizing behavior, thus supporting these measures of empathy in young adulthood as independent predictors of externalizing behavior by young adulthood. The association between RHR and externalizing behavior may be more salient when RHR is measured in childhood (W1) as opposed to early adolescence (W3). It is primarily the parasympathetic nervous system which is predominant in resting conditions that is responsible for RHR (Cacioppo et al., 2017), which has been found to have a different maturational trajectory than the sympathetic nervous system which prevails when the body is active (Harteveld et al., 2021). The parasympathetic cardiac activity has a complex maturational pattern, which plateaus toward adolescence, potentially because of hormonal changes during puberty. Thus, our null- and weak findings regarding the RHR-externalizing behavior association may reflect a biological effect as outlined above.
The interaction between RHR in adolescence and empathy in predicting externalizing behavior by young adulthood suggests that physiological dysregulation as indexed by lower RHR and deficits in empathy may increase the risk of engaging in externalizing behavior. This could imply that interventions that target physiological regulation as well as empathy skills may be particularly effective for individuals at risk of externalizing behavior. Our study findings may also suggest that recognizing individuals with a lower RHR provides a potential opportunity for targeted interventions, specifically focusing on enhancing empathic skills. By tailoring interventions to address the needs of this group, it may be possible to buffer against the risk of externalizing behavior. Results also suggest that there is a need for a multidisciplinary approach to the study of externalizing behavior, in which research should be targeted toward both biological and psychological factors which together may be important to our understanding of externalizing behavior. Furthermore, adopting such a multidisciplinary approach will not only enhance our theoretical understanding but also pave the way for more effective and targeted interventions to address externalizing behavior. By bridging the gap between biological and psychological perspectives, research can inform holistic strategies that consider the intricate interplay of these factors, ultimately contributing to more comprehensive solutions for individuals exhibiting externalizing behavior.

Limitations and Future Directions

The current study provides support for an interaction between a biological and a psychological risk factor for externalizing behavior; however, findings should be interpreted with caution due to the small sample (although relatively large from a psychophysiological perspective) and somewhat wide confidence intervals surrounding interaction effects which likely reflect unstable findings. The effect sizes in the current study further reflect quite small effects. Thus, the implications of the current study should be considered in light of this.
It is also important to note that we were unable to adjust for physical fitness in our analyses, which could be a potential confounder in the association between RHR and externalizing behavior. Other studies have reported increased relative risks for externalizing behavior among individuals with lower levels of RHR, after adjusting for level of physical fitness (Latvala et al., 2015; Oskarsson et al., 2021). Thus, it may be that our reported associations are underestimated.
With the limitations of the current study stated, it is also important to shed light on some notable strengths. We used a rich longitudinal data set with a diverse participant sample and assessments across waves, which enabled us to examine a moderating effect of a psychological risk factor measured in young adulthood (empathy) on the association between an early biological risk factor measured in childhood and early adolescence (RHR). Even though the sample was reduced from the original study sample due to missing data, a sample size of the W1 subsample but also the W3 subsample would be considered fairly large for a psychophysiological study.

Conclusion

In the current study, we found that empathy in young adulthood moderated the association between resting heart rate in early adolescence and externalizing behavior by young adulthood: among adolescents with low but not high empathy, a lower RHR was predictive of an increased risk of externalizing behavior. Our results in combination with theoretical perspectives about resting heart rate, empathy and externalizing behavior indicate that interventions aiming to enhance empathic skills in young individuals with psychophysiological risk profiles could be beneficial.

Acknowledgements

S Ling and C Tuvblad acknowledge funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 101,030,220. C Tuvblad acknowledges funding from the Swedish Research Council (2018 − 01041).

Declarations

Ethical Approval

Informed consent was obtained from the caregivers of all participants in the RFAB project at W1 and from the participants themselves at W5. The Institutional Review Board at USC approved of the project (Baker et al., 2013).
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Voetnoten
1
The declining effect sizes of the association between RHR and externalizing behavior may have several explanations such as regression toward the mean, publication bias, and sample size effects but also the definition of externalizing behavior. However, the association between RHR and externalizing behavior is robust and has, in addition to several meta-analyses, been demonstrated in several large-scale population-based studies (e.g., Latvala et al., 2015, 2016; Oskarsson et al., 2021).
 
2
In the current dataset, zero-order associations showed no significant association between RHR and internalizing behavior in the W1 and W3 subsamples (r’s = 0.003, and − 0.002, p’s > 0.05). Linear regressions adjusting for BMI and race/ethnicity showed no significant associations between RHR and internalizing behavior in the W1 and W3 subsamples (Est. − 0.001, and, -0.003, p’s > 0.05).
 
3
Meta-analyses tend to show a consistent but varying association between empathy and externalizing behavior, likely due to the conceptualization of both constructs. This may reflect a complex association between empathy and externalizing behavior where certain types of both constructs are more related than others.
 
4
In line with previous findings (Bertoldi et al., 2022a); getting in trouble with the police by W5 differed significantly between race/ethnicity in the W1 subsample (X2 = 9.72, p < .05) but not in the W3 subsample (Fisher’s exact test = p > .05). Mixed race participants in the W1 subsample were more likely to have been in trouble with the police compared to White participants (OR = 2.21, 95% CI = 1.26, 3.89). Scores on the externalizing behavior scale did not differ between race/ethnicity.
 
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Metagegevens
Titel
Interaction of Resting Heart Rate with Empathy in Predicting Externalizing Behavior
Auteurs
Sofi Oskarsson
Bridget M. Bertoldi
Anneli Andersson
Rebecca Siponen
Shichun Ling
Adrian Raine
Laura Baker
Brittany Evans
Catherine Tuvblad
Publicatiedatum
15-02-2024
Uitgeverij
Springer US
Gepubliceerd in
Journal of Psychopathology and Behavioral Assessment / Uitgave 1/2024
Print ISSN: 0882-2689
Elektronisch ISSN: 1573-3505
DOI
https://doi.org/10.1007/s10862-024-10123-6

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