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Articles Autonomic and brain electrical activity in securely- and insecurely-attached infants of depressed mothers Geraldine Dawson*, Sharon B. Ashman, David Hessl, Susan Spieker, Karin Frey, Heracles Panagiotides, Lara Embry Department of Psychology and Center on Human Development and Disability, University of Washington, Seattle, WA 98195, USA Received 19 March 2001; revised 9 May 2001; accepted 5 July 2001 Abstract The present study examined the combined influences of maternal depression and attachment security on infants’ brain activity and autonomic activity. Brain electrical activity, heart rate, and vagal tone were recorded from 159 13–15 month old infants of depressed, subthreshold depressed, and nondepressed mothers during a baseline and two social interaction conditions. Attachment behavior was observed during the traditional Strange Situation. It was found that infants of depressed mothers exhibited reduced left relative to right frontal brain activity during all conditions. Moreover, regardless of mother’s depression status, insecurely attached infants exhibited relative reduced left frontal brain activity. Infants of depressed mothers were also found to exhibit higher heart rates across all conditions. These results indicate that both maternal depression and attachment security are associated with alterations in infants’ psychophysiological responses. © 2001 Elsevier Science Inc. All rights reserved. Keywords: Maternal depression; Attachment; Brain activity; Heart rate 1. Introduction Research has demonstrated that maternal depression is a risk factor for the development of emotional and behavior problems in childhood (Downey & Coyne, 1990; Murray & Cooper, 1997; Radke-Yarrow, 1998). Indeed, some of these disturbances are apparent in * Corresponding author. Tel.: 1-206-543-1051; fax: 1-206-543-5771. E-mail address: [email protected] (G. Dawson). Infant Behavior & Development 24 (2001) 135–149 0163-6383/01/$ – see front matter © 2001 Elsevier Science Inc. All rights reserved. PII: S0163-6383(01)00075-3

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Page 1: Autonomic and brain electrical activity in securely- and insecurely-attached infants of depressed mothers

Articles

Autonomic and brain electrical activity in securely- andinsecurely-attached infants of depressed mothers

Geraldine Dawson*, Sharon B. Ashman, David Hessl, Susan Spieker,Karin Frey, Heracles Panagiotides, Lara Embry

Department of Psychology and Center on Human Development and Disability, University of Washington,Seattle, WA 98195, USA

Received 19 March 2001; revised 9 May 2001; accepted 5 July 2001

Abstract

The present study examined the combined influences of maternal depression and attachmentsecurity on infants’ brain activity and autonomic activity. Brain electrical activity, heart rate, and vagaltone were recorded from 159 13–15 month old infants of depressed, subthreshold depressed, andnondepressed mothers during a baseline and two social interaction conditions. Attachment behaviorwas observed during the traditional Strange Situation. It was found that infants of depressed mothersexhibited reduced left relative to right frontal brain activity during all conditions. Moreover, regardlessof mother’s depression status, insecurely attached infants exhibited relative reduced left frontal brainactivity. Infants of depressed mothers were also found to exhibit higher heart rates across allconditions. These results indicate that both maternal depression and attachment security are associatedwith alterations in infants’ psychophysiological responses. © 2001 Elsevier Science Inc. All rightsreserved.

Keywords: Maternal depression; Attachment; Brain activity; Heart rate

1. Introduction

Research has demonstrated that maternal depression is a risk factor for the developmentof emotional and behavior problems in childhood (Downey & Coyne, 1990; Murray &Cooper, 1997; Radke-Yarrow, 1998). Indeed, some of these disturbances are apparent in

* Corresponding author. Tel.: �1-206-543-1051; fax: �1-206-543-5771.E-mail address: [email protected] (G. Dawson).

Infant Behavior & Development 24 (2001) 135–149

0163-6383/01/$ – see front matter © 2001 Elsevier Science Inc. All rights reserved.PII: S0163-6383(01)00075-3

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infancy. Infants of depressed mothers have been found to exhibit poorer mental and motordevelopment, and increased emotion regulation problems (Murray & Cooper, 1997). Duringinteractions with their mothers, infants of depressed mothers tend to display fewer affec-tionate behaviors and positive emotional expressions and more tantrums and negativeexpressions (Dawson et al., 1999; Field, 1995).

Maternal depression is associated with genetic, prenatal, and postnatal risk factors thatmay potentially influence the development of children of depressed mothers (Goodman &Gotlib, 1999; Lundy et al., 1999; Nurnberger, Goldin, & Gershon, 1986; Tsuang & Faraone,1990). In particular, research has focused on disturbed mother-child interactions as onepossible risk factor associated with maternal depression. Some researchers have posited thata depressed mother’s failure to respond contingently to her infant’s emotional signals or toprovide adequate levels of positive affect or stimulation may interfere with infant emotionaldevelopment (Dawson, Panagiotides, Grofer Klinger, & Hill, 1992; Field, 1986; Goodman &Gotlib, 1999). Others have proposed that poorly coordinated mother-infant interactions maylead infants to experience more negative affect. After repeated failures to positively engagetheir mothers, these infants may withdraw and use less mature, self-directed regulatorystrategies to cope with negative emotions (Tronick & Gianino, 1986).

Several studies have provided evidence to support these hypotheses by demonstrating howmaternal depression can disrupt mother-infant interactions. Studies have documented twodistinct ways in which depressed mothers tend to interact with their infants, characterized bywithdrawn versus intrusive and controlling maternal behavior (Cohn, Matias, Tronick,Connell, & Lyons-Ruth, 1986). During face-to-face interactions with their infants, depressedmothers who display a withdrawn style of interacting express less positive and more negativeaffect, talk less, and disengage more than nondepressed mothers (Cohn & Tronick, 1989;Cohn et al., 1986; Field, 1986; Field et al., 1988; Field, 1995). Intrusive depressed motherstend to overstimulate their infants by poking, restraining, directing their infant’s attention, oraggressively introducing or withdrawing a toy (Cohn et al., 1986; Hart, Field, del Valle, &Pelaez-Nogueras, 1998; Jones et al., 1997). Finally, researchers have found that, comparedto nondepressed mothers, depressed mothers are generally less sensitively attuned to theirinfants’ cries (Donovan, Leavitt, & Walsh, 1998).

It is well established that sensitive and responsive caretaking is important for the devel-opment of a secure attachment relationship (Teti & Nakagawa, 1990). Given the character-istics of a depressed mother’s interactions with her infant described above, one might expectinfants of depressed mothers to be more vulnerable to developing insecure attachmentrelationships. Several studies have supported this hypothesis (Lyons-Ruth, Connell, Grune-baum, & Botein, 1990; Radke-Yarrow, Cummings, Kuczynski, & Chapman, 1985; Rosen-blum, Mazet, & Benony, 1997; Teti, Gelfand, Messinger, & Isabella, 1995). Rosenblum etal. (1997) reported that specific subtypes of maternal depression are associated with differenttypes of insecure attachment. Specifically, irritable/stressed depression was found to beassociated with insecure-ambivalent attachment, and dull/slow depression was associatedwith insecure-avoidant attachment. Rosenblum et al. (1997) suggested that infants of dull/slow depressed mothers develop insecure-avoidant attachments as a self-regulatory strategyin response to the withdrawn behaviors of their mothers.

Maternal depression is not invariably associated with insecure attachment, however. In

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one study, DeMulder & Radke-Yarrow (1991) reported rates of insecure attachment inchildren of unipolar depressed mothers equivalent to children of healthy mothers. Infants aremost likely to develop insecure attachments when the mother’s affective disorder is severeand/or chronic (Teti et al., 1995), bipolar (Radke-Yarrow et al., 1995; DeMulder & Radke-Yarrow, 1991), or combined with other risk factors, such as low socioeconomic status (SES)or marital dissatisfaction (Lyons-Ruth et al., 1990; Shaw & Vondra, 1993). In a recentmeta-analysis, Martins & Gaffan (2000) found that, even within a set of studies selected tominimize confounding factors, such as poverty and family discord, the effects of maternaldepression on attachment were diverse. Thus, the relation between maternal depression andinfant attachment security is likely complex. Maternal depression is likely to be one ofseveral risk factors that collectively contribute to the development of insecure attachment.

In the present study, we were concerned with how maternal depression affects not onlyinfant attachment behaviors, but also the physiological responses that may be directly orindirectly related to both maternal depression and attachment status. Researchers, for exam-ple, have documented associations between attachment classification and stress responses ininfancy. Spangler & Grossman (1993) reported that, during the Strange Situation, infantheart rate increased during maternal separation regardless of attachment classification. Onlyinsecurely attached infants exhibited an elevated salivary cortisol response to the StrangeSituation, however. They have suggested that the heightened stress response observed ininsecurely attached infants reflects the lack of an appropriate coping strategy. Izard et al.(1991) found a positive relation between increased heart-rate variability (vagal tone) andgreater likelihood of attachment insecurity. In addition, research has found that securelyattached infants exhibit heart rate deceleration in response to the stranger’s entrance duringthe Strange Situation, while insecurely attached infants fail to have a consistent pattern ofautonomic responding to such an episode (Donovan & Leavitt, 1985).

Altered autonomic reactivity has also been found in infants of depressed mothers. Fieldand colleagues (Field et al., 1988) examined infant autonomic activity and stress hormonelevels during mother-infant interactions. They reported that infants of depressed mothers hadhigher heart rate, lower vagal tone, and higher stress hormone levels than infants ofnondepressed mothers, suggesting that infants of depressed mothers experienced socialinteractions with their mothers as stressful.

In the present study, we were interested in both infant frontal brain activity and infantautonomic responses as psychobiological indicators of risk for psychopathology in childrenof depressed mothers. For decades, researchers have recognized the central role of theprefrontal cortex in the expression and regulation of emotion (LeDoux, 1987; Luria, 1966;Nauta, 1971). Electroencephalographic (EEG) studies have demonstrated that the left andright frontal regions differentially mediate different types of emotion expression (Davidson& Fox, 1988, 1989; Dawson, Panagiotides et al., 1992). In both adults and infants, relativeleft frontal activation has been found to be associated with “approach” emotions, such as joyand interest, and relative right frontal activation has been found to be associated with“withdrawal” emotions, such as sadness and distress (Davidson & Fox, 1988, 1989; Dawson,Panagiotides et al., 1992). Furthermore, research has indicated that depressed adults exhibitreduced left frontal brain activation (Baxter et al., 1989; Henriques & Davidson, 1990).

In a previous study with this same sample of infants and mothers, Dawson and colleagues

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(Dawson et al., 1999; Dawson, Frey, Panagiotides, Osterling, & Hessl, 1997) reported thatinfants of depressed mothers exhibit atypical patterns of frontal EEG activity. Compared toinfants of nondepressed mothers, infants of depressed mothers showed reduced relative leftfrontal brain activation during a baseline condition, during playful interactions with theirmothers, and during playful interactions with a familiar experimenter. In the present study,we extended this research by examining how the mother-infant attachment relationship mayinform our understanding of the relation between maternal depression and both infant brainactivity and autonomic activity (heart rate and vagal tone). In a previous study of lowincome, depressed teenage mothers, Dawson, Grofer Klinger, Panagiotides, Spieker, & Frey(1992) found that securely attached infants of depressed mothers exhibited significantlyreduced left frontal electroencephalographic (EEG) activity compared to securely attachedinfants of nondepressed mothers. Brain activity did not differ between insecurely attachedinfants of depressed and nondepressed mothers; however, the small sample size for thiscomparison makes conclusions based on these results tentative.

We predicted that infants of depressed mothers would exhibit increased heart rate andlower vagal tone in social interactions, compared to infants of nondepressed mothers. Inaddition, based on previous research associating insecure attachment with less optimalpsychophysiological responses (Donovan & Leavitt, 1985; Izard et al., 1991; Spangler &Grossman, 1993), we predicted that insecurely attached infants would exhibit reduced leftfrontal brain activity and increased heart rate and vagal tone, and that maternal depressionand attachment security may act in an additive fashion in their effects on infants’ physio-logical responding.

2. Method

2.1. Participants

Participants were 159 mothers and their 13–15-month-old infants (Mean infant age �13.92 � 0.51 months; 89 females and 70 males) recruited into a longitudinal study of theeffects of maternal depression on children’s psychophysiological and behavioral develop-ment. This is the same sample of infants and mothers for whom EEG data has already beenreported in previous publication (Dawson et al., 1997; Dawson et al., 1999). Mothers wererecruited from the Psychology Department infant subject pool, newspaper advertisements,and community clinics. Upon entry into the study, mothers were carefully screened and wereexcluded if they reported substance use or abuse, serious medical conditions, attendance inspecial education classes, bipolar disorder, psychosis, immanent suicide, significant preg-nancy or birth complications, and/or contact by Child Protective Services. All infants werefull term (no more than 3 weeks early or late) with no reported history of chronic seizures,central nervous system infection, head injury, prolonged hospitalization, chronic medicalcondition, surgery, physical malformations, sensory or motor problems, prenatal exposure todrugs, foster care, and/or current medications.

The ethnic composition of the mothers in this sample was 85% white, 1% Hispanic, 1%

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Native American, 1% African American, and 2% Multi-Ethnic. Ten percentage of the samplefailed to classify themselves as belonging to an ethnic group.

2.1.1. Diagnostic groupsMothers were classified into diagnostic groups based on information obtained from the

Structured Clinical Interview for the DSM-III-R (SCID; Spitzer, Williams, Gibbon, & First,1989) and the Center for Epidemiologic Studies—Depression Questionnaire (CES-D; Rad-loff, 1977). Of the mothers in this study, 90 received a current diagnosis of depression orsubthreshold depression based on the SCID and/or the CES-D. Twenty-seven of thesemothers were classified as having major depression, and 63 were classified as havingsubthreshold depression. The remaining 69 mothers were classified as nondepressed. Thecriterion for classification as depressed was having either a current diagnosis of MajorDepression (N � 25) or Double Depression (N � 2) on the SCID. Classification assubthreshold depressed was achieved by having a current SCID diagnosis of subthresholddepression (N � 9), dysthymia (N � 2), or depression in partial remission (N � 25), or byhaving a score of 16 or above on the CES-D (N � 27). Participants who were classified asnondepressed had scores lower than 9 on the CES-D and reported no current or lifetimehistory of depression on the SCID.

There were significant differences among the diagnostic groups on three demographicvariables of interest. The likelihood of being married differed among the depression group-ings with the subthreshold depression group having the highest likelihood of being notmarried (19%), followed by the depressed group (15%) and the nondepressed (4%; �2(2) �7.02, p � .03). The number of children in the family also differed slightly among depressiongroupings, with subthreshold mothers having an average of 1.9 (SD � 0.87) children, whichwas significantly higher than the nondepressed group average of 1.54 (SD � 0.78; F(2,156) � 3.26, p � .04, Posthoc Tukey’s HSD) children. Depressed mothers had an averageof 1.78 (SD � 0.89) children. Mother’s age also differed significant among depressiongroupings, with depressed mothers (Mean age � 32.6) being significantly older thannondepressed mothers (Mean age � 29.9; F(2, 156) � 2.99, p � .053). Other demographicvariables did not distinguish the groups, including mother’s ethnicity, pregnancy problems,number of hours the mother spent working outside the home, mother’s or father’s educa-tional level, family SES as assessed by the Hollingshead (1975), biological father’s age,infant age or gender, or number of hours the infant spent in daycare (see Table 1). Maritalstatus, mother’s age, and number of children in family were used as covariates whereappropriate.

2.2. Procedure

2.2.1. Experimental conditions for psychophysiological measuresInfant psychophysiological testing occurred in the Developmental Psychophysiology

Laboratory at the Center for Human Development and Disability at the University ofWashington. The infant was videotaped and infant electrical brain activity (EEG) and heartrate were recorded during 5 different experimental conditions administered in the followingorder: Baseline, mother play, stranger enters, experimenter play, and mother leaves. During

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the baseline condition (1 min), the experimenter stood out of the infant’s view, behind ablack curtain and blew soap bubbles over the curtain. The bubbles were designed to attractand hold the infant’s attention. During the mother play condition, mothers were instructed toplay peek-a-boo with their infants for 1 min. After this activity, a person whom the infant hadnever seen before entered the room, walked slowly toward the infant, sat and stared at theinfant, and then backed out of the room all while maintaining a neutral expression. Thisstranger condition was followed by a 1-min peek-a-boo activity between the infant and afamiliar experimenter. Finally, for the mother leaves condition, mothers stood up, waved andsaid “bye-bye,” and then walked slowly out of the door. Mothers remained outside the roomfor 20 s, than returned to comfort their infants. EEG and heart rate recording ended when themothers were reunited with their infants. During the experimental conditions, infants werevideotaped from a camera hidden behind a curtain in the testing room. Only data from thebaseline and two play conditions are reported in this paper. These conditions were selectedfor three reasons: 1) Previous research has found that infants of depressed mothers haveelevated heart rates during social interactions (Dawson et al., 1994; Field et al., 1988), 2)eliminating the mother leave condition permitted observation of infant psychophysiologyindependent of the attachment relationship, and 3) selecting these conditions maximized thesample size as more infants were missing data during the stranger enter and mother leaveconditions. Of the 140 infants with attachment security ratings (see below), 118 had completeEEG data across the three conditions.

Table 1Demographic characteristics of the sample

Nondepressed(N � 69)

Sub-threshold(N � 63)

Depressed(N � 27)

Statistic

Child CharacteristicsGender

Female (%) 56% 59% 48%Male (%) 44% 41% 52%

Age (months) 13.9 � .4 13.9 � .5 14.0 � .7Time spent in daycare (hrs/wk) 13.3 � 17.1 11.6 � 15.9 9.9 � 17.0

Mother CharacteristicsAge (years) 29.9 � 4.8 30.5 � 4.6 32.6 � 5.3 F (2,156) � 2.99*Education Level 5.3 � .9 5.4 � .9 5.3 � .9Marital Status �2(2) � 7.02*

Married 96% 81% 85%Not married 4% 19% 15%

Time spent working away fromhome (average hrs/wk)

14.8 � 15.9 14.2 � 17.4 9.1 � 15.8

Pregnancy ProblemsNo 41% 44% 30%Yes 59% 56% 70%

Family CharacteristicsSES 43.4 � 9.8 44.1 � 14.1 47.0 � 13.3Father’s education level 5.2 � 1.2 4.6 � 2.3 4.9 � 2.3# of children in family 1.5 � .8 1.9 � .9 1.8 � .9 F (2,156) � 3.26*

Note: *p � .05.

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2.2.2. EEG recording and analysisIn order to prepare the infant for EEG testing, an assistant entertained the infant with toys

while an experimenter used Omni-Prep to abrade the scalp areas before attaching individualsilver-silver chloride electrodes to the scalp with Grass EEG cream. Infant EEG was recordedfrom four scalp locations: left and right frontal and parietal (F3, F4, P3, P4; International10–20 system). EEG leads were referenced to mastoid electrodes, and identical impedanceswere obtained for right and left mastoid using a potentiometer. Additional electrodesincluded a forehead electrode, which served as ground, and EOG electrodes, which wereused for offline removal of ocular artifact. All impedances were under 5 K�.

EEG was recorded using a Grass Neurodata Acquisition System (Model 12). Settings forthe high pass active filter and low pass filter were 1 Hz and 30 Hz, respectively. Analog-to-digital conversion was based on a 512 points/sec sampling rate. Digitized data were storedcontinuously on an IBM PC-AT.

James Long Co. (Caroga Lake, NY) EEGEDIT software was used to inspect and edit EEGdata for motor artifacts, including EOG. The amount of artifact-free EEG data available didnot differ by maternal depression grouping. In order to be included in the analyses, aminimum of 15 s of artifact-free EEG needed to be available. Discrete Fourier analyses wereperformed on artifact-free EEG using software developed by James Long Co. (Caroga Lake,NY). This analysis yielded spectral power in the 3–5, 6–9, and 10–12 Hz bands. Analysesfocused solely on the 6–9 Hz range as previous research (see review by Fox, 1991) has foundthat the 6–9 Hz band is the dominant high-frequency band during infancy and is believed toreflect infant “alpha.” In order to normalize the distributions, EEG spectral power scoreswere natural log transformed. Subsequently, asymmetry scores (ln right EEG power minusln left EEG power) were computed to determine relative activity of homologous right and lefthemisphere regions. Negative asymmetry scores indicate relative right-hemisphere activityand positive asymmetry scores indicate relative left-hemisphere activity.

2.2.3. Heart rate recording and analysisHeart-rate data were obtained by placing two electrodes on the infants, one on the sternum

and a second one on the lower left costal region. The ECG signal was then amplified andfiltered through a high pass filter set at 0.1 Hz. The signal was then digitized through anAnalog to Digital (A/D) converter at 512 samples per second. The digitized data were storedon a hard disk for off-line processing. The timing of the R-waves was extracted using aprogram designed by James Long, Inc. (Caroga Lake, NY). The output of the R-wavedetection was edited and corrected by visual inspection. The corrected records were in turnsegmented by experimental condition and R-to-R-wave intervals were entered into ananalysis program designed by Steve Porges that computed heart rate.

Heart-rate variability (vagal tone) was computed from the ECG record. Interbeat intervals(IBI) between R-waves were algorithmically extracted. The records were then visuallyinspected and corrected for errors. IBI values were then entered into Mxedit for further visualinspection and heart rate variability computation. Mxedit uses the Porges-Bohrer algorithmfor band-pass filtering of IBI data that is based on a moving polynomial to removenonstationarities. Filtering values for children between 0.24 and 1.04 with a polynomialorder of 3 and a coefficient number of 21 were used in each condition analysis.

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2.2.4. Attachment classificationInfant attachment status was assessed based on observations of the infants’ behaviors

during the traditional Strange Situation, which was conducted on a separate day from thepsychophysiological testing. This procedure consists of 8 structured, 3-min episodes duringwhich the infant is videotaped in a laboratory playroom. The episodes include two separa-tions from the mother, once when the mother leaves the infant with a stranger and once whenthe mother leaves the infant alone. Each episode involved changes in the social environmentand was designed to be mildly stressful in order to elicit the infant’s attachment behaviors.Of the original sample of 159 infants 140 completed the attachment paradigm and had theirvideotaped sessions rated. All attachment coding was performed by a coding team led bySusan Spieker at the University of Washington.

Attachment videotapes were coded using the Main and Solomon (1990) classificationscheme. Using the Main classification scheme, infants were coded as demonstrating secure(B) or insecure (A—avoidant, C—resistant, D—disorganized, U—unclassifiable) attach-ment. Using this system, 39% of infants were classified as secure and 61% were classifiedas insecure. Infants also received a D-rating on Main’s 9-point disorganization rating scale,in which 1 means “no signs of disorganization/disorientation” and 9 means “definite qual-ification for D attachment status with indices of disorganization and disorientation that arestrong, frequent, or extreme.” All tapes were double-coded and disagreements were coded byconsensus, as were all cases with D-ratings that disagreed by more than 2 points. Agreementacross coder pairs and across the four A B C D/U categories was 83% (Kappa � 0.70).

3. Results

3.1. Attachment security in infants of depressed and nondepressed mothers

Table 2 displays the percentage of infants in each attachment classification by maternaldepression group. Attachment classification (A,B,C,D/U) did not differ significantly bymaternal depression group (�2 (6) � 7.95, p � .24). However, attachment security (securevs. insecure) significantly differed by maternal depression group (�2 (2) � 6.39, p � .04,2-tailed). Posthoc 2 � 2 chi-squares revealed that infants of mothers with subthresholddepression were more likely to be insecurely attached than infants of mothers with majordepression (�2 (1) � 6.40, p � .015, 2-tailed). Attachment security in infants of nonde-

Table 2Infant attachment classification by history of maternal depression

Category Nondepressed Sub-threshold Depressed Major Depression

A 11 (18%) 7 (13%) 2 (8%)B 24 (39%) 15 (28%) 15 (58%)C 9 (15%) 11 (21%) 3 (11%)D 16 (26%) 13 (25%) 6 (23%)U 1 (2%) 7 (13%) 0

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pressed mothers did not differ significantly from attachment security in infants of depressedmothers, as a whole.

In order to further explore the relation between subthreshold maternal depression andinsecure infant attachment, data were analyzed separately based on mother’s marital status.Previous research has demonstrated that maternal depression is more likely to be associatedwith insecure attachment in the context of other contextual risk factors, such as maritaldissatisfaction (Lyons-Ruth et al., 1990; Shaw & Vondra, 1993). Given that, in this sample,mothers with subthreshold depression were also more likely to be unmarried, separated ordivorced (19% vs. 15% and 4% for depressed and nondepressed mothers respectively),analyses were conducted to determine whether mother’s marital status might be moderatingthe relation between maternal depression and infant attachment security. Results revealedthat infants of mothers with subthreshold depression were more likely to be insecurelyattached only if their mother was also unmarried (�2 (2) � 11.84, p � .003). Among marriedmothers, the likelihood of insecure attachment did not differ among depression groups (�2

(2) � 2.32, p � .31). This difference was not accounted for by the amount of time that themother spent working away from home, as this variable did not differ by attachment security(t(138) � �1.75, p � .08) or mother’s marital status (t(157) � �0.02, p � .98).

3.2. Relations among maternal depression, attachment security, and psychophysiology

3.2.1. Maternal depression, infant attachment security, and EEG activityA 3 (Nondepressed vs. Subthreshold vs. Major depression) x 2 (secure vs. insecure) x 3

(Condition: baseline, experimenter peek-a-boo, and mother peek-a-boo) repeated measuresANOVA with frontal EEG asymmetry scores as the dependent variable revealed significantmain effects of depression group (F(2, 112) � 6.18, p � .003) and attachment security (F(1,112) � 4.58, p � .035), and a trend for a significant depression group by attachment securityinteraction (F(2, 112) � 2.73, p � .07). On average, infants of mothers with majordepression had lower frontal EEG asymmetry scores than infants of subthreshold andnondepressed mothers, and insecurely attached infants had lower frontal EEG asymmetryscores than securely attached infants (see Figs. 1 and 2). When securely and insecurelyattached infants were examined separately, it was revealed that, among insecurely attachedinfants, infants of mothers with major depression had lower frontal EEG asymmetry scoresthan infants of nondepressed or subthreshold depressed mothers (F(2, 68) � 6.23, p � .003;Posthoc Tukey’s HSD). Analyses were conducted with and without covariates and the resultsremained essentially the same. Analyses of the parietal EEG revealed no main effects ofmaternal depression or attachment security.

3.2.2. Maternal depression, infant attachment security, and infant autonomic activityA 3 (Nondepressed vs. Subthreshold vs. Major depression) � 2 (secure vs. insecure) �

3 (Condition: baseline, experimenter peek-a-boo, and mother peek-a-boo) repeated measuresANOVA with infant heart rate (beats/min) as the dependent variable revealed significantmain effects of depression grouping (F(2, 124) � 4.14, p � .018) and condition (F(2, 248) �32.10, p � .001), and a trend for a significant condition by depression group interaction (F(4,248) � 2.14, p � .077). Posthoc Tukey’s HSD tests revealed that, on average, infants of

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mothers with major depression had higher heart rates than infants of mothers with subthresh-old depression or no depression (see Fig. 3). Analyses were conducted with and withoutcovariates and the results remained essentially the same.

A 3 (Nondepressed vs. Subthreshold vs. Major depression) � 2 (secure vs. insecure) �3 (Condition: baseline, experimenter peek-a-boo, and mother peek-a-boo) repeated measuresANOVA with infant vagal tone as the dependent variable revealed a significant main effectof condition (F(2, 250) � 6.83, p � .001). Infants had lower vagal tone during the interactionconditions compared to the baseline condition. Analyses were conducted with and withoutcovariates and the results remained essentially the same.

Recent research suggests that disorganized attachment may be associated with increasedheart rate during separation from mother (Willemsen-Swinkels, Bakermans-Kranenburg,

Fig. 1. Infant frontal EEG asymmetry (ln right minus ln left EEG power) in infants of nondepressed, subthreshold,and depressed mothers.

Fig. 2. Infant frontal EEG asymmetry (ln right minus ln left EEG power) in securely and insecurely attachedinfants.

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Buitelaar, van IJzendoorn, & van Engeland, 2000). A separate analysis of the D categoryrevealed no significant main effects of disorganized attachment classification on any of thepsychophysiological variables assessed.

4. Discussion

In this sample, infants of mothers with subthreshold depression were more likely to beinsecurely attached than infants of mothers with major depression. This finding supportsprevious research indicating that the relation between maternal depression and attachmentsecurity is not straightforward, and that some types of depression may place a child at greaterrisk for insecure attachment than others (DeMulder & Radke-Yarrow, 1991). Furthermore,in the present sample, mothers experiencing subthreshold depression were less likely to bemarried. Indeed, mothers with subthreshold depression who also were unmarried were morelikely to have infants who were insecurely attached. This finding supports the notionadvanced by previous researchers that maternal depression is one of a number of risk factorsthat may combine to contribute to insecure attachment (Lyons-Ruth et al., 1990; Shaw &Vondra, 1993). It may be that mothers who are depressed and are under additional stress suchas that conveyed by single parenthood are less likely to be sensitive and responsive in theirinteractions with their children. Less sensitive and responsive parenting might then result ininsecure attachment status. Alternatively, since single mothers may spend more time awayfrom their infants (e.g. working), their increased absence might contribute to the infant’sinsecure attachment. However, the findings do not support this contention because unmarriedand married mothers in this study spent equal amounts of time working away from home.

That subthreshold depression was more strongly associated with insecure attachment thanmajor depression corroborates recent research which suggests that the effects of maternaldepression on infant attachment are diverse, even among studies such as this one that attemptto minimize confounding factors, such as poverty and family discord (Martins & Gaffan,

Fig. 3. Infant heart rate (beats/min) in infants of nondepressed, subthreshold, and depressed mothers.

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2000). Martins & Gaffan (2000) speculate that some of this variability may relate to eitherthe age of the infant at assessment or the presence of protective factors in the lives of thedepressed mothers. In this sample, the middle-class mothers with major depression may havehad protective influences that buffered the effects of maternal depression on the infants. Forexample, mothers with major depression may have had greater access to treatments fordepression, such as supportive psychotherapy and medications. The presence of alternativecaretakers (e.g. fathers, grandparents) might also have buffered infants from the effects ofmaternal depression. It will be important for future research to examine the influence of suchprotective factors in the relation between maternal depression and infant attachment security.

As was reported earlier with this sample of infants and their mothers (Dawson et al., 1997)infants of mothers with major depression exhibited reduced relative left frontal brainactivation compared to infants of nondepressed mothers and mothers with subthresholddepression. And, as reported earlier, this pattern of reduced left frontal activation wasapparent across all conditions (baseline, mother play, experimenter play) (Dawson et al.,1999). Furthermore, in the present study, it was found that insecurely attached infants,regardless of mother’s history of depression, also demonstrated reduced relative left frontalbrain activation compared to securely attached infants. It was also found that the reducedrelative left frontal brain activity exhibited by infants of depressed mothers was accentuatedfor insecurely attached infants of depressed mothers, suggesting additive effects. However,the additive effects were statistically not strong and should be interpreted with caution.Research indicates that the left prefrontal cortex is specialized for the expression of approachemotions, while the right prefrontal cortex is specialized for the expression of withdrawalemotions (Davidson & Fox, 1988, 1989; Dawson, Panagiotides et al., 1992). It is possiblethat reduced left frontal brain activity in infants of depressed mothers may index a greaterpropensity to use withdrawal-type emotion regulatory strategies, such as turning away fromthe external environment, in order to cope with negative arousal. Such an explanation isconsistent with the model proposed by Tronick & Gianino (1986). The novel finding thatinsecurely attached infants also exhibit this atypical pattern of frontal brain activity raises thequestion of whether an insecure attachment may reflect a failure to use appropriate approach-type regulatory strategies, such as adaptive approach of the mother during reunion episodes.

This study extends previous research by examining the relation among maternal depres-sion, attachment, and infant autonomic activity. The primary finding was that infants ofmothers with major depression exhibited elevated heart rate across all conditions indicatingthat these infants were generally more aroused. Thus, for both psychophysiological mea-sures, infants of mothers with major depression were more likely to show altered psycho-physiological responses as compared to mothers with subthreshold depression and thosewithout depression. However, contrary to our predictions, infants who displayed insecureattachment did not show increases in heart rate across the conditions relative to securelyattached infants. The absence of an effect of attachment security on heart rate was somewhatsurprising, given previous research linking stress response to attachment security (Donovan& Leavitt, 1985; Izard et al., 1991; Spangler & Grossman, 1993).

In interpreting the psychophysiological findings, it is important to keep in mind that therelation between maternal depression and infant psychophysiological responses may bemediated by a number of risk factors associated with maternal depression, including genetic

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vulnerabilities, prenatal variations in the intrauterine environment, mother-infant interac-tions, or a variety of contextual factors in the postnatal environment, such as marital conflict.An infant may be exposed to one or more of these risk factors, and these factors may act inan additive fashion or interact with the infant’s own temperament to affect the child’sdevelopment. Given the correlational nature of this study, it is impossible to determine themechanism or mechanisms underlying the association between maternal depression andaltered infant psychophysiological responses. Further research is needed to elucidate thefactors that might account for these findings.

Future research should also address the long-term consequences of atypical psychobiologyamong infants of depressed mothers, as well as among insecurely attached infants. Longi-tudinal research will be helpful in determining whether such psychobiological measuresindex increased risk for negative outcomes in childhood and adolescence. Maternal depres-sion typically exists in the context of other risk factors, such as marital discord, life stress,and low social support. It will be important to address how combinations of risk andprotective factors may operate to increase or decrease the risk for negative outcomes inchildren of depressed mothers. It also is currently unknown whether these psychophysio-logical patterns are relatively stable, or likely to change given decreases in maternaldepression or other changes in the environment.

Acknowledgments

This study was supported by a grant from the National Institute of Mental Health (No.MH47117). We wish to gratefully acknowledge the women and infants who participated inthis study, and the following individuals who made substantial contributions to this work:Cathy Brock, Jan St. John, Dick McDonald, Julie Osterling, Al Ross, Sally Shuh, andnumerous student research assistants.

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