Definitional issues

Respiratory sinus arrhythmia (RSA), skin conductance level (SCL), and cardiac preejection period (PEP) are the indices of ANS functioning most commonly studied in the context of family conflict. We focus on these ANS parameters and define them below.

RSA can be used as an estimate of vagal tone or PNS influence on the heart, and change in RSA from baseline to stress can be used to index vagal reactivity. In this paper, we use the terms vagal tone and vagal reactivity when referring to the constructs at a conceptual level; we use the term RSA when reporting study findings. RSA is the rhythmic fluctuation of heart rate during spontaneous breathing and is governed by the myelinated vagus nerve (Porges, Reference Porges1995). Vagal tone (indexed by resting RSA) reflects the activity of the PNS at rest and perhaps the ability to sustain attention, regulate emotion, and engage in social communication (Porges, Reference Porges2007; Thayer & Lane, Reference Thayer and Lane2009). Vagal reactivity refers to changes in RSA from baseline to challenging conditions, and may be characterized as vagal withdrawal (decreased RSA) or vagal augmentation (increased RSA). Vagal withdrawal accelerates heart rate and increases metabolic output rapidly and incrementally, and may reflect awareness of environmental challenge and mobilization of physiological resources to mount an active coping response (Fox & Calkins, Reference Fox and Calkins2003; Porges, Reference Porges2007). Conversely, vagal augmentation decelerates heart rate in response to challenge and may reflect failure to engage with environmental demands or immobilization responses (Calkins, Reference Calkins1997; Calkins & Dedmon, Reference Calkins and Dedmon2000). Of importance, vagal withdrawal and vagal augmentation occur along a continuum such that greater or lesser degrees of change from baseline conditions occur. RSA has been well validated as a marker of the vagus nerve's influence on the heart; and within a broad range of normal physiological functioning, it is considered a valid measure of vagal tone (Grossman & Taylor, Reference Grossman and Taylor2007). Pharmacological blockade studies demonstrate that the vagus nerve influences the attenuation or elimination of RSA (Berntson et al., Reference Berntson, Bigger, Eckberg, Grossman, Kaufmann and Malik1997; Hayano et al., Reference Hayano, Sakakibara, Yamada, Yamada, Mukai and Fujinami1991; Sherwood, Allen, Obrist, & Langer, Reference Sherwood, Allen, Obrist and Langer1986).

Evidence for sex differences in RSA is inconclusive. Girls exhibited higher RSA than boys in some studies (Fabes, Eisenberg, Karbon, Troyer, & Switzer, Reference Fabes, Eisenberg, Karbon, Troyer and Switzer1994), but findings were reversed in other studies (El-Sheikh, Reference El-Sheikh2005a; Hinnant, Staton, & El-Sheikh, Reference Hinnant, Staton and El-Sheikh2010; Salomon, Reference Salomon2005). Furthermore, some studies revealed no sex differences in RSA (Alkon et al., Reference Alkon, Goldstein, Smider, Essex, Kupfer and Boyce2003; Calkins, Graziano, & Keane, Reference Calkins, Graziano and Keane2007; Gazelle & Druhen, Reference Gazelle and Druhen2009; Graziano, Keane, & Calkins, Reference Graziano, Keane and Calkins2007; Hessler & Fainsilber Katz, Reference Hessler and Fainsilber Katz2007; Suess, Porges, & Plude, Reference Suess, Porges and Plude1994). Few studies have examined race differences, although at least one recent study reported higher RSA among African American children compared to European American children (Hinnant et al., Reference Hinnant, Staton and El-Sheikh2010).

SCL and SCL reactivity (SCL-R) refer to electrodermal activity and reactivity, respectively. SCL and SCL-R are governed by the activity of sweat glands, which are innervated by the SNS component of the ANS. It is well established that SCL and SCL-R are influenced by SNS activity (Boucein, 1992; Siepmann et al., Reference Siepmann, Heine, Kluge, Ziemssen, Muck-Weymann and Kirch2007; Venables & Christie, Reference Venables, Christie, Martin and Venables1980). The SNS is activated in response to perceived stress or threat, equipping the body for a fight/flight/freeze response. Individuals with heightened SCL and SCL-R may experience high anxiety or fearfulness and exhibit inhibited behavior when faced with perceived threat, often resulting in avoidant (flight) responses (Beauchaine, Reference Beauchaine2001; Fowles, Kochanska, & Murray, Reference Fowles, Kochanska and Murray2000). Note that SCL and RSA tend to be uncorrelated (El-Sheikh et al., Reference El-Sheikh, Kouros, Erath, Cummings, Keller and Staton2009). Girls may have higher SCL than boys (e.g., Boucsein, Reference Boucsein1992; El-Sheikh, Reference El-Sheikh2007), although findings are relatively mixed (e.g., Venables & Mitchell, Reference Venables and Mitchell1996). Race differences are more consistent, such that European American children tend to exhibit higher SCL than African American children (e.g., Boucsein, Reference Boucsein1992; El-Sheikh, Keiley, & Hinnant, Reference El-Sheikh, Keiley and Hinnant2010); this finding may be explained by the inverse relation between number of sweat glands and darker skin pigmentation (Boucsein, Reference Boucsein1992).

Many of the studies to date on child risk in the context of family conflict have examined skin conductance. Another index of SNS functioning is PEP, which is also termed ventricular ejection time. PEP is the time between when the heart fills with blood and when the blood is ejected out of the heart, and it can be assessed using impedence cardiography (Andreassi, Reference Andreassi2007). Lower PEP indicates higher SNS activity and heart rate acceleration (Quigley & Stifter, Reference Quigley and Stifter2006). PEP is an established measure of SNS activity (Berntson, Cacioppo, & Fieldstone, Reference Berntson, Cacioppo and Fieldstone1994; Quigley & Stifter, Reference Quigley and Stifter2006), and the cardiac sympathetic nerves effects on the myocardium are reflected in the shortening or lengthening of preejection period (Imrich et al., Reference Imrich, Eldadah, Bentho, Pechnik, Sharabi and Holmes2008; Larkin & Kasprowicz, Reference Larkin and Kasprowicz1986). Despite the relatively small number of studies that have examined children's PEP, it may be an important index of SNS functioning that reflects trait impulsivity or approach motivation under conditions of reward (Brenner, Beauchaine, & Sylvers, Reference Brenner, Beauchaine and Sylvers2005; Richter & Gendolla, Reference Richter and Gendolla2009), whereas SCL may more specifically reflect inhibition or anxiety (e.g., Beauchaine, Hong, & Marsh, Reference Beauchaine, Hong and Marsh2008).

Alpha-amylase has recently begun to be considered as a possible marker of the SNS (Bishop, Walker, Scanlon, Richards, & Rogers, Reference Bishop, Walker, Scanlon, Richards and Rogers2006; Chatterton, Vogelsong, Lu, Ellman, & Hudgens, Reference Chatterton, Vogelsong, Lu, Ellman and Hudgens1996; Granger, Kivlighan, El-Sheikh, Gordis, & Stroud, Reference Granger, Kivlighan, El-Sheikh, Gordis and Stroud2007). However, this is still a point of debate among scholars (Nater et al., Reference Nater, Rohleder, Gaab, Berger, Jud and Kirschbaum2005, Reference Nater, La Marca, Florin, Moses and Koller2006; Rohleder, Nater, Wolf, Ehlert, & Kirschbaum, Reference Rohleder, Nater, Wolf, Ehlert and Kirschbaum2004).

Conceptual issues

Polyvagal theory is exceptionally informative as a conceptual framework for understanding the role of ANS in the context of both stress exposure and psychopathology. Below, we provide a brief overview of polyvagal theory, followed by consideration of Beauchaine's important integration of Gray's motivational theory with Porges' polyvagal theory.

As a general principle, polyvagal theory (Porges, Reference Porges2007) posits that vestiges of earlier, less complex stress response systems are available in humans and activated when more contemporary systems fail or become overwhelmed. The first response system to evolve was the dorsal vagal complex, or vegetative vagus, which is distinguished by nonmyelinated vagal motor fibers that originate in the dorsal motor nucleus of the brain. It is proposed that dorsal motor nucleus fibers become active only when innervation from the nucleus ambiguus (NA) branch of the vagus, a more recent evolutionary adaptation (discussed below), is withdrawn. In response to threat, the vegetative vagus minimizes oxygen usage and energy demand by slowing heart rate and reallocating energy throughout the body. Thus, vegetative vagus activity results in subsequent behavioral responses such as freezing in the service of avoidance.

The next evolutionary development is the SNS, which fosters mobilization. To prepare the body for action, the SNS increases cardiac output and sweat gland secretion while simultaneously inhibiting gastrointestinal tract activity. Thus, the body shifts energy from normal homeostatic functions to allow an active behavioral response. The most recent evolutionary development involves the ventral vagal complex, or smart vagus. This complex includes the myelinated vagus and portions of other cranial nerves originating in the NA, which project to various organs in the body. The trigeminal and facial nerves are also commonly considered part of this complex. Collectively, this system influences facial expression, sucking, swallowing, listening, and vocalization, and thus has been described as a social engagement system (Porges, Reference Porges2007).

In addition, activity of the ventral vagal complex exerts an inhibitory influence on the heart, and its withdrawal stimulates a heart rate increase, independent of sympathetic activity. The myelination of vagal fibers originating in the NA allows for firm control and speed in responding to the environment. Thus, the “vagal brake” can be withdrawn or instated to produce rapid changes in cardiovascular output to meet environmental demands. Furthermore, the ventral vagal complex allows for a metabolically conservative response to the environment by promoting incremental changes in heart rate to support regulated emotional responses (Porges, Reference Porges2007).

According to the polyvagal theory (Porges, Reference Porges2007), when confronted with a challenge, mammals automatically respond by first orienting then disengaging the vagal brake, inhibiting parasympathetic influence. This response results in a rapid increase in heart rate that allows the individual to engage attention in the environment, gather information, and/or use appropriate social strategies (such as enlisting complex emotions) to ameliorate the threat. If the challenge diminishes, the vagal brake can quickly reengage to reduce arousal and minimize metabolic expenditure. This ability to transiently engage and disengage with the environment allows for temporary shifts in energy, such as those required for the listening and communication phases of social interaction (Porges, Reference Porges1998). However, if the stressor is intense or chronic, then the SNS may be activated. SNS activation enables fight/flight/freeze behaviors, but is consequently more metabolically demanding than the initial vagal response. Likewise, if the sympathetic response is not sufficient to meet external challenge, then the dorsal vagal complex may engage, resulting in an immobilization response such as freezing. Although this framework is helpful as a general guideline, the progression does not occur in simple discrete steps; instead, it is characterized by “transitional blends” among systems (Porges, Reference Porges1998, p. 844). Thus, even when the PNS is adaptively regulating arousal, one or both of the other systems may be activated. Research has firmly established that stress-induced changes in heart rate can be caused by parasympathetic withdrawal, sympathetic engagement, or a combined action of the systems (Cacioppo, Uchino, & Berntson, Reference Cacioppo, Uchino and Berntson1994).

The ANS and its neural substrates serve both regulatory and social engagement functions, according to the polyvagal theory. The regulatory or calming function is explained by the inhibitory influence of the myelinated vagus on the cardiac pacemaker, and the social engagement function stems from the neuroanatomical integration of neural networks that control the vagus and neural networks that control muscles of the face and head, which regulate facial orienting and expression, speaking, and listening (Porges, Reference Porges2007). The calming and social engagement functions of the ANS may support adaptive responding in the context of family conflict and protect against the development of psychopathology.

Drawing on ideas from polyvagal theory and Gray's motivational theory (Gray, Reference Gray1987), Beauchaine (Reference Beauchaine2001) explained that regulational functions of the ANS are under PNS control, whereas motivational functions of the ANS are under SNS control. The SNS can be further divided into dimensions that stem from the neural network that governs either behavioral inhibition (BIS) and sensitivity to threat or behavioral activation (BAS) and sensitivity to appetitive stimuli (Gray, Reference Gray1987). Beauchaine's integrated conceptualization of the PNS, BIS, and BAS draws distinctions between forms of psychopathology associated with different psychophysiological profiles that cannot be drawn based on single physiological systems. For example, he indicated that most forms of psychopathology are characterized by low vagal tone, which may be considered a nonspecific marker of emotion dysregulation. To draw distinctions between different forms of psychopathology (e.g., externalizing, anxiety, depression), markers of the PNS (e.g., RSA), BIS (e.g., SCL), and BAS (e.g., PEP) should be considered. This model has been useful, for example, in distinguishing between adolescents with conduct disorder plus attention-deficit/hyperactivity disorder, who exhibited reduced electrodermal responding and reduced SNS-linked cardiac activity (i.e., lengthened PEP; see also Crowell et al., Reference Crowell, Beauchaine, Gatzke-Kopp, Sylvers, Mead and Chipman-Chacon2006), and adolescents with attention-deficit/hyperactivity disorder only, who exhibited reduced electrodermal responding but not lengthened PEP (Beauchaine et al., Reference Beauchaine, Katkin, Strassberg and Snarr2001). Research to elucidate the connection between neurophysiological motivational constructs (e.g., BIS, BAS) and peripheral autonomic measures (e.g., SCL, PEP) continues to evolve (e.g., Brenner et al., Reference Brenner, Beauchaine and Sylvers2005).

Beauchaine and colleagues (e.g., Beauchaine Reference Beauchaine2001; Beauchaine et al., Reference Beauchaine, Gatzke-Kopp and Mead2007; Beauchaine, Klein, Crowell, Derbidge, & Gatzke-Kopp, Reference Beauchaine, Klein, Crowell, Derbidge and Gatzke-Kopp2009) have described a developmental model in which inherited impulsivity, marked by low SNS activity and reactivity, may or may not develop into severe conduct problems, depending upon emotion socialization in the family. Early childhood behavior problems may lead to poor PNS (i.e., vagal) and emotion regulation, as well as severe conduct problems in middle childhood, via coercive family processes, in which negative affect and aggressive behavior are negatively reinforced (Patterson et al., Reference Patterson, Reid and Dishion1992). Alternatively, a protective family environment, characterized by consistent positive reinforcement of appropriate behavior and controlled consequences for aggressive behavior, may foster PNS and emotion regulation abilities that buffer impulsive children from developing angry and aggressive behavioral patterns (Beauchaine et al., Reference Beauchaine, Gatzke-Kopp and Mead2007).

The conceptual frameworks described above demonstrate the value of contemporaneous consideration of the SNS and PNS to fully understand psychological adjustment in the context of family conflict. Next, we review the literature on family conflict and both child adjustment and ANS activity, followed by the literature linking ANS activity with children's maladjustment, and we conclude with research documenting interactions among family conflict and indices of ANS activity, which is the focus of our paper and the subject of most attention.

Family conflict and child adaptation

In this review, we focus on marital conflict and parent–child conflict, broadly construed; other important forms of family conflict, such as sibling conflict, have yet to be investigated in combination with ANS functioning. Because abusive parent–child interactions are different in form and severity from normative forms of family conflict, and may have different associations with either our focal variables (e.g., ANS activity) or different psychopathology processes (e.g., posttraumatic disorders), we do not focus on child abuse. We refer to destructive forms of marital conflict that involve physical aggression, nonverbal or verbal hostility, or threat to the intactness of the family (Cummings, Goeke-Morey, & Papp, Reference Cummings, Goeke-Morey and Papp2004). Associations between marital conflict and various dimensions of children's internalizing and externalizing problems have been documented thoroughly, and explained in terms of emotional insecurity (Davies, Harold, Goeke-Morey, & Cummings, Reference Davies, Harold, Goeke-Morey and Cummings2002), cognitive representations of threat and self-blame (Grych & Fincham, Reference Grych and Fincham1990), social learning of aggressive behavior (Bandura, Reference Bandura1977), specific emotions (Crockenberg & Langrock, Reference Crockenberg and Langrock2001), and negative spillover into the parent–child relationship (Erel & Burman, Reference Erel and Burman1995). Recent studies have investigated a broader range of health outcomes, finding that children's exposure to marital conflict also increases their risk for sleep disturbances (El-Sheikh, Buckhalt, Mize, & Acebo, Reference El Sheikh, Buckhalt, Mize and Acebo2006) and physical health problems (El-Sheikh, Cummings, Kouros, Elmore-Staton, & Buckhalt, Reference El-Sheikh, Cummings, Kouros, Elmore-Staton and Buckhalt2008; Troxel & Matthews, Reference Troxel and Matthews2004).

In addition, numerous studies have linked parent–child conflict with children's externalizing and internalizing problems, and the association appears to be reciprocal (Burt, McGue, Krueger, & Iacono, Reference Burt, McGue, Krueger and Iacono2005; Pettit & Arsiwalla, Reference Pettit and Arsiwalla2008). For example, harsh parenting refers to coercive acts and negative emotional expressions that parents direct toward children, including verbal and physical aggression; the association between harsh parent–child interactions and externalizing behaviors is robust (Gershoff, Reference Gershoff2002). Psychological control in the parent–child relationship (e.g., inducing guilt, withdrawing love, invalidating the child's perspective), in contrast, is linked especially with child internalizing symptoms (for a review, see Barber & Harmon, Reference Barber, Harmon and Barber2002). Despite some evidence for specificity, however, marital conflict and various forms of parent–child conflict have been linked with both internalizing and externalizing problems. Some investigators have suggested that environmental stressors, such as family conflict, operate as nonspecific risk factors in the elicitation of child maladjustment, with physiological arousal and regulation shaping the specific form of maladjustment that emerges (Steinberg & Avenevoli, Reference Steinberg and Avenevoli2000).

Family conflict and ANS functioning

Several studies offer important evidence for associations linking negative parent–child interactions and marital conflict with patterns of ANS functioning that are generally considered maladaptive. For example, mothers' negative and controlling parenting behaviors have been linked with lower RSA (Kennedy, Rubin, Hastings, & Maisel, Reference Kennedy, Rubin, Hastings and Maisel2004) and lower task-related reductions in RSA (Calkins, Smith, Gill, & Johnson Reference Calkins, Smith, Gill and Johnson1998) in young children. Marital conflict also has been linked with lower RSA in infants (Porter, Wouden-Miller, Silva, & Porter, Reference Porter, Wouden-Miller, Silva and Porter2003) and lower reductions in RSA during a peer provocation task in middle childhood (Katz, Reference Katz2007). A recent study reported that adolescents with a history of mental health problems and lower levels of secure-base support from their parent exhibited weaker RSA reductions and RSA recovery during a stress task and reunion with the parent (Willemen, Schuengel, & Koot, Reference Willemen, Schuengel and Koot2009).

In addition, El-Sheikh (Reference El-Sheikh2005b) reported that aggressive marital conflict was associated with higher baseline SCL (girls and boys) and higher SCL-R reactivity (boys only). These findings are consistent with the allostatic load model, which contends that unremitting exposure to intense stress, failure to habituate to moderate stress, or unchecked activation of stress responses incurs wear and tear on physiological systems (McEwen, Reference McEwen1998). Over time, these physiological systems may become dysregulated and uncoordinated, increasing risk for psychological problems as well as cardiovascular problems and physical illnesses (Gunnar & Vazquez, Reference Gunnar, Vazquez, Cicchetti and Cohen2006; McEwen & Lasley, Reference McEwen and Lasley2002; Repetti, Taylor, & Seeman, Reference Repetti, Taylor and Seeman2002).

Employing another measure of SNS activity, Salomon, Matthews, and Allen (Reference Salomon, Matthews and Allen2000) reported that higher child- and parent-reported family conflict were associated with a combination of increased PEP and decreased RSA during reactivity tasks in the lab (reaction time, mirror-tracing, social competence interview). It is interesting to note that, across two studies, some form of family conflict has been linked with elevations in SCL responses (El-Sheikh, Reference El-Sheikh2005b) and increases in PEP (Salomon et al., Reference Salomon, Matthews and Allen2000). This pattern of responding across SCL and PEP, representing high activation of the BIS and low activation of the BAS, has been tied to depression in children (Beauchaine, Reference Beauchaine2001), and the combination of exposure to marital conflict and higher skin conductance reactivity has been linked to internalizing symptoms among girls (El-Sheikh, Reference El-Sheikh2005b). These findings highlight the advantages of investigating multiple physiological markers and distinguishing their roles in emotional and behavioral regulation. Of course, further research is necessary before conclusions can be drawn about specific links between family conflict and different dimensions of the SNS; efforts to discern the role of lab task in physiological responses will be especially important.

ANS functioning and child adaptation

Interactions between family conflict and ANS functioning

Indices of PNS functioning have been examined relatively thoroughly as moderators of marital conflict. In almost all of these studies, higher vagal tone and vagal withdrawal have operated as protective factors in the context of family conflict; that is, the association between marital conflict and child maladjustment is less pronounced among children with higher vagal tone or vagal withdrawal, compared to children with lower vagal tone or vagal augmentation (for an exception, see Obradovic, Bush, Stamperdahl, Adler, & Boyce, Reference Obradovic, Bush, Stamperdahl, Adler and Boyce2010). The protective function of higher RSA or greater reductions in RSA during stress or challenge has been evident across cross-sectional (El-Sheikh, Harger, & Whitson, Reference El-Sheikh, Harger and Whitson2001; Katz & Gottman, Reference Katz and Gottman1995) and longitudinal studies (El-Sheikh & Whitson, Reference El-Sheikh and Whitson2006; Katz & Gottman, Reference Katz and Gottman1997; Leary & Katz, Reference Leary and Katz2004); across multi-informant (El-Sheikh et al., Reference El-Sheikh, Harger and Whitson2001; El-Sheikh & Whitson, Reference El-Sheikh and Whitson2006; Katz & Gottman, Reference Katz and Gottman1995) and observational (Katz & Gottman, Reference Katz and Gottman1995; Leary & Katz, Reference Leary and Katz2004) sources; and across externalizing, internalizing (El-Sheikh et al., Reference El-Sheikh, Harger and Whitson2001; El-Sheikh & Whitson, Reference El-Sheikh and Whitson2006; Katz & Gottman, Reference Katz and Gottman1995, Reference Katz and Gottman1997), social (Leary & Katz, Reference Leary and Katz2004), and physical health (El-Sheikh et al., Reference El-Sheikh, Harger and Whitson2001; Whitson & El-Sheikh, Reference Whitson and El-Sheikh2003) outcomes. Similarly, the protective effects of higher RSA have been documented in the context of parent–child conflict (Whitson & El-Sheikh, Reference Whitson and El-Sheikh2003) and child maltreatment (Gordis, Feres, Olezeski, Rabkin, & Trickett, Reference Gordis, Feres, Olezeski, Rabkin and Trickett2010). The purported protective effect of higher vagal tone and vagal withdrawal in the context of marital conflict has been attributed to the ways in which these PNS processes may reflect or support emotion regulation and social engagement (Porges, Reference Porges2007).

Despite the overall evidence for the protective functions of higher vagal tone and increased vagal withdrawal in the context of family conflict, evidence for gender differences is somewhat mixed. For example, in cross-sectional analyses, greater reductions in RSA protected only boys against externalizing and health problems associated with verbal and physical marital conflict, respectively (El-Sheikh et al., Reference El-Sheikh, Harger and Whitson2001). In contrast, in longitudinal analyses, greater reductions in RSA protected only girls against internalizing problems associated with marital conflict (El-Sheikh & Whitson, Reference El-Sheikh and Whitson2006). Although some sex differences exist across particular studies with particular outcomes, the protective functions of higher vagal tone and increased vagal withdrawal have been replicated among boys and girls.

Several studies have investigated interactions between family conflict and SNS functioning. For example, El-Sheikh (Reference El-Sheikh2005b) found a stronger association between marital conflict and both internalizing and externalizing behavior among girls with higher SCL-R, compared to girls with lower SCLR. In longitudinal analyses with the same sample, El-Sheikh, Keller, and Erath (Reference El-Sheikh, Keller and Erath2007) reported that marital conflict predicted increased externalizing problems among boys with lower SCLR and among girls with either lower or higher SCLR (but especially among girls with higher SCLR). Thus, in the context of marital conflict, some existing evidence suggests that higher SCLR may be a stronger vulnerability factor among girls compared to boys (El-Sheikh, Reference El-Sheikh2005b; El-Sheikh et al., Reference El-Sheikh, Keller and Erath2007), which is consistent with evidence that aggressive girls exhibit higher electrodermal activity than nonaggressive girls (Beauchaine et al., Reference Beauchaine, Hong and Marsh2008).

Two recent studies provided evidence that externalizing behavior may be high and stable from middle to late childhood among boys with relatively harsh parents and lower SCLR, compared to boys with relatively harsh parents and higher SCLR, whose externalizing behavior may increase during later childhood (age 8 to age 10; Erath, El-Sheikh, & Cummings, Reference Erath, El-Sheikh and Cummings2009; Erath, El-Sheikh, Hinnant, & Cummings, Reference Erath, El-Sheikh, Hinnant and Cummings2010). In these studies, girls and boys with less harsh parents exhibited relatively lower externalizing behavior throughout late childhood irrespective of their SCLR.

Collectively, these studies are relatively consistent in showing that boys with lower SCLR exhibit elevated levels of externalizing problems, particularly in the context of either marital conflict (El-Sheikh et al., Reference El-Sheikh, Keller and Erath2007) or harsh parenting (Erath et al., Reference Erath, El-Sheikh and Cummings2009, Reference Erath, El-Sheikh, Hinnant and Cummings2010). These findings may be interpreted by integrating learning theories with models of psychophysiology and antisocial behavior. Reduced SCLR may reflect a predisposition toward behavioral disinhibition or punishment insensitivity (Beauchaine, Reference Beauchaine2001), which may be more common among boys compared to girls. This temperamental characteristic may set the stage for coercive parent–child exchanges, and perhaps increase the likelihood that children will learn aggression from harsh parenting (e.g., observational learning, negative reinforcement) rather than feel punished by it (Dadds & Salmon, Reference Dadds and Salmon2003; Patterson et al., Reference Patterson, Reid and Dishion1992; Reid, Patterson, & Snyder, Reference Reid, Patterson and Snyder2002).

Evidence has been less consistent regarding the risk for psychological maladjustment among children with higher SCLR in the context of family conflict. In El-Sheikh (Reference El-Sheikh2005b) and El-Sheikh et al (Reference El-Sheikh, Keller and Erath2007), higher SCLR was a vulnerability factor for externalizing and internalizing problems in the context of marital conflict among girls. In Erath et al. (Reference Erath, El-Sheikh, Hinnant and Cummings2010), however, only boys with higher SCLR and relatively harsh parents exhibited increases in externalizing behavior from middle childhood to late childhood. It is possible that family conflict predicts externalizing behavior over time among children with higher SCLR because their behavior is particularly responsive to environmental stress and contingencies, potentially reflecting susceptibility to environmental influences (Belsky & Pluess, Reference Belsky and Pluess2009) or biological sensitivity to context (Boyce & Ellis, Reference Boyce and Ellis2005). Wootton, Frick, Shelton, and Silverthorn (Reference Wootton, Frick, Shelton and Silverthorn1997) reported that children without callous-unemotional traits, consistent with normal or high SCLR, exhibited elevated conduct problems only in the context of ineffective parenting (see also, Shannon, Beauchaine, Brenner, Neuhaus, and Gatzke-Kopp, Reference Shannon, Beauchaine, Brenner, Neuhaus and Gatzke-Kopp2007). Children who exhibit higher SCLR, who may be more sensitive to aversive circumstances than children with lower SCLR, may be especially likely to react negatively to family conflict or harsh parenting during a developmental period characterized by increasing needs for autonomy from parents. Thus, existing research suggests that the risk associated with SCLR may depend on age, gender, and type of family conflict.

Interactions between the SNS and PNS

Investigations of interactions between family conflict and single indices of autonomic activity (i.e., either SNS or PNS) have provided important insights about risk and resilience in children. However, similar to environmental factors that moderate the influence of one another (e.g., Lindsey, Caldera, & Tankersley, Reference Lindsey, Caldera and Tankersley2009; Pettit, Bates, Dodge, & Meece, Reference Pettit, Bates, Dodge and Meece1999), single physiological systems do not operate in isolation. Multiple physiological systems cooperate to serve homeostatic functions under ideal circumstances and to meet individual or environmental demands under challenging conditions (Bauer, Quas, & Boyce, Reference Bauer, Quas and Boyce2002). Because of innate biological vulnerabilities or experiences of intense or chronic stress, however, physiological systems may become uncoordinated or dysregulated, potentially exacerbating the toll of exposure to family stress (Bauer et al., Reference Bauer, Quas and Boyce2002).

Investigators have begun to consider the joint action of the two branches of the ANS, the SNS and PNS, and we expect that further research along these lines will help clarify inconsistencies in the literature on family stress and psychophysiological processes. For example, Beauchaine (Reference Beauchaine2001) explained that low vagal tone is linked with a range of negative child outcomes, including internalizing and externalizing problems; to predict whether low vagal tone will manifest as an externalizing or internalizing problem, the SNS must be considered as well.

Another model, the doctrine of autonomic space, concerns the simultaneous action of the SNS and PNS on target organs that are innervated by both branches of the ANS (e.g., heart; Berntson et al., Reference Berntson, Cacioppo and Quigley1991; Berntson & Cacioppo, Reference Berntson, Cacioppo, Malik and Camm2004). It is important to note that the autonomic space literature refers specifically to SNS-linked cardiac reactivity (e.g., cardiac PEP), which is discussed in further detail below. The autonomic space model does not refer to electrodermal measures of the SNS (i.e., SCL). However, given the much larger body of research linking electrodermal measures (compared to PEP) with family conflict and children's psychological functioning, and the opportunity to test interactions between PNS measures and electrodermal measures in many existing data sets, we believe it is worthwhile to consider whether the effects of SNS activation or inhibition, reflected in electrodermal measures, may be conditional upon PNS activation or inhibition, reflected in measures of RSA. Thus, we consider the synergistic action of the PNS and SNS, like the autonomic space model (El-Sheikh et al., Reference El-Sheikh, Kouros, Erath, Cummings, Keller and Staton2009), but acknowledge that our focus on SCL as a marker of SNS activity diverges from the autonomic space model.

According to the autonomic space model (Berntson et al., Reference Berntson, Cacioppo and Quigley1991; Berntson & Cacioppo, Reference Berntson, Cacioppo, Malik and Camm2004), reciprocal activation refers to conditions under which both branches of the ANS promote the same directional response in a target organ or system (e.g., see Table 1). Reciprocal sympathetic activation involves sympathetic activation and parasympathetic inhibition, both of which upregulate physiological processes such as heart rate and cardiovascular output. By comparison, reciprocal parasympathetic activation is characterized by sympathetic inhibition and parasympathetic activation, both of which downregulate similar physiological processes, serving homeostatic and calming functions. Nonreciprocal activation refers to conditions under which branches of the ANS promote opposing responses in target systems. Specifically, coactivation refers to increased sympathetic and parasympathetic action, and coinhibition refers to decreased action of both branches. Because sympathetic and parasympathetic actions serve opposing physiological functions, such parallel, or nonreciprocal, activation may promote opposing physiological outcomes.

Table 1.

Autonomic nervous system profiles

Note: SNS, sympathetic nervous system; PNS, parasympathetic nervous system; SCL, skin conductance level; RSA, respiratory sinus arrhythmia.

Berntson et al. (Reference Berntson, Cacioppo and Quigley1991) explain that modes of reciprocal activation can produce strong, unidirectional changes in the system under autonomic influence. Thus, reciprocal sympathetic activation may be well-suited for adjustments to challenge or stress, particularly when the necessary coping response is well defined, whereas reciprocal parasympathetic activation may be most appropriate for situations in which a calm physiological state is beneficial. Modes of nonreciprocal activation, in contrast, yield a more ambivalent physiological response because the action of ANS branches is in opposition. In the case of coactivation or coinhibition, it is actually possible that little or no change in the state of the target system would occur if the relative activation of sympathetic and parasympathetic branches was equivalent. Thus, nonreciprocal modes may operate to preserve the baseline functional state of an organ or system in situations without challenge or stress. It is also possible that nonreciprocal activation occurs when the optimal behavioral response in a novel or challenging situation is unclear to the individual (Berntson et al., Reference Berntson, Cacioppo and Quigley1991).

Studies that have utilized the autonomic space framework have found that reciprocal sympathetic activation is a normative response to stress among children and adolescents (Salomon et al., Reference Salomon, Matthews and Allen2000). However, the most common response profile may vary developmentally (Alkon et al., Reference Alkon, Goldstein, Smider, Essex, Kupfer and Boyce2003), and children with externalizing behavior problems often exhibit coinhibition in response to laboratory challenges (Beauchaine et al., Reference Beauchaine, Gatzke-Kopp and Mead2007; Boyce et al, Reference Boyce, Quas, Alkon, Smider, Essex and Kupfer2001). In a series of studies informed by Berntson and colleagues (1991), as well as models reviewed above (Beauchaine, Reference Beauchaine2001; Porges, Reference Porges2007), SNS × PNS interactions were examined in the context of marital conflict as predictors of children's externalizing behaviors, as described below (El-Sheikh et al., Reference El-Sheikh, Kouros, Erath, Cummings, Keller and Staton2009).

Interactions among the SNS, PNS, and family conflict

A core principle of developmental psychopathology is that child outcomes are best understood in terms of transactions among multiple individual and environmental variables (Masten, Reference Masten2006). Likewise, a critical next step is to apply integrated conceptualizations of SNS and PNS responses to stressful environmental contexts that evoke ANS reactivity. As such, interactions between SCL and RSA were investigated as moderators of the relation between marital conflict and child externalizing behavior (El-Sheikh et al., Reference El-Sheikh, Kouros, Erath, Cummings, Keller and Staton2009).

Analyses revealed that opposing action of the PNS and SNS (i.e., coactivation and coinhibition in autonomic space terms) operated as a vulnerability factor for externalizing behavior in the context of marital conflict, whereas reciprocal action of the PNS and SNS (i.e., reciprocal sympathetic activation and reciprocal parasympathetic activation in autonomic space terms) operated as a protective factor (El-Sheikh et al., Reference El-Sheikh, Kouros, Erath, Cummings, Keller and Staton2009). This pattern of findings emerged consistently in three studies with multimethod and multi-informant designs, including mother, father, and child reports of marital conflict; mother, father, and teacher reports of various child externalizing problems, and physiological data on child responses to different laboratory stress tasks. Of note, Gordis et al. (Reference Gordis, Feres, Olezeski, Rabkin and Trickett2010) also reported that coinhibition, reflected in low levels of both basal RSA and SCL reactivity, and coactivation, reflected in high levels of both basal RSA and SCL reactivity, exacerbated the association between child maltreatment and aggressive behavior among girls. On the basis of these results, we offered the following tentative assertions about the functions of autonomic profiles in the context of marital conflict (El-Sheikh et al., Reference El-Sheikh, Kouros, Erath, Cummings, Keller and Staton2009).

Coactivation may indicate that the PNS response is insufficient for managing a stressor (as reflected in vagal augmentation rather than vagal withdrawal), prompting activation of a significant SNS response. As such, coactivation may reflect physiological overarousal, given the potential SNS “override” of the PNS response (Porges, Reference Porges1995, Reference Porges2001), and thus it is possible that coactivation enables dysregulated, fight/flight/freeze responses to conflict as well as child involvement in marital conflict. Such high emotional reactivity may set the stage for coercive exchanges between parents and their children, in which children are negatively reinforced for aggressive attempts to end conflict (Patterson, Reference Patterson, Reid, Patterson and Snyder2002). High emotional reactivity may also contribute to increased child involvement and exposure to conflict, and thereby enhance sensitization to conflict (Cummings & Davies, Reference Cummings and Davies1994).

Coinhibition may reflect an ambivalent physiological response in which the PNS equips the child for action by withdrawing its inhibitory influence, whereas the sympathetic system, conversely, fails to produce the metabolic output needed for an active behavioral or emotional response. Potentially, such a physiological response may promote passive vigilance, which could result in increased exposure to marital conflict and limited efforts to reduce exposure, such as by communicating upset feelings to parents. It is possible that coinhibition of ANS branches is more characteristic of children with underaroused antisocial behavior (Raine, Reference Raine2002), or callous–unemotional traits (Frick & Ellis, Reference Frick and Ellis1999). For example, low vagal tone may reflect poor emotion regulation, and diminished SNS arousal may suggest fearlessness, failure of avoidance learning, or punishment insensitivity (Raine, Reference Raine2002).

Reciprocal sympathetic activation may reflect an efficient parasympathetic response to stress (as reflected in vagal withdrawal) and a corresponding (moderate) sympathetic response to meet metabolic demands. In the context of marital conflict, reciprocal sympathetic activation may indicate appropriate concern or anger, yet also promotes constructive attempts to address worries with adults or attempts to reduce exposure to conflict. In contrast, reciprocal parasympathetic activation and sympathetic inhibition may occur when marital conflict is not interpreted as especially threatening, and is managed efficiently and effectively through vagal withdrawal, without resorting to SNS activation. This type of ANS response pattern may reflect effective self-soothing in the context of marital conflict.

Although our work diverges from the autonomic space model (Berntson et al., Reference Berntson, Cacioppo and Quigley1991) in that we examined SCL versus cardiac measures of SNS activity, our findings and those of Gordis et al. (Reference Gordis, Feres, Olezeski, Rabkin and Trickett2010) are consistent with this body of work in that SCL appeared to operate like PEP in conjunction with PNS activity to predict child behavior. Although both SCL and PEP are influenced by the SNS, it is important for future research to further support the application of electrodermal measures to the autonomic space model. In addition, although the autonomic space literature focuses on physiological reactivity, we examined all combinations of SCL and RSA at baseline and in response to laboratory tasks and demonstrated their effects (see also Gordis et al., Reference Gordis, Feres, Olezeski, Rabkin and Trickett2010).

Likewise, our findings can be interpreted in the context of our expansion on polyvagal theory propositions (Porges, Reference Porges2007). Specifically, although Porges did not focus on interactions among the PNS, SNS, and dorsal vagal systems per se, he proposed that responses across these systems in the face of stress do not proceed in a linear fashion and are often characterized by blending of physiological activity across these systems. Findings (El-Sheikh et al., Reference El-Sheikh, Kouros, Erath, Cummings, Keller and Staton2009; Gordis et al., Reference Gordis, Feres, Olezeski, Rabkin and Trickett2010) suggest that reciprocal modes of ANS responding may indicate that more evolutionarily advanced response strategies have been effective and sufficient, whereas coactivation and coinhibition may suggest a breakdown in regulation, in which either the PNS or SNS system fails to perform its adaptive function in response to stress.

Our findings are also consistent with Beauchaine's and colleagues' (2001, 2007) research, which suggests that children with clinical levels of externalizing problems are likely characterized by coinhibition, or reduced activity of both the parasympathetic and sympathetic branches. Findings reported in the Monograph (El-Sheikh et al., Reference El-Sheikh, Kouros, Erath, Cummings, Keller and Staton2009) build on Beauchaine's work and extend it, particularly by showing that certain patterns of SNS and PNS activity can operate as vulnerability or protective factors in the context of marital conflict. It is important to note that neither the polyvagal theory nor autonomic space model deal specifically with exposure to family stress. Our model is most similar to that of Beauchaine and colleagues in its integration of family stress, autonomic activity, and psychopathology, although we focus more on interactions between family risk and the two branches of the ANS in the prediction of psychopathology.

Developmental progressions

The vast majority of research on children's ANS functioning and psychological adaptation in the context of family conflict has employed cross-sectional or short-term longitudinal designs with two data collection points. Multiyear studies that cross developmental periods and transitions (e.g., transition to elementary school, puberty) are necessary to illuminate the direction of associations, the malleability of ANS functioning, and the potential of developmental change in the intervening role of ANS functioning (e.g., mediation, moderation). To this point, investigators have put forth several intriguing developmental models that warrant further empirical examination.

For example, according to the biological sensitivity to context model (e.g., Boyce & Ellis, Reference Boyce and Ellis2005; Ellis & Boyce, Reference Ellis and Boyce2006), children may develop heightened sensitivity to their family context, reflected in high ANS reactivity, under conditions of nurturance and support or under conditions of stress and adversity (for a complementary theory, see differential susceptibility to environmental influence; Belsky, Reference Belsky, Ellis and Bjorklund2005). In the former case, high ANS reactivity is an evolutionarily adaptive response that maximizes exposure to enriching qualities of the environment, whereas in the latter case, high reactivity is an adaptive response (at least in the short term) that promotes vigilance to environmental hazards. In addition, as reviewed above, Beauchaine and colleagues (e.g., Beauchaine, Reference Beauchaine2001; Beauchaine et al., Reference Beauchaine, Gatzke-Kopp and Mead2007) have discussed a developmental model in which inherited impulsivity, marked by low SNS activity and reactivity, may or may not develop into severe conduct problems depending upon family processes (e.g., coercive parent–child interactions) that either support or undermine emotional and physiological regulation.

Although the specific hypotheses of the developmental models discussed above require further longitudinal investigation, some empirical support exists for the proposition that ANS activity is responsive to early environmental influence. For example, Gottman, Katz, and Hooven (Reference Gottman, Katz and Hooven1996) reported that parental emotion coaching predicted higher baseline RSA during middle childhood. A growing body of studies has linked responsive and synchronous parenting with infants' higher RSA (for a review, see Propper & Moore, Reference Propper and Moore2006), and concordance between mothers' and children's vagal withdrawal to environmental challenges appears to increase from infancy through early childhood (Bornstein & Suess, Reference Bornstein and Suess2000). Prevention and intervention studies also support the malleability of ANS functioning. For instance, educational, social–emotional, and health enrichment in early childhood has been linked with adaptive SNS arousal in response to laboratory tasks (i.e., increased amplitude and speed of electrodermal responding) during preadolescence in a controlled, experimental trial (Raine et al., Reference Raine, Venables, Dalais, Mellingen, Reynolds and Mednick2001). Habitual exercise and other lifestyle factors have also been linked with changes in vagal tone over time in adults (Rennie et al., Reference Rennie, Hemingway, Kumari, Brunner, Malik and Marmot2003; Thayer & Lane, Reference Thayer and Lane2007). Preliminary evidence also supports the utility of acupuncture to increase vagal tone in depressed women, which in turn results in decreased depression (Chambers & Allen, Reference Chambers and Allen2002). In addition, RSA may be alterable using biofeedback (Hatch, Borcherding, & German, Reference Hatch, Borcherding and German1992) or medication (Porges, Reference Porges and Reese1976).

Psychophysiological response patterns probably retain some malleability throughout the lifespan, as suggested by the studies described above, but research suggests that ANS responses become more stable over time. In particular, evidence has emerged for moderate stability in baseline and reactivity levels of SNS and PNS activity in middle to late childhood (Bornstein & Suess, Reference Bornstein and Suess2000; Calkins & Keane, Reference Calkins and Keane2004; Doussard-Roosevelt, Montgomery, & Porges, Reference Doussard-Roosevelt, Montgomery and Porges2003; El-Sheikh, Reference El-Sheikh2005a, Reference El-Sheikh2007); lower levels of stability are observed for reactivity than resting SNS and PNS measures. As such, one possibility is that, following a period of greater susceptibility to family and general environmental influence, ANS reactivity to stressors becomes relatively stable around late childhood or early adolescence, at which time it can be considered an individual difference variable that exacerbates or ameliorates the risk for adjustment problems in the context of family conflict (El-Sheikh, Reference El-Sheikh2001; El-Sheikh et al., Reference El-Sheikh, Keller and Erath2007). Our proposition that family factors may exert influences on children's ANS reactivity more strongly in infancy and early childhood, and then primarily function to interact with physiological patterns in late childhood and adolescence, requires further empirical investigation. This hypothesis is similar to Barlow's (Reference Barlow2000) conceptualization of the development of internalizing disorders in which individual vulnerabilities associated with internalizing symptoms are fostered by environmental stressors early in life (i.e., mediation model), yet go on to amplify environmental stressors later in life (i.e., moderation model).

To understand developmental changes in the intervening role (e.g., mediation or moderation) of ANS activity, we must also understand its normative developmental course. Few studies have examined the developmental course of ANS activity, but existing research suggests some important directions for future research. There is evidence that baseline RSA increases from infancy through middle childhood (Propper & Moore, Reference Propper and Moore2006). However, Salomon (Reference Salomon2005) found that greater reductions in RSA during lab stress protocols in prepubertal 8- to 10-year-olds predicted lower resting RSA approximately 3 years later, controlling for earlier resting RSA. Salomon suggested that repeated vagal withdrawal to stress may alter the set point for resting vagal tone, as the PNS adapts to anticipate continued homeostatic disturbances in the future. As such, under conditions of chronic stress in which children repeatedly withdraw vagal tone to increase vigilance and active coping, resting vagal tone may become conditioned to anticipate circumstances that require vigilance and coping, and thus decline over time.

The implications are intriguing. Several studies have shown that vagal withdrawal in the context of stress or challenge is associated positively with social and emotional regulation, and also operates as a protective factor in the context of family stress. One tentative possibility, however, is that despite the apparently adaptive function of vagal withdrawal in the short term, it could operate as a risk factor for lower resting vagal tone and the associated mental and physical health problems in the long term in the context of high stress exposure.

The altered operation of the HPA axis in the context of chronic stress (e.g., Miller, Chen, & Zhou, Reference Miller, Chen and Zhou2007) is an interesting parallel to the declining basal levels of PNS activity among children who exhibit vagal withdrawal earlier in development. According to the hypercortisolism hypothesis, chronic stress sensitizes the HPA axis to subsequent stress, such that the HPA axis increasingly generates physiological resources to cope with perceived threat. In turn, sustained elevations in HPA activity produce allostatic load and damage the development and functioning of neural and cognitive systems, resulting in child health problems and psychological maladjustment (Gunnar & Vazquez, Reference Gunnar, Vazquez, Cicchetti and Cohen2006; McEwen, Reference McEwen1998; McEwen & Lasley, Reference McEwen and Lasley2002; Repetti et al., Reference Repetti, Taylor and Seeman2002). In contrast, the hypocortisolism hypothesis (Miller et al., Reference Miller, Chen and Zhou2007) suggests that chronic HPA activation can result in blunting of responses over time, which is also associated with negative psychological outcomes. Likewise, children may become psychologically sensitized to intense marital conflict, such that they begin to interpret even mild stressors in the family as precursors of serious threat, inducing heightened distress and impeding effective coping (Davies & Cummings, Reference Davies, Cummings, Cicchetti and Cohen2006). Thus, initially adaptive physiological and psychological responses may become maladaptive over time due to intense and frequent exposure to environmental stress.

These findings (e.g., Salomon, Reference Salomon2005) may be interpreted within the biological sensitivity to context framework (Boyce & Ellis, Reference Boyce and Ellis2005), which proposes that highly reactive children, who are presumably most susceptible to environmental influence, should demonstrate the best outcomes under positive conditions and the worst outcomes under negative conditions (for a complementary theory, see differential susceptibility to environmental influence; Belsky, Reference Belsky, Ellis and Bjorklund2005). Highly reactive children (e.g., very high vagal withdrawal) may experience particularly negative outcomes under adverse conditions, at least in part, because repeated incidents of stress exposure may contribute to a state of increased reactivity to stressors over time. Clearly, this is an area of research in which many important questions remain unanswered. Further investigation may yield critical information about when in development adjustment problems are most likely to emerge among children who experience chronic or intense family conflict, depending on their ANS profile.

Further examination of individual systems

Multisystem interactions

In the sections above, we described recent research on SNS × PNS interactions, including ANS interactions contextualized by family conflict. Although our focus in this paper is on interactions between ANS indices and conflict, HPA axis activity is a major component of the stress response system, and the ANS and HPA systems are linked anatomically and functionally (see Benarroch, Reference Benarroch1993; Thayer & Lane, 2006, Reference Thayer and Lane2009). Thus, HPA activity may modulate the functioning of the ANS and further interact with family conflict in the prediction of psychopathology (Gordis, Granger, Susman, & Trickett, 2008). In this section, we discuss the emerging literature on two-way interactions between the ANS and HPA activity, and call for investigations of ANS × HPA interactions in the family context.

Differential effects depending on source of stress, lab stimuli, and child outcomes