Physiological Arousal and Its Dysregulation in Child Maladjustment

Abstract

Arousal and its regulation are key components of emotion, temperament, and flexible responding needed for healthy adjustment. This article presents a biosocial vulnerability model suggesting that maladjustment arises when psychological mechanisms are disrupted by changes in nervous system functioning that cause the discoordination of physiological regulatory systems, potentially leading to hyper- or hypoarousal and arousal dysregulation. The model posits bidirectional relationships with adverse social context at any level, ultimately derailing affective, cognitive, and interpersonal processes, which can increase psychopathology. Applications are made to childhood aggression and autism spectrum disorder as two examples of how differences in arousal and its dysregulation can impact child adjustment.

Keywords

arousal arousal dysregulation child maladjustment heart rate heart rate variability

Emotions (e.g., fear, anger, joy) involve whole-body responses of cognitive and physiological changes that direct tendencies to approach or avoid (Lang, Bradley, & Cuthbert, 1998). Physiological arousal, the body’s response to an emotional stimulus, is integral to the emotion experience and is closely tied to temperament, defined as individual differences in reactivity and regulation (Rothbart & Derryberry, 1981). Reactivity refers to the reflexive nervous system response (i.e., emotional, motor, attentional) to a stimulus, whereas regulation refers to the modulation of that response to changing situational contexts.

In this article, I focus on physiological arousal and its regulation¹ as key components of emotions and as an index of the integrity of the nervous system’s response to environmental or sensory stimuli. In its Research Domain Criteria project, the National Institute of Mental Health identifies “arousal/regulatory systems” as one of the five critical domains of functioning underlying mental disorders (see http://www.nimh.nih.gov/research-priorities/rdoc/index.shtml). I will explain how physiological arousal and its dysregulation may impact multiple developmental functions and thereby increase the risk for childhood² maladjustment.

I assume herein a model of biosocial vulnerability to child maladjustment (Scarpa & Raine, 2003), which proposes that children are guided by physiological processes that influence emotional and temperamental responses and occur within a social context that can qualify their effects. Because of the strong association with emotion and temperament, I will focus this review on the role of physiological arousal and its dysregulation, as they impact interpersonal, cognitive, and emotional dysfunction. Childhood aggression and autism spectrum disorder (ASD) are used as two examples of how differences in arousal reactivity and regulation impact childhood adjustment.

The Biosocial Vulnerability Model of Child Maladjustment

Consistent with the developmental-psychopathology perspective of individual and environmental influences that transact to produce child outcomes (Hinshaw, 2013), the biosocial vulnerability model proposes that genetic and epigenetic variations change the physiological functioning of regulatory systems, including autonomic (ANS) and central nervous system (CNS), immune system, and neuroendocrine functioning, which in turn disrupt psychological (i.e., affective, cognitive, and interpersonal) processes and can thereby lead to maladjustment (Fig. 1). Each level in the process can affect and/or be affected by environmental and social experiences, which implies that the results of biological vulnerabilities may be expressed, attenuated, or enhanced in the presence of certain psychosocial experiences (Scarpa & Raine, 2003).

Fig. 1.

Illustration of the biosocial vulnerability model. As a result of nested influences, genetic and epigenetic factors change physiological functioning in regulatory systems (e.g., autonomic nervous system [ANS], central nervous systems [CNS], immune, neuroendocrine). These systems in turn affect psychological (affective, cognitive, interpersonal) mechanisms involving temperament and personality, which may increase the probability of psychopathology or other maladjustment. The social environment may reciprocally impact, mediate, or moderate at any level of this model.

This model specifically focuses on effects of stress or adversity that increase vulnerability to negative outcomes. It serves as a heuristic that can be broadened by other models suggesting variations in susceptibility to both positive and negative environments (e.g., Belsky & Pluess, 2009; Ellis & Boyce, 2008) and, similarly, can be narrowed by testing specific risk or protective factors (e.g., interactions of ANS with family conflict; El-Shiekh & Erath, 2011). Based on the tenets of developmental psychopathology, it is meant as a guide through which to think of nested biological and psychological systems that can transact with one another, as well as with the larger social context in which they are embedded, to enhance or worsen outcomes. As such, there is more depth to the model than is necessarily represented in this brief review.

The model specifies multiple biological (e.g., genetic, CNS, neuroendocrine) influences that coordinate the body’s adaptive functioning, but I will focus on the ANS because it is closely tied to emotions and to stress responses and because it acts as a conduit of information to and from the CNS via the brain stem. The ANS is divided into sympathetic (SNS) and parasympathetic (PNS) branches, which typically interact reciprocally to produce varying levels of arousal. The excitatory sympathetic branch, referred to as our “fight or flight” system, mobilizes energy to prepare the body for challenge and is characterized by physiological reactions such as increased heart rate, respiration, and sweating. The inhibitory parasympathetic branch, referred to as our “rest and digest” system, plays a restorative role during states of safety and stability and is characterized by lower physiological arousal, including reduced heart rate.

The ANS allows individuals to transition between high- and low-arousal states in accord with situational demands. Such flexible autonomic responding is thought to be indexed by parasympathetically mediated heart rate variability,³ the normal variation in heartbeat interval as a function of respiration, also referred to as respiratory sinus arrhythmia (Appelhans & Luecken, 2006). Specifically, the vagus (i.e., a cranial nerve that interfaces with the PNS to modulate the heart) typically puts a “brake” on heart rate, whereas vagal withdrawal acts like an accelerator. Although the heart is innervated by both sympathetic and parasympathetic branches, changes in sympathetic activation occur slowly (i.e., 4–20 seconds from peak to recovery) relative to the very quick vagal response on the heart (i.e., 0.5–1 second from peak to recovery). Thus, whereas the SNS prepares the body for mobilization, the PNS rapidly modulates heart rate to efficiently respond to momentary demands.

I use the term arousal to mean either heightened (over- or hyperarousal) or attenuated (under- or hypoarousal) autonomic activity at baseline or resting states, which is the result of combined tonic influences of the SNS and PNS and is assumed to reflect individual differences in one’s natural tendency toward emotional reactivity. I use arousal regulation specifically to mean baseline parasympathetic modulation of that arousal to adjust to changing internal and external demands; arousal regulation also reflects individual differences in emotion-regulation ability. Although the model can be applied to autonomic reactivity to specific stimuli (e.g., vagal withdrawal to a laboratory stressor) or to recovery after a stressor, that research is not covered here.

Theoretical Perspectives

The relationship of the ANS to emotions can be understood within the context of three seminal theoretical perspectives: Gray’s motivational theory (Gray, 1991), the polyvagal theory (Porges, 2001), and the neurovisceral integration model (Thayer & Lane, 2000). Gray (1991) proposed that different neural circuits underlie motivations to approach (i.e., the behavioral activation system, BAS) or avoid (i.e., the behavioral inhibition system, BIS) emotional stimuli. Beauchaine (2001) extended Gray’s model to suggest that the BAS (which reflects novelty seeking) and the BIS (which reflects harm avoidance) are both under sympathetic control, as indexed by pre-ejection period in reward contexts and skin conductance in punishment contexts, respectively. According to Gray, the BAS and the BIS oppose one another, such that either approach or passive avoidance predominate according to the perceived stimulus.

The polyvagal theory (Porges, 2001) proposes that the mammalian nervous system, organized in three subsystems, evolved to promote survival by preparing the organism to address different levels of threat or safety through immobilization in response to life endangerment (via the dorsal unmyelinated vagus), active mobilization (i.e., fight or flight) in response to threat (via the SNS), and social engagement in response to safe situations (via the parasympathetic ventral vagal complex, its fast-acting myelinated vagus, and connections to other cranial nerves supporting social communication). The three systems work together in a graduated and blended fashion to respond to challenges, but the ventral vagal complex’s rapid control of heart rate (measured through indices of heart rate variability) subserves our ability to self-soothe and quickly engage or disengage from the environment. This system is therefore viewed as having emotion-regulation and social-engagement functions. If this system is not sufficient to deal with the challenge, the SNS and the dorsal vagal complex then become activated in turn.

The neurovisceral integration model (Thayer & Lane, 2000) proposes that the central autonomic network integrates the CNS and ANS to coordinate cognitive, behavioral, and physiological elements needed for regulation of emotional arousal. This network is in constant communication with the heart through the vagus, which allows it to adjust physiological arousal to internal and external changes (i.e., arousal regulation). When the system becomes too rigidly coupled, it leads to autonomic inflexibility and psychopathology (Friedman, 2007).

Taken together, these theories suggest several conclusions about emotion-related arousal and arousal regulation. First, Gray (1991) sets the stage to support neural underpinnings of emotional reactivity (i.e., approach, avoidance) to emotional stimuli. Second, Porges (2001) specifies that fight-or-flight tendencies emerge from sympathetically mediated mobilization to threat, and Beauchaine (2001) adds that increased sympathetic arousal can also be associated with inhibited responses to cues of punishment. Third, Porges (2001) and Thayer and Lane (2000) propose that heart rate responses can be regulated through the ventral vagal complex and the central autonomic network through parasympathetically mediated inhibition or disinhibition. As a result, physiological arousal and its regulation permit us to react to and flexibly respond to changes in the internal and external environment, thus representing capacity for reactivity and regulation to emotional stimuli.

Applications to Child Maladjustment

Within the context of the biosocial vulnerability model, these theories support the notion of CNS-ANS changes in arousal and its regulation leading to important cognitive, affective, and social changes that can in turn increase risk for child maladjustment and psychopathology. However, the patterns of arousal and dysregulation may differ across syndromes. The remainder of this article focuses on impacts of arousal and its regulation or dysregulation as applied to two childhood maladjustment problems—aggressive behavior and ASD—drawing upon research by myself and colleagues.

Childhood aggression

Childhood physical aggression predicts future diagnoses of conduct disorder, physical violence, legal infractions, and impaired functioning throughout adolescence and into adulthood (e.g., Lahey et al., 1998; Loeber, Green, Lahey, & Kalb, 2000; Nagin & Tremblay, 1999; Tremblay & Nagin, 2005). As such, a greater understanding of factors contributing to childhood aggression can have a major public health impact.

There is a strong case for the importance of ANS underarousal and, specifically, low heart rate in relation to aggressive behavior. Two independent meta-analyses examining almost 60 studies found that low resting (or baseline) heart rate is associated with increased antisocial and aggressive behavior in children and adolescents, leading to the conclusion that low resting heart rate is the best-replicated biological correlate of antisocial behavior to date (Lorber, 2004; Ortiz & Raine, 2004). Moreover, it seems to particularly characterize antisocial offenders whose deviant behavior starts early and persists into adulthood. During childhood, individuals in this subgroup show high levels of aggression and have multiple biological and social risk factors (Moffitt & Caspi, 2001).

In line with the biosocial vulnerability model, low resting heart rate may reflect a predisposition to psychological traits such as fearlessness, callousness or unemotionality, poor passive avoidance, disinhibited temperament, impulsivity, and sensation seeking. These traits increase the likelihood of engaging in aggression (Scarpa & Raine, 2004; Scarpa, Raine, Venables, & Mednick, 1997; Wilson & Scarpa, 2011). Moreover, underarousal may interact with psychosocial risk factors. In a study of community children, for example, community-violence victimization was positively related to proactive/premeditated aggression; however, this relationship existed only in children with low resting heart rate (Scarpa, Tanaka, & Haden, 2008).

Several studies have also suggested that aggression is associated with arousal dysregulation. These studies indicated that reduced heart rate variability (i.e., poor regulation) corresponded to increased levels of aggression among boys exposed to parental marital conflict, externalizing behavior among brothers of adjudicated delinquents, and antisocial behavior among inner-city males (Beauchaine, 2001). More recently, low heart rate variability was associated with reactive/impulsive aggression but not with proactive/premeditated aggression in children from a community sample (Scarpa, Haden, & Tanaka, 2010).

Taken together, these findings indicate that persistently aggressive children may be characterized by both low arousal (i.e., low resting heart rate) and arousal dysregulation (i.e., low heart rate variability). These results (i.e., reductions in both sympathetic and parasympathetic influences) appear to contradict the typical reciprocal nature of the PNS and SNS; however, several explanations can be considered. First, it is possible that low arousal is related to the callousness seen in proactive/premeditated aggression, whereas arousal dysregulation is linked to the anger identified in reactive/impulsive aggression (Scarpa et al., 2010; Scarpa et al., 2008). Second, to the extent that aggressive children are also potential victims of violence or family conflict, reduced SNS and PNS functioning could indicate co-inhibition (Berntson, Cacioppo, & Quigley, 1991), which has been identified as a risk factor in some individuals with histories of trauma or exposure to marital conflict (El-Shiekh & Erath, 2011; Patriquin, Wilson, Kelleher, & Scarpa, 2012). Third, Beauchaine (2001) has argued that behavioral reactivity is moderated by emotion regulation. He proposed that sympathetic underarousal leads to behavioral reactivity in the form of trait impulsivity. Trait impulsivity may then increase aggression, but only when poorly regulated.

Autism spectrum disorder

ASD represents a set of neurodevelopmental conditions that share impairments in reciprocal social interaction, communication, and the presence of stereotyped behavior, interests, or activities. The Centers for Disease Control (Wingate et al., 2014) has estimated that 1 in 68 children in the United States meet ASD diagnostic criteria, representing a 123% increase in prevalence from 2002. These complex disorders are usually lifelong and affect development, learning, and adaptation in all settings, thus representing a pressing public health issue.

Emotional and behavioral disorders are heightened in children with ASD, and emotion dysregulation can explain their difficulty with emotional competence and resultant psychiatric comorbidity (Mazefsky et al., 2013). Multiple studies have shown chronic hyperarousal and arousal dysregulation in at least a subset of children with ASD. In comparison to typically developing peers, for example, children with ASD exhibit increased basal heart rate (e.g., Goodwin et al., 2006; Kushki et al., 2013) and decreased basal heart rate variability (e.g., Bal et al., 2010; Guy et al., 2014; Neuhaus, Bernier, & Beauchaine, 2014). These studies suggest that sympathetic arousal and decreased vagal control of the heart are associated with ASD and may be considered an endophenotype (Klusek, Roberts, & Losh, 2015).

Though multiple interpretations exist, research supports the theory that some individuals with ASD present in a chronically mobilized or defensive state of physiological activation, which would correspond with reductions in the vagal regulation that normally supports social engagement (Porges, 2001). Research from my lab has affirmed that poor arousal regulation in ASD is associated with social-reciprocity difficulty. More specifically, we showed that reduced baseline heart rate variability was associated with fewer gestures and joint attention in young children with ASD (Patriquin, Scarpa, Friedman, & Porges, 2013). However, we also found that low basal heart rate variability was related to more caregiver-reported language and cognitive delays, as well as to the lack of language, in these same children (Patriquin, Lorenzi, & Scarpa, 2013). Moreover, in a community sample of typically developing infants from 5 to 48 months of age, trajectory analyses indicated that children with consistently low heart rate variability had significantly more behavioral problems at 48 months, including pervasive developmental problems as well as increased withdrawal, aggressive behavior, and oppositional defiant problems (Patriquin, Lorenzi, Scarpa, Calkins, & Bell, 2015). Taken together, our results suggest that heart rate variability may reflect a broad marker of adjustment including not only social processes but also cognitive, emotional, and behavioral functioning.

To my knowledge, no studies have examined the interactive effects of adverse social context (e.g., poverty, victimization) on hyperarousal and arousal dysregulation in ASD. Children with disabilities are more likely to experience victimization, and a recent review concluded that children with ASD are frequent victims of bullying relative to the general population and to children with other disabilities (Sreckovic, Brunsting, & Able, 2014). In light of such reports and the likelihood that some children with ASD may be in hyperaroused states and respond to stress with dysregulation, it seems imperative to examine such biosocial interactions.

Conclusions and Future Directions

In this article, I have focused on arousal and its regulation as key components of emotions, temperament, and flexible adaptive responding. A biosocial vulnerability model applied to the ANS suggests that maladjustment arises when social and biological variables mediate or moderate one another, leading to hyper- or hypoarousal and arousal dysregulation, which disrupts typical emotional, cognitive, and interpersonal functioning. In particular, the CNS and ANS control arousal experiences as well as the ability to transition from high- and low-arousal states to meet situational demands. When this process is compromised through deficient arousal activity and/or arousal dysregulation, children may experience maladjustment and related psychopathology.

As an example, researchers have suggested that persistent childhood aggression is characterized by low arousal and arousal dysregulation, potentially leading to callous/unemotional traits or impulsive behaviors that are compounded by inflexible responding. These effects are especially pronounced in children facing social adversity. Children on the autism spectrum, however, may be characterized by chronic hyperarousal and arousal dysregulation, which increase emotional and behavioral problems through their effects on overall developmental processes, including heightened affective sensitivity, social disengagement and lack of reciprocity, and cognitive (i.e., attention and language) dysfunction.

This line of research highlights how physiological regulatory systems may show different patterns across childhood problems, suggesting further lines of inquiry. For example, inconsistencies in ANS patterns suggest that psychological mechanisms may vary across different forms and functions of childhood aggression. The lack of research on the effects of social adversity on physiological functioning in children with ASD is also highlighted. It is also worth noting that the majority of research on biosocial effects has been conducted in relation to internalizing and externalizing problems, but biosocial research in ASD is emerging. The findings discussed here suggest that the study of arousal and regulation, and the broader model of biosocial transactions, are worth further examination in ASD.

Moreover, the biosocial vulnerability model is a heuristic that involves multiple biological and social influences and transdiagnostic processes. As such, the model can be reviewed, expanded, and tested in multiple ways. For example, the biosocial roles of other physiological systems besides ANS (e.g., neuroendocrine, neurobiological, immune) can be explored, including how they interface with each other within levels (e.g., CNS with ANS) or across levels (e.g., ANS with executive cognitive dysfunction) in specific social contexts. This review has focused on heart rate and heart rate variability, but additional measures of ANS (e.g., electrodermal activity, heart rate reactivity and recovery, vagal withdrawal or augmentation) as well as other response systems (e.g., cortisol, immune responses) would provide a richer interpretation of arousal dysregulation and coordination among regulatory systems. Additional measures of social context (e.g., socioeconomic status, educational enrichment) could be used to explore whether certain contexts confer protection. The model can also be applied to other childhood problems and psychopathology (e.g., depression, anxiety, trauma, eating disorders). Finally, the model is optimistic in that it does not view arousal and regulation as “fixed” but, rather, as modifiable by environmental influences and therefore malleable to intervention.

Footnotes

Acknowledgements

Many thanks go to my former mentor Adrian Raine, colleagues, and graduate students. The work presented in this article could not have been completed without them.

Declaration of Conflicting Interests

The author declared no conflicts of interest with respect to the authorship or the publication of this article.

Notes

References

Gross

J. J.

Jazaieri

(2014). Emotion, emotion regulation, and psychopathology: An affective science perspective. Clinical Psychological Science, 2, 387–401. An article that provides further details about emotions and emotional regulation as applied to a broad range of psychopathology.

Porges

S. W.

(2003). The Polyvagal Theory: Phylogenetic contributions to social behavior. Physiology & Behavior, 79, 503–513. A theoretical article that provides a full discussion of the polyvagal theory and its clinical implications for autism.

Raine

(2002). Biosocial studies of antisocial and violent behavior in children and adults: A review. Journal of Abnormal Child Psychology, 30, 311–326. A clearly written and accessible overview of the biosocial model applied to antisocial behavior.

Scarpa

Reyes

N. M.

(2011). Improving emotion regulation with CBT in young children with high functioning autism spectrum disorders: A pilot study. Behavioural and Cognitive Psychotherapy, 39, 495–500. An original research article on the benefits of cognitive behavioral therapy for treating emotion dysregulation, including heightened arousal, in autism.

Thayer

J. F.

Lane

R. D.

(2000). (See References). The first article to formulate the neurovisceral integration model, for those who wish to learn more about the topic.

Appelhans

B. M.

Luecken

L. J.

(2006). Heart rate variability as an index of regulated emotional responding. Review of General Psychology, 10, 229–240.

Bal

Harden

Lamb

Van Hecke

A. V.

Denver

J. W.

Porges

S. W.

(2010). Emotion recognition in children with autism spectrum disorders: Relations to eye gaze and autonomic state. Journal of Autism and Developmental Disorders, 40, 358–370.

Beauchaine

(2001). Vagal tone, development, and Gray’s motivational theory: Toward an integrated model of autonomic nervous system functioning in psychopathology. Development and Psychopathology, 13, 183–214.

Belsky

Pluess

(2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885–908.

10.

Berntson

G. G.

Cacioppo

J. T.

Quigley

K. S.

(1991). Autonomic determinism: The modes of autonomic control, the doctrine of autonomic space, and the laws of autonomic constraint. Psychological Review, 98, 459–487.

11.

Ellis

B. J.

Boyce

W. T.

(2008). Biological sensitivity to context. Current Directions in Psychological Science, 17, 183–187.

12.

El-Shiekh

Erath

S. A.

(2011). Family conflict, autonomic nervous system functioning, and child adaptation: State of science and future directions. Development and Psychopathology, 23, 703–721.

13.

Friedman

B. H.

(2007). An autonomic flexibility–neurovisceral integration model of anxiety and cardiac vagal tone. Biological Psychology, 74, 185–199.

14.

Goodwin

M. S.

Groden

Velicer

W. F.

Lipsitt

L. P.

Baron

M. G.

Hofmann

S. G.

Groden

(2006). Cardiovascular arousal in individuals with autism. Focus on Autism and Other Developmental Disabilities, 21, 100–123.

15.

Gray

J. A.

(1991). Neural systems of motivation, emotion and affect. In Madden

(Ed.), Neurobiology of learning, emotion and affect (pp. 273–306). New York, NY: Raven Press.

16.

Guy

Souders

Bradstreet

DeLussey

Herrington

J. D.

(2014). Brief report: Emotion regulation and respiratory sinus arrhythmia in autism spectrum disorder. Journal of Autism and Developmental Disorders, 44, 2614–2620.

17.

Hinshaw

S. P.

(2013). Developmental psychopathology as a scientific discipline. In Beauchaine

T. P.

Hinshaw

S. P.

(Eds.), Child and adolescent psychopathology (2nd ed., pp. 3–28). Hoboken, NJ: John Wiley & Sons.

18.

Klusek

Roberts

J. E.

Losh

(2015). Cardiac autonomic regulation in autism and Fragile X Syndrome: A review. Psychological Bulletin, 141, 141–175.

19.

Kushki

Drumm

Mobarak

M. P.

Tanel

Dupuis

Chau

Anagnostou

(2013). Investigating the autonomic nervous system response to anxiety in children with autism spectrum disorders. PLoS ONE, 8(4), e59730. Retrieved from http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0059730

20.

Lahey

B. B.

Loeber

Quay

H. C.

Applegate

Shaffer

Waldman

. . . Bird

H. R.

(1998). Validity of DSM-IV subtypes of conduct disorder based on age of onset. Journal of the American Academy of Child & Adolescent Psychiatry, 37, 435–442.

21.

Lang

P. J.

Bradley

M. M.

Cuthbert

B. N.

(1998). Emotion, motivation, and anxiety: Brain mechanisms and psychophysiology. Biological Psychiatry, 44, 1248–1263.

22.

Loeber

Green

S. M.

Lahey

B. B.

Kalb

(2000). Physical fighting in childhood as a risk factor for later mental health problems. Journal of the American Academy of Child & Adolescent Psychiatry, 39, 421–428.

23.

Lorber

M. F.

(2004). Psychophysiology of aggression, psychopathy, and conduct problems: A meta-analysis. Psychological Bulletin, 130, 531–552.

24.

Mazefsky

C. A.

Herrington

Siegel

Scarpa

Maddox

B. B.

Scahill

White

S. W.

(2013). The role of emotion regulation in autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 679–688.

25.

Moffitt

T. E.

Caspi

(2001). Childhood predictors differentiate life-course persistent and adolescent limited pathways among males and females. Development and Psychopathology, 13, 355–375.

26.

Nagin

Tremblay

R. E.

(1999). Trajectories of boys’ physical aggression, opposition, and hyperactivity on the path to physically violent and nonviolent juvenile delinquency. Child Development, 70, 1181–1196.

27.

Neuhaus

Bernier

Beauchaine

T. P.

(2014). Brief report: Social skills, internalizing and externalizing symptoms, and respiratory sinus arrhythmia in autism. Journal of Autism and Developmental Disorders, 44, 730–737.

28.

Ortiz

Raine

(2004). Heart rate level and antisocial behavior in children and adolescents: A meta-analysis. Journal of the American Academy of Child & Adolescent Psychiatry, 43, 154–162.

29.

Patriquin

M. A.

Lorenzi

Scarpa

(2013). Relationship between respiratory sinus arrhythmia, heart period, and caregiver-reported language and cognitive delays in children with autism spectrum disorders. Applied Psychophysiology and Biofeedback, 38, 203–207.

30.

Patriquin

M. A.

Lorenzi

Scarpa

Calkins

S. D.

Bell

M. A.

(2015). Broad implications for respiratory sinus arrhythmia development: Associations with childhood symptoms of psychopathology in a community sample. Developmental Psychobiology, 57, 120–130.

31.

Patriquin

M. A.

Scarpa

Friedman

B. H.

Porges

S. W.

(2013). Respiratory sinus arrhythmia: A marker for positive social functioning and receptive language skills in children with autism spectrum disorders. Developmental Psychobiology, 55, 101–112.

32.

Patriquin

M. A.

Wilson

L. C.

Kelleher

S. A.

Scarpa

(2012). Psychophysiological reactivity to abuse-related stimuli in sexually revictimized women. Journal of Aggression, Maltreatment & Trauma, 21, 758–775.

33.

Porges

S. W.

(2001). The Polyvagal Theory: Phylogenetic substrates of a social nervous system. International Journal of Psychophysiology, 42, 123–146.

34.

Rothbart

M. K.

Derryberry

(1981). Development of individual differences in temperament. In Lamb

M. E.

Brown

A. L.

, Advances in Developmental Psychology (pp. 37–86). Hillsdale, NJ: Lawrence Erlbaum.

35.

Scarpa

Haden

S. C.

Tanaka

(2010). Being hot-tempered: Autonomic, emotional, and behavioral distinctions between childhood reactive and proactive aggression. Biological Psychology, 84, 488–496.

36.

Scarpa

Raine

(2003). The psychophysiology of antisocial behavior: Interactions with environmental experiences. In Walsh

Ellis

(Eds.), Biosocial criminology: Challenging environmentalism’s supremacy (pp. 209–226). Hauppauge, NY: Nova Science Publishers.

37.

Scarpa

Raine

(2004). The psychophysiology of child misconduct. Pediatric Annals, 33, 296–304.

38.

Scarpa

Raine

Venables

P. H.

Mednick

S. A.

(1997). Heart rate and skin conductance in behaviorally inhibited Mauritian children. Journal of Abnormal Psychology, 106, 182–190.

39.

Scarpa

Tanaka

Haden

S. C.

(2008). Biosocial bases of reactive and proactive aggression: The roles of community violence exposure and heart rate. Journal of Community Psychology, 36, 969–988.

40.

Sreckovic

M. A.

Brunsting

N. C.

Able

(2014). Victimization of students with autism spectrum disorder: A review of prevalence and risk factors. Research in Autism Spectrum Disorders, 8, 1155–1172.

41.

Thayer

J. F.

Lane

R. D.

(2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61, 201–216.

42.

Tremblay

R. E.

Nagin

D. S.

(2005). The developmental origins of physical aggression in humans. In Tremblay

R. E.

Hartup

W. W.

Archer

(Eds.), Developmental origins of aggression (pp. 83–106). New York, NY: Guilford Press.

43.

Wilson

L. C.

Scarpa

(2011). The link between sensation seeking and aggression: A meta-analytic review. Aggressive Behavior, 37, 81–90.

44.

Wingate

Kirby

R. S.

Pettygrove

Cunniff

Schulz

Ghosh

. . . Yeargin-Allsopp

(2014). Prevalence of autism spectrum disorder among children aged 8 years—Autism and Developmental Disabilities Monitoring Network, 11 sites, United States, 2010. Centers for Disease Control and Prevention, MMWR Surveillance Summaries, 63(2). Retrieved from http://www.cdc.gov/mmwr/preview/mmwrhtml/ss6302a1.htm