infant reactivity: physiological correlates of newborn and 5-month temperament

7
Developmental Psychology 1990, Vol. 26, No. 4,582-588 Copyright 1990 by the American Psychological Association, Inc. O012-1649/90/SO0.75 Infant Reactivity: Physiological Correlates of Newborn and 5-Month Temperament Cynthia A. Stifter Department of Human Development and Family Studies Pennsylvania State University Nathan A. Fox Institute for Child Study University of Maryland The relation between measures of heart period and vagal tone and infant reactivity was investigated in a longitudinal study of infants from birth to 5 months of age. At 2 days of age, electrocardiogram (EKG) was recorded and a pacifier-withdrawal task was administered. At 5 months of age, EKG was recorded, after which infants and mothers participated in a laboratory session designed to elicit positive and negative reactivity. Maternal ratings of 5-month infant temperament were also obtained. There was a significant concurrent relation between 5-month vagal tone and negative reactivity elic- ited in the laboratory and maternal ratings of activity level and smiling behavior. Newborn vagal tone predicted maternal ratings of frustration and fear. Moderate stability was found for infant reactivity. Central to most theories of temperament is the notion that individual differences in behavior are biologically determined or constitutionally based (Buss & Plomin, 1984; Rothbart & Derryberry, 1981; Thomas & Chess, 1977; Thomas, Chess, Birch, Hertzig, & Korn, 1963). Attempts at identifying physio- logical measures that are related to temperament in infants range from motor movement (Birns, 1965; Korner, Hutchinson, Koperski, Kraemer, & Schneider, 1981) to heart rate and heart rate variability (Kagan, Reznick, & Snidman, 1987; Stifter, Fox, & Porges, 1989), cortisol (Gunnar, Isensee, & Fust, 1987; Span- gler, Meindl, & Grossmann, 1988), and electroencephalogram asymmetry (Davidson & Fox, 1989). Relations between autonomic patterning and personality have had a long history in psychological research. Eppinger and Hess (1910) were among the first to discuss a relation between the patterning of the sympathetic and parasympathetic branches of the autonomic nervous system and behavior. They postulated that extremes in vagal tone were related to psychopa- thology. Wenger (1941; Wenger & Cullen, 1972) and Lacey and Lacey (1958) presented evidence to support a relation between autonomic patterning and certain personality types. Individuals with high autonomicfluctuationswere found to be high-strung, nervous, and motorically reactive, whereas those with little au- tonomic variability were passive and nonreactive. Porges (1976) has speculated that heart rate variability may be related to different personality styles through the variability in attention. This article is based on Cynthia A. Stifter's dissertation submitted to the University of Maryland in partial fulfillment of the requirements for the PhD degree. The research was supported in part by Grant HD17899 from the National Institute of Health to Nathan A. Fox. We would like to thank Ann Leubering, Laura Miller, and Barbara Sutton for their assistance in data collection, and Stephen W. Porges for his support in data analysis. Special thanks go to the parents and chil- dren who participated in the study. Correspondence concerning this article should be addressed to Cyn- thia A. Stifter, Department of Human Development and Family Stud- ies, Pennsylvania State University, University Park, Pennsylvania 16802. He proposed that sustained attention, which is associated with high vagal control, is related to psychopathy, whereas inatten- tion, which is associated with low vagal tone, is related to hyper- activity. Recently, Kagan and colleagues (Garcia-Coll, Kagan, & Rez- nick, 1984; Kagan, 1982; Kagan, Reznick, Clarke, Snidman, & Garcia-Coll, 1984; Reznick et al., 1986) have focused their research on the relation between sympathetic activity and ex- tremes in temperament. In a longitudinal study of children 21 months to 7 years of age, Kagan identified a group of children he labeled behaviorally inhibited. These children are character- ized by withdrawing, shy behavior; high and stable heart rate (low heart rate variability); and other physiological indexes that may be the result of sympathetic arousal (e.g., pupil dilation, cortisol secretion). The counterpart to behaviorally inhibited children are those children who exhibited socially outgoing be- havior and low and variable heart rate. Data from Kagan's (1982) lab have demonstrated stability of both physiological and behavioral manifestations of inhibition beginning at around 21 months of age. There has been, however, little research on the origins of this behavior pattern. In part, the reason stems from the lack of stability of certain global infant behaviors across the first year and the lack of reliability of cer- tain measures of maternal report of infant temperament (Hu- bert, Wachs, Peters-Martin, & Gandour, 1982). There is, however, support for the stability of behaviors such as irritability (Birns, Barten, & Bridger, 1969; Riese, 1987; Wor- obey & Lewis, 1988) and activity level (Buss, Block, & Block, 1980; Korner et al., 1985) measured from birth. In addition, there are data that point to the convergence between maternal ratings of temperament and behavioral observations (Rothbart, 1986; Wilson, 1982; Wilson AMatheney, 1983). The measurement of heart rate variability has changed con- siderably over the past 20 years. Advances in computer technol- ogy allow collection of large data sets. Changes in the approach to the analysis of the heart period data have contributed to new methods for measuring the sympathetic and parasympathetic contributions to heart rate variability (see Fox & Davidson, 1986, for a review). For example, Porges (1986) developed a 582

Upload: nathan-a

Post on 12-Dec-2016

212 views

Category:

Documents


0 download

TRANSCRIPT

Developmental Psychology1990, Vol. 26, No. 4,582-588

Copyright 1990 by the American Psychological Association, Inc.O012-1649/90/SO0.75

Infant Reactivity: Physiological Correlates ofNewborn and 5-Month Temperament

Cynthia A. StifterDepartment of Human Development and Family Studies

Pennsylvania State University

Nathan A. FoxInstitute for Child StudyUniversity of Maryland

The relation between measures of heart period and vagal tone and infant reactivity was investigatedin a longitudinal study of infants from birth to 5 months of age. At 2 days of age, electrocardiogram(EKG) was recorded and a pacifier-withdrawal task was administered. At 5 months of age, EKG wasrecorded, after which infants and mothers participated in a laboratory session designed to elicitpositive and negative reactivity. Maternal ratings of 5-month infant temperament were also obtained.There was a significant concurrent relation between 5-month vagal tone and negative reactivity elic-ited in the laboratory and maternal ratings of activity level and smiling behavior. Newborn vagal tonepredicted maternal ratings of frustration and fear. Moderate stability was found for infant reactivity.

Central to most theories of temperament is the notion thatindividual differences in behavior are biologically determinedor constitutionally based (Buss & Plomin, 1984; Rothbart &Derryberry, 1981; Thomas & Chess, 1977; Thomas, Chess,Birch, Hertzig, & Korn, 1963). Attempts at identifying physio-logical measures that are related to temperament in infantsrange from motor movement (Birns, 1965; Korner, Hutchinson,Koperski, Kraemer, & Schneider, 1981) to heart rate and heartrate variability (Kagan, Reznick, & Snidman, 1987; Stifter, Fox,& Porges, 1989), cortisol (Gunnar, Isensee, & Fust, 1987; Span-gler, Meindl, & Grossmann, 1988), and electroencephalogramasymmetry (Davidson & Fox, 1989).

Relations between autonomic patterning and personalityhave had a long history in psychological research. Eppinger andHess (1910) were among the first to discuss a relation betweenthe patterning of the sympathetic and parasympatheticbranches of the autonomic nervous system and behavior. Theypostulated that extremes in vagal tone were related to psychopa-thology. Wenger (1941; Wenger & Cullen, 1972) and Lacey andLacey (1958) presented evidence to support a relation betweenautonomic patterning and certain personality types. Individualswith high autonomic fluctuations were found to be high-strung,nervous, and motorically reactive, whereas those with little au-tonomic variability were passive and nonreactive. Porges (1976)has speculated that heart rate variability may be related todifferent personality styles through the variability in attention.

This article is based on Cynthia A. Stifter's dissertation submitted tothe University of Maryland in partial fulfillment of the requirements forthe PhD degree. The research was supported in part by Grant HD17899from the National Institute of Health to Nathan A. Fox.

We would like to thank Ann Leubering, Laura Miller, and BarbaraSutton for their assistance in data collection, and Stephen W. Porges forhis support in data analysis. Special thanks go to the parents and chil-dren who participated in the study.

Correspondence concerning this article should be addressed to Cyn-thia A. Stifter, Department of Human Development and Family Stud-ies, Pennsylvania State University, University Park, Pennsylvania16802.

He proposed that sustained attention, which is associated withhigh vagal control, is related to psychopathy, whereas inatten-tion, which is associated with low vagal tone, is related to hyper-activity.

Recently, Kagan and colleagues (Garcia-Coll, Kagan, & Rez-nick, 1984; Kagan, 1982; Kagan, Reznick, Clarke, Snidman,& Garcia-Coll, 1984; Reznick et al., 1986) have focused theirresearch on the relation between sympathetic activity and ex-tremes in temperament. In a longitudinal study of children 21months to 7 years of age, Kagan identified a group of childrenhe labeled behaviorally inhibited. These children are character-ized by withdrawing, shy behavior; high and stable heart rate(low heart rate variability); and other physiological indexes thatmay be the result of sympathetic arousal (e.g., pupil dilation,cortisol secretion). The counterpart to behaviorally inhibitedchildren are those children who exhibited socially outgoing be-havior and low and variable heart rate.

Data from Kagan's (1982) lab have demonstrated stability ofboth physiological and behavioral manifestations of inhibitionbeginning at around 21 months of age. There has been, however,little research on the origins of this behavior pattern. In part, thereason stems from the lack of stability of certain global infantbehaviors across the first year and the lack of reliability of cer-tain measures of maternal report of infant temperament (Hu-bert, Wachs, Peters-Martin, & Gandour, 1982).

There is, however, support for the stability of behaviors suchas irritability (Birns, Barten, & Bridger, 1969; Riese, 1987; Wor-obey & Lewis, 1988) and activity level (Buss, Block, & Block,1980; Korner et al., 1985) measured from birth. In addition,there are data that point to the convergence between maternalratings of temperament and behavioral observations (Rothbart,1986; Wilson, 1982; Wilson AMatheney, 1983).

The measurement of heart rate variability has changed con-siderably over the past 20 years. Advances in computer technol-ogy allow collection of large data sets. Changes in the approachto the analysis of the heart period data have contributed to newmethods for measuring the sympathetic and parasympatheticcontributions to heart rate variability (see Fox & Davidson,1986, for a review). For example, Porges (1986) developed a

582

INFANT REACTIVITY 583

method that extracts that portion of the variance in heart ratedue solely to respiratory sinus arrhythmia (RSA). This tech-nique uses complex detrending of the heart period process andtime-series analysis of the residual data. Because RSA is medi-ated via the vagus nerve, this derived measure (V) can bethought of as an estimate of vagal tone or vagal influence at thelevel of the heart. In a series of studies, Porges and colleagues(McCabe, Yongue, Porges, & Ackles, 1984; Porges, McCabe, &Yongue, 1982; Yongue et al., 1982) have demonstrated the phys-iological significance of respiratory sinus arrhythmia and therelation between vagal tone and RSA.

Vagal tone has recently been linked to behaviors reflectingemotional responsivity and temperament in infants and youngchildren (DiPietro, Larson, & Porges, 1987; Fox, 1989; Fox &Field, 1989; Stifter et al., 1989). For example, newborn infantswith high vagal tone were more reactive and irritable (DiPietroetal., 1987). In another study (Stifter etal., 1989), 5-month-oldinfants with greater cardiac vagal tone were found to be moreexpressive in response to an approaching stranger than were in-fants with low vagal tone. Likewise, 14-month-old infants withhigh vagal tone were more sociable and explorative of their envi-ronment and were less inhibited in their responses to an unfa-miliar adult (Fox, 1989). In a study of preschool adjustment, 3-year-old children with high vagal tone adapted more quickly toa new preschool environment and were rated as less difficult intheir temperament (Fox & Field, 1989). These studies togethersuggest that individual differences in vagal tone might be animportant marker reflecting variations in behavioral reactivityeven in the early months of life.

The purpose of the present article was to test this hypothesiswith a sample of newborn infants followed longitudinally overthe first 5 months of life. The questions addressed were (a) Whatis the relation between vagal tone and behavioral reactivity mea-sured during the newborn period and at 5 months of age? (b) Isnewborn vagal tone predictive of 5-month mother-rated tem-perament or 5-month temperamental behavior as assessed inthe laboratory? (c) Is behavioral reactivity stable from birth to5 months of age? and (d) Do parental ratings of temperamentconverge with laboratory ratings?

Method

Subjects

Subjects were 88 healthy, term newborn infants, 48 girls and 40 boys.Subjects were recruited through a university hospital newborn nursery.Criteria for selection were gestational age between 38 and 42 weeks(M = 39.6 weeks, SD = 1.3 weeks), birthweight between 2,500 and4,090 g (M = 3,584 g, SD = 490.8 g), vaginal or cesarean delivery, Apgarscores of at least 7 at 1 min and at least 8 at 5 min, and a normal pediat-ric exam. Pregnancies were uncomplicated by serious illness, and deliv-eries did not involve mid or high forceps or general anesthesia. On aver-age, newborn subjects were tested at 48 hr of age (SD = 24 hr).

A total of 63 subjects returned to the laboratory for follow-up at 5months of age (M = 20.2 weeks, SD = 1.28 weeks). Of these 63 follow-up subjects, 33 were girls and 30 were boys.'

nancy, prenatal care, and choice of feeding method, as well as demo-graphic data, were collected from the mothers before testing began.

Subjects were tested at least 1 hr after their last feeding. Electrocardio-gram (EKG) and sleep behavior were recorded from each infant whilehe or she was lying in a bassinet in an empty patient room on the mater-nity ward. Curtains were partially drawn to allow low levels of naturallight for the recording of eye, face, and body movements.

Electrocardiogram recording and sleep observation. Infant EKG wasrecorded by placing three disposable pediatric electrodes in a triangularpattern on the infant's chest. Electrode leads were connected to a GrassModel PI5 Preamplifier, and the EKG signal was recorded onto onechannel of a Vetter Model C-4 instrumentation recorder for off-linequantification and analysis. Newborn EKG was recorded for an averageof 10 min. The infants' state was coded every 25 s using the behavioralcriteria defined by Anders, Emde, and Parmelee (1971). Infant EKGand state were recorded until it was determined that 10 min of continu-ous active sleep had elapsed.

Pacifier withdrawal. The pacifier-withdrawal procedure was adminis-tered when the infant was in a quiet, alert state. Pacifier withdrawal orsucking interruption has been used in several neonatal studies investi-gating infant reactivity (Bell, Weller, & Waldrop, 1971;McGrade, 1968;Yang & Halverston, 1976). Infants were given a pacifier and allowed tosuck for 60 s, after which the pacifier was gently removed on thedropped-jaw phase of a suck. A series of soothing techniques was ad-ministered if the infant remained distressed 1 min after the removal ofthe pacifier. After calming, a second trial of pacifier withdrawal was be-gun. The subjects' reactions (e.g., fussing, crying) were recorded on acassette tape recorder. From these recordings the measures of latency tocry, number of cries, and the length of time from the first cry to a calmstate (soothe time) were coded.

5-Month Follow-Up

A laboratory visit was arranged when the infants were approximately5 months of age. A letter confirming the appointment was mailed alongwith the Infant Behavior Questionnaire (IBQ; Rothbart, 1981). TheIBQ is a 94-item measure that asks respondents to rate on a 7-pointscale infant behaviors that occurred within the last week. Six subscalesare computed from these data: Activity Level, Duration of Orientation,Smiling/Laughter, Distress to Limitations, Distress and Latency to Ap-proach the Novel, and Soothability.

Mothers and infants participated in a set of procedures designed toelicit reactivity. The order of procedures for the 5-month follow-up were(a) EKG recording, (b) peek-a-boo game with mother, (c) peek-a-boogame with a stranger, and (d) arm-restraint procedure.

Electrocardiogram recording. Five minutes of resting heart rate wererecorded while the infant sat quietly in mother's lap. The EKG electrodeplacement and recording equipment were the same as that used to re-cord newborn heart rate. Infants were videotaped during the recording,and frequency of motor movement (of arms and legs and trunk) wasscored. Epochs of EKG containing gross motor movement were elimi-nated from further analysis.

Peek-a-boo game. The procedure used to elicit smiling and laughterwas a peek-a-boo game with mother and an unfamiliar woman (Sroufe6 Waters, 1976). During this procedure, infants sat in an infant seat ateye level across from the mother and the stranger. Mothers and strangerwere instructed to interact normally with the infant and then, on a cuefrom the experimenter, begin to play peek-a-boo for 90 s. The only re-

Procedures

Newborn Period

Mothers of infants who met subject criteria were approached in theirhospital rooms, and informed consent was obtained. Data on preg-

1 The remaining 25 subjects were contacted but could not participatein the follow-up study. To test whether the infants who returned for thefollow-up were different in newborn autonomic activity than those whodid not return, a t statistic was computed on the groups and found tobe nonsignificant for heart period, f(72) = 0.03, p < .98, and vagal tone,472)= 1.17, p < . 2 4 .

584 CYNTHIA A. STIFTER AND NATHAN A. FOX

quirement, other than "to play peek-a-boo as you normally would," wasfor mothers and stranger to elicit the infant's attention by calling hisor her name or making sounds before exposing her face and smiling.Videotaping was done through a one-way mirror.

The peek-a-boo procedure produced the following measures: latencyto smile, which was calculated as the difference in time between thefirst exposure of the mother and stranger's smiling face and the time ofinfant's first coded smile; frequency of smiles; intensity of smiles; andduration of smiles, which was measured from the start of a smilethrough peak intensity to the end of a smile. Emotion expressions werecoded using EMFACS (Ekman & Friesen, 1983).

Arm-restraint procedure. To elicit distress or anger, an arm-restraintprocedure (Provost & Gouin-Decarie, 1979) was used. The mothergently held down her infant's arms for up to 2 min while the infant satin an infant seat across from her. The mother was instructed to maintaina blank, neutral face and to refrain from interacting with her infantduring this segment. If the infant began to cry during the arm-restraintprocedure, the mother was cued to release her infant's arms after 20 sof distress. During the next minute, the mother maintained a neutralcomposure and did not attempt to soothe her infant. If the infant re-mained distressed after 1 min, the mother was instructed to begin sooth-ing her infant. Videotaping of this procedure was done through a one-way mirror.

The following measures were coded from the arm-restraint proce-dure: latency to respond to arm restraint, frequency of facial expres-sions of emotion, and intensity of facial expressions of emotion. Thelater two measures were obtained with EMFACS (Ekman & Friesen,1983).

Quantification of Data

Heart rate. The EKG tapes were quantified off-line. The R-R intervalwas timed to the nearest millisecond, and the interbeat intervals wereorganized into a heart period data file using a level detector and PDP11/23 computer. The heart period data were edited for artifact, and themean heart period (mean of the timed interbeat intervals) and Porges'svagal tone statistic, V, were computed.

To compute the V measure, the heart period data was statisticallyfiltered with a 21-point moving polynomial to remove complex trendsassociated with nonstationarity. The residual data were band pass fil-tered to extract the variability in heart period in the frequency bandassociated with breathing (0.3 to 1.3 Hz for newborns, 0.24 to 1.04 Hzfor 5-month-olds). The V statistic was derived by taking the natural log-arithm of this variance (Porges, 1985).

EMFACS. The EMFACS (Ekman & Friesen, 1983) is an anatomicallybased facial coding system designed to score affect-related facial activ-ity. On the basis of the microanalytic system FACS (Ekman & Friesen,1978), EMFACS identifies those facial configurations that in combina-tion represent certain emotions. For example, an anger expression in-volves the lowering and drawing together of the brows (Action Unit 4),the narrowing of the eyes (Action Unit 7), and the raising of the upperlip (Action Unit 10). Because of the excess of fatty tissue on an infantsface, FACS has been adapted for use with infants (Oster & Rosenstein,1982).

The EMFACS may also be used for the coding of the duration andintensity of an emotion. Duration is coded by noting the beginning andend of an emotion expression. Intensity is coded on a 5-point scale.

In the present study, reliabilities were calculated for the emotiontranslations, the duration of each emotion expression, and the intensityof facial action units using Pearson correlations. Reliabilities for thetwo EMFACS coders ranged from .60 to .80 for these three parameters.Conferences between the coders and the experimenter resolved any dis-crepancies. (Both coders and the experimenter have been tested reliableon FACS prior to the coding of the expressivity data.)

Summary variables. Summary variables representing the dimen-sions of positive reactivity and negative reactivity were created from the

5-month data. Because the variables included in the summary scorewere scaled differently, z scores were computed for each variable andthen summed. The positive reactivity variable was composed of themeasures of frequency, duration, and intensity of smiles coded fromboth peek-a-boo procedures and the arm-restraint procedure. Themean positive reactivity z score was -0.2 (SD = 8.10).

The summary variable representing negative reactivity was createdfrom the frequency and intensity measures of negative affect, anger, anddisgust expressions displayed during arm restraint, as well as from thelatency to cry measure. The frequency of negative expressions of emo-tion displayed during the peek-a-boo procedures was also included. Themean negative summary z score was 0.01 (SD = 4.15). The correlationbetween the two summary variables was nonsignificant.

Results

Our data analytic strategy was first to examine within-agecorrelations between the autonomic and behavioral variables.Because of the dichotomous pattern of response that we foundat both the newborn and 5-month assessments on measures de-signed to tap reactivity (pacifier withdrawal and arm restraint),we grouped subjects by their cry response and reanalyzed theautonomic and mother-rated temperament variables. We alsocomputed within-group correlations to examine individualdifferences among infants who reacted to a procedure. Finally,we examined the stability of reactivity using the behavioralmeasures.

Newborn Autonomic Activity and Behavior

An average of 12.6 min (SD - 6.2 min) of newborn EKG wasrecorded while the infant was in an active sleep state.2 Of the 88newborns tested, 74 had EKG data free of movement artifact.Table 1 presents the means and standard deviations for heartperiod and vagal tone (V) computed from the EKG data duringactive sleep. The correlation between mean heart period and V,r(74) = .56, was significant at the .001 level.

Of the 82 newborns who participated in the pacifier-with-drawal task, 44 cried during at least one trial. The mean latencyto cry was 23.5 s (SD = 15.2 s). On average, infants exhibited12 cries (SD = 12.1). The mean soothing time for newborn cri-ers was 97.7 s (SD = 36.7 s).

Because only 44 of the subjects responded with a cry to paci-fier withdrawal, the three cry measures were normalized usinga square root transformation. Correlations between these trans-formed variables and the EKG measures were computed. Therewere no significant relations. Group differences were testedwith cry reaction (cry or no cry) as the independent variableand heart period and vagal tone as the dependent measures.Again, no significant differences were found.

5-Month Data

Autonomic activity. A total of 54 infants had usable EKGdata free of artifact. Table 1 presents the means and standard

2 Of the 74 newborns with heart rate data during active sleep, electro-cardiogram during quiet sleep was available on 41 newborn subjects.Correlations between heart period (HP) and vagal tone (V) recordedduring active sleep and HP and V recorded during quiet sleep revealedstrong positive associations, HP = r(39) = .82; V = r(39) = .91.

INFANT REACTIVITY 585

Table 1Means and Standard Deviations for Autonomic Data for theNewborn (n = 74) and 5-Month Samples (n = 54)

Data

Heart period (ms)Vagal tone (In V)

Newborn

M SD

494.96 38.183.94 0.97

5-month-old

M

421.992.99

SD

30.630.88

Note. In = natural logarithm.

deviations for the autonomic measures of heart period and va-gal tone. As with the newborn data, correlations between thesevariables revealed a strong positive relationship, r(54) = .67,p < .001. Analyses of variance (ANOVAS) with heart period andvagal tone as the dependent factors and sex and feeding methodas the independent factors revealed a significant effect for feed-ing, F\ 1,50) = 4.29, p < .05. Infants who were being breast-fedat 5 months of age exhibited greater heart period (slower heartrate; M = 414.49, SD = 28.11).

Five-month temperament. The IBQ data yielded six sub-scales: Activity Level (Af = 3.95, SD = .97), Duration of Orien-tation (M = 4.25, SD = .10), Smiling/Laughter (M = 4.88,SD = .87), Distress to Limitations (M = 2.99, SD = .69), Dis-tress and Latency to Approach the Novel (M = 2.07, SD = .69),and Soothability (M = 4.99, SD = .81). Intercorrelationsamong these subscales produced several significant relations(see Table 2). Infants who were rated by their mothers as easilysoothed were also rated as displaying more smiling behavior andlonger durations of looking. Infants who were rated as beingmore fearful (latency to approach novel persons and objects)were also rated as being more frustrated (distress to limitations)and active than were infants rated as less fearful.

Relations among the 5-month variables. To investigate therelation between the 5-month autonomic measures and positiveand negative reactivity, Pearson correlations were computed. Ascan be seen in Table 3, a positive relation emerged between Vand negative reactivity, r(52) = .28, p < .05. Infants who exhib-ited higher vagal tone exhibited greater negative reactivity thandid infants with lower vagal tone.

Table 2Intercorrelations Among the Mother-RatedTemperament Variables (n = 58)

Variable

1. Activity level2. Duration of

orientation3. Smiling and

laughter4. Soothability5. Distress to

limitations6. Latency to

approachnovel

1 2

— -.01

3

.20

.47**

4

-.07

.43 **

.32**

5

.34**

.14

.13

.03

6

.23*

.18

.04- .11

.23*

Table 3Intercorrelations Among the 5-Month Autonomicand Behavioral Measures

Autonomic measures Reactivity

Measure

Reactivity (n -• 54)PositiveNegative

Heart period

-.04.10

Mother-rated temperament

Activity levelDistressLatency/novelOrientationSmile/laughSoothability

.12-.04

.04-.02-.30*-.18

Note. V = vagal tone statistic.•p<.05.

V

.10

.28*

.25*

.12-.04-.11-.27*-.19

Positive

-.17-.02

.15-.15

.08

.28*

Negative

-.03

-.04-.02-.22*

.04- .11- .23*

The relation between 5-month autonomic activity and moth-er-rated temperament was also tested. Table 3 presents thesedata. A significant negative correlation between both heart pe-riod and V and the IBQ subscale Smiling/Laughter was found.Infants with greater heart period and vagal tone were rated bytheir mothers as exhibiting less smiling and laughter. Infantswith higher vagal tone were also rated by their mothers as moreactive.

To test the association between mother-rated temperamentand the summary variables of positive and negative reactivity,Pearson correlations were computed. As can be seen in Table3, infants who exhibited greater negative reactivity in the labo-ratory were rated by their mothers as being less fearful. Infantswho exhibited more positive reactivity in the lab were rated bytheir mothers as more easily soothed, whereas infants who dis-played more negative reactivity were rated as less able to besoothed.

The convergent validity for laboratory measures of reactivitywith mother-rated measures of temperament was further sup-ported when the infants were grouped by their cry response (i.e.,cried or did not cry in response to arm restraint).3 Of the 62infants who participated in the arm-restraint procedure, 27cried. The ANOVAS computed on positive reactivity and the sixtemperament dimensions revealed only one significant finding,a main effect for mother-rated soothability, F{1,53) = 3.77, p <.05. Infants who cried in response to arm restraint were ratedas more difficult to soothe (M = 4.75, SD = 0.83) than wereinfants who did not cry (M = 5.17, SD = 0.77).

The ANOVAS were computed to test for differences in heartperiod and V between 5-month criers and noncriers, and a trendwas found for \,F{1,45) = 3.52, p < .07. Criers tended to ex-

*p<.05. **/?<.01.

3 Although the majority of infants who exhibited negative emotionexpressions during arm restraint cried, 56% of the infants who did notcry in response to arm restraint exhibited high incidences of negativeaffect. Infants who did not cry during arm restraint were coded as exhib-iting more disgust and contempt expressions than did infants who criedin response to arm restraint. These data are available from the first au-thor (Stifter, 1988).

586 CYNTHIA A. STIFTER AND NATHAN A. FOX

hibit higher vagal tone (Af = 3.24, SD = 0.94) than did noncri-ers (A/= 2.76, SZ> = 0.82).

Predictions to 5-Month Autonomic Activity and Behavior

A total of 47 infants had usable EKG data at birth and at 5months. The relation between newborn and 5-month auto-nomic activity was tested using Pearson correlations and wasfound to be nonsignificant for both heart period, r(45) = .01,p < .5, and V, r(45) = -.07, p < .3. As can be seen in Table1, both heart period and vagal tone decreased from birth to 5months. This difference was significant for both measures, heartperiod, *(46) = 10.3, p < .01; and V, t(46) = 4.03, p < .01.

The relation between newborn autonomic activity and 5-month reactivity as measured in the laboratory and rated bymothers was tested using Pearson correlations. The only sig-nificant relations to emerge were between V and the tempera-ment dimensions of distress to limitations, r(46) = .28, p < .05,and latency to approach the novel, r(46) = .32, p < .05. New-borns who exhibited greater vagal tone were rated by theirmothers at 5 months of age as being more easily frustrated andfearful.

To examine the relation between newborn behavioral reactiv-ity and 5-month behavior, ANOVAS were performed on the 5-month reactivity and temperament dimensions with newborncry reaction as the independent factor. Neonatal reaction to thewithdrawal of the pacifier was not related to either positive ornegative reactivity. Only mother-rated activity level was foundto be related to newborn cry behavior, F(l, 53) = 6.43, p < .01.Newborns who cried in response to pacifier removal were ratedby their mothers at 5 months of age as more active (M = 4.29,SD = 0.96) than were newborns who did not cry (M = 3.64,SD = 0.92).

Of the 44 newborns who cried and the 38 newborns who didnot cry to the removal of the pacifier, 30 criers and 29 noncriersparticipated in the 5-month follow-up. Cry behavior was stablefrom birth to 5 months. Of the newborn criers, more than onehalf (16) cried to arm restraint at 5 months, whereas 72% (21)of the noncriers did not cry to arm restraint, x2O, N = 59) =4.05, p<. 05.

To further investigate whether infants who showed stabilityof crying over the 5-month period were different on laboratoryand mother-rated temperament, ANOVAS were performed withpositive reactivity and maternal reports of temperament as thedependent measures and infant cry group at both ages as theindependent factor (cry both times or no cry both times). Asignificant effect was found for mother ratings of distress to lim-itations, F\\, 32) = 5.63, p < .05, and soothability, F{\, 32) =4.22, p < .05. Infants who cried in response to pacifier with-drawal at the newborn period and to arm restraint at 5 monthswere rated by their mothers as more easily frustrated (M = 3.17,SD = 0.65) and more difficult to soothe (M = 4.64, SD = 0.86)than infants who did not cry at both ages (distress, M = 2.55,SD = 0.74; soothability, M = 5.32, SD = 0.75).

Discussion

The four goals of this study were (a) to examine the relationbetween vagal tone and reactivity at both the newborn and 5-month period, (b) to determine if level of newborn vagal tone

predicted 5-month behavioral reactivity, (c) to examine if infantreactivity was stable over the 5-month study period, and (d) toexamine relations between parent report and laboratory mea-sures of infant temperament. With regard to the first goal, thedata from this study suggest that infants with high vagal tone at5 months of age are more reactive to mildly frustrating eventsthan are infants with low vagal tone. Infants with high vagaltone displayed more negative affect emotion expressions duringthe arm-restraint procedure compared with those with low va-gal tone. These infants were also rated as displaying less positiveaffect and as being more active. The infants who displayed nega-tive reactivity during the arm-restraint procedure were alsorated as being less fearful of novel objects and were rated as lesseasily soothed upon distress. The picture, then, that emergesfrom these data is of a group of infants with high vagal tone whodisplay negative reactions when frustrated but are highly activeand not fearful of novelty.

Vagal tone is a measure of the degree of neural influence onthe heart. The variability in heart rate due to respiration hasbeen called respiratory sinus arrhythmia and is known to bemediated by the action of the vagus nerve at the sinoatrial nodeof the heart. The neurotransmitter involved at this site is acety-choline. Changes in the tonus of the vagus may reflect changesin peripheral and central cholinergic balance. These differencesin cholinergic activity may be related to the motor arousal sys-tem, a system that responds with orienting, attention, and ap-proach behaviors to novel stimuli (Porges, 1976).

The relations between cognitive and emotional behaviors andinfant tonic vagal tone have now been examined in a numberof independent studies. These data reveal that infants with highvagal tone display better performance on the Fagan visual dis-crimination task (Linnemeyer & Porges, 1986), exhibit greatersustained attention to visual stimuli (Richards, 1987), show agreater frequency of emotion expression to novel events (Stifteret al., 1989), and display more positive developmental outcomescompared with infants with low vagal tone (Fox & Porges,1985). The common behavioral dimension across these studiesis the infant's reactive response to novelty. Thus, vagal tone maybe a good index of individual differences in infant reactivityduring the first year of life.

The relation between high vagal tone and negative reactivitymight, at first glance, seem in contrast to the data on behavioralinhibition in young children. Kagan et al. (1987) have reportedthat infants with fast and stable heart rates (and presumablywith low vagal tone) were more shy and fearful. However, thestimulus situations used in these studies may be tapping differ-ent dimensions of reactivity. The arm-restraint procedure hasbeen used to elicit anger in infants (Provost & Gouin-Decarie,1979). The emotion of anger, according to several theorists,functions to motivate the infant to remove barriers that blockor interrupt ongoing behavior (Sroufe, 1979) or that preventthe attainment of a desirable goal (Darwin, 1872; Izard, 1977).Bowlby (1973) proposed that anger or protest upon separationfrom the attachment object functions to assist in overcomingobstacles to reunion. In the present study, the predominantaffect expression was that of anger. Thus, the negative reactivityexpressed by the infants in the current study was appropriateto the frustrating and anger-producing situation. The negativeresponses observed during paradigms used by Kagan and col-leagues (Garcia-Coll et al., 1984; Kagan etal., 1984,1987; Rez-

INFANT REACTIVITY 587

nick et al., 1986) are designed to elicit social withdrawal, fear,or anxiety. This reactive response is quite different from the typedescribed in the current work. Indeed, reactivity to frustrationand negative responses to novel social events appear to be unre-lated. The negative relation between our measure of negativereactivity in the laboratory, which did not include fear, and ma-ternal ratings of fearfulness support this notion.

Another important difference between the present study andKagan et al.'s (1984,1987) data involves the age groups studiedand the measurement of heart rate variability. Kagan's longitu-dinal study began with a group of 22-month-old infants thathe followed through 7 years of age. The current study followedinfants from birth to S months of age. In addition, Kagan usedthe standard deviation of heart period as a measure of heartrate variability, whereas our measure was a quantification ofthe amplitude of RSA. Nevertheless, the current study indicatesthat negative reactivity exhibited in the laboratory is associatedwith high parasympathetic tone and not sympathetic arousal.

Newborn vagal tone was not predictive of 5-month behav-ioral reactivity. Indeed, the correlation between newborn and 5-month autonomic measures was negligible. Although it is possi-ble that the lack of relation may be the result of differences ininfant state during recording (active sleep at newborn and quietalert at 5 months), it is more likely that they reflect maturationalchanges in parasympathetic control that occur during this pe-riod (Harper, Hoppenbrouwers, Sterman, McGinty, & Hodg-man, 1976; Lewis, Wilson, Ban, & Baumel, 1970; Schechtman,Harper, & Kluge, 1989). There are data that indicate an in-crease in mylenation of the vagus nerve during the first year oflife (Sachis, Armstrong, & Becker, 1982). This is supported byKagan et al.'s (1987) finding of moderate stability in heart rateand heart rate variability beginning at 2 years of age. Finally, itmay be that by recording EKG within 2 days after birth, a timeof great physiological instability, we were measuring the effectsof the birth process and not an individual characteristic.

Our finding of a decrease in vagal tone is also in contrast toseveral studies that have found an increase in measures of vari-ability within the first few months of life (Harper et al., 1978;Richards & Cameron, 1989). For example, Richards (1987)found a modest increase in RSA in early infancy, but this periodwas limited to a 14- to 26-week age range and did not includenewborn measures. Again, the timing of measurement mayhave contributed to these differences.

Newborn infant reactivity was stable across the 5-month pe-riod. Infants who cried to pacifier withdrawal were more likelyto cry to arm restraint, and those who did not respond duringthe newborn period did not cry at 5 months. There are now anumber of studies in the literature that describe stable patternsof infant reactivity during the 1st year (Birnsetal., 1969; Woro-bey & Lewis, 1988). And there are data that indicate that infantreactivity—specifically, infant crying and irritability—is pre-dictive of social interaction during the 2nd and 3rd years of life(Bates, 1986; Riese, 1987; Yang & Halverston, 1976). The lackof stability in vagal tone and the moderate stability in reactivityacross the first 5 months of life underscore the necessity of usingbehavior as the primary anchor for studying temperament, par-ticularly within the first 6 months of life. They also indicate thatno single physiological measure reflects temperamental differ-ences early in the 1st year.

References

Anders, T., Emde, R., & Parmelee, A. (1971). A manual of standardizedterminology, techniques, and criteria for scoring of states of sleep andwakefulness in newborn infants. Los Angeles: BRI Publications.

Bates, J. E. (1986). On the relation between temperament and behav-ioral problems. In G. A. Kohnstaman (Ed.), Temperament discussed(pp. 181 -189). Berwyn, PA: Swets North America.

Bell, R. Q., Weller, G. M., & Waldrop, M. F. (1971). Newborn and pre-school: Organization of behavior and relations between periods.Monographs of the Society for Research in Child Development, 36(Serial No. 142).

Birns, B. (1965). Individual differences in human neonate's responsesto stimulation. Child Development, 36, 249.

Birns, B., Barten, S., & Bridger, W. H. (1969). Individual differences intemperamental characteristics of infants. Transactions of the NewYork Academy of Sciences, 31, 1071-1082.

Bowlby, J. (1973). Separation: Anxiety and anger. New 'Vbrk: BasicBooks.

Buss, D. M., Block, J. H., & Block, J. (1980). Preschool activity level:Personality correlates and developmental implications. Child Devel-opment, 51, 401-408.

Buss, A. H., & Plomin, R. (1984). Temperament: Early developing per-sonality traits. Hillsdale, NJ: Erlbaum.

Darwin, C. (1872). The expression of the emotions in man and animals.London: John Murray.

Davidson, R. J., & Fox, N. A. (1989). Frontal brain assymetry predictsinfant responses. Journal of Abnormal Psychology, 98, 127-131.

DiPietro, J. A., Larson, S. K., & Porges, S. W. (1987). Behavioral andheart rate pattern differences between breast- and bottle-fed neo-nates. Developmental Psychology, 23,467-474.

Ekman, P., & Friesen, W. V. (1978). Facial Action Coding System. PaloAlto, CA: Consulting Psychologists Press.

Ekman, P., & Friesen, W. V. (1983). EMFACS facial coding manual. SanFrancisco, CA.

Eppinger, H., & Hess, L. (1910). Vagotonia: A clinical study in vegeta-tive neurology. Journal of Nervous and Mental Disease, 20, 1-93.

Fox, N. A. (1989). Psychophysiological correlates of emotional reactiv-ity during the first year of life. Developmental Psychology, 25, 364-372.

Fox, N. A., & Davidson, R. (1986). Psychophysiological measures ofemotion: New directions in developmental research. In C. E. Izard(Ed.), Measuring emotions in infants and children (Vol. 2, pp. 13-47).Cambridge, England: University of Cambridge Press.

Fox, N. A., & Field, T. M. (1989). Individual differences in young chil-dren's adjustment to preschool. Journal of Applied DevelopmentalPsychology, 10, 527-540.

Fox, N. A., & Porges, S. W. (1985). The relation between neonatal heartperiod patterns and developmental outcome. Child Development, 56,28-37.

Garcia-Coll, C, Kagan, J., & Reznick, J. S. (1984). Behavioral inhibi-tion in young children. Child Development, 55, 1005-1019.

Gunnar, M., Isensee, J., & Fust, L. S. (1987). Adrenocortical activityand the Brazelton Neonatal Assessment Scale: Moderating effects ofthe newborn'sbiomedical status. Child Development, 58,1448-1458.

Harper, R. M., Hoppenbrouwers, T, Sterman, M. B., McGinty, D. J.,& Hodgman, J. (1976). Polygraphic studies of normal infants duringthe first 6 months of life: 1. Heart rate and variability as a functionof state. Pediatric Research, 10, 945-951.

Harper, R. M., Walter, D. Q, Leake, B., Hoffman, H. J., Sieck, G. C,Sterman, M. B., Hoppenbrouwers, T., & Hodgman, H. (1978). Devel-opment of sinus arrhythmia during sleeping and waking states in nor-mal infants. Sleep, 1, 33-48.

Hubert, N. C, Wachs, T. D., Peters-Martin, P., & Gandour, M. J. (1982).The study of early temperament: Measurement and conceptual is-sues. Child Development, 53, 571-600.

588 CYNTHIA A. STIFTER AND NATHAN A. FOX

Izard, C. E. (1977). Human emotions. New York: Plenum Press.Kagan, J. (1982). Heart rate and heart rate variability as signs of a tem-

peramental dimension in infancy. In C. E. Izard (Ed.), Measuringemotions in infants and children (pp. 38-66). Cambridge, England:Cambridge University Press.

Kagan, J., Reznick, J. S., Clarke, C , Snidman, N., & Garcia-Coll, C.(1984). Behavioral inhibition to the unfamiliar. Child Development,55,2212-2225.

Kagan, J., Reznick, J. S., & Snidman, N. (1987). The physiology andpsychology of behavioral inhibition in children. Child Development,58, 1459-1473.

Korner, A. F., Hutchinson, C. A., Koperski, J., Kraemer, H. C , &Schneider, P. (1981). Stability of individual differences of neonatalmotor and crying patterns. Child Development, 52, 83-90.

Korner, A. F., Zeanah, C. H., Linden, J., Berkowitz, R. I., Kraemer,H. C , & Agras, W. S. (1985). The relation between neonatal and lateractivity and temperament. Child Development, 56, 38-42.

Lacey, J. I., & Lacey, B. C. (1958). The relationship of resting autonomicactivity to motor impulsivity. Research Publications Association forResearch in Nervous and Mental Disease, 36,144-209.

Lewis, M., Wilson, C. D., Ban, P., & Baumel, M. H. (1970). An explor-atory study of resting cardiac rate and variability from the last trimes-ter of prenatal life through the first year of postnatal life. Child Devel-opment, 4 7,799-812.

Linnemeyer, S. A., & Porges, S. W. (1986). Recognition memory andcardiac vagal tone in 6-month-old infants. Infant Behavior and Devel-opment, 9, 43-56.

McCabe, P. M , Yongue, B. G., Porges, S. W., & Ackles, P. K. (1984).Changes in heart period, heart period variability and a spectral analy-sis estimate of respiratory sinus arrhythmia during aortic nerve stim-ulation in rabbits. Psychophysiology, 21, 149-158.

McGrade, B. J. (1968). Newborn activity and emotional response ateight months. Child Development, 39, 1247-1252.

Oster, H., & Rosenstein, D. (1982). Analyzing facial movement in in-fants. Unpublished manuscript.

Porges, S. W. (1976). Peripheral and neurochemical parallels of psycho-pathology: A psychophysiological model relating autonomic imbal-ance to hyperactivity, psychopathy, and autism. In H. W. Reese (Ed.),Advances in child development and behavior (Vol. 2, pp. 35-65). NewYork: Academic Press.

Porges, S. W. (1985). Method and apparatus for evaluating rhythmic os-cillations in aperiodic physiological response systems. Patent No.4,510,944.

Porges, S. W. (1986). Respiratory sinus arrhythmia: Physiological basis,quantitative methods, and clinical implications. In P. Grossman, K.Janssen, & D. Vaitl (Eds.), Cardiac respiratory and somatic psycho-physiology (pp. 206-211). New York: Guilford Press.

Porges, S. W., McCabe, P. M., & Yongue, B. G. (1982). Respiratory-heart rate interactions: Physiological implications for pathophysiol-ogy and behavior. In J. Cacioppo & R. Petty (Eds.), Perspectives incardiovascular psychophysiology (pp. 223-264). New York: GuilfordPress.

Provost, M. A., & Gouin-Decarie, T. (1979). Heart rate reactivity of9- and 12-month-old infants showing specific emotions in a naturalsetting. International Journal of Behavioral Development, 2, 109-120.

Reznick, J. S., Kagan, J., Snidman, N., Gersten, M., Baak, K., & Rosen-berg, A. (1986). Inhibited and uninhibited children: A follow-upstudy. Child Development, 57, 660-680.

Richards, J. E. (1987). Infant visual sustained attention and respiratorysinus arrhythmia. Child Development, 58, 488-496.

Richards, J. E., & Cameron, D. (1989). Infant heart rate variability and

behavioral developmental status. Infant Behavior and Development,12, 45-58.

Riese, M. L. (1987). Temperament stability between the neonatal pe-riod and 23 months. Developmental Psychology, 23,216-222.

Rothbart, M. K. (1981). Measurement of temperament in infancy.Child Development, 52, 569-578.

Rothbart, M. K. (1986). Longitudinal observation of infant tempera-ment. Developmental Psychology, 22, 356-365.

Rothbart, M. K., & Derryberry, D. (1981). Development of individualdifferences in temperament. In M. E. Lamb & A. L. Brown (Eds.),Advances in developmental psychology(Vol. 1, pp. 37-86). Hillsdale,NJ: Erlbaum.

Sachis, P. N.r Armstrong, D. L., & Becker, L. E. (1982). Myelinationof the human vagus nerve from 24 weeks post-conceptional age toadolescence. Journal ofNeuropathology and Experimental Neurology,41, 466-472.

Schechtman, V. L., Harper, R. M., & Kluge, K. A. (1989). Developmentof heart rate variation over the first 6 months of life in normal infants.Pediatric Research, 26, 343-346.

Spangler, G., Meindl, E., & Grossmann, K. (1988, April). Behavioralorganization and adrenocortical activity in newborns. Paper pre-sented at the International Conference on Infant Studies, Washing-ton, DC.

Sroufe, L. A. (1979). Socioemotional development. In J. Osofsky (Ed.),Handbook of infant development (pp. 462-516). New York: Wiley.

Sroufe, L. A., & Waters, E. (1976). The ontogenesis of smiling andlaughter: A perspective on the organization of development in in-fancy. Psychological Review, 83, 173-189.

Stifter, C. A. (1988, April). Negative expressivity in five-month-old in-fants. Paper presented at the International Conference on InfantStudies, Washington, DC.

Stifter, C. A., Fox, N. A., & Porges, S. W. (1989). Facial expressivity andvagal tone in five- and ten-month-old infants. Infant Behavior andDevelopment, 12, 127-137.

Thomas, A., & Chess, S. (1977). Temperament and development. NewYork: Brunner/Mazel.

Thomas, A., Chess, S., Birch, H. G., Hertzig, M. E., & Korn, S. (1963).Behavioral individuality in early childhood. New York: New YorkUniversity Press.

Wenger, M. A. (1941). The measurement of individual differences inautonomic balance. Psychosomatic Medicine, 3, 427-434.

Wenger, M. A., & Cullen, T. D. (1972). Studies in autonomic balancein children and adults. In N. S. Greenfield & R. A. Sternbach (Eds.),Handbook of psychophysiology (pp. 535-569). New York: Holt, Rine-hart & Winston.

Wilson, R. S. (1982). Intrinsic determinants of temperament. In M.Rutter (Ed.), Temperamental differences in infants and young chil-dren (pp. 121-140). London: Pittman.

Wilson, R. S., & Matheney, A. P. (1983). Assessment of temperamentin infant twins. Developmental Psychology, 19, 172-183.

Worobey, J., & Lewis, M. (1988). Individual differences in the reactivityof young infants. Unpublished manuscript.

Yang, R. K., & Halverston, C. F. (1976). A study of the "inversion ofintensity" between newborn and preschool-age behavior. Child De-velopment, 47, 350-359.

Yongue, B. G., McCabe, P. M., Porges, S. W, Rivera, M., Kelley, S. L.,& Ackles, P. K. (1982). The effects of pharmacological manipulationsthat influence vagal control of the heart on heart period, heart-periodvariability, and respiration in rats. Psychophysiology, 19,426-432.

Received April 5,1988Revision received June 15,1989

Accepted July 17,1989 •