Development and Psychopathology, 13 (2001), 183–214
Copyright 2001 Cambridge University Press
Printed in the United States of America
Vagal tone, development, and Gray’s
motivational theory: Toward an integrated
model of autonomic nervous system
functioning in psychopathology
University of Washington
In the last decade, cardiac vagal tone has emerged as a psychophysiological marker of many aspects of behavioral
functioning in both children and adults. Research efforts during this time have produced an extensive list of vagal
tone correlates that includes temperamental variables as well as both anxious/internalizing and disruptive/
externalizing behaviors. This potentially confusing state of affairs is compounded by developmental shifts in vagal
tone–behavior relations that to date have not been elucidated. In this paper, the vagal tone literature is reviewed, and
discrepancies, including the lack of specificity of vagal tone as a psychophysiological marker, are clarified. Such
clarification requires that we (a) view vagal tone–behavior relations in developmental context, (b) juxtapose vagal
tone–behavior relations in typical and atypical samples, and (c) consider the parasympathetic underpinnings of vagal
tone as but one component in a broader model of autonomic nervous system functioning. Such a model is provided
by combining Gray’s motivational theory with Porges’s polyvagal theory. Together these models account for
behavioral and emotional differences in a diverse range of psychological disorders that are not differentiated by
either model alone. Moreover, use of the integrated model offers a theory-driven approach to the study of autonomic
nervous system–behavior relations.
Cardiac vagal tone has received considerable Simmons, Haynes, & Cohen, 1991), empathic
responding (e.g., Fabes, Eisenberg, Karbon,attention in recent years as a psychophysio-
logical marker of emotion regulation, and of Troyer, & Switzer, 1994), social competence
(Eisenberg, Fabes, Murphy, Maszk, Smith, &certain aspects psychological adjustment. In
infant and child samples, individual differ- Karbon, 1995), attentional capacity (Suess,
Porges, & Plude, 1994), behavioral inhibitionences in indices of vagal tone and vagal reac-
tivity have been demonstrated to reflect emo- (e.g., Kagan & Snidman, 1991), and aggres-
sion (e.g., Pine, Wasserman, Coplan, Fried,tional expressiveness (Stifter, Fox, & Porges,
1989), temperamental reactivity (e.g., Cal- Sloan, Myers, Greenhill, Shaffer, & Parsons,
1996). Additionally, studies of adolescentskins, 1997), attachment status (Izard, Porges,
and adults have linked atypical vagal tone to
hostility (Sloan, Shapiro, Bigger, Bagiella,
This work was supported by National Research Service
Steinman, & Gorman, 1994), aggression
Award 1F31MH12209 from the National Institute of
Mental Health. The author expresses thanks to Edward S. (Mezzacappa, Tremblay, Kindlon, Saul, Arse-
Katkin and Robert M. Kelsey for their helpful comments
neault, Seguin, Pihl, & Earls, 1997), depres-
on earlier versions of this manuscript.
sion (e.g., Carney, Saunders, Freedland, Stein,
Address correspondence and reprint requests to: The-
Rich & Jaffe, 1995), anxiety (Thayer, Fried-
odore P. Beauchaine, Department of Psychology, Univer-
man, & Borkovec, 1996), panic (Friedman,
sity of Washington, Box 351525, Seattle, WA 98195–
1525; E-mail: firstname.lastname@example.org. Thayer, Borkovec, Tyrrell, Johnson, & Col-
umbo, 1993), bulimia (Kennedy & Hesle- that the Earth is a noncentral component of a
larger solar system. Although the implicationsgrave, 1989), anorexia (Petretta, Bonaduce,
Scalfi, de Filippo, Marciano, Migaux, Them- here may be less profound, it will be sug-
gested in the sections to follow that many ofistoclakis, Ianniciello, & Contaldo, 1997),
hypnotic susceptibility (Harris, Porges, Clem- the disparities in the vagal tone literature are
clarified when the vagal system is viewed asenson Carpenter, & Vincenz, 1993), and func-
tional dyspepsia (Haug, Svebak, Hausken, a noncentral component of the autonomic ner-
vous system. It will further be suggested thatWilhelmsen, Berstad, & Ursin, 1994). Thus,
the correlates of vagal tone and vagal reactiv- these findings reflect a coherent and meaning-
ful pattern when viewed from the perspectiveity include a broad range of psychological ad-
justment variables, both adaptive and mal- of developmental psychopathology.
adaptive, that span developmental stages from
infancy to adulthood. This pattern supports
the assertion that the biobehavioral system in-
Tenets of Developmental Psychopathology
dexed by vagal tone subserves core regulatory
functions implicated in the development and The developmental psychopathology perspec-
tive was formalized by Sroufe and Ruttermaintenance of both normal and pathological
behavior patterns (Porges, 1996; Porges, (1984), who outlined several broad tenets that
set the field apart from related scientific disci-Doussard–Roosevelt, & Maiti, 1994).
However, the breadth of vagal tone corre- plines. First, developmental psychopatholo-
gists are concerned with outlining the courselates also raises questions about the specificity
and thus utility of the index as a marker of of disorders at a greater level of specificity
than epidemiologic description. Thus, theypsychological functioning, as do several in-
consistencies represented in the literature, wish to relate the emergence of disorders to
specific vulnerabilities, both biological andmany of which are well replicated. As the
above list suggests, reduced vagal tone re- psychological, that compromise one’s ability
to negotiate developmental milestones suc-flects both externalizing disorders, such as
antisocial behavior and aggression, and inter- cessfully. Because of the assumption that be-
havioral and emotional repertoires differenti-nalizing disorders, such as anxiety and de-
pression. Moreover, vagal tone is a positive ate hierarchically over time, with success at
one developmental period laying the ground-correlate of behavioral reactivity and tempera-
mental difficulty in infancy, yet a negative work for future successes (Werner, 1957),
identifying such vulnerabilities is consideredcorrelate of similar measures during the pre-
school years (Porges, Doussard–Roosevelt, an essential step toward a comprehensive un-
derstanding of the etiology and course of mostPortales, & Suess, 1994). Vagal tone has also
been interpreted as an index of both emotion disorders (see Cicchetti, 1990).
Second, maladaptive development can beregulation (see Porges et al., 1994), which is
often presumed to be socialized, and tempera- fully understood only when juxtaposed with
adaptive development. To the extent thatmental reactivity (Calkins, 1997; Stifter &
Fox, 1990), which is largely inherited (Cam- pathological development represents devia-
tion from optimal functioning, both typicalpos, Barrett, Lamb, Goldsmith, & Stenberg,
1983). and atypical developmental trajectories must
be mapped and compared in order to properlyThese apparent disparities suggest that re-
lations between vagal tone and psychological conceptualize, diagnose, and treat disorders
(Cicchetti & Toth, 1998). A corollary of thisadjustment are more complex than has often
been supposed. Indeed, in the history of scien- tenet is that studying biological and psycho-
logical variability in normative samples maytific inquiry similar paradoxes have often pre-
cipitated theoretical shifts that confer a greater not be informative with respect to high-risk
groups, both because the number of deviantlevel of understanding of complex systems.
Planetary motion, for example, could not be cases is typically insufficient to generalize
from and because differences in develop-explained sufficiently before the recognition
Vagal tone and psychopathology 185
mental trajectories may be washed out by the thetic functioning with Gray’s (1982a, 1982b,
1987a, 1987b) motivational theory will belarge proportion of normative cases.
Third, Sroufe and Rutter (1984) suggested presented. Before doing so, however, it is nec-
essary to define and operationalize vagal tonethat the processes and structures involved in
both normal and atypical development are and vagal reactivity, which are assessed by
measuring heart rate variability.likely to be complex. This sentiment has been
echoed and elaborated on by others (e.g., Cic-
chetti & Toth 1998; Kagan, 1997; Thelen &
Heart Rate Variability and
Smith, 1998), who have called for more thor-
Parasympathetic Cardiac Control
ough assessment of multiple biological and
psychological determinants of behavioral de- The autonomic nervous system (ANS) com-
prises the sympathetic (SNS) and parasympa-velopment. According to this tenet, no single
biological system, such as that indexed by va- thetic (PNS) branches, both of which inner-
vate most internal organs and bodily systems.gal tone, can be expected to contribute toward
a meaningful understanding of behavior, ei- The effects on a target organ of SNS and PNS
activation are generally antagonistic. Patternsther adaptive or maladaptive, since behavior
is the product of multiple systemic inputs. of cardiac activity, for instance, are deter-
mined primarily by the dynamic interaction ofIn this paper, the potential contribution of
these principles toward clarifying the diverse acceleratory SNS activation and deceleratory
PNS activation (see Berntson, Cacioppo, &pattern of empirical correlates of vagal tone
and vagal reactivity will be presented. As the Quigley, 1993; Berntson, Cacioppo, Quig-
ley, & Fabro, 1994). The deceleratory para-following literature review will reveal, most
of the research on psychological adjustment sympathetic component is provided by the va-
gus, or tenth cranial nerve.and vagal tone has been descriptive, and thus
guided little by developmental theory. Al- The vagus nerve includes both efferent and
afferent fibers, so neural traffic through it isthough the polyvagal theory of Porges (1995)
has been influential, it is largely a phylogenic bidirectional. Efferent fibers originating in the
brain stem terminate on the sinoatrial (SA)and functional account of the vagal system
and includes limited elaboration on develop- node, which serves as the cardiac pacemaker.
Because vagal efference is inhibitory, activitymental or systemic considerations. Where de-
velopment is considered, it is primarily in re- through these fibers slows heart rate by de-
creasing SA node firing (see Levy & Warner,lation to the integrity of the vagal system in
determining health outcomes vis-a
-vis high- 1994). Vagal afferent fibers, on the other
hand, originate in the heart and project to therisk infants (see Porges, 1996). Moreover,
while the theory represents a significant step nucleus tractus solitarius (see Porges, Dous-
sard–Roosevelt, Portales, & Greenspan, 1996).forward in our understanding of the contribu-
tion of the autonomic nervous system to both These fibers provide continuous feedback to
the brain, facilitating regulation of cardiacadaptive and maladaptive behavior, it speaks
primarily to parasympathetic functioning. functioning (see Porges et al., 1996).
Vagal tone is typically estimated from res-Thus, the theory implicitly minimizes the role
of the sympathetic nervous system, and of piratory sinus arrhythmia (RSA), or the de-
gree of ebbing and flowing of heart rate dur-possible sympathetic–parasympathetic inter-
actions, in affecting behavior. ing the respiratory cycle (Berntson, Bigger,
Eckberg, Grossman, Kaufmann, Malik, Na-In the sections to follow, polyvagal theory
will be briefly outlined, and the literature re- garaja, Porges, Saul, Stone, & van der Molen,
1997; Hayano, Sakakibara, Yamada, Yamada,garding vagal tone and vagal reactivity re-
viewed, from infancy through adulthood. Em- Mukai, Fujinami, Yokoyama, Watanabe, &
Takata, 1991; Katona & Jih, 1975). RSA re-pirical relations which are not well accounted
for without considering developmental pro- sults from increases in vagal efference during
exhalation, which decelerate heart rate, andcesses will be highlighted. Finally, the utility
of combining Porges’s theory of parasympa- decreases in vagal efference during inhalation,
which accelerate heart rate. Heart rate cannot yond the scope of this paper to review these
methods in detail, evidence suggests that esti-be used to assess vagal tone directly, how-
ever, because acceleratory sympathetic pro- mates of RSA derived from each are highly
correlated with one another, and with the de-jections to the SA node also contribute to
chronotropic (rate-related) cardiac activity scriptive approaches previously outlined
(Grossman et al., 1990). In addition, the(see Randall, 1994). Thus, measures of RSA
have been sought that are devoid of sympa- Porges method is highly correlated with de-
scriptive measures of heart period variance inthetic influences. Although consensus regard-
ing the most preferable method has only be- infants (Izard et al., 1991). It should be noted,
however, that convergence of these alternativegun to emerge (see Berntson et al., 1997), all
such measures index heart rate variability indices may be dependent on statistical con-
trol of respiration rate (Grossman et al.,(HRV), or beat to beat differences in the
length of the cardiac cycle over time. 1990), which is inversely related to RSA (see
Berntson et al., 1997; Grossman et al., 1991).The simplest methods of assessing HRV
involve calculating descriptive statistics on In addition, Grossman and colleagues
(1991) have demonstrated that changes in res-series of electrocardiographic (ECG) R
waves. Such indices, including standard devi- piration rate and tidal volume influence RSA
independent of vagal tone. This point de-ation, variance, and mean successive differ-
ence, correlate highly with one another, and serves elaboration because RSA and vagal
tone have been treated as equivalent in muchwith vagal efference as assessed via pharma-
cologic blockade (Hayano et al., 1991). Con- of the literature to be reviewed. Although cor-
relations between vagal tone (as assessed viacern has emerged over the use of these mea-
sures, however, both because of failures to pharmacologic blockade) and RSA can ap-
proach .9 during paced breathing (Hayano etreplicate fully the results of blockade studies
(Grossman, Karemaker, & Wieling, 1991)
al., 1991), and when respiration rate and tidal
volume are statistically controlled (Grossmanand because RSA accounts for only about half
of observed HRV (Grossman, van Beek, & et al., 1991), these correlations drop to be-
tween .5 and .7 in the absence of such con-Wientjes, 1990). Thus, alternative indices
have been developed that statistically elimi- trols (Grossman et al., 1991; Grossman &
Kollai, 1993). Thus, RSA is an imperfect in-nate influences on HRV that are extraneous
to RSA. Examples include Porges’s moving dex of cardiac vagal tone (see also Jennings &
McKnight, 1994), so the terms should not bepolynomial algorithm (Porges, 1986), which
has been used extensively in infant and child used interchangeably. Moreover, few attempts
to control for respiration have been includedwork, and Grossman’s peak–valley technique
(Grossman et al., 1990), which has more often in studies involving children, providing a po-
tential confound for many extant findings, anbeen applied with adults. Although it is be-
issue that will be revisited in later sections of
1. Two methods of vagal tone assessment via pharmaco-
Additionally, although the more advanced
logic blockade are represented in the literature. Both
techniques described thus far can eliminate or
involve the administration of a beta-adrenergic antago-
nist, which eliminates sympathetic nervous system in- reduce influences on HRV that are not attrib-
fluences on heart rate. In the simpler method (e.g.,
utable to RSA, none can resolve those influ-
Grosman et al., 1991), vagal tone is taken as the differ-
ences. This has prompted many researchers to
ence between preblockade heart period, which is sym-
turn to spectral analysis in their assessments
pathetically and parasympathetically mediated, and
of vagal tone. Spectral analysis involves the
postblockade heart period, after sympathetic effects
have been removed. In the second method (e.g., Gross- decomposition of heart rate time series into
man & Kollai, 1993; Hayano et al., 1991) a parasym-
component frequencies through Fourier trans-
pathetic antagonist is also administered, and the reduc-
formations. These components are divided
tion in HRV between the beta-adrenergic and the
into low-frequency variability (less than 0.04
parasympathetic blockers is used to represent cardiac
Hz), midfrequency variability (0.04–0.15 Hz),
vagal tone. This method also eliminates nonneural in-
fluences on HRV from vagal estimates. and high-frequency variability (greater than
Vagal tone and psychopathology 187
Figure 1. Fictitious heart rate signals and associated power spectra. The top panels represent
pure high-frequency variability (0.25 Hz), as associated with RSA. The middle panels repre-
sent low-frequency variability (0.07 Hz), primarily of sympathetic and nonneural origin.
the bottom panels represent the combined signal including both high- and low-frequency
components. Actual heart rate signals include spectral power at additional frequencies
(adapted from Mezzacappa et al., 1994).
0.15 Hz; see Mezzacappa, Kindlon, Earls, & how contributions to HRV outside the RSA
band can be resolved using spectral analysis.Saul, 1994; Mezzacappa et al., 1997). Phar-
macologic blockade studies have suggested Regardless of the method employed, the
assumption underlying the assessment of RSAthat sympathetic influences on HRV are con-
fined to the low and midfrequencies, whereas is that, as a peripheral measure of ANS activ-
ity, it serves as a proxy for more central regu-parasympathetic influences, including RSA,
are observed primarily in the high-frequency latory processes that cannot be measured non-
invasively (Porges, 1996). The origins ofrange (Akselrod, Gordon, Ubel, Shannon,
Barger, & Cohen, 1981; Akselrod, Gordon, these regulatory processes, both at neuroana-
tomical and phylogenic levels of analysis, areMadwed, Snidman, Shannon, & Cohen, 1985;
Berger, Saul, & Cohen, 1989; Pomeranz, Ma- outlined in Porges’s (1995) polyvagal theory.
caulay, Caudill, Kutz, Adam, Gordon, Kil-
born, Barger, Shannon, Cohen, & Benson,
1985; Saul, Berger, Chen, & Cohen, 1989;
Saul, Berger, Albrecht, Stein, Chen, & Cohen,
1991). Sample heart rate time series and asso- Porges (1995) specified two sources of vagal
efference to the heart, one originating in theciated spectra are presented in Figure 1. The
area under a given peak represents the power, dorsal motor nucleus and the other in the nu-
cleus ambiguus, and both terminating on theor amplitude, of heart rate oscillation at that
frequency band. In the example pictured, SA node. The dorsal motor nucleus controls
what Porges refers to as the vegetative vagus,spectral power in the respiratory (high-fre-
quency) range, which represents vagal which mediates reflexive cardiac activity, in-
cluding the deceleration of heart rate associ-influences, is roughly double that in the low-
frequency range, where sympathetic and non- ated with orienting. This vagal branch is phy-
logenetically older, and presumably rooted inneural influences predominate. This illustrates
the primary coping strategy of reptiles, which appear to reflect temperamental reactivity and
emotionality. In contrast, shifts in RSA in re-freeze when threatened.
In contrast, the smart vagus, which origi- sponse to environmental demands appear to
reflect attentional focus, emotion regulation,nates in the nucleus ambiguus, is distinctly
mammalian, and mediates cardiac activity and mood state. A potential source of confu-
sion in the literature to be reviewed is the usewhen environmental demands require extra-
reptilian coping. After orienting, mammals of the term vagal tone to refer to (a) tonic
measures of RSA, (b) reactivity measures ofmust either attend to and engage with the ini-
tial threat or resort to fight–flight responding. RSA, and (c) Porges’s (1986) moving polyno-
mial method of RSA quantification. These al-Engagement requires sustained attention,
which is accompanied by vagally mediated in- ternative usages present two problems. First,
as previously mentioned, the validity of RSAhibition of heart rate (e.g., Suess et al., 1994;
Weber, van der Molen, & Molendaar, 1994). as an index of vagal tone is moderate when
respiration is not controlled. Thus, in the pres-Alternatively, fighting and fleeing are accom-
panied by rage and panic, respectively, which ent article, the term vagal tone will be re-
served for theoretical discussion and will notare characterized by near complete vagal
withdrawal and large sympathetically medi- be used to refer to any indices of RSA. Sec-
ond, referring to both tonic RSA and RSA re-ated heart rate accelerations (George, Nutt,
Walker, Porges, Adinoff, & Linnoila, 1989; activity as vagal tone masks important dis-
tinctions in the aspects of functioning markedsee Porges, 1995, 1996). Thus, the association
between intense emotional experience and va- by each. Thus, RSA and RSA reactivity will
be treated separately in an effort to clarifygal withdrawal is functional, facilitating
bursts of metabolic output in situations of these distinctions. It is to the empirical rela-
tion between tonic RSA and temperament thatdanger.
The assertion that vagal outflow from the this article now turns.
nucleus ambiguus is functionally linked to at-
tentional and emotional processing is further
RSA and Temperament
supported by structural characteristics of the
mammalian brain stem. The nucleus ambi-
guus also innervates the larynx, which is used
by most mammals to produce vocalization, Rothbart and Bates (1998) define tempera-
ment as “constitutionally based individual dif-the primary means of communicating emo-
tional state. Additionally, the facial and jaw ferences in emotional, motor, and attentional
reactivity and self regulation” (p. 109). Ac-muscles, which are implicated in both vocal
and nonvocal expressions of emotion, are in- cording to this definition and others, a central
component of temperament is emotionalitynervated by the trigeminal and facial motor
nuclei, adjacent to the nucleus ambiguus. The (see Gunnar, 1990), which refers to individual
differences in displays of positive and nega-facial motor nucleus also innervates the inner
ear, which is implicated in both attentional tive affect in response to environmental de-
mands (Buss & Plomin, 1975). Historically,and communicative processes. Moreover, the
actions of all of these source nuclei are coor- work with infants has focused more on nega-
tive emotionality, which has been referred todinated in concert by the reticular formation
(Butler & Hodos, 1996). Taken together, as anger proneness (Goldsmith, 1996), dis-
tress to limitations (Rothbart, 1981), fussi-these structural characteristics lend support to
the assertion that vagal regulation is linked to ness–difficultness (Bates, Freeland, & Louns-
bury, 1979), irritability (Sanson, Prior,attentional and emotional processing.
The empirical literature generally supports Garino, Oberklaid, & Sewell, 1987), irritable
distress (Rothbart & Mauro, 1990), and nega-this assertion, although relations between va-
gal outflow, attention, and emotion are com- tive mood (Carey & McDevitt, 1978). Infants
high on negative affectivity are apt to respondplex. Tonic indices of RSA obtained during
periods of relative quiescence, for example, to environmental stressors with marked pro-
Vagal tone and psychopathology 189
test, including behavioral reactivity and with mothers and strangers, despite limited
power due to a small sample size. Moreover,crying.
Much of the work by Porges and col- the finding of greater positive facial expressiv-
ity was replicated by Stifter et al. (1989), usingleagues suggests that RSA is a psychophysio-
logical marker of behavioral reactivity and Izard and Dougherty’s (1980) AFFEX coding
system. Higher RSA infants exhibited more joyemotionality in infancy. High RSA infants
subjected to a pacifier withdrawal procedure, and interest expressions toward a stranger than
did their lower RSA counterparts.for instance, cried more than their low RSA
counterparts (Stifter, Fox, & Porges, 1986). In Finally, high RSA newborns are more re-
sponsive to a variety of environmental stimuliresponse to circumcision, newborn males with
high RSA exhibited greater pain reactivity, as than are low RSA newborns. Porges, Arnold,
and Forbes (1973), for example, demonstratedassessed by heart rate acceleration and funda-
mental cry frequencies (Porter, Porges, & that infants with high as opposed to low base-
line heart rate variability responded to the on-Marshal, 1988). Additionally, in a sample of
premature infants DiPietro and Porges (1991) set of a stimulus tone with greater heart rate
acceleration, and to the offset of the tone withreported greater behavioral reactivity for high
RSA neonates in response to a feeding proce- greater heart rate deceleration. Porges, Stamps,
and Walter (1974) obtained similar findingsdure requiring a tube run through the nose or
mouth. Moreover, newborns with higher RSA when subjecting infants to changes in illumina-
tion. Moreover, only high RSA newborns ex-have exhibited larger cortisol responses to a
heel-stick procedure for drawing blood, sug- hibited conditioned heart rate deceleration in re-
sponse to a tone stimulus that had been pairedgesting greater stress reactivity (Gunnar, Por-
ter, Wolf, Rigatuso, & Larson, 1995). with a pattern of blinking lights (Stamps &
Porges, 1975). Richards (1985a) reported thatHigh RSA at 9 months also predicts mater-
nal ratings of temperamental difficulty (Porges high RSA infants attended to novel stimuli for
shorter periods of time than low RSA infants.et al., 1994), as assessed by the Infant Charac-
teristics Questionnaire (Bates et al., 1979). In Because a similar pattern was observed for
older (20-week) as opposed to younger (14-two additional studies, 5-month-old infants
with high RSA displayed more negative reac- week) participants, the result was interpreted
as evidence for greater attentional capacitytivity to a standardized procedure in which
their arms were restrained by their mothers and processing speed in the high RSA group.
Further support for this conjecture is provided(Fox, 1989; Stifter & Fox, 1990). Ratings of
emotional expression were derived from Ek- by the finding that high RSA infants were less
likely to be distracted, as assessed by gazeman and Friesen’s (1984) EM-FACS coding
system. Similar results were obtained by Cal- aversion toward a peripherally presented in-
terrupting stimulus (Richards, 1987). Finally,kins and Fox (1992), who reported greater
RSA in 5-month-old infants who cried in re- Linnemeyer and Porges (1986) demonstrated
that high RSA 6-month-olds looked at famil-sponse to the presentation of novel geometric
patterns, and to pacifier withdrawal, than in iar stimuli for shorter periods, but at unfamil-
iar stimuli for longer periods, than did infantsinfants who cried in response to one or neither
of the events. with lower RSA.
Taken together, these reports suggest thatThese findings imply that high RSA in in-
fancy is a marker of negative emotionality RSA reflects the capacity of infants to engage
actively with the environment. Such engage-and difficulty. Yet RSA also predicts positive
affective expression in infants and may there- ment includes behavioral, attentional, and
emotional responsiveness, both positive andfore index general behavioral and emotional re-
activity rather than negative emotionality alone. negative, to external events and challenges.
Indeed, Richards and Cameron (1989) foundIn the study reported above, Fox (1989) ob-
tained a near significant relation (p = .06) be- positive associations between RSA and the
approach subscale of the Infant Temperamenttween infant RSA and EM-FACS-coded posi-
tive reactivity during a peek-a-boo procedure Questionnaire (Carey & McDevitt, 1978) at
ages 14, 20, and 26 weeks. Moreover, inhib- uya (1997) reported reduced baseline RSA in
18 children with attention-deficit hyperactiv-ited children who are low on approach and
high on fear exhibit low RSA (Kagan, Rez- ity disorder (ADHD) compared to 49 controls.
This study, however, was characterized bynick, & Snidman, 1987; Rubin, Hastings,
Stewart, Henderson, & Chen, 1997), as do the several methodological shortcomings, includ-
ing imprecise ECG recordings, and failure tosocially and affectively inexpressive infants
of depressed mothers (Field, Pickens, Fox, rule out comorbid conduct disorder, the im-
portance of which will be presented in laterNawrocki, & Gonzalez, 1995; Field, Lang,
Martinez, Yando, Pickens, & Bendell, 1996). sections of this paper. Suess et al. (1994) sub-
jected fourth- and fifth-graders to a continu-
ous performance task in which they were re-
quired to depress a keyboard space bar whenChild studies
a prespecified pattern of numbers was dis-
played. Children with higher baseline RSAAssociations between temperament and RSA
also occur in 2- and 3-year-olds (Calkins, performed better, as indexed by signal detec-
tion sensitivity, within the first of three 3-min1997), although alternative patterns begin to
emerge. While individual differences in RSA blocks, than did children with low RSA. Hyde
and Izard (1997), however, reported no rela-(Porges et al., 1994; Porter, Bryan, & Hsu,
1995) and in indices of activity and reactivity tion between length of attention span and
baseline RSA in a longitudinal study of 3-, 4-,(Worobey & Blajda, 1989) exhibit moderate
to high stability after about 3 months of age, and 5-year-olds. In that study, children
watched a 5-min videotaped story while theirrelations between RSA and behavior do not.
This pattern is perhaps best demonstrated in gaze fixation, motor activity, frequency of
speech, and facial expressions were moni-the work of Porges and colleagues (1994),
who as expected reported positive associa- tored. None of the variables was related to
RSA. These two reports represent the onlytions between RSA, behavioral reactivity, and
maternal-rated temperamental difficulty in 9- studies addressing associations between RSA
and attention in preschool children, thus con-month-olds, as assessed by Bates’ (1984)
Infant Characteristics Questionnaire. By age straining conclusions.
Eisenberg and colleagues have demon-3 years, however, the same 9-month RSA
measure was a negative correlate of maternal- strated in a series of experiments that high
RSA predicts both expressions of empathy forrated difficulty, after the relation between 9-
month RSA and 9-month difficulty was statis- others in distress and general social compe-
tence, particularly in boys. Kindergarten andtically removed. Additional studies suggest
that this finding is not anomalous. Premature second-grade children exposed to a crying in-
fant, for instance, were more likely to talk tonewborns who exhibited relatively high RSA
at birth, for instance, were rated as more so- the infant and offer instrumental help if they
exhibited high RSA (Fabes et al., 1994). Sim-cially competent at age 3 years on the Califor-
nia Preschool Social Competency Scale (Le- ilarly, high-RSA third-grade boys exposed to
a film of two frightened children were ratedvine, Elzey, & Lewis, 1969) than were their
low-RSA counterparts (Doussard–Roosevelt, as more concerned, based on facial expres-
sions of emotion (Fabes, Eisenberg, & Eisen-Porges, Scanlon, Alemi, & Scanlon, 1997).
Similarly, Fox and Field (1989) found that 3- bud, 1993). The high-RSA boys were also
more likely to report subjective feelings ofyear-olds with high RSA and a high activity
level were better adjusted to preschool than sympathy, less likely to become autonomi-
cally aroused (as assessed by skin conduc-their low-RSA peers, as assessed by the
amount of interactive play they engaged in. tance), and less likely to disengage by looking
away. No significant relations were reportedCompared to the infant literature, fewer
studies have addressed the relations between for girls. Moreover, in a sample of 6- to 8-
year-olds, boys with high RSA were rated asRSA and attentional processes in preschool
and grade-school children. Shibagaki and Fur- more sociable by their teachers, and more
Vagal tone and psychopathology 191
emotionally regulated by their parents, than ronments beyond expressing displeasure,
which is the predominant emotion in their af-were boys with low RSA (Eisenberg et al.,
1995). Curiously, teacher-report findings were fective repertoires for the first few weeks of
life. Over the next year, as parasympatheticreversed for girls, and RSA was unrelated to
any parent-report ratings. Similar sex differ- influence on cardiac control increases
(Harper, Walter, Leake, Hoffman, Sieck, Ster-ences in peer ratings of social competence
have also been reported (Eisenberg, Fabes, man, Hoppenbrouwers, & Hodgman, 1978;
Katona, Franz, & Egbert, 1980; Richards,Karbon, Murphy, Wosinski, Polazzi, Carlo, &
Juhnke, 1996). 1985b), expressions of positive emotion be-
come more common, and expressions of neg-The sex effects in these three studies raise
questions regarding the generalizability of ative emotion more differentiated, including
displays of both anger and fear (Sroufe,RSA–behavior relations across gender. In
part, the differences may be attributable to re- 1979). During the 2nd year of life, positive
affect differentiates, as emotions such as joystricted ranges on all indices for girls. In the
first analysis (Fabes et al., 1993), girls were and excitement are observed. This develop-
mental sequence, with negative emotions andrated as more sympathetic, in the second
(Eisenberg et al., 1995) as more socially reactivity emerging and differentiating before
positive emotions, may be in part responsibleskilled and better regulated, and in the third
(Eisenberg et al., 1996) as more prosocial. for the tendency of temperament researchers
to focus primarily on negative emotionalityMoreover, although null findings have been
reported (Fabes et al., 1993; Suess et al., when studying infants (Fox & Stifter, 1989).
Moreover, frequent expressions of negative1994), several researchers have found higher
RSA in girls than in boys (e.g., Fabes et al., affect in infancy are normative (Greenspan,
1991) and may serve as a marker for ANS1994; Stamps & Porges, 1975) and in women
than in men (see Lehofer, Moser, Hoehn– integrity (e.g., Porges, 1996). This raises the
possibility that RSA marks emotional compe-Saric, McLeod, Liebmann, Drnovsek, Egner,
Hildenbrandt, & Zapotoczky, 1997). Thus, re- tence in both infancy and toddlerhood and
that the apparent shift in RSA–behavior rela-duced variability in both RSA and in mea-
sures of social competence may have attenu- tions from negative toward positive emotion-
ality is an artifact of normative developmentalated correlations. Indeed, girls’ scores were
characterized by lower variance than boys’ shifts in emotional expression. Consistent
with this interpretation, high negative reactiv-scores on 29 of the 40 behavioral and emo-
tional indices employed in these studies. Nev- ity scores of appropriately responsive infants
are not predictive of negative emotionalityertheless, sex differences deserve further scru-
tiny, particularly given the above pattern, later in life (see Gunnar, 1990). This observa-
tion may also stem from the types of taskswhere disparities appear to become more
marked with increasing age, and given that employed by researchers assessing emotional-
ity in infant samples. Frequently, negativemost researchers have ignored sex as a pre-
dictor of RSA. emotionality is assessed using somewhat in-
trusive challenges, such as the arm restraintSex effects notwithstanding, changes in
RSA from a marker of negative emotionality procedure employed by Fox (1989; Stifter &
Fox, 1990). Negative emotional expression inin infancy, to a marker of positive emotional-
ity in toddlerhood, to a marker of social com- response to arm restraint may thus reflect
adaptive reactivity and is not, in and of itself,petence in preschool and grade school, cannot
be accounted for without considering devel- predictive of subsequent negative outcomes,
such as toddler noncompliance (Stifter, Spin-opment. As outlined by others, the period
from infancy to toddlerhood is one of dra- rad, & Braungart–Rieker, 1999).
In addition, because positive affect differ-matic emotional and behavioral differentiation
(e.g., Cole, Michel, & O’Donnell Teti, 1994; entiates before social behaviors, it is also pos-
sible that RSA–social competence relationsGunnar, 1990). Newborns have few means at
their disposal for impacting upon their envi- are effected through emotionality. This inter-
pretation seems particularly likely given the hostility did not affect the high-RSA partici-
pants in the manner predicted by the Calkinspreviously mentioned findings by Eisenberg
and colleagues (Eisenberg et al., 1995; Fabes and Fox model. Moreover, emergent evidence
suggests that RSA may be reduced rather thanet al., 1994) relating emotion regulation to so-
cial competence. elevated in behaviorally disordered children
and adolescents. Such evidence was reportedIt has also been suggested that the age
range from infancy to toddlerhood is a critical by Pine and colleagues (Pine, Wasserman,
Coplan, Fried, Sloan, et al.,1996; Pine, Was-period for the development of emotion regula-
tion, or the ability to modulate affective states serman, Miller, Coplan, Bagiella, Kovelenku,
Myers, & Sloan, 1998), using a sample of theinternally. Calkins and Fox (1992; Calkins,
1994; Fox & Calkins, 1993) have proposed a 6.5- to 10.5-year-old brothers of convicted de-
linquents. RSA was inversely related to scoresmodel in which temperamental reactivity in-
teracts with caretaking style to result in spe- on the externalizing scale of the Child Behav-
ior Checklist (Achenbach, 1991), a findingcific behavioral patterns. According to this
model, two possibilities obtain for the emo- also reported by Field, Lang, Martinez,
Yando, Pickens, and Bendell (1996) in thetionally and behaviorally reactive infant who
exhibits high RSA. If the primary caretaker children of dysphoric mothers. Similar results
have been reported by Eisenberg and col-characteristically meets infant emotional reac-
tivity with negative affect and intrusive con- leagues (1995), who found negative correla-
tions between RSA and externalizing behav-trol attempts, which tend to escalate rather
than regulate arousal (e.g., Snyder, Edwards, ior problems in 6- to 8-year-old boys, a
pattern also observed in adolescent and adultMcGraw, Kilgore, & Holton, 1994), behav-
iors and emotions will not differentiate, re- samples, to which this discussion now turns.
sulting in an aggressive toddler. Alternatively,
if the primary caretaker is responsive and
Adolescent and adult studies
carefully modulates affective expressions
through unintrusive deescalation, a highly so- In a study of 15-year-old adolescent males,
Mezzacappa et al. (1997) reported reducedcial, outgoing toddler results. Note that this
model implicitly predicts two groups with RSA in a group of 63 aggressive participants,
compared to 59 controls. Aggression scoreshigh RSA, one socially competent and appro-
priately expressive and the other aggressive were derived from a variety of measures col-
lected yearly via mother, teacher, and self-re-and emotionally unregulated. The studies re-
viewed thus far, which were all conducted us- port, at ages 10–15 years. RSA was also re-
lated inversely to trait hostility in a sample ofing normative samples, address only the for-
mer group. Support for the model might be young adults (Sloan et al., 1994), as indexed
by the Cook–Medley Hostility Scale (Cook &suggested if aggressive samples were found to
exhibit baseline RSA equivalent to that ob- Medley, 1954). No additional studies address-
ing the relation between RSA and aggressionserved in socially competent children, or if
children with high RSA who were exposed to have been reported. Thus, although the num-
ber of findings is not large, results from bothcoercive parenting were found to be aggres-
sive. Because no studies have addressed this children and adults suggest reduced parasym-
pathetic tone in aggression.question in the toddler age range, the Calkins
and Fox model has not been tested directly. In These reports have come as a surprise to
many researchers, who subscribed to the as-samples of older children, however, no such
patterns are represented in the literature. Gott- sumption that vagotonia (Eppinger & Hess,
1910/1915), or an autonomic imbalance fa-man and Katz (1995), for instance, found no
relationship between externalizing behavior voring the PNS, was a marker of delinquent
and aggressive behavior (see Venables, 1988).problems and exposure to marital hostility for
children with high RSA. Marital hostility was This assumption is rooted in two empirical re-
lations that merit further discussion. First, ata strong predictor of behavior problems, how-
ever, for low-RSA children. Thus, parental all age ranges considered, aggressive samples
Vagal tone and psychopathology 193
are characterized by reduced resting heart rate Consistent with this interpretation, Meza-
cappa and colleagues (Mezzacappa, Trem-relative to controls, a finding that has been
widely replicated (e.g., Kindlon, Tremblay, blay, Kindlon, Saul, Arseneault, Pihl, & Earls,
1996; Mezzacappa et al., 1997), reported re-Mezzacappa, Earls, Laurent, & Schaal, 1995;
Raine, Venables, & Mednick, 1997; Roge- duced heart rate and reduced RSA in antiso-
cial adolescents, compared to controls.ness, Cepeda, Macedo, Fischer, & Harris,
1990; Wadsworth, 1976; see also Raine, The inverse relation between RSA and ag-
gression is also surprising given similar pat-1993, for a review). Second, both within- and
between-subjects comparisons suggest that terns of parasympathetic functioning in both
anxiety and depression. Although few suchheart rate is inversely related to RSA, as as-
sessed across a variety of task conditions, and reports were available when Dalack and
Roose (1990) suggested that elevated rates ofin response to pharmacologic blockade (e.g.,
Cacioppo, Uchino, & Berntson, 1994; Gross- cardiovascular disease in depressed patients
were due to reduced vagal influence, severalman et al., 1991; Grossman & Kollai, 1993;
Grossman & Svebak, 1987; Hayano et al., empirical reports have appeared in the litera-
ture since. However, because both tricyclic1991; see also Berntson, Cacioppo, & Quig-
ley, 1995, for a review). Taken together, these and tetracyclic antidepressants attenuate RSA
(Mezzacappa, Steingard, Kindlon, Saul, &findings suggest that aggression should be
marked by increased RSA, which is contrary Earls, 1998; Yeragani, Pohl, Balon, Ramesh,
Glitz, Weinberg, & Merlos, 1992; Jakobsen,to the results reported above. However, only
recently has the relation between heart rate Hauksson, & Vestergaard, 1984), and because
studies of selective serotonin reuptake inhibi-and RSA been explored in aggressive groups.
Thus, the vagotonia hypothesis is an extrapo- tors suggest both increases (Tucker, Adam-
son, Miranda, Scarborough, Williams, Groff, &lation from heart rate-RSA relations in nonag-
gressive samples, a practice that has been McLean, 1997) and decreases (Rissanen,
Naukkarinen, Virkkunen, Rawlings, & Lin-questioned by developmental psychopatholo-
gists, as outlined in the introduction of this noila, 1998) in parasympathetic functioning,
this discussion will be restricted to the subsetarticle.
Moreover, recall that both the sympathetic of reports in which depressed patients were
medication free during RSA assessment.and the parasympathetic branches of the ANS
contribute to patterns of cardiac activity. Be- As alluded to, these studies suggest that
depressed patients exhibit reduced RSA.cause each branch can function somewhat in-
dependently of the other, inferences regarding Light, Kothandapini, and Allen (1998), for in-
stance, reported that mildly depressed women,sympathetic or parasympathetic activation
based on heart rate alone are of questionable as assessed by the Beck Depression Inventory
(BDI; Beck, Ward, Mendelson, & Erbaugh,validity (see Berntson et al., 1994). This is
because the activity of each branch can take 1961), exhibited significantly lower baseline
RSA than nondepressed controls. Similaron any number of values toward producing a
given heart rate. Thus, concurrent sympathetic findings were reported by Rechlin, Weis,
Spitzer, and Kaschka (1994) in patients meet-and parasympathetic dysregulation could re-
sult in both reduced heart rate and reduced ing DSM-III-R criteria for major depression,
melancholic type. Moreover, these patientsRSA. Baseline sympathetic underarousal has
been suggested as the cause of the low resting exhibited lower RSA than a group diagnosed
with reactive depression. This pattern sug-heart rates observed in aggressive samples
(Raine, Venables, & Williams, 1990a; Raine, gests that the attenuated RSA in the former
group may have resulted from enduring con-Venables, & Williams, 1990b). If combined
with reduced parasympathetic tone, as sug- stitutional characteristics. Two additional
studies have been reported in which melan-gested by the studies previously cited, sympa-
thetic underarousal provides a potential expla- cholic and reactive subgroups were not sepa-
rated. In each case, nonsignificant trends werenation for the observed reductions in both
heart rate and RSA in aggressive groups. reported, with depressed participants exhibit-
ing reduced baseline RSA compared to con- that RSA is attenuated in patients who experi-
ence panic symptoms (see Friedman &trols (Moser, Lehofer, Hoehn–Saric, McLeod,
Hildebrandt, Seinbrenner, Voica, Lieb- Thayer, 1998a). Friedman et al. (1993), for
example, reported significantly reduced RSAmann, & Zapotoczky, 1998; Yeragani, Pohl,
Balon, Ramesh, Glitz, Jung, & Sherwood, in a sample of female undergraduates who
had experienced at least one panic attack in1991). It is conceivable that significant effects
were masked in these studies by including the past month, compared to a control group
of blood phobics. This finding was later repli-both depression subtypes in one group. Fi-
nally, two studies have reported significantly cated with an expanded sample including
male undergraduates and a normal controlreduced RSA (Carney et al., 1995; Krittaya-
phong, Cascio, Light, Sheffield, Golden, Fin- group (Friedman & Thayer, 1998b). More-
over, similar results have been reported in pa-kel, Glekas, Koch, & Sheps, 1997), and one
a trend toward reduced RSA (Carney, Rich, tients who meet DSM-III-R criteria for panic
disorder (Yeragani, Pohl, Berger, Balon,teVelde, Saini, Clark, & Freedland, 1988), in
depressed versus nondepressed patients with Ramesh, Glitz, Srinivasan, & Weinberg,
1993). Of particular interest is the finding ofcoronary artery disease. In each case, 24-hr
ambulatory ECG monitoring was employed. Yeragani et al. (1991), who demonstrated sig-
nificantly lower RSA in panic disorder pa-Thus, group differences reflect both RSA and
RSA reactivity, which complicates interpreta- tients than in both depressed patients and con-
trols, suggesting more severely compromisedtion. Nevertheless, these studies provide addi-
tional evidence of attenuated RSA in cases of parasympathetic functioning in the panic
Similar results obtain in anxiety-disordered
patients. Once again, however, discussion
Summary and implications
must be restricted to reports in which medica-
tions were not employed, since benzodiaze- Two important points follow from this discus-
sion. First, the empirical literature regardingpines, which are commonly used to treat anxi-
ety, alter vagal outflow (Adinoff, Mefford, RSA is most interpretable when viewed
within a developmental context. RSA appearsWaxman, & Linnoila, 1992; Tulen et al.,
1994). Lyonfields, Borkovec, and Thayer to mark the capacity for active engagement of
infants with the environment, as reflected by(1995) reported reduced RSA in patients who
met DSM-III-R criteria for generalized anxi- temperamental reactivity, attentional capacity,
and negative emotionality. In later infancyety disorder (GAD), a finding that they later
replicated (Thayer et al., 1996). In the only and toddlerhood, RSA marks measures of so-
cial competence and expressions of positiveother report addressing GAD in the literature,
Kollai and Kollai (1992) found no significant affect, including empathy. This apparent shift
parallels normative developmental increasesRSA effect, although a trend was observed in
the predicted direction. Similar differences in RSA (Harper et al., 1978; Katona et al.,
1980; Richards, 1985b), and age-appropriatehave been found between control participants
and patients with functional dyspepsia, a dis- changes in affective expression in the first
years of life. Thus, at all age ranges consid-order characterized by chronic indigestion and
epigastric discomfort with no definable or- ered, RSA indexes appropriate engagement
and emotion regulation, which is manifestedganic cause (Haug et al., 1994; Hveem,
Svebak, Hausken, & Berstad, 1998). Of note, in older children as social competence. Con-
sistent with this interpretation, girls, who arepatients with functional dyspepsia are charac-
teristically anxious and often depressed often more socially skilled and emotionally
regulated than boys (e.g., Eisenberg et al.,(Langeluddecke, Goulston, & Tennant, 1990).
Finally, reduced RSA has also been reported 1995, 1996; Fabes et al., 1993), exhibit higher
RSA.in anxious adolescent males (Mezzacappa et
al., 1997). Second, studies of atypical samples sug-
gest emotional deficits in cases of attenuatedA growing body of literature also suggests
Vagal tone and psychopathology 195
RSA. A now sizable body of literature links Porges, 1986; Richards, 1985a, 1987; Rich-
ards & Gibson, 1997). According to Porgesreduced baseline vagal activity to depression,
anxiety, and panic in adults. Although few re- and colleagues, these decreases in heart rate
reflect activity of the “vagal brake,” which,ports speak to internalizing disorders in child-
hood, those that do suggest a similar pattern. according to polyvagal theory, moderates
sympathetic output when attentional alloca-Moreover, reduced RSA also characterizes
aggressive adolescents and hostile adults. Al- tion is the appropriate coping strategy (see
Porges et al., 1996). Thus, during periods ofthough the behavioral dissimilarities among
these disorders are extensive, all share the sustained attention requiring minimal physical
or psychological effort, heart rate decelera-common feature of a dysregulated affective
style. Aggression is characterized by anger tions are presumed to be parasympathetically
mediated. However, when RSA reactivity isand rage, depression by sadness and dyspho-
ria, and anxiety by fear and panic. Thus, there measured directly during such tasks, the ob-
served heart rate decreases are paralleled byappears to be a link between emotional inflex-
ibility and baseline RSA, a topic that will be concurrent reductions in RSA, which suggests
decreased vagal influence. Such RSA reduc-returned to in later sections of this article.
tions have been observed in infants (Rich-
ards & Casey, 1991), children (Weber et al.,
Vagal Reactivity, Emotion Regulation,
1994), and adults (see Van der Molen, Ba-
shore, Halliday, & Callaway, 1991). One in-
terpretation of these findings, given the inde-
pendent effects of respiratory parameters on
vagal tone outlined previously (see BerntsonBecause researchers were not yet aware that
RSA and RSA reactivity mark somewhat dif- et al., 1993, 1997), is that attention-related re-
ductions in respiratory depth and tidal volumeferent aspects of psychological functioning,
early studies rarely included assessments of result in reduced RSA, despite increases in
vagal efference. This interpretation is un-the latter index. Consequently, fewer reports
of RSA reactivity are available for review. likely, however, given the findings of Rich-
ards and Casey (1991), who reported a nega-Moreover, few of the studies in which infant
or child RSA reactivity has been reported tive correlation between heart rate and
respiration during sustained attention in 14-tohave controlled for respiration rate, the impor-
tance of which has been outlined previously. 26-week-old infants, but no relation between
RSA and respiration. Thus, although RSAThus, reported changes in RSA in response to
environmental demands may be confounded was suppressed during attention phases, the
suppression could not have resulted from res-with changes in respiration rate and tidal vol-
ume. Reports of heart rate reactivity, which piratory influences. Nevertheless, the authors
attributed attention-related heart rate decelera-are more common, are also difficult to infer
vagal reactivity from because of the afore- tions to increased vagal efference. The ration-
ale for this interpretation is that RSA resultsmentioned dual innervation of the heart by
both the sympathetic and parasympathetic from brain stem mechanisms, as previously
outlined (see also Berntson et al., 1993),ANS branches. Due to these caveats, the ex-
tant research addressing RSA and heart rate whereas heart rate reactivity during sustained
attention is influenced by neocortical struc-reactivity in infants and children is somewhat
difficult to interpret. Nevertheless, a review is tures that directly inhibit vagal efferent traffic
(see Richards & Casey, 1991). Thus, heartpresented below.
Although researchers assessing infant at- rate deceleration may be a more valid index
of vagal reactivity than RSA during tasks re-tention have generally not measured RSA re-
activity directly, heart rate decelerations dur- quiring sustained attention.
To complicate interpretive efforts further,ing visual stimulus presentations have been
widely replicated (Casey & Richards, 1988; researchers have reported RSA reductions, ac-
companied by either no change in heart rateLansink & Richards, 1997; Linnemeyer &
(Huffman, Bryan, del Carmen, Pedersen, preted with caution due to small sample sizes,
these studies, along with the Huffman et al.Doussard–Roosevelt, & Porges, 1998), or
heart rate accelerations (e.g., Fracasso, (1998) article, suggest that RSA reductions in
response to challenge mark competent regula-Porges, Lamb, & Rosenberg, 1994), during
more challenging tasks that require active en- tion. According to polyvagal theory, this RSA
suppression reflects vagal withdrawal, whichgagement. Moreover, heart rate decelerations
in the absence of RSA changes have also been facilitates sympathetically mediated metabolic
output, as reflected in heart rate increases, toreported (Porges et al., 1996). Thus, further
studies are required toward clarifying the rela- cope efficiently with environmental demands
(see Huffman et al., 1998). By this reasoning,tion between RSA reactivity and environmen-
tal challenge in infants. the larger reductions in RSA reported by well-
regulated infants reflect competent engage-Regarding behavioral correlates of RSA re-
activity during such tasks, Huffman et al. ment with challenge.
In addition, most studies that have assessed(1998) demonstrated that 3-month-old infants
who responded to a laboratory-administered both RSA and vagal reactivity have demon-
strated significant relations between the two,assessment of temperament with reduced
RSA, were rated higher by their mothers on with high baseline RSA predicting degree of
vagal reactivity (Calkins, 1997; Porges et al.,the soothability and the duration of orienting
scales of the Infant Behavior Questionnaire 1996; Porter et al. 1988; Richards, 1985a).
This has been interpreted as indicating thatthan were infants who exhibited RSA in-
creases. DeGangi, DePietro, Greenspan, and high-RSA infants, who are behaviorally and
emotionally reactive, are able to regulate theirPorges (1991) compared baseline RSA and
RSA reactivity between groups of normal and reactivity by appropriately allocating cogni-
tive and motivational resources, as reflectedregulatory-disordered 8- to 11-month-old in-
fants. The latter group, which was character- in the application of the vagal brake. As men-
tioned previously, however, larger reactivityized by maternal reports of distractibility, ir-
regular sleeping and feeding patterns, lengthy can be expected of those with higher baseline
scores, and no statistical controls for baselinebouts of crying, and excessive irritability, did
not differ from controls on baseline RSA. RSA were employed in any of the above re-
ports. Moreover, respiratory frequency hasHowever, within-groups analyses identified
an inverse relation in the dysregulated group been reported to vary inversely with task dif-
ficulty during attention demanding or cogni-between RSA and RSA reactivity during ad-
ministration of the Bayley Scales of Infant tively challenging tasks (Denot–Ledunois,
Vardon, Perruchet, & Gallego, 1998). Thus,Development (Bayley, 1969). Thus, contrary
to the law of initial values, which suggests further studies are required in which both res-
piration rate and baseline RSA are controlledthat participants with higher basal levels on
a psychophysiological measure have a greater before the vagal brake hypothesis can be con-
firmed.capacity for decreases (Benjamin, 1963), reg-
ulatory-disordered infants with high RSA ex- Reports have also emerged suggesting that
vagal reactivity reflects emotional responsive-hibited the least RSA suppression during cog-
nitive challenge, a pattern that was reversed ness, as indexed by shifts in mood state. Baz-
henova and Porges (1997), for instance, elic-for the control group. Finally, 9-month-old in-
fants who exhibited relatively small reduc- ited RSA increases in 5-month-old infants by
manipulating emotional state toward the posi-tions in RSA during administration of the
Bayley Scales were rated by their mothers as tive, and RSA decreases by manipulating
emotional state toward the negative. Thus,more aggressive, more depressed, and more
withdrawn on the Child Behavior Checklist at RSA was highest during a toy presentation
condition, and lowest during a still-face con-age 3 years than were infants who exhibited
larger RSA reductions (Porges et al., 1996). dition in which the experimenter gazed unex-
pressively at the infant. Although RSA reduc-Although both the DeGangi et al. (1991) and
Porges et al. (1996) articles should be inter- tions in the latter condition could have
Vagal tone and psychopathology 197
resulted from attentional processes, such an nett, 1994), which are characterized by vagal
dysregulation in adults. In addition, excessiveinterpretation is unlikely for two reasons.
First, the procedure has been associated with vagal influence from the dorsal motor nucleus
(i.e., the vegetative vagus) has been suggestedexpressions of negative affect, and similar re-
ductions in RSA elsewhere (Weinberg & as a possible cause of asthma (Porges, 1995).
Moreover, no control group was employed,Tronick, 1996). Second, the RSA reductions
were accompanied by heart rate acceleration and the only other report assessing vagal reac-
tivity in response to mood induction producedrather than deceleration, a pattern suggestive
of vagal withdrawal, which is commonly ob- a null result (Cole, Zahn–Waxler, Fox,
Usher, & Welsh, 1996). Thus, further study isserved in older participants while performing
tasks that are psychologically stressful (Bernt- required before drawing any conclusions
about mood state and vagal responding in thisson, Cacioppo, Binkley, Uchino, Quigley, &
Fieldstone, 1994; Cacioppo et al., 1994; Mur- age group.
As with infant studies, a clearer relationphy, Alpert, Willey, & Somes, 1988; Kelsey,
1991). Regarding positive affect, DiPietro, exists between vagal reactivity and attention.
When asked to count target tones presentedPorges, and Uhly (1992), in a similar proce-
dure, demonstrated that infants who reacted to within a string of distracters, 5- to 9-year-old
boys exhibited reduced heart rate and reduceda toy stimulus with phasic increases in RSA,
engaged subsequently in more exploratory RSA from baseline (Weber et al., 1994). In
addition, during more demanding tasks, re-play.
duced RSA and heart rate accelerations have
been observed in both fourth- and fifth-grad-
ers (Suess et al., 1994), and 7- to 12-year-olds
(Hickey, Suess, Newlin, Spurgeon, & Porges,Three studies have reported relations between
mood state and vagal reactivity in older 1995). These findings are consistent with re-
ports from the infant literature linking heartchildren. Calkins (1997) subjected 2- and 3-
year-olds to conditions designed to elicit both rate and RSA reactivity to sustained attention
and cognitive challenge.positive and negative affect. In the former
condition, children were engaged in a puppet
game, while in the latter they were prevented
Adolescent and adult studies
from playing with a musical toy that was
placed in a clear plastic box. In both cases, Although few studies have directly assessed
the relation between vagal reactivity and sus-RSA was suppressed from baseline. Once
again, however, these results are difficult to tained attention in adolescents or adults, the
results of those that have are consistent withinterpret because attentional and respiratory
processes might have contributed to the re- the infant and child literature. Porges and
Raskin (1969), for example, reported reducedductions in RSA. An alternative possibility,
since the children were not prevented from RSA and heart rate in college students during
tasks requiring them to count both auditorymoving, is that vagal withdrawal associated
with metabolic output suppressed RSA. In the and visual stimuli. Additionally, Coles (1972)
reported heart rate deceleration during simplesecond study, Miller and Wood (1997) moni-
tored RSA while asthmatic children watched visual search tasks. As with infant and child
studies, when psychological stress is imposeda video containing both sad and happy scenes.
Increases in RSA and decreases in heart rate by increasing task difficulty (e.g., by requir-
ing participants to perform serial subtraction),were observed in response to both types of
scenes, with maximal change during the sad heart rate increases are observed, a finding
that is well replicated (Berntson et al., 1994;presentations. These findings are inconsistent
with reports from infant samples, and they are Cacioppo et al., 1994; Murphy et al., 1988;
Kelsey, 1991).particularly difficult to interpret because asth-
matic children are known to experience in- The bulk of the remaining studies in which
vagal reactivity has been assessed have exam-creased rates of affective disorders (e.g., Ben-
ined samples of depressed and anxiety-disor- treatments that are effective in reducing anxi-
ety augment RSA. Lehrer, Hochron, Mayne,dered adults. When group differences have
been found, panic disorder patients have ex- Isenberg, Lasoski, Carlson, Gilchrist, and
Porges (1997), for example, reported in-hibited greater vagal reactivity than depressed
patients, anxiety disordered patients, or con- creased RSA in asthmatic adults during relax-
ation therapy. Although interpretational issuestrols. Yeragani et al. (1991), for example, ex-
amined vagal withdrawal in panic patients have already been noted with respect to asth-
matic participants, similar increases in RSAwhen moving from a supine to a standing po-
sition. Although such postural changes are as- have been reported in a variety of samples
during hypoventilation (Asmundson & Stein,sociated with normative drops in vagal output,
reductions were more profound in the panic 1994; Yeragani et al., 1991, 1993), after pro-
longed exercise training (Al-Ani, Munir,group than in depressed or control groups,
who did not significantly differ from one an- White, Townsend, & Coote, 1996; Shi, Ste-
vens, Foresman, Stern, & Raven, 1995) andother. Moreover, no differences were found in
posture-induced blood pressure changes, after massage therapy (Field, 1995). All of
these procedures offer known anxiolytic ef-eliminating this as a potential mediator, via
baroreceptor-induced parasympathetic with- fects. Thus, several sources of evidence sug-
gest that vagal reactivity reflects intraindivid-drawal, of the group difference in vagal reac-
tivity. In a second study using a similar proce- ual shifts in anxiety level, and that those with
low baseline RSA are at particular risk fordure, significant differences in RSA were
found between panic and control patients in panic attacks during periods of acute vagal
withdrawal.both supine and standing positions (Yeragani
et al., 1993). Although the groups exhibited Finally, Gottman and colleagues (Gottman,
Jacobson, Rushe, Shortt, Babcock, La Tail-comparable drops across conditions, RSA in
the former group was consistently lower. lade, & Waltz, 1995; Jacobson, Gottman, &
Shortt, 1995), reported vagal withdrawal dur-Thus, contrary to the “law of initial values”
(Benjamin, 1963), the proportion of RSA re- ing marital conflict in 80% of a sample of vio-
lent males. When considered in conjunctionduction, as a function of basal RSA, was
larger in the panic patients. These findings with the findings presented above regarding
and panic attacks and anxiety, excessive vagalsuggest a link between excessive vagal with-
drawal and panic attacks, an assertion that is withdrawal may be a nonspecific marker of
emotional lability.supported by studies in which RSA was atten-
uated by hyperventilation and sodium lactate
infusion, which are known to precipitate panic
Summary and implications
symptoms (e.g., Asmundson & Stein, 1994;
George, 1989). Although the research addressing RSA reac-
tivity is less extensive and more difficult toIn addition, two studies have linked worry-
ing, which characterizes both generalized anx- interpret than the research addressing basal
RSA, several patterns emerge, most of whichiety and panic disorder, to vagal withdrawal.
Thayer et al. (1996) subjected a group of pa- should be interpreted with caution. Increased
vagal efference, as inferred from heart rate de-tients who met DSM-III-R criteria for gener-
alized anxiety disorder to a relaxation condi- celeration, appears to characterize periods of
sustained attention, a relation that has beention, and to a condition in which they were
instructed to imagine a topic of greatest con- observed at all age ranges considered. Al-
though this finding is consistent with the po-cern. Compared to control participants, gener-
alized anxiety patients exhibited reduced RSA lyvagal hypothesis that vagal inhibition sub-
serves mammalian attentional processing,in both conditions. In addition, both groups
demonstrated significant reductions in RSA further research is required in which respira-
tory parameters and basal RSA are controlledfrom relaxation to worry. Similar findings
have been reported by others (e.g., Lyonfields before definitive conclusions are drawn. Dur-
ing more challenging tasks that require activeet al., 1995). Moreover, nonpharmacological
Vagal tone and psychopathology 199
cognitive effort, competent engagement is re- itself, however, polyvagal theory cannot ac-
count for the behavioral dissimilarities be-flected in partial vagal withdrawal, which pre-
sumably facilitates preparedness of the SNS tween disorders characterized by aggression
and disorders characterized by anxiety andto respond to upcoming demands, in anticipa-
tion of potential increases in metabolic output. panic. Although both may represent excessive
fight–flight responding related to vagal dys-Also consistent with polyvagal theory, ex-
cessive vagal withdrawal appears to be related function, nothing in polyvagal theory suggests
why anger and aggression predominate into emotional lability of a fight–flight nature.
This is suggested by research with panic pa- some disorders, whereas anxiety and panic
predominate in others. As outlined in earliertients, who consistently exhibit vagal with-
drawal that is disproportionate given their al- sections, these responses are presumed to be
mediated by the SNS only when inhibitoryready low baseline RSA, and from the finding
of reduced RSA during marital conflict in vio- parasympathetic influence is either chroni-
cally insufficient or suddenly removed. Thus,lent males. To the extent that large reductions
in RSA are associated with adaptive re- explanation of individual differences in char-
acteristically angry versus anxious responsesponses to danger, those with reduced basal
RSA may be at risk for such fight–flight re- sets requires a theory of SNS regulation. Such
a theory has been described in detail by Graysponding in situations of psychological or
cognitive challenge. Thus, the hypothesis set (1982a, 1982b, 1987a, 1987b) and applied to-
ward characterizing disorders of behavioralforth here is that moderate vagal withdrawal
is associated with optimal engagement and disinhibition in childhood by Quay (1988,
1993). A brief description of Gray’s theory aspreparedness to respond, whereas excessive
vagal withdrawal is associated with emotional applied to undersocialized aggressive conduct
disorder and attention deficit hyperactivitylability.
Relations between vagal reactivity and nor- disorder follows.
mative shifts in mood state are less clear, both
because fewer studies have addressed the is-
Gray’s Motivational Theory
sue and because movement artifacts, uncon-
trolled respiratory parameters, and attentional Gray (1982a, 1982b, 1987a, 1987b) proposed
three functionally distinct yet interdependentprocesses could explain many of the results.
Nevertheless, findings from these analyses, brain systems that govern behavior: the fight–
flight (F/F) system; the reward system, or be-and from exercise, relaxation, and anxiety-in-
duction studies, suggest that intraindividual havioral activation system (BAS); and the
punishment system, or behavioral inhibitionfluctuations in vagal outflow reflect emotional
state. When combined with the empirical system (BIS). The F/F system subserves both
escape behaviors and defensive reactions un-findings previously reviewed regarding RSA,
two broad conclusions are implied regarding der conditions of frustration, punishment, and
pain. Gray was least elaborative regarding thispsychopathology. First, as already suggested,
baseline deficiencies in parasympathetic tone system, although he suggested that brain cir-
cuits in the ventromedial hypothalamus, theare related to negative emotional traits, in-
cluding disorders of depression, anxiety, and central gray matter, and the amygdala mediate
F/F responding. Activity within this pathwayaggression. Second, excessive vagal with-
drawal is related to negative emotional states, is determined in part by the emotional signifi-
cance attributed to a stimulus, which, as pre-most notably panic and anger.
Thus, the vagal system appears to reflect viously outlined, is also reflected in vagal re-
activity. Indeed, both the F/F system and theattentional and emotional processes. This is
consistent with polyvagal theory, in which vagus nerve receive direct input from the dor-
sal motor nucleus (see Heimer, 1995), provid-both structural and functional aspects of emo-
tion are presumed to have evolved in conjunc- ing a structural link between vagal withdrawal
and the F/F emotions panic and rage. Thus,tion with fight–flight responding and associ-
ated attentional processes in mammals. By nonspecific activity within this pathway ac-
companies F/F responding. The hypothesis avoidance motivation. Activity in the BAS is
therefore likely to be reflected in SNS ac-presented here is that the form of such re-
sponding is primarily determined by Gray’s tivity.
Behavioral inhibition, on the other hand, isother motivational systems, the BAS and the
BIS, described below. reflected in electrodermal responding (Fowles,
1980, 1988), evidence for which is twofold.Initially referred to as the reward system,
but later renamed by Fowles (1980), the BAS First, nonspecific skin conductance responses
(SCRs) increase under threat of punishmentsubserves appetitive motivational functions,
governing both approach and active avoid- (e.g., Katkin, 1965); second, well-controlled
experiments suggest that such responses areance behaviors. Thus, the system is responsi-
ble for maximizing rewards (approach behav- unaffected by reward. Tranel (1983) reported
increases in SCRs in participants exposed toior) and for minimizing punishments in
situations where behavioral responses are re- feedback for incorrect responses during a con-
tinuous performance task, but not in partici-quired (active avoidance). According to Gray
(1987a), neural mediation of the BAS is pants who received a monetary reward for
correct responses. Furthermore, when partici-rooted in the dopaminergic pathway that in-
cludes the ventral tegmental area, the nucleus pants’ monetary incentives are dependent on
active responding, changes in skin conduc-accumbens, and the ventral striatum.
The BIS, on the other hand, subserves tance are reduced in comparison to those who
are instructed to inhibit responding (Sosnow-aversive motivational functions, controlling
passive avoidance and extinction. Through the ski, Nurzynska, & Polec, 1991). Thus, skin
conductance changes are observed duringproduction of fear and anxiety, the system ac-
tively inhibits appetitive behaviors when aver- punishment and passive avoidance, thereby
reflecting BIS activity. Moreover, the eccrinesive consequences are anticipated. Gray hy-
pothesized that neural mediation of the BIS is sweat glands from which electrodermal activ-
ity is derived are enervated exclusively byrooted in both the serotonergic projections of
the raphe nucleus and the noradrenergic pro- cholinergic fibers of the SNS, with no para-
sympathetic input (see Fowles, 1986).jections of the locus ceruleus.
Psychophysiological evidence suggests Finally, Gray suggested that the BAS and
BIS are actively opposed to one another, withthat both motivational systems are effected
through the sympathetic branch of the ANS. net output impacting upon behavior. When
BAS functioning predominates, either ap-With respect to the BAS, support for this con-
jecture is derived from three observations. proach or active avoidance results. When BIS
functioning predominates, passive avoidanceFirst, behavioral activation requires expendi-
tures of energy, and the functional role of the is likely. This active opposition has been cen-
tral to theories of behavior disorders in child-SNS has been viewed traditionally as one of
mobilizing resources to deal with environ- hood, including both undersocialized aggres-
sive conduct disorder (UACD) and ADHDmental demands (e.g., Heimer, 1995). Second,
increases in cardiac output, which are re- (Fowles, 1980, 1988; Quay, 1993; Rogeness,
Javors, & Pliszka 1992). A brief descriptionquired of behavioral activation, are facilitated
in part by sympathetically mediated changes of each disorder follows.
in the contractile force of the left ventricle
(see Sherwood, Allen, Fahrenberg, Kelsey,
UACD and ADHD
Lovallo, & van Doornen, 1990; Sherwood,
Allen, Obrist, & Langer, 1986). Third, the re- Conduct disorder (CD) is currently defined as
a behavioral pattern of persistent and repeatedticular nuclei that control PNS influences on
cardiac functioning are phylogenically new violations of social rules and the rights of oth-
ers (American Psychiatric Association, 1994).developments, with maximum differentiation
in the mammalian brain stem (Porges, 1994). Diagnostic features of CD include aggression
toward people and animals, destruction ofThus, these structures evolved after the biobe-
havioral systems subserving approach and property, deceitfulness and theft, and serious
Vagal tone and psychopathology 201
violations of social norms. Each of these fea- tive–impulsive, or combined. Although those
diagnosed with the latter two subtypes sharetures includes several specific criteria, with
the endorsement of any three being sufficient behavioral disinhibition with UACD groups,
they are not characteristically aggressive.for a formal diagnosis. Thus, none of the four
features is defining, allowing a given case to Rather, their impulsivity is manifested in
marked impatience, interruption of others, andmeet diagnostic criteria without any aggres-
sive symptoms. Much of the literature on CD difficulty regulating excitement.
Despite these differences, the behavioraland delinquency however, supports a distinc-
tion between CD cases low in aggression, and disinhibition of both disorders is proposed to
result from an imbalance in BAS and BISa subgroup characterized by heightened im-
pulsivity, lack of empathy, failure to form functioning favoring behavioral activation.
With few exceptions (e.g., Tremblay, Pihl,loyal bonds with peers, and persistent use of
instrumental aggression (see Quay, 1986). Vitaro, & Dobkin, 1994), this imbalance is
theorized to result from an underactive BIS,The third edition of the Diagnostic and Statis-
tical Manual of Mental Disorders (DSM-III; which leads to impulsivity because the BAS
operates relatively unopposed.American Psychiatric Association, 1980) re-
flected this distinction by including the Consistent with this interpretation, aggres-
sive children and adolescents exhibit dimin-UACD subtype.
Although subsequent versions of the DSM ished electrodermal activity at baseline (e.g.,
Delameter & Lahey, 1983), in response to ori-have subsumed all CD cases into an inclusive
diagnostic category, the validity of the UACD enting stimuli (e.g., Schmidt, Solanto, &
Bridger, 1985), and in response to mentaldistinction has been supported at several lev-
els of analysis. Members of this subgroup are stressors (McBurnett, Harris, Swanson, Pfiff-
ner, Freedland, & Tamm, 1993). Thus, UACDless competent socially (Henn, Bardwell, &
Jenkins, 1980), exhibit delinquent characteris- groups, who are deficient in behavioral inhibi-
tion, exhibit reductions in electrodermal activ-tics across a greater variety of situations (see
Moffitt, 1993) and are more likely to become ity across multiple paradigms.
Moreover, evidence at the neurotransmitterantisocial adults (Huesmann, Eron, Lefkow-
itz, & Walder, 1984; Robins, 1966) than are level for an underactive BIS in UACD is sub-
stantial. Kruesi, Rapoport, Hamburger, Hibbs,their nonaggressive counterparts. In addition,
twin studies suggest that the genetic loading Potter, Lenane, and Brown (1990) reported a
significant negative correlation between ag-for aggression is significantly higher than for
otherwise delinquent but nonaggressive acts gressive symptoms and concentrations of the
serotonin metabolite 5-hydroxyindoleacetic(Edelbrock, Rende, Plomin, & Thompson,
1995; Jary & Stewart, 1985). Finally, those acid (5-HIAA) in the cerebrospinal fluid of 29
children, a finding that has also been reportedmeeting UACD criteria are more behaviorally
disinhibited than other CD cases (Daugh- in aggressive adults (Linnoila, Virkkunen,
Scheinin, Nuutila, Rimon, & Goodwin 1983).erty & Quay, 1991; Shapiro, Quay, Hogan, &
Schwartz, 1988). Similarly, Birmaher, Stanley, Greenhill, Two-
mey, Gavrilescu, and Rabinovich (1990) re-Behavioral disinhibition is also a core attri-
bute of ADHD. Diagnostic features of ADHD ported an inverse correlation between aggres-
sion and available blood platelet binding sitesinclude both inattention and hyperactivity–
impulsivity (American Psychiatric Associa- for serotonin. Each of these findings suggests
dysregulated serotonergic functioning, as pre-tion, 1994). Each feature includes several spe-
cific criteria, with any combination of six dicted by the underactive BIS hypothesis. Addi-
tionally, noradrenergic functioning has beenbeing sufficient for a formal diagnosis. Be-
cause the criterion lists for both inattention tied to impulsive aggression. In UACD boys,
Rogeness and colleagues (Rogeness, Hernan-and hyperactivity–impulsivity are lengthy (13
criteria each), neither feature is defining. dez, Macedo, & Mitchell, 1982; Rogeness, Her-
nandez, Macedo, Suchakorn, & Hoppe, 1986;Thus, diagnoses are subtyped as predomi-
nantly inattentive, predominantly hyperac- Rogeness, Maas, Javors, Macedo, Harris, &
Hoppe, 1988) have repeatedly demonstrated noradrenergic functioning has also been im-
plicated in anxiety and depression in adultssignificant reductions in plasma dopamine-
beta-hydroxylase, an enzymatic precursor of (Brawman–Mintzer & Lydiard, 1997; Lake,
Pickar, Ziegler, Lipper, Slater, & Murphy,norepinephrine (NE), the neurotransmitter of
the noradrenergic system. Similar results ob- 1982; Leonard, 1997; Veith, Lewis, Linares,
Barnes, Raskind, Villacres, Murburg, Ash-tain in adult populations of impulsive aggres-
sives (see Kavoussi, Armstead, & Coccaro, leigh, Castillo, Peskind, Pascualy, & Halter,
1994).1997). Thus, both serotonergic and noradren-
ergic regulation are related to impulsive ag- To summarize, although both inhibited and
disinhibited samples exhibit vagal deficits andgression, findings consistent with Quay’s
(1993) argument of deficient BIS functioning are therefore not differentiated on parasympa-
thetic functioning, the groups do exhibit alter-in UACD.
Similar sources evidence also support the native motivational profiles. Anxiety and de-
pression are characterized by heightened BISunderactive BIS hypothesis for ADHD. In a
study by Iaboni, Douglas, and Ditto (1997), activity, whereas UACD and ADHD are char-
acterized by reduced BIS functioning. Gray’sADHD children were rewarded with a mone-
tary incentive for turning off a specified light theory does not account, however, for the be-
havioral differences between disinhibited sub-(among five). Extinction trials then ensued in
which no rewards were given. ADHD chil- groups. Both ADHD and UACD groups are
impulsive, yet the elevated levels of aggres-dren exhibited significantly smaller changes
from baseline in skin conductance during ex- sion by the latter group are not well accounted
for by attenuated BIS activity alone. As thetinction than did controls, suggesting insensi-
tivity to punishment and reduced BIS func- above literature review suggests, however, ag-
gressive samples are characterized by defi-tioning.
Additionally, Rogeness et al. (1986) have ciencies in parasympathetic functioning.
reported an inverse correlation between dopa-
mine-beta-hydroxylase levels and attention
An Integrated Model of
deficit symptoms. Relative to controls,
ADHD groups also exhibit reduced urinary
MHPG (Shekim, Dekirmenjian, Chapel, & Such findings suggest that the role of the
ANS in these disorders might be clarifiedDavis, 1982; Shekim, Sinclair, Glaser, Hor-
witz, Javaid, & Bylund, 1987; Yu-cun & Yu- through analyses of complex interactions be-
tween the SNS and PNS branches. Whilefeng, 1984), a metabolite reflective of NE ac-
tivity in the central nervous system, the ANS, compromised RSA and excessive vagal reac-
tivity suggest emotional dysregulation,and the adrenal gland. Thus, ADHD samples
may also be characterized by noradrenergic whether or not that dysregulation is mani-
fested in aggression, anxiety, or depression, isdysregulation.
In comparison, anxiety and depressive dis- reflected in characteristic sympathetic re-
sponse patterns. Moreover, the SNS branchorders are proposed to result from an imbal-
ance in BAS and BIS functioning favoring be- must be parsed into two motivational subsys-
tems, the BIS and the BAS, to account fullyhavioral inhibition. Research by Kagan et al.
(1987), in which behaviorally inhibited chil- for behavioral differences across these disor-
ders. This integrated model of ANS function-dren exhibited increased urinary NE metabo-
lites, supports this assertion. Additionally, ing is presented in Figure 2. Motivational pre-
dispositions, as reflected in BAS and the BISRogeness et al. (1988) have reported positive
associations between plasma dopamine-beta- functioning, fall under SNS control. Regula-
tional functioning, as reflected in vagal tonehydroxylase levels, separation anxiety disor-
der, and depressive disorders in child inpa- and vagal reactivity, falls under PNS control.
Note that both ANS branches contribute inde-tients. These results suggest increased NE,
and thus heightened BIS functioning in anxi- pendently to behavioral and emotional predis-
positions.ety and depression. Moreover, dysregulated
Vagal tone and psychopathology 203
Figure 2. An integrated model of autonomic nervous system-behavior relations in which
motivational functioning falls under sympathetic nervous system control and regulational
functioning falls under parasympathetic nervous system control. Note that both branches
contribute to behavioral predispositions.
Specific patterns of autonomic activity for Both the motivational component, contributed
by the BIS and the BAS, and the regulationalthe disorders addressed in this paper are sum-
marized in Table 1. Heightened BAS activity component, contributed by the vagal system,
are required.characterizes appetitive behavioral tendencies,
including those exhibited in extraversion, ag- Although most of the cells presented in Ta-
ble 1, particularly those related to vagal tone,gression, impulsivity, and panic, the latter of
which is dominated by active avoidance. vagal reactivity, and BIS functioning, are sup-
ported by the literature review presented,Heightened BIS activity characterizes passive
and fearful behavioral tendencies, including those related to BAS functioning are more
speculative. Evidence reviewed previously,those exhibited in introversion, depression,
anxiety, and, once again, panic. Note that the for example, suggests that both anxiety and
depression are characterized by heightenedclusters of behaviors related to BAS and BIS
dysregulation map almost directly onto the BIS functioning and reduced vagal tone, yet
little is known about BAS activity in eithernovelty-seeking and harm-avoidance dimen-
sions, respectively, of Cloninger’s personality disorder. Similarly, while aggressive partici-
pants exhibit reduced BIS activity, reducedtypology (Cloninger, 1987; Cloninger, Svrakic,
& Przybeck, 1993; Cloninger, Svrakic, & RSA, and heightened RSA reactivity, little di-
rect evidence exists regarding BAS activity inSvrakic, 1997), and are thus rooted in vali-
dated patterns of behavioral functioning. disorders of disinhibition. Moreover, two
schools of thought are represented in the liter-Regarding the PNS, low RSA characterizes
dysregulated emotional states, including ature. As suggested previously, one proposes
that aggression results from reward domi-anger, depression, and anxiety. Excessive va-
gal reactivity, on the other hand, characterizes nance, or an overactive BAS (Fowles, 1980,
1988; Milich, Hartung, Martin, & Haigler,emotional lability, as reflected in panic at-
tacks and impulsive aggression. According to 1994; Quay, 1988, 1993). Others, however,
have suggested that trait aggression representsthis model, outcome cannot be predicted by
the activity or reactivity in any single system. a form of sensation seeking that results from
Table 1. Patterns of autonomic nervous system functioning in common
psychopathologies and personality types
Motivational Behavioral Activation Inhibition Trait (RSA
Predisposition Manifestation (BAS) (BIS) (RSA) Reactivity)
Disinhibition Impulsivity (ADHD) High Low — —
Aggression (UACD) High Low Low High
Panic High High Low High
Extraversion High — — —
Inhibition Anxiety — High Low —
Depression Low High Low —
Panic High High Low High
Introversion — High — —
None Emotional stability — — High —
Emotional lability — — — High
Note: High, atypically high activity; Low, atypically low activity. Dashes represent normal activity. En-
tries in the BIS, RSA, and RSA reactivity columns are supported by the literature reviewed herein. En-
tries in the BAS column are more speculative and require empirical confirmation.
insensitivity to reward, and by implication an and high RSA reactivity. Because those with
ADHD are impulsive due to their BAS/BISunderactive BAS. According to this account,
aggressive probands require larger rewards to motivational profile, even typical degrees of
vagal reactivity may place them at risk for ag-experience hedonic states equivalent to those
of controls. Thus, in the absence of sufficient gressive behavior, suggesting that CD symp-
toms should be common in ADHD groups.inhibitory mechanisms (contributed by the
BIS) these probands engage in instrumental Prevalence figures from both epidemiological
and clinical samples support this supposition,aggression to attain satisfactory reward states.
It should be noted that such stimulation-seek- with 30–50% of ADHD cases exhibiting co-
morbid CD (Moffitt, 1990; Quay, 1988; Sand-ing formulations have a long history in the
personality and aggression literatures (see berg, Weiselberg, & Shaffer, 1980). More-
over, because UACD shares each autonomicEysenck & Gudjonsson, 1989; Quay, 1965;
Raine, 1993, 1996; Zuckerman & Como, feature of ADHD, those with UACD should
exhibit ADHD symptoms almost without ex-1983), and that similar accounts have been of-
fered for ADHD (Haenlein & Caul, 1987). ception, a prediction that is also borne out em-
pirically (e.g., Klein, Abikoff, Klass, Ganeles,These alternative interpretations can be re-
solved only through direct assessments of Seese, & Pollack, 1997). Similar reasoning
suggests a potential explanation for the highBAS functioning, which to date have not been
conducted. rates of comorbidity observed among anxiety
and depressive disorders (Maser & Cloninger,Note also that activity levels within the
BAS, BIS, and vagal systems are assumed to 1990), where differences along a continuum
of BAS activity are the only discriminatingreflect continuously distributed individual dif-
ferences, which may help to account for ob- autonomic feature in an otherwise identical
profile.served patterns of comorbidity within inter-
nalizing and externalizing disorder domains. Patterns of comorbidity observed across
internalizing and externalizing disorders pres-Both ADHD and UACD, for instance, are
proposed to be characterized by dysregulated ent a more difficult problem. The overlap be-
tween CD and depression, for example, hasBAS and attenuated BIS functioning. The lat-
ter disorder is also characterized by low RSA been estimated at as high as 35% in adoles-
Vagal tone and psychopathology 205
cents (Kovacs, Paulauskas, Gatsonis, & Rich- autonomic systems and on more direct assess-
ment of BAS functioning, two practices thatards, 1988). Yet the only common feature that
has been empirically documented across these to date have not been represented in the devel-
opmental psychopathology literature. To adisorders is low vagal tone. There are several
potential explanations for this dilemma. Evi- large degree, this is probably due to the lack
of an integrative theory of ANS functioningdence suggests that BAS dysregulation in ex-
ternalizing disorders may be specific to situa- in psychopathology. In addition, findings of
heart rate changes in response to incentivetions in which external incentives are present
(see Milich et al., 1994). Thus, while conduct motivation, which have been proposed to in-
dex BAS functioning (Fowles, 1980, 1988),disordered participants are able to inhibit on-
going behaviors when those behaviors are not are difficult to interpret because heart rate is
not a valid index of sympathetic activity,paired with external reinforcers (Schachar &
Logan, 1990), they are not able to do so when since both branches of the ANS contribute to
chronotropic cardiac regulation (see Berntsoncues for reward are present (Daugherty &
Quay, 1991; Shapiro et al., 1988). Consistent et al., 1994). Thus, estimates of group differ-
ences in BAS activity that are based on heartwith these findings, the proactive aggression
characteristic of CD is not engaged in indis- rate are systematically confounded with dif-
ferences in parasympathetic outflow. Al-criminately; it is often motivated toward instru-
mental rewards such as valued objects or social though estimates of vagal influence are ob-
tainable through the methods previouslydominance (see Bandura, 1983; Dodge, 1991).
In contrast, dysregulated BIS functioning may described, until recently limitations in tech-
nology have precluded noninvasive assess-not be situation specific. As previously re-
viewed, UACD and ADHD participants ex- ment of purely sympathetic effects on the
heart. By using impedance cardiography,hibit reduced electrodermal responding across
multiple paradigms (e.g., Delameter & Lahey, however, these limitations may be overcome.
This technique enables researchers to assess1983; McBurnett et al., 1993; Schmidt et al.,
1985). In addition, reports of reduced seroto- cardiac preejection period (PEP), or the time
between left ventricular depolarization andnin metabolites (Birmaher et al., 1990; Lin-
noila et al., 1983) and NE precursors (Roge- ejection into the aorta (see Sherwood et al.,
1990). This interval is determined by beta-ness et al., 1982, 1986, 1988) in aggressive
samples also suggest chronic BIS dysregula- adrenergic, and thus sympathetic, influences
(McCubbin, Richardson, Langer, Kizer, &tion. These findings raise the possibility that
concurrent BAS and BIS dysregulation could Obrist, 1983; Mezzacappa, Kelsey, & Katkin,
in press), with shorter intervals indicatingresult in ongoing depression, punctuated by
episodic aggressive outbursts when instru- greater sympathetic activity. Moreover, the
equipment employed is noninvasive, which ismental gains are accessible.
Finally, all depressive symptoms are prob- also the case for assessments of both skin con-
ductance and RSA. Thus, the exploration ofably not rooted in autonomic dysregulation.
Aggressive behaviors exact many conse- complex sympathetic and vagal interactions
through concurrent assessment of BIS, BAS,quences for conduct disordered individuals,
including damage to interpersonal relation- and vagal reactivity is now possible. Doing
so is of course essential toward validating theships, loss of access to resources, and institu-
tionalization. For those with some degree of proposed autonomic model.
We are currently conducting such an as-insight, such consequences may be sufficient
to precipitate depressive symptoms of an ex- sessment with UACD, ADHD, and control
groups of adolescent males. PEP, skin con-ogenous nature.
ductance, and RSA are being monitored dur-
ing baseline, reward, extinction, and passive
of ANS Patterns
coping with threat. As previously suggested,
the reward condition is expected to elicit BASClarifying many of these ambiguities depends
upon the simultaneous assessment of multiple reactivity, as indexed by PEP, whereas the ex-
tinction condition is expected to elicit BIS re- sive groups. Many researchers assumed that
the index would be elevated in aggressive par-activity, as indexed by skin conductance re-
sponses. The passive coping task, in which ticipants, because of (a) the positive associa-
tion between RSA and negative emotionalityparticipants view a videotape of an escalating
conflict between peers, will be informative in infancy, (b) reports of reduced RSA in
cases of anxiety and depression, and (c) thewith respect to BAS, BIS, and vagal reactivity
to social stimuli, which are more ecologically well-replicated finding of reduced heart rate
in aggressive populations. As reviewed, how-valid than incentive reward tasks. Both the
UACD and ADHD subjects are expected to ever, direct comparisons between controls and
aggressive samples suggest that reduced RSAbe differentiated from controls on electroder-
mal reactivity. Additionally, the UACD sub- characterizes anger as well as anxiety, and is
thus a nonspecific marker of dysregulatedjects are expected to be differentiated from
ADHD subjects on PEP and RSA. The hy- emotion.
This brings us to the final tenet, that behav-pothesized pattern of results would support
the need for concurrent assessment of both ior is multiply determined by complex inter-
actions among biological and psychologicalautonomic branches in characterizing behav-
iorally disinhibited groups. Subsequent stud- systems. In this paper, the biological compo-
nent was addressed through the advancementies are planned that will involve similar
assessments with anxious and depressed sam- of an integrated theory of ANS functioning in
psychopathology. Considerable evidence wasples.
presented outlining the importance of assess-
ing separate motivational systems governing
approach behaviors (the BAS), avoidance be-
haviors (the BIS), and emotional regulationAt the outset of this paper, it was suggested
that several apparent discrepancies in the va- (the vagal system). It was further suggested
that complex interactions among these sys-gal tone literature could be accounted for by
adopting three broad tenets set forth by devel- tems must be assessed, because in isolation
none can sufficiently account for the diversityopmental psychopathologists. The first of
these tenets underscores the importance of of findings reviewed.
Equally important, however, is to empha-studying development in our efforts toward
understanding behavior. The consistent find- size that although development must be con-
sidered toward explaining the large set of va-ing that RSA predicts behavioral reactivity
and negative emotionality in infancy, but pos- gal tone–behavior associations presented, this
is not a theory of vagal or emotional develop-itive emotionality and social competence in
later childhood, is no longer perplexing when ment. Because the current literature represents
a set of correlational associations, causal in-linked to normative emotional development
and differentiation. At all age ranges consid- ferences regarding the role of vagal tone in
the development of emotion regulation, or re-ered, vagal tone marks competent emotional
expression and active engagement with the garding the role of socialization processes in
the development of vagal tone and vagal re-environment. Such engagement is tied to neg-
ative emotionality in infancy because negative sponding, are not possible. The theory of
emotional and behavioral differentiation of-affect dominates the normative emotional rep-
ertoire at that age. Later, vagal tone marks fered by Calkins and Fox (1992; Calkins,
1994; Fox & Calkins, 1993), which representspositive affect and emotion regulation capa-
bilities, following normative shifts in social the only attempt to address the role of social-
ization in PNS development and associatedand emotional development.
The importance of the second tenet, that emotion regulation capacities, has not re-
ceived empirical support. Furthermore, few oftypical and atypical development must be
juxtaposed toward fully understanding behav- the substantial number of articles reviewed di-
rectly address issues of development throughioral disorders, is illustrated by the unex-
pected finding that RSA is lower in aggres- longitudinal research designs. Thus, although
Vagal tone and psychopathology 207
vagal tone marks emotional competence at all born with the former and develop the latter,
the position taken here is more agnostic. Theages, these relations are currently descriptive
and support no causal interpretations. extent to which genetic and environmental
factors determine autonomic output is likelyIn addition, our future understanding of the
role of the ANS in behavioral and emotional to involve complex interactions (Cicchetti &
Tucker, 1994). Moreover, the current data arefunctioning will be greatly enhanced if stan-
dardized methods of assessment are adopted open to interpretation. Field et al. (1995), for
example, have reported emerging differencesby researchers in this area. As indicated in
several sections of this paper, psychophysio- in RSA across the 1st year of life between
children of depressed and nondepressed moth-logical indices of vagal functioning are diffi-
cult to interpret without controlling for respi- ers. Although the authors leaned toward an
environmental explanation, differential devel-ration rate, attentional load, and movement
artifacts, which have been largely ignored in opmental trajectories can be genetically deter-
mined, as was also acknowledged. It is possi-the infant and child literature to date. Our un-
derstanding of ANS functioning in psycho- ble and perhaps likely that genes determine a
range of potential autonomic functioning,pathology will be further enhanced when di-
rect assessments of both sympathetic and within which transactions between the devel-
oping organism and the environment contrib-parasympathetic influences on cardiac func-
tioning are employed. The practice of infer- ute to observed levels of functioning. Parent–
child relationship characteristics are thoughtring the activity of either autonomic branch
from heart rate alone is outdated and unlikely to impact other genetically influenced biologi-
cal systems in such a manner (e.g., Pine, Was-to be fruitful in the future.
Finally, it should be noted that this theory serman, Coplan, Fried, Huang, et al., 1996).
Thus, further research is required to addressis not intended to be a comprehensive account
of personality, nor is this article intended to the extent to which autonomic functioning is
malleable. Such research may have importantsuggest that autonomically influenced behav-
iors are immutable. As Cloninger et al. (1997) implications for future intervention efforts ad-
dressing impulsive and otherwise dysregulatedhave noted, personality is comprised of both
temperamental traits, which this paper ad- behaviors. It is hoped that in the future these
efforts and others will include concurrent as-dresses, and character traits, which it does not.
Although Cloninger has suggested that we are sessments of multiple autonomic systems.
Achenbach, T. M. (1991). Manual for the Child Behavior American Psychiatric Association. (1980). Diagnostic
and statistical manual of mental disorders (3rd ed.).Checklist/4–18 and 1991 Profile, Burlington, VT:
University of Vermont, Department of Psychiatry. Washington, DC: Author.
American Psychiatric Association. (1994). DiagnosticAdinoff, B., Mefford, I., Waxman, R., & Linnoila, M.
(1992). Vagal tone decreases following intravenous and statistical manual of mental disorders (4th ed.).
Washington, DC: Author.diazepam. Psychiatry Research, 41, 89–97.
Akselrod, S., Gordon, D., Madwed, J. B., Snidman, Asmundson, G. J. G., & Stein, M. B. (1994). Vagal atten-
uation in panic disorder: An assessment of parasym-N. C., Shannon, D. C., & Cohen, R. J. (1985). Hemo-
dynamic regulation: Investigation by spectral analy- pathetic nervous system function and subjective reac-
tivity to respiratory manipulations. Psychosomaticsis. American Journal of Physiology, 249, H867–
H875. Medicine, 56, 187–193.
Bandura, A. (1983). Psychological mechanisms of ag-Akselrod, S., Gordon., D., Ubel, F. A., Shannon, D. C.,
Barger, A. C., & Cohen, R. J. (1981). Power spectrum gression. In R. Geen & E. Donnerstein (Eds.), Ag-
gression: Theoretical and empirical reviews: Vol. 1.analysis of heart rate fluctuation: A quantitative of
beat-to-beat cardiovascular control. Science, 213, Theoretical and methodological issues (pp. 1–40).
New York: Academic Press.220–222.
Al-Ani, M., Munir, S. M., White, M., Townsend, J., & Bates, J. E. (1984). The Infant Characteristics Question-
naire. Bloomington, IN: Indiana University Depart-Coote, J. H. (1996). Changes in R-R variability before
and after endurance training measured by power spec- ment of Psychology.
Bates, J. E., Freeland, C. A. B., & Lounsbury, M. L.tral analysis and by the effect of isometric muscle
contraction. European Journal of Applied Physiology, (1979). Measurement of infant difficultness. Child
Development, 50, 794–803.74, 397–403.
Bayley, N. (1969). Bayley Scales of Infant Development. Calkins, S. D., & Fox, N. A. (1992). The relations among
infant temperament, security of attachment, and be-New York: Psychological Corporation.
Bazhenova, O. V., & Porges, S. W. (1997). Vagal reac- havioral inhibition at twenty-four months. Child De-
velopment, 63, 1456–1472.tivity and affective adjustment in infants: Convergent
response systems. Annals of the New York Academy Campos, J. J., Barrett, K. C., Lamb, M. E., Goldsmith,
H. H., & Stenberg, C. (1983). Socioemotional devel-of Sciences, 807, 469–471.
Beck, A. T., Ward, C. H., Mendelson, M., & Erbaugh, J. opment. In P. H. Mussen (Series Ed.) & M. M.
Haith & J. J. Campos (Vol. Eds.), Handbook of child(1961). An inventory for measuring depression. Ar-
chives of General Psychiatry, 46, 243–250. psychology: Vol. II. Infancy and developmental biol-
ogy (4th ed., pp. 783–916). New York: Wiley.Benjamin, L. S. (1963). Statistical treatment of the law
of initial values in autonomic research: A review and Carey, W. B., & McDevitt, S. C. (1978). Revision of the
infant temperament questionnaire. Pediatrics, 61,recommendation. Psychosomatic Medicine, 25, 556–
Carney, R. M., Rich, M. W., teVelde, A., Saini, J., Clark,Bennett, D. S. (1994). Depression among children with
chronic medical problems: A meta-analysis. Journal K., & Freedland, K. E. (1988). The relationship be-
tween heart rate, heart rate variability, and depressionof Pediatric Psychiatry, 19, 149–169.
Berger, R. D., Saul, J. P., & Cohen, R. J. (1989). Transfer in patients with coronary artery disease. Journal of
Psychosomatic Research, 32, 159–164.function analysis of autonomic regulation. I. Canine
atrial response. American Journal of Physiology, 256, Carney, R., Saunders, R. D., Freedland, K. E., Stein, P.,
Rich, M. W., & Jaffe, A. S. (1995). Association ofH142–H152.
Berntson, G. G., Bigger, T. J., Eckberg, D. L., Grossman, depression with reduced heart rate variability in coro-
nary artery disease. American Journal of Cardiology,P., Kaufmann, P. G., Malik, M., Nagaraja, H. N.,
Porges, S. W., Saul, J. P., Stone, P. H., & van der 76, 562–564.
Casey, B. J., & Richards, J. E. (1988). Sustained visualMolen, M. W. (1997). Heart rate variability: Origins,
methods, and interpretive caveats. Psychophysiology, attention in young infants measured with an adapted
version of the visual preference paradigm. Child De-34, 623–648.
Berntson, G. G., Cacioppo, J. T., Binkley, P. F., Uchino, velopment, 59, 1514–1521.
Cicchetti, D. (1990). A historical perspective on the disci-B. N., Quigley, K. S., & Fieldstone, A. (1994). Auto-
nomic cardiac control. III. Psychological stress and pline of developmental psychopathology. In J. Rolf,
A. S. Masten, D. Cicchetti, K. H. Nuechterlein, & S.cardiac response in autonomic space as revealed by
pharmacological blockades. Psychophysiology, 31, Weintraub (Eds.), Risk and protective factors in the
development of psychopathology (pp. 2–28). New599–608.
Berntson, G. G., Cacioppo, J. T., & Quigley, K. (1993). York: Cambridge University Press.
Cicchetti, D., & Toth, S. L. (1998). Perspectives on re-Respiratory sinus arrhythmia: Autonomic origins,
physiological mechanisms, and psychophysiological search and practice in developmental psychopathol-
ogy. In W. Damon (Series Ed.) & I. E. Sigel & K. A.implications. Psychophysiology, 30, 183–196.
Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. Renninger (Vol. Eds.), Handbook of child psychol-
ogy: Vol. 4. Child psychology in practice (5th ed., pp.(1995). The metrics of cardiac chronotropism: Biome-
tric perspectives. Psychophysiology, 32, 162–171. 479–583). New York: Wiley.
Cicchetti, D., & Tucker, D. (1994). Development andBerntson, G. G., Cacioppo, J. T., Quigley, K. S., & Fabro,
V. T. (1994). Autonomic space and psychophysiolog- self-regulatory structures of the mind. Development
and Psychopathology, 6, 533–549.ical response. Psychophysiology, 31, 44–61.
Birmaher, B., Stanley, M., Greenhill, L., Twomey, J., Cloninger, C. R. (1987). A systematic method for clinical
description and classification of personality variants:Gavrilescu, A., & Rabinovich, H. (1990). Platelet
imipramine binding in children and adolescents with A proposal. Archives of General Psychiatry, 44, 573–
588.impulsive behavior. Journal of the American Acad-
emy of Child & Adolescent Psychiatry, 29, 914–918. Cloninger, C. R., Svrakic, D. M., & Przybeck, T. R.
(1993). A psychobiological model of temperamentBrawman–Mintzer, O., & Lydiard, R. B. (1997). Biologi-
cal bases of generalized anxiety disorder. Journal of and character. Archives of General Psychiatry, 50,
975–990.Clinical Psychiatry, 58(Suppl. 3), 16–25.
Buss, A. H., & Plomin, R. (1975). A temperament theory Cloninger, C. R., Svrakic, N. M., & Svrakic, D. M.
(1997). Role of personality self-organization in devel-of personality development. New York: Wiley.
Butler, A. B., & Hodos, W. (1996). Comparative verte- opment of mental order and disorder. Development
and Psychopathology, 9, 881–906.brate neuroanatomy: Evolution and adaptation. New
York: Wiley–Liss. Cole, P. M., Michel, M. K., & O’Donnell Teti, L. (1994).
The development of emotion regulation and dysregu-Cacioppo, J. T., Uchino, B. N., & Berntson, G. G. (1994).
Individual differences in autonomic origins of heart lation: A clinical perspective. Monographs of the So-
ciety for Research in Child Development, 59(2–3, Se-rate reactivity: The psychometrics of respiratory sinus
arrhythmia and preejection period. Psychophysiology, rial No. 240).
Cole, P. M., Zahn–Waxler, C., Fox, N. A., Usher,31, 412–419.
Calkins, S. D. (1994). Origins and outcomes of individual B. A., & Welsh, J. D. (1996). Individual differences
in emotion regulation and behavior problems in pre-differences in emotion regulation. Monographs of the
Society for Research in Child Development, 59(2–3, school children. Journal of Abnormal Psychology,
105, 518–529.Serial No. 240).
Calkins, S. D. (1997). Cardiac vagal tone indices of tem- Coles, M. G. (1972). Cardiac and respiratory activity dur-
ing visual search. Journal of Experimental Psychol-peramental reactivity and behavioral regulation in
young children. Developmental Psychobiology, 31, ogy, 96, 371–379.
Cook, W. W., & Medley, D. M. (1954). Proposed hostil-125–135.
Vagal tone and psychopathology 209
ity and pharisiac-virtue scales for the MMPI. Journal Switzer, G. (1994). The relations of children’s emo-
tion regulation to their vicarious emotional responsesof Applied Psychology, 38, 414–418.
Dalack, G. W., & Roose, S. P. (1990). Perspectives on and comforting behaviors. Child Development, 65,
1678–1693.the relationship between cardiovascular disease and
affective disorder. Journal of Clinical Psychiatry, 51, Field, T. (1995). Infant message therapy. In T. Field
(Ed.), Touch in early development (pp. 105–114).4–9.
Daughtery, T. K., & Quay, H. C. (1991). Response per- Hillsdale, NJ: Erlbaum.
Field, T., Lang, C., Martinez, A., Yando, R., Pickens,severation and delayed responding in childhood be-
havior disorders. Journal of Child Psychology and J., & Bendell, D. (1996). Preschool follow-up of in-
fants of dysphoric mothers. Journal of Clinical ChildPsychiatry, 32, 453–461.
DeGangi, G. A., DiPietro, J. A., Greenspan, S. I., & Psychology, 25, 272–279.
Field, T., Pickens, J., Fox, N. A., Nawrocki, T., & Gonza-Porges, S. W. (1991). Psychophysiological character-
istics of the regulatory disordered infant. Infant Be- lez, J. (1995). Vagal tone in infants of depressed
mothers. Development and Psychopathology, 7, 227–havior and Development, 14, 37–50.
Delameter, A. M., & Lahey, B. B. (1983). Psychophysio- 231.
Fowles, D. C. (1980). The three arousal model: Implica-logical correlates of conduct problems and anxiety in
hyperactive and learning-disabled children. Journal of tions of Gray’s two-factor learning theory for heart
rate, electrodermal activity, and psychopathy. Psycho-Abnormal Child Psychology, 11, 85–100.
Denot–Ledunois, S., Vardon, G., Perruchet, P., & Gal- physiology, 17, 87–104.
Fowles, D. C. (1986). The eccrine system and electroder-lego, J. (1998). The effect of attentional load on the
breathing pattern in children. International Journal of mal activity. In M. G. H. Coles, E. Donchin, & S. W.
Porges (Eds.), Psychophysiology: Systems, processes,Psychophysiology, 1, 13–21.
DiPietro, J. A., & Porges, S. W. (1991). Vagal respon- and applications (pp. 51–96). New York: Guilford
Press.siveness to gavage feeding as an index of preterm
stress. Pediatric Research, 29, 231–236. Fowles, D. C. (1988). Psychophysiology and psychopath-
ology: A motivational approach. Psychophysiology,DiPietro, J. A., Porges, S. W., & Uhly, B. (1992). Reac-
tivity and developmental competence in preterm and 25, 373–391.
Fox, N. A. (1989). Psychophysiological correlates offull term infants. Developmental Psychology, 28,
831–841. emotional reactivity during the first year of life. De-
velopmental Psychology, 25, 364–372.Dodge, K. A. (1991). The structure and function of reac-
tive and proactive aggression. In D. J. Peppler & Fox, N. A., & Calkins, D. D. (1993). Pathways to aggres-
sion and social withdrawal: Interactions among tem-K. H. Rubin (Eds.), The development and treatment
of childhood aggression (pp. 201–218). Hillsdale, NJ: perament, attachment, and regulation. In K. H. Ru-
bin & J. Asendorpf (Eds.), Social withdrawal,Erlbaum.
Doussard–Roosevelt, J. A., Porges, S. W., Scanlon, shyness, and inhibition in childhood (pp. 81–100).
Hillsdale, NJ: Erlbaum.J. W., Alemi, B., & Scanlon, K. B. (1997). Vagal reg-
ulation of heart rate in the prediction of develop- Fox, N. A., & Field, T. M. (1989). Individual differences
in preschool entry behavior. Journal of Applied De-mental outcome for very low birth weight preterm in-
fants. Child Development, 68, 173–186. velopmental Psychology, 10, 527–540.
Fox, N. A., & Stifter, C. A. (1989). Biological and behav-Edelbrock, C., Rende, R., Plomin, R., & Thompson, L. A.
(1995). A twin study of competence and problem be- ioral differences in infant reactivity and regulation. In
G. A. Kohnstamm, J. E. Bates, & M. K. Rothbarthavior in childhood and early adolescence. Journal of
Child Psychology and Psychiatry, 36, 775–785. (Eds.), Temperament in childhood (pp. 169–183).
New York: Wiley.Eisenberg, N., Fabes., R. A., Karbon, M., Murphy, B. C.,
Wosinski, M., Polazzi, L., Carlo, G., & Juhnke, C. Fracasso, M. P., Porges, S. W., Lamb, M. E., & Rosen-
berg, A. A. (1994). Cardiac activity in infancy: Relia-(1996). The relations of children’s dispositional pro-
social behavior to emotionality, regulation, and social bility and stability of individual differences. Infant
Behavior and Development, 17, 277–284.functioning. Child Development, 67, 974–992.
Eisenberg, N., Fabes, R. A., Murphy, B., Maszk, P., Friedman, B. H., & Thayer, J. F. (1998a). Autonomic bal-
ance revisited: Panic anxiety and heart rate variabil-Smith, M., & Karbon, M. (1995). The role of emo-
tionality and regulation in children’s social function- ity. Journal of Psychosomatic Research, 44, 133–151.
Friedman, B. H., & Thayer, J. F. (1998b). Anxiety anding: A longitudinal study. Child Development, 66,
1360–1384. autonomic flexibility: A cardiovascular approach. Bi-
ological Psychology, 47, 243–263.Ekman, P., & Friesen, W. V. (1984). EMFACS facial
coding manual. San Francisco: Consulting Psychol- Friedman, B. H., Thayer, J. F., Borkovec, T. D., Tyrrell,
R. A., Johnson, B., & Columbo, R. (1993). Auto-ogy Press.
Eppinger, H., & Hess, L. (1915). Vagotonia; A Clinical nomic characteristics of nonclinical panic and blood
phobia. Biological Psychiatry, 34, 298–310.study in negative neurology (W. M. Kraus & S. E.
Jelliffe, Trans.). New York: The Nervous and Mental George, D. T., Nutt, D. J., Walker, W. V., Porges,
S. W., Adinoff, B., & Linnoila, M. (1989). LactateDisease Publishing Company. (Original work pub-
lished 1910) and hyperventilation substantially attenuate vagal
tone in normal volunteers: A possible mechanism ofEysenck, H. J., & Gudjonsson, G. H. (1989). The causes
and cures of criminality. New York: Plenum Press. panic provocation? Archives of General Psychiatry,
46, 153–156.Fabes, R. A., Eisenberg, N., & Eisenbud, L. (1993). Be-
havioral and physiological correlates of children’s re- Goldsmith, H. H. (1996). Studying temperament via con-
struction of the Toddler Behavior Assessment Ques-actions to others in distress. Developmental Psychol-
ogy, 29, 655–663. tionnaire. Child Development, 67, 218–235.
Gottman, J. M., Jacobson, N. S., Rushe, R. H., Shortt,Fabes, R. A., Eisenberg, N., Karbon, N., Troyer, D., &
J. W., Babcock, J., La Taillade, J. J., & Waltz, J. Hayano, J., Sakakibara, Y., Yamada, A., Yamada, M.,
Mukai, S., Fujinami, T., Yokoyama, K., Watanabe,(1995). The relationship between heart rate reactivity,
emotionally aggressive behavior, and general vio- Y., & Takata, K. (1991) Accuracy of assessment of
cardiac vagal tone by heart rate variability in normallence in batterers. Journal of Family Psychology, 9,
227–248. subjects. American Journal of Cardiology, 67, 199–
204.Gottman, J. M., & Katz, L. F. (1995). Vagal tone protects
children from marital conflict. Development and Psy- Heimer, L. (1995). The human brain and spinal cord.
New York: Springer–Verlag.chopathology, 7, 83–92.
Gray, J. A. (1982a). The neuropsychology of anxiety: An Henn, F. A., Bardwell, R., & Jenkins, R. L. (1980). Juve-
nile delinquents revisited. Archives of General Psy-enquiry into the function of the septo-hippocampal
system. New York: Oxford University Press. chiatry, 37, 1160–1163.
Hickey, J. E., Suess, P. E., Newlin, D. B., Spurgeon,Gray, J. A. (1982b). Precis of the neuropsychology of
anxiety: An enquiry into the functions of the septo- L., & Porges, S. W. (1995). Vagal tone regulation
during sustained attention in boys exposed to opiateshippocampal system. The Behavioral and Brain Sci-
ences, 5, 469–534. in utero. Addictive Behaviors, 2, 43–59.
Huesmann, L. R., Eron, L. D., Lefkowitz, M. M., & Wal-Gray, J. A. (1987a). Perspectives on anxiety and impul-
sivity: A commentary. Journal of Research in Per- der, L. O. (1984). Stability of aggression over time
and generations. Developmental Psychology, 20,sonality, 21, 493–509.
Gray, J. A. (1987b). The psychology of fear and stress. 1120–1134.
Huffman, L. C., Bryan, Y. E., del Carmen, R., Pedersen,New York: Cambridge University Press.
Greenspan, S. I. (1991). Infancy and early childhood: The F. A., Doussard–Roosevelt, J. A., & Porges, S. W.
(1998). Infant temperament and cardiac vagal tone:practice of clinical assessment and intervention with
emotional and developmental challenges. Madison, Assessments at twelve weeks of age. Child Develop-
ment, 69, 624–635.CT: International Universities Press.
Grossman, P. (1983). Respiration, stress, and cardiovas- Hveem, K., Svebak, S., Hausken, T., & Berstad, A.
(1998). Effect of mental stress and cisapride on auto-cular function. Psychophysiology, 20, 284–300.
Grossman, P., Karemaker, J., & Wieling, W. (1991). Pre- nomic nerve functions in functional dyspepsia. Scan-
dinavian Journal of Gastroenterology, 33, 123–127.diction of tonic parasympathetic cardiac control using
respiratory sinus arrhythmia: The need for respiratory Hyde, C., & Izard, C. E. (1997). Cardiac rhythmicities
and attention in young children. Psychophysiology,control. Psychophysiology, 28, 201–216.
Grossman, P., & Kollai, M. (1993). Respiratory sinus ar- 34, 547–552.
Iaboni, F., Douglas, V. I., & Ditto, B. (1997). Psycho-rhythmia, cardiac vagal tone, and respiration: Within-
and between-individuals relations. Psychophysiology, physiological response of ADHD children to reward
and extinction. Psychophysiology, 34, 116–123.30, 486–495.
Grossman, P., & Svebak, S. (1987). Respiratory sinus ar- Izard, C. E., & Dougherty, L. M. (1980). A system for
identifying affect expressions by holistic judgementsrhythmia as an index of parasympathetic cardiac con-
trol during active coping. Psychophysiology, 24, 228– (AFFEX). Newark, DE: Instructional Resources
Grossman, P., van Beek, J., & Wientjes, C. (1990). A Izard, C. E., Porges, S. W., Simons, R. F., Haynes,
O. M., & Cohen, B. (1991) Infant cardiac activity:comparison of three quantification methods for esti-
mation of respiratory sinus arrhythmia. Psychophysi- Developmental changes and relations with attach-
ment. Developmental Psychology, 27, 432–439.ology, 27, 702–714.
Gunnar, M. R. (1990). The psychobiology of infant tem- Jacobson, N. S., Gottman, J. M., & Shortt, J. W. (1995).
The distinction between Type 1 and Type 2 batter-perament. In J. Colombo & J. Fagen (Eds.), Individ-
ual differences in infancy: Reliability, stability, pre- ers—Further considerations: Reply to Ornduff et al.
(1995), Margolin et al. (1995), and Walker (1995).diction (pp. 387–409). Hillsdale, NJ: Erlbaum.
Gunnar, M. R., Porter, F. L., Wolf, C. M., Rigatuso, J., & Journal of Family Psychology, 9, 272–279.
Jakobsen, J., Hauksson, P., & Vestergaard, P. (1984).Larson, M. C. (1995). Neonatal stress reactivity: Pre-
dictions to later emotional temperament. Child Devel- Heart rate variation in patients treated with antide-
pressants. An index of anticholinergic effects? Psy-opment, 66, 1–13.
Haenlein, M., & Caul, W. F. (1987). Attention deficit dis- chopharmacology, 84, 544–548.
Jary, M. L., & Stewart, M. A., (1985). Psychiatric disor-order with hyperactivity: A specific hypothesis of re-
ward dysfunction. Journal of the American Academy der in the parents of adopted children with aggressive
conduct disorder. Neuropsychobiology, 13, 7–11.of Child & Adolescent Psychiatry, 26, 356–362.
Harper, R. M., Walter, D. O., Leake, B., Hoffman, H. J., Jennings, R. J., & McKnight, J. D. (1994). Inferring vagal
tone from heart rate variability. Psychosomatic Medi-Sieck, G. C., Sterman, M. B., Hoppenbrouwers, T., &
Hodgman, J. (1978). Development of sinus arrhyth- cine, 56, 194–196.
Kagan, J. (1997). Conceptualizing psychopathology: Themia during sleep and waking states in normal infants.
Sleep, 1, 33–48. importance of developmental profiles. Development
and Psychopathology, 9, 321–334.Harris, R. M., Porges, S. W., Clemenson Carpenter,
M. E., & Vincenz, L. M. (1993). Hypnotic suscepti- Kagan, J., Reznick, J. S., & Snidman, N. (1987). The
physiology and psychology of behavioral inhibition inbility, mood state, and cardiovascular reactivity.
American Journal of Clinical Hypnosis, 36, 15–25. children. Child Development, 58, 1459–1473.
Kagan, J., & Snidman, J. (1991). Infant predictors of in-Haug, T. T., Svebak, S., Hausken, T., Wilhelmsen, I.,
Berstad, A., & Ursin, H. (1994). Low vagal activity hibited and uninhibited profiles. Psychological Sci-
ence, 2, 40–44.as mediating mechanism for the relationship between
personality factors and gastric symptoms in functional Katkin, E. S. (1965). Relationship between manifest anxi-
ety and two indices of autonomic response to stress.dyspepsia. Psychosomatic Medicine, 56, 181–186.
Vagal tone and psychopathology 211
Journal of Personality and Social Psychology, 2, S. W. (1997). Relationship between changes in EMG
and respiratory sinus arrhythmia in a study of relax-324–333.
Katona, P. G., Frasz, A., & Egbert, J. R. (1980). Matura- ation therapy for asthma. Applied Psychophysiology
and Biofeedback, 22, 183–191.tion of cardiac control in full-term and preterm infants
during sleep. Early Human Development, 4, 145–159. Leonard, B. E. (1997). The role of noradrenaline in de-
pression: A review. Journal of Psychopharmacology,Katona, P. G., & Jih, R. (1975). Respiratory sinus ar-
rhythmia: A noninvasive measure of parasympathetic 11(Suppl. 4), 39–47.
Levine, M., Elzey, F. F., & Lewis, M. (1969). Californiacardiac control. Journal of Applied Physiology, 39,
801–805. Preschool Competency Scale. Palo Alto, CA: Con-
sulting Psychologists Press.Kavoussi, R., Armstead, P., & Coccaro, E. (1997). The
neurobiology of impulsive aggression. The Psychiat- Levy, M. N., & Warner, M. R. (1994). Parasympathetic
effects on cardiac function. In J. A. Armour & J. L.ric Clinics of North America, 20, 395–403.
Kelsey, R. M. (1991). Electrodermal lability and myocar- Ardell (Eds.), Neurocardiology (pp. 77–94). New
York: Oxford University Press.dial reactivity to stress. Psychophysiology, 28, 619–
631. Light, K. C., Kothandapani, R. V., & Allen, M. T. (1998).
Enhanced cardiovascular and chatecholamine re-Kennedy, S. H., & Heslegrave, R. J. (1989). Cardiac reg-
ulation in bulimia nervosa. Journal of Psychiatric Re- sponses in women with depressive symptoms. Inter-
national Journal of Psychophysiology, 28, 157–166.search, 23, 267–273.
Kindlon, D. L., Tremblay, R. E., Mezzacappa, E., Earls, Linnemeyer, S. A., & Porges, S. W. (1986). Recognition
memory and cardiac vagal tone in 6-month-old in-F., Laurent, D., & Schaal, B. (1995). Longitudinal
patterns of heart rate and fighting behavior in 9- fants. Infant Behavior and Development, 9, 43–56.
Linnoila, M., Virkkunen, M., Scheinin, M., Nuutila, A.,through 12-year-old boys. Journal of the American
Academy of Child & Adolescent Psychiatry, 34, 371– Rimon, R., & Goodwin, F. K. (1983). Low cerebro-
spinal fluid 5-hydroxyindoleacetic acid concentration377.
Klein, R. G., Abikoff, H., Klass, E., Ganeles, D., Seese, differentiates impulsive from nonimpulsive violent
behavior. Life Sciences, 33, 2609–2614.L. M., & Pollack, S. (1997). Clinical efficacy of
methylphenidate in conduct disorder with and without Lyonfields, J. D., Borkovec, T. D., & Thayer, J. F.
(1995). Vagal tone in generalized anxiety disorderattention deficit hyperactivity disorder. Archives of
General Psychiatry, 54, 1073–1080. and the effects of aversive imagery and worrisome
thinking. Behavior Therapy, 26, 457–466.Kollai, M., & Kollai, B. (1992). Cardiac vagal tone in
generalized anxiety disorder. British Journal of Psy- Maser, J. D., & Cloninger, C. R. (1990). Comorbidity of
mood and anxiety disorders. Washington, DC: Amer-chiatry, 161, 831–835.
Kovacs, M., Paulauskas, S., Gatsonis, C., & Richards, C. ican Psychiatric Press.
McBurnett, K., Harris, S. M., Swanson, J. M., Pfiffner,(1988). Depressive disorders in childhood III. A lon-
gitudinal study of comorbidity with and risk for con- L. J., Freedland, D., & Tamm, L. (1993). Neuropsy-
chological and psychophysiological differentiationduct disorders. Journal of Affective Disorders, 15,
205–217. of inattention/overactivity and aggression/defiance
symptom groups. Journal of Clinical Child Psychol-Krittayaphong, R., Cascio, W. E., Light, K. C., Sheffield,
D., Golden, R. N., Finkel, J. B., Glekas, G., Koch, ogy, 22, 165–171.
McCubbin, J. A., Richardson, J. E., Langer, A. W., Kizer,G. G., & Sheps, D. S. (1997). Heart rate variability
in patients with coronary artery disease: Differences J. S., & Obrist, P. A. (1983). Sympathetic neuronal
function and left ventricular performance during be-in patients with higher and lower depression scores.
Psychosomatic Medicine, 59, 231–235. havioral stress in humans: The relationship between
plasma catecholamines and systolic time intervals.Kruesi, M. J. P., Rapoport, J. L., Hamburger, S., Hibbs,
E., Potter, W. Z., Lenane, M., & Brown, G. L. (1990). Psychophysiology, 20, 102–110.
Mezzacappa, E. R., Kelsey, R. M., & Katkin, E. S. (inCerebrospinal fluid monoamine metabolites, aggres-
sion, and impulsivity in disruptive behavior disorders press). The effects of epinephrine administration on
impedance cardiographic measures of cardiovascularof children and adolescents. Archives of General Psy-
chiatry, 47, 419–426. function. International Journal of Psychophysiology.
Mezzacappa, E., Kindlon, D., Earls, F., & Saul, J. P.Lake, C. R., Pickar, D., Ziegler, M. G., Lipper, S., Slater,
S., & Murphy, D. L. (1982). High plasma norepineph- (1994). The utility of spectral analytic techniques in
the study of autonomic regulation of beat-to-beatrine levels in patients with major affective disorder.
American Journal of Psychiatry, 139, 1315–1318. heart rate variability. International Journal of Meth-
ods in Psychiatric Research, 4, 29–44.Langeluddecke, P., Goulston, K., & Tennant, C. (1990).
Psychological factors in dyspepsia of unknown cause: Mezzacappa, E., Steingard, R., Kindlon, D., Saul, J. P., &
Earls, F. (1998). Tricyclic antidepressants and cardiacA comparison with peptic ulcer disease. Journal of
Psychosomatic Research, 34, 215–222. autonomic control in children and adolescents. Jour-
nal of the American Academy of Child & AdolescentLansink, J. M., & Richards, J. E. (1997). Heart rate and
behavioral measures of attention in six-, nine-, and Psychiatry, 37, 52–59.
Mezzacappa, E., Tremblay, R. E., Kindlon, D., Saul,twelve-month-old infants during object exploration.
Child Development, 68, 610–620. J. P., Arseneault, L., Pihl, R. O., & Earls, F. (1996).
Relationship of aggression and anxiety to autonomicLehofer, M., Moser, M., Hoehn–Saric, R., McLeod, D.,
Liebmann, P., Drnovsek, B., Egner, S., Hildenbrandt, regulation of heart rate variability in adolescent
males. Annals of the New York Academy Sciences,G., & Zapotoczky, H. (1997). Major depression and
cardiac autonomic control. Biological Psychiatry, 42, 794, 376–378.
Mezzacappa, E., Tremblay, R. E., Kindlon, D., Saul,914–919.
Lehrer, P. M., Hochron, S. M., Mayne, T., Isenberg, S., J. P., Arseneault, L., Seguin, J., Pihl, R. O., & Earls,
F. (1997). Anxiety, antisocial behavior, and heart rateLasoski, A. M., Carlson, V., Gilchrist, J., & Porges,
regulation in adolescent males. Journal of Child Psy- tervention. Development and Psychopathology, 8,
43–58.chology and Psychiatry, 38, 457–469.
Milich, R., Hartung, C. M., Martin, C. A., & Haigler, Porges, S. W., Arnold, W. R., & Forbes, E. J. (1973).
Heart rate variability: An index of attentional respon-E. D. (1994). Behavioral disinhibition and underlying
processes in adolescents with disruptive behavior dis- sivity in human newborns. Developmental Psychol-
ogy, 8, 85–92.orders, In D. K. Routh (Ed.), Disruptive behavior dis-
orders in childhood. New York: Plenum Press. Porges, S. W., Doussard–Roosevelt, J. A., & Maiti, A. K.
(1994). Vagal tone and the physiological regulation ofMiller, B. D., & Wood, B. L. (1997). Influence of spe-
cific emotional states on autonomic reactivity and emotion. Monographs of the Society for Research in
Child Development, 59(2–3, Serial No. 240).pulmonary function in asthmatic children. Journal of
the American Academy of Child & Adolescent Psychi- Porges, S. W., Doussard–Roosevelt, J. A., Portales,
A. L., & Greenspan, S. I. (1996). Infant regulation ofatry, 36, 669–677.
Moffitt, T. E. (1990). Juvenile delinquency and attention the vagal “brake” predicts child behavior problems:
A psychobiological model of social behavior. Devel-deficit disorder: Boys’ developmental trajectories
from age 3 to age 15. Child Development, 61, 893– opmental Psychobiology, 29, 697–712.
Porges, S. W., Doussard–Roosevelt, J. A., Portales,910.
Moffitt, T. E. (1993). Adolescent-limited and life-course- A. L., & Suess, P. E. (1994). Cardiac vagal tone: Sta-
bility and relation to difficultness in infants and 3-persistent antisocial behavior: A developmental tax-
onomy. Psychological Review, 100, 674–701. year-olds. Developmental Psychobiology, 27, 289–
300.Moser, M., Lehofer, M., Hoehn–Saric, R., McLeod,
D. R., Hildebrandt, G., Seinbrenner, B., Voica, M., Porges, S. W., & Lipsitt, L. P. (1993). Neonatal respon-
sivity to gustatory stimulation: The gustatory–vagalLiebmann, P., & Zapotoczky, H. (1998). Increased
heart rate in depressed subjects in spite of unchanged hypothesis. Infant Behavior and Development, 16,
487–494.autonomic balance? Journal of Affective Disorders,
48, 115–124. Porges, S. W., & Raskin, D. C. (1969). Respiratory and
heart rate components of attention. Journal of Experi-Murphy, J. K., Alpert, B. S., Willey, E. S., & Somes,
G. W. (1988). Cardiovascular reactivity to psycholog- mental Psychology, 81, 497–503.
Porges, S. W., Stamps, L. E., & Walter, G. F. (1974).ical stress in healthy children. Psychophysiology, 25,
144–152. Heart rate variability and newborn heart rate re-
sponses to illumination changes. Developmental Psy-Petretta, M., Bonaduce, D., Scalfi, L., de Filippo, E.,
Marciano, F., Migaux, M., Themistoclakis, S., Ianni- chology, 10, 507–513.
Porter, C. L., Bryan, Y. E., & Hsu, H. (1995). Physiologi-ciello, A., & Contaldo, F. (1997). Heart rate variabil-
ity as a measure of autonomic nervous system func- cal markers in early infancy: Stability of 1-to 6-month
vagal tone. Infant Behavior and Development, 18,tion in anorexia nervosa. Clinical Cardiology, 20,
Porter, F. L., Porges, S. W., & Marshal, R. E. (1988).Pine, D. S., Wasserman, G., Coplan, J., Fried, J., Sloan,
R., Myers, M., Greenhill, L., Shaffer, D., & Parsons, Newborn pain cries and vagal tone: Parallel changes
in response to circumcision. Child Development, 59,B. (1996). Serotonergic and cardiac correlates of ag-
gression in children. Annals of the New York Academy 495–505.
Quay, H. C. (1965). Psychopathic personality as patho-of Sciences, 794, 391–393.
Pine, D. S., Wasserman, G. A., Coplan, J., Fried, J. A., logical stimulation seeking. American Journal of Psy-
chiatry, 122, 180–183.Huang, Y., Kassir, S., Greenhill, L., Shaffer, D., &
Parsons, B. (1996). Platelet serotonin 2A (5-HT
) re- Quay, H. C. (1986). Conduct disorders. In H. C. Quay &
J. S. Werry (Eds.), Psychopathological disorders ofceptor characteristics and parenting factors for boys at
risk for delinquency: A preliminary report. American childhood (3rd ed., pp. 35–72). New York: Wiley.
Quay, H. C. (1988). Attention deficit disorder and theJournal of Psychiatry, 153, 538–544.
Pine, D. S., Wasserman, G. A., Miller, L., Coplan, J. D., behavioral inhibition system: The relevance of the
neuropsychological theory of Jeffrey A. Gray. InBagiella, E., Kovelenku, P., Myers, M. M., & Sloan,
R. P. (1998). Heart period variability and psychopath- L. M. Bloomingdale & J. A. Sergeant (Eds.), Atten-
tion deficit disorder: Criteria, cognition, interventionology in urban boys at risk for delinquency. Psycho-
physiology, 35, 521–529. (pp. 117–125). Oxford: Pergamon.
Quay, H. C. (1993). The psychobiology of undersocial-Pomeranz, B., Macaulay, R. J. B., Caudill, M. A., Kutz,
I., Adam, D., Gordon, D., Kilborn, K. M., Barger, ized aggressive conduct disorder: A theoretical per-
spective. Development and Psychopathology, 5, 165–A. C., Shannon, D. C., Cohen, R. J., & Benson, H.
(1985). Assessment of autonomic function in humans 180.
Raine, A. (1993). The psychopathology of crime: Crimi-by heart rate spectral analysis. American Journal of
Physiology, 248, H151–H153. nal behavior as a clinical disorder. San Diego, CA:
Academic Press.Porges, S. W. (1986). Respiratory sinus arrhythmia:
Physiological basis, quantitative methods, and clinical Raine, A. (1996). Autonomic nervous system activity and
violence. In D. M. Stoff & R. F. Cairns (Eds.), Theimplications. In P. Grossman, K. Janssen, & D. Vaitl
(Eds.), Cardiorespiratory and cardiosomatic psycho- neurobiology of clinical aggression. Hillsdale, NJ:
Earlbaum.physiology (pp. 101–115). New York: Plenum Press.
Porges, S. W. (1995). Orienting in a defensive world: Raine, A., Venables, P. H., & Mednick, S. A. (1997).
Low resting heart rate at age 3 years predisposes toMammalian modifications of our evolutionary heri-
tage. A polyvagal theory. Psychophysiology, 32, 301– aggression at age 11 years: Evidence from the Mauri-
tius Child Health Project. Journal of the American318.
Porges, S. W. (1996). Physiological regulation in high- Academy of Child and Adolescent Psychiatry, 36,
1457–1464.risk infants: A model for assessment and potential in-
Vagal tone and psychopathology 213
Raine, A., Venables, P. H., & Williams, M. (1990a). Au- Rothbart, M. K. (1981). Measurement of temperament in
infancy. Child Development, 52, 569–578.
tonomic orienting responses in 15-year-old male sub-
Rothbart, M. K., & Bates, J. E. (1998). Temperament. In
jects and criminal behavior at age 24. American Jour-
W. Damon (Series Ed.), & N. Eisenberg (Vol. Ed.),
nal of Psychiatry, 147, 933–937.
Handbook of child psychology: Vol. 3. Social, emo-
Raine, A., Venables, P. H., & Williams, M. (1990b). Re-
tional, and personality development (5th ed., pp.
lationships between central and autonomic measures
105–176). New York: Wiley.
of arousal at age 15 years and criminality at age 24
Rothbart, M. K., & Mauro, J. A. (1990). Questionnaire
years. Archives of General Psychiatry, 47, 1003–
approaches to the study of infant temperament. In J.
W. Fagan & J. Colombo (Eds.), Individual differences
Randall, W. C. (1994). Efferent sympathetic innervation
in infancy: Reliability, stability, and prediction (pp.
of the heart. In J. A. Armour & J. L. Ardell (Eds.),
411–429). Hillsdale, NJ: Erlbaum.
Neurocardiology (pp. 77–94). New York: Oxford
Rubin, K. H., Hastings, P. D., Stewart, S. L., Henderson,
H. A., & Chen, X. (1997). The consistency and con-
Rechlin, T., Weis, M., Spitzer, A., & Kaschka, W. P.
comitants of inhibition: Some of the children, all of
(1994). Are affective disorders associated with alter-
the time. Child Development, 68, 467–483.
ations of heart rate variability? Journal of Affective
Sandberg, S. T., Weiselberg, M., & Shaffer, D. (1980)
Disorders, 32, 271–275.
Hyperkinetic and conduct problem children in a pri-
Richards, J. E. (1985a). Respiratory sinus arrhythmia pre-
mary school population: Some epidemiological con-
dicts heart rate and visual responses during visual at-
siderations. Journal of Child Psychology and Psychi-
tention in 14 and 20 week old infants. Psychophysiol-
atry, 21, 293–311.
ogy, 22, 101–109.
Sanson, A. V., Prior, M., Garino, E., Oberklaid, F., &
Richards, J. E. (1985b). The development of sustained
Sewell, J. (1987). The structure of infant tempera-
visual attention in infants from 14 to 26 weeks of age.
ment: Factor analysis of the Revised Infant Tempera-
Psychophysiology, 22, 409–416.
ment Questionnaire. Infant Behavior and Develop-
Richards, J. E. (1987). Infant visual sustained attention
ment, 10, 97–104.
and respiratory sinus arrhythmia. Child Development,
Saul, J. P., Berger, R. D., Albrecht, P., Stein, S. P., Chen,
M. H., & Cohen, R. J. (1991). Transfer function anal-
Richards, J. E., & Cameron, D. (1989). Infant heart-rate
ysis of the circulation: Unique insights into cardiovas-
variability and behavioral developmental status. In-
cular regulation. American Journal of Physiology,
fant Behavior and Development, 12, 45–58.
Richards, J. E., & Casey, B. J. (1991). Heart rate variabil-
Saul, J. P., Berger, R. D., Chen, M. H., & Cohen, R. J.
ity during attention phases in young infants. Psycho-
(1989). Transfer function analysis of autonomic regu-
physiology, 28, 43–53.
lation II. Respiratory sinus arrhythmia. American
Richards, J. E., & Gibson, T. L. (1997). Extended visual
Journal of Physiology, 256, H153–H161.
fixation in young infants: Look distributions, heart
Schachar, R., & Logan, G. D. (1990). Impulsivity and
rate changes, and attention. Child Development, 68,
inhibitory control in normal development and child-
hood psychopathology. Developmental Psychology,
Rissanen, A., Naukkarinen, H., Virkkunen, M., Rawlings,
R. R., & Linnoila, M. (1998). Fluoxetine normalizes
Schmidt, K., Solanto, M. V., & Bridger, W. H. (1985).
increased cardiac vagal tone in bulimia nervosa. Jour-
Electrodermal activity of undersocialized aggressive
nal of Clinical Psychopharmacology, 18, 26–32.
children. Journal of Child Psychology and Psychia-
Robins, L. (1966). Deviant children grown up. Baltimore,
try, 26, 653–660.
MD: Williams & Wilkins.
Shapiro, S. K., Quay H. C., Hogan, A. E., & Schwartz,
Rogeness, G. A., Cepeda, C., Macedo, C. A., Fischer,
K. P. (1988). Response perseveration and delayed re-
C., & Harris, W. R. (1990). Differences in heart rate
sponding in undersocialized aggressive conduct disor-
and blood pressure in children with conduct disorder,
der. Journal of Abnormal Psychology, 97, 371–373.
major depression, and separation anxiety. Psychiatry
Shekim, W. O., Dekirmenjian, H., Chapel, J. L., & Davis,
Research, 33, 199–206.
J. M. (1982). Effects of d-amphetamine on urinary
Rogeness, G. A., Hernandez, J. M., Macedo, C. A., &
metabolites of dopamine and norepinephrine in hy-
Mitchell, E. L. (1982). Biochemical differences in
peractive boys. American Journal of Psychiatry, 139,
children with conduct disorder socialized and under-
socialized. American Journal of Psychiatry, 139,
Shekim, W. O., Sinclair, E., Glaser, R., Horwitz, E., Ja-
vaid, J., & Bylund, D. B. (1987). Norepinephrine and
Rogeness, G. A., Hernandez, J. M., Macedo, C. A., Su-
dopamine metabolites and educational variables in
chakorn, A. A., & Hoppe, S. K. (1986). Near-zero
boys with attention deficit disorder and hyperactivity.
dopamine-β-hydroxylase and conduct disorder in
Journal of Child Neurology, 2, 50–56.
emotionally disturbed boys. Journal of the American
Sherwood, A., Allen, M. T., Fahrenberg, J., Kelsey,
Academy of Child Psychiatry, 25, 521–527.
R. M., Lovallo, W. R., & van Doornen, L. J. P.
Rogeness, G. A., Javors, M. A., & Pliszka, S. R. (1992).
(1990). Committee report: Methodological guidelines
Neurochemistry and child and adolescent psychiatry.
for impedance cardiography. Psychophysiology, 27,
Journal of the American Academy of Child & Adoles-
cent Psychiatry, 31, 765–781.
Sherwood, A., Allen, M. T., Obrist, P. A., & Langer,
Rogeness, G. A., Maas, J. W., Javors, M. A., Macedo,
A. W. (1986). Evaluation of beta-adrenergic influ-
C. A., Harris, W. R., & Hoppe, S. K. (1988). Diagno-
ences on cardiovascular and metabolic adjustments to
ses, catecholamine metabolism, and plasma dopa-
physical and psychological stress. Psychophysiology,
mine-β-hydroxylase. Journal of the American Acad-
Shi, X., Stevens, G. H. J., Foresman, B. H., Stern,emy of Child & Adolescent Psychiatry, 27, 121–125.
S. A., & Raven, P. B. (1995). Autonomic nervous etine increases heart rate variability in panic disorder.
Journal of Clinical Psychopharmacology, 17, 370–
system control of the heart: Endurance exercise train-
ing. Medicine and Science in Sports and Exercise, 27,
Tulen, J. H. M., Mulder, G., Pepplinkhuizen, L., Man in
’t Veld, A. J., van Steenis, H. G., & Moleman, P.
Shibagaki, M., & Furuya, T. (1997). Baseline respiratory