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

Infant Behavior & Development 24 (2001) 135–149

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). 0163-6383/01/$ – see front matter © 2001 Elsevier Science Inc. All rights reserved. PII: S 0 1 6 3 - 6 3 8 3 ( 0 1 ) 0 0 0 7 5 - 3

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infancy. Infants of depressed mothers have been found to exhibit poorer mental and motor development, and increased emotion regulation problems (Murray & Cooper, 1997). During interactions with their mothers, infants of depressed mothers tend to display fewer affectionate behaviors and positive emotional expressions and more tantrums and negative expressions (Dawson et al., 1999; Field, 1995). Maternal depression is associated with genetic, prenatal, and postnatal risk factors that may 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 one possible risk factor associated with maternal depression. Some researchers have posited that a depressed mother’s failure to respond contingently to her infant’s emotional signals or to provide adequate levels of positive affect or stimulation may interfere with infant emotional development (Dawson, Panagiotides, Grofer Klinger, & Hill, 1992; Field, 1986; Goodman & Gotlib, 1999). Others have proposed that poorly coordinated mother-infant interactions may lead infants to experience more negative affect. After repeated failures to positively engage their mothers, these infants may withdraw and use less mature, self-directed regulatory strategies to cope with negative emotions (Tronick & Gianino, 1986). Several studies have provided evidence to support these hypotheses by demonstrating how maternal depression can disrupt mother-infant interactions. Studies have documented two distinct ways in which depressed mothers tend to interact with their infants, characterized by withdrawn versus intrusive and controlling maternal behavior (Cohn, Matias, Tronick, Connell, & Lyons-Ruth, 1986). During face-to-face interactions with their infants, depressed mothers who display a withdrawn style of interacting express less positive and more negative affect, 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 mothers tend to overstimulate their infants by poking, restraining, directing their infant’s attention, or aggressively 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, compared to nondepressed mothers, depressed mothers are generally less sensitively attuned to their infants’ cries (Donovan, Leavitt, & Walsh, 1998). It is well established that sensitive and responsive caretaking is important for the development of a secure attachment relationship (Teti & Nakagawa, 1990). Given the characteristics of a depressed mother’s interactions with her infant described above, one might expect infants of depressed mothers to be more vulnerable to developing insecure attachment relationships. Several studies have supported this hypothesis (Lyons-Ruth, Connell, Grunebaum, & Botein, 1990; Radke-Yarrow, Cummings, Kuczynski, & Chapman, 1985; Rosenblum, Mazet, & Be´ nony, 1997; Teti, Gelfand, Messinger, & Isabella, 1995). Rosenblum et al. (1997) reported that specific subtypes of maternal depression are associated with different types of insecure attachment. Specifically, irritable/stressed depression was found to be associated with insecure-ambivalent attachment, and dull/slow depression was associated with insecure-avoidant attachment. Rosenblum et al. (1997) suggested that infants of dull/ slow depressed mothers develop insecure-avoidant attachments as a self-regulatory strategy in 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 in children of unipolar depressed mothers equivalent to children of healthy mothers. Infants are most likely to develop insecure attachments when the mother’s affective disorder is severe and/or chronic (Teti et al., 1995), bipolar (Radke-Yarrow et al., 1995; DeMulder & RadkeYarrow, 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 recent meta-analysis, Martins & Gaffan (2000) found that, even within a set of studies selected to minimize confounding factors, such as poverty and family discord, the effects of maternal depression on attachment were diverse. Thus, the relation between maternal depression and infant attachment security is likely complex. Maternal depression is likely to be one of several risk factors that collectively contribute to the development of insecure attachment. In the present study, we were concerned with how maternal depression affects not only infant attachment behaviors, but also the physiological responses that may be directly or indirectly related to both maternal depression and attachment status. Researchers, for example, have documented associations between attachment classification and stress responses in infancy. Spangler & Grossman (1993) reported that, during the Strange Situation, infant heart rate increased during maternal separation regardless of attachment classification. Only insecurely attached infants exhibited an elevated salivary cortisol response to the Strange Situation, however. They have suggested that the heightened stress response observed in insecurely 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) and greater likelihood of attachment insecurity. In addition, research has found that securely attached infants exhibit heart rate deceleration in response to the stranger’s entrance during the Strange Situation, while insecurely attached infants fail to have a consistent pattern of autonomic responding to such an episode (Donovan & Leavitt, 1985). Altered autonomic reactivity has also been found in infants of depressed mothers. Field and colleagues (Field et al., 1988) examined infant autonomic activity and stress hormone levels during mother-infant interactions. They reported that infants of depressed mothers had higher heart rate, lower vagal tone, and higher stress hormone levels than infants of nondepressed mothers, suggesting that infants of depressed mothers experienced social interactions with their mothers as stressful. In the present study, we were interested in both infant frontal brain activity and infant autonomic responses as psychobiological indicators of risk for psychopathology in children of depressed mothers. For decades, researchers have recognized the central role of the prefrontal cortex in the expression and regulation of emotion (LeDoux, 1987; Luria, 1966; Nauta, 1971). Electroencephalographic (EEG) studies have demonstrated that the left and right frontal regions differentially mediate different types of emotion expression (Davidson & Fox, 1988, 1989; Dawson, Panagiotides et al., 1992). In both adults and infants, relative left frontal activation has been found to be associated with “approach” emotions, such as joy and 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 exhibit reduced 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 that infants of depressed mothers exhibit atypical patterns of frontal EEG activity. Compared to infants of nondepressed mothers, infants of depressed mothers showed reduced relative left frontal brain activation during a baseline condition, during playful interactions with their mothers, and during playful interactions with a familiar experimenter. In the present study, we extended this research by examining how the mother-infant attachment relationship may inform our understanding of the relation between maternal depression and both infant brain activity and autonomic activity (heart rate and vagal tone). In a previous study of low income, depressed teenage mothers, Dawson, Grofer Klinger, Panagiotides, Spieker, & Frey (1992) found that securely attached infants of depressed mothers exhibited significantly reduced left frontal electroencephalographic (EEG) activity compared to securely attached infants of nondepressed mothers. Brain activity did not differ between insecurely attached infants of depressed and nondepressed mothers; however, the small sample size for this comparison makes conclusions based on these results tentative. We predicted that infants of depressed mothers would exhibit increased heart rate and lower vagal tone in social interactions, compared to infants of nondepressed mothers. In addition, based on previous research associating insecure attachment with less optimal psychophysiological responses (Donovan & Leavitt, 1985; Izard et al., 1991; Spangler & Grossman, 1993), we predicted that insecurely attached infants would exhibit reduced left frontal brain activity and increased heart rate and vagal tone, and that maternal depression and attachment security may act in an additive fashion in their effects on infants’ physiological 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 the effects of maternal depression on children’s psychophysiological and behavioral development. This is the same sample of infants and mothers for whom EEG data has already been reported in previous publication (Dawson et al., 1997; Dawson et al., 1999). Mothers were recruited from the Psychology Department infant subject pool, newspaper advertisements, and community clinics. Upon entry into the study, mothers were carefully screened and were excluded if they reported substance use or abuse, serious medical conditions, attendance in special education classes, bipolar disorder, psychosis, immanent suicide, significant pregnancy or birth complications, and/or contact by Child Protective Services. All infants were full 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 medical condition, surgery, physical malformations, sensory or motor problems, prenatal exposure to drugs, 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 sample failed to classify themselves as belonging to an ethnic group. 2.1.1. Diagnostic groups Mothers 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; Radloff, 1977). Of the mothers in this study, 90 received a current diagnosis of depression or subthreshold depression based on the SCID and/or the CES-D. Twenty-seven of these mothers were classified as having major depression, and 63 were classified as having subthreshold depression. The remaining 69 mothers were classified as nondepressed. The criterion for classification as depressed was having either a current diagnosis of Major Depression (N ⫽ 25) or Double Depression (N ⫽ 2) on the SCID. Classification as subthreshold depressed was achieved by having a current SCID diagnosis of subthreshold depression (N ⫽ 9), dysthymia (N ⫽ 2), or depression in partial remission (N ⫽ 25), or by having a score of 16 or above on the CES-D (N ⫽ 27). Participants who were classified as nondepressed had scores lower than 9 on the CES-D and reported no current or lifetime history of depression on the SCID. There were significant differences among the diagnostic groups on three demographic variables of interest. The likelihood of being married differed among the depression groupings with the subthreshold depression group having the highest likelihood of being not married (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 depression groupings, with subthreshold mothers having an average of 1.9 (SD ⫽ 0.87) children, which was 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 average of 1.78 (SD ⫽ 0.89) children. Mother’s age also differed significant among depression groupings, with depressed mothers (Mean age ⫽ 32.6) being significantly older than nondepressed mothers (Mean age ⫽ 29.9; F(2, 156) ⫽ 2.99, p ⫽ .053). Other demographic variables 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 educational 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). Marital status, mother’s age, and number of children in family were used as covariates where appropriate. 2.2. Procedure 2.2.1. Experimental conditions for psychophysiological measures Infant psychophysiological testing occurred in the Developmental Psychophysiology Laboratory at the Center for Human Development and Disability at the University of Washington. The infant was videotaped and infant electrical brain activity (EEG) and heart rate were recorded during 5 different experimental conditions administered in the following order: Baseline, mother play, stranger enters, experimenter play, and mother leaves. During

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Table 1 Demographic characteristics of the sample

Child Characteristics Gender Female (%) Male (%) Age (months) Time spent in daycare (hrs/wk) Mother Characteristics Age (years) Education Level Marital Status Married Not married Time spent working away from home (average hrs/wk) Pregnancy Problems No Yes Family Characteristics SES Father’s education level # of children in family

Nondepressed (N ⫽ 69)

Sub-threshold (N ⫽ 63)

Depressed (N ⫽ 27)

56% 44% 13.9 ⫾ .4 13.3 ⫾ 17.1

59% 41% 13.9 ⫾ .5 11.6 ⫾ 15.9

48% 52% 14.0 ⫾ .7 9.9 ⫾ 17.0

29.9 ⫾ 4.8 5.3 ⫾ .9

30.5 ⫾ 4.6 5.4 ⫾ .9

32.6 ⫾ 5.3 5.3 ⫾ .9

96% 4% 14.8 ⫾ 15.9

81% 19% 14.2 ⫾ 17.4

41% 59% 43.4 ⫾ 9.8 5.2 ⫾ 1.2 1.5 ⫾ .8

44% 56% 44.1 ⫾ 14.1 4.6 ⫾ 2.3 1.9 ⫾ .9

Statistic

F (2,156) ⫽ 2.99*

␹2(2) ⫽ 7.02*

85% 15% 9.1 ⫾ 15.8 30% 70% 47.0 ⫾ 13.3 4.9 ⫾ 2.3 1.8 ⫾ .9

F (2,156) ⫽ 3.26*

Note: *p ⱕ .05.

the baseline condition (1 min), the experimenter stood out of the infant’s view, behind a black curtain and blew soap bubbles over the curtain. The bubbles were designed to attract and hold the infant’s attention. During the mother play condition, mothers were instructed to play peek-a-boo with their infants for 1 min. After this activity, a person whom the infant had never seen before entered the room, walked slowly toward the infant, sat and stared at the infant, and then backed out of the room all while maintaining a neutral expression. This stranger condition was followed by a 1-min peek-a-boo activity between the infant and a familiar experimenter. Finally, for the mother leaves condition, mothers stood up, waved and said “bye-bye,” and then walked slowly out of the door. Mothers remained outside the room for 20 s, than returned to comfort their infants. EEG and heart rate recording ended when the mothers were reunited with their infants. During the experimental conditions, infants were videotaped from a camera hidden behind a curtain in the testing room. Only data from the baseline and two play conditions are reported in this paper. These conditions were selected for three reasons: 1) Previous research has found that infants of depressed mothers have elevated heart rates during social interactions (Dawson et al., 1994; Field et al., 1988), 2) eliminating the mother leave condition permitted observation of infant psychophysiology independent of the attachment relationship, and 3) selecting these conditions maximized the sample size as more infants were missing data during the stranger enter and mother leave conditions. Of the 140 infants with attachment security ratings (see below), 118 had complete EEG data across the three conditions.

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2.2.2. EEG recording and analysis In 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 individual silver-silver chloride electrodes to the scalp with Grass EEG cream. Infant EEG was recorded from four scalp locations: left and right frontal and parietal (F3, F4, P3, P4; International 10 –20 system). EEG leads were referenced to mastoid electrodes, and identical impedances were obtained for right and left mastoid using a potentiometer. Additional electrodes included a forehead electrode, which served as ground, and EOG electrodes, which were used for offline removal of ocular artifact. All impedances were under 5 K⍀. EEG was recorded using a Grass Neurodata Acquisition System (Model 12). Settings for the high pass active filter and low pass filter were 1 Hz and 30 Hz, respectively. Analogto-digital conversion was based on a 512 points/sec sampling rate. Digitized data were stored continuously on an IBM PC-AT. James Long Co. (Caroga Lake, NY) EEGEDIT software was used to inspect and edit EEG data for motor artifacts, including EOG. The amount of artifact-free EEG data available did not differ by maternal depression grouping. In order to be included in the analyses, a minimum of 15 s of artifact-free EEG needed to be available. Discrete Fourier analyses were performed 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. Analyses focused solely on the 6 –9 Hz range as previous research (see review by Fox, 1991) has found that the 6 –9 Hz band is the dominant high-frequency band during infancy and is believed to reflect infant “alpha.” In order to normalize the distributions, EEG spectral power scores were natural log transformed. Subsequently, asymmetry scores (ln right EEG power minus ln left EEG power) were computed to determine relative activity of homologous right and left hemisphere regions. Negative asymmetry scores indicate relative right-hemisphere activity and positive asymmetry scores indicate relative left-hemisphere activity. 2.2.3. Heart rate recording and analysis Heart-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 and filtered through a high pass filter set at 0.1 Hz. The signal was then digitized through an Analog to Digital (A/D) converter at 512 samples per second. The digitized data were stored on a hard disk for off-line processing. The timing of the R-waves was extracted using a program designed by James Long, Inc. (Caroga Lake, NY). The output of the R-wave detection was edited and corrected by visual inspection. The corrected records were in turn segmented by experimental condition and R-to-R-wave intervals were entered into an analysis 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 visually inspected and corrected for errors. IBI values were then entered into Mxedit for further visual inspection and heart rate variability computation. Mxedit uses the Porges-Bohrer algorithm for band-pass filtering of IBI data that is based on a moving polynomial to remove nonstationarities. Filtering values for children between 0.24 and 1.04 with a polynomial order of 3 and a coefficient number of 21 were used in each condition analysis.

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Table 2 Infant attachment classification by history of maternal depression Category

Nondepressed

Sub-threshold Depressed

Major Depression

A B C D U

11 (18%) 24 (39%) 9 (15%) 16 (26%) 1 (2%)

7 (13%) 15 (28%) 11 (21%) 13 (25%) 7 (13%)

2 (8%) 15 (58%) 3 (11%) 6 (23%) 0

2.2.4. Attachment classification Infant attachment status was assessed based on observations of the infants’ behaviors during the traditional Strange Situation, which was conducted on a separate day from the psychophysiological testing. This procedure consists of 8 structured, 3-min episodes during which the infant is videotaped in a laboratory playroom. The episodes include two separations from the mother, once when the mother leaves the infant with a stranger and once when the mother leaves the infant alone. Each episode involved changes in the social environment and 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 their videotaped sessions rated. All attachment coding was performed by a coding team led by Susan Spieker at the University of Washington. Attachment videotapes were coded using the Main and Solomon (1990) classification scheme. Using the Main classification scheme, infants were coded as demonstrating secure (B) or insecure (A—avoidant, C—resistant, D— disorganized, U— unclassifiable) attachment. Using this system, 39% of infants were classified as secure and 61% were classified as 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 qualification for D attachment status with indices of disorganization and disorientation that are strong, frequent, or extreme.” All tapes were double-coded and disagreements were coded by consensus, as were all cases with D-ratings that disagreed by more than 2 points. Agreement across 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 maternal depression group. Attachment classification (A,B,C,D/U) did not differ significantly by maternal depression group (␹2 (6) ⫽ 7.95, p ⫽ .24). However, attachment security (secure vs. 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 subthreshold depression were more likely to be insecurely attached than infants of mothers with major depression (␹2 (1) ⫽ 6.40, p ⫽ .015, 2-tailed). Attachment security in infants of nonde-

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pressed mothers did not differ significantly from attachment security in infants of depressed mothers, as a whole. In order to further explore the relation between subthreshold maternal depression and insecure infant attachment, data were analyzed separately based on mother’s marital status. Previous research has demonstrated that maternal depression is more likely to be associated with insecure attachment in the context of other contextual risk factors, such as marital dissatisfaction (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 or divorced (19% vs. 15% and 4% for depressed and nondepressed mothers respectively), analyses were conducted to determine whether mother’s marital status might be moderating the relation between maternal depression and infant attachment security. Results revealed that infants of mothers with subthreshold depression were more likely to be insecurely attached only if their mother was also unmarried (␹2 (2) ⫽ 11.84, p ⫽ .003). Among married mothers, 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 the mother 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 activity A 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 measures ANOVA with frontal EEG asymmetry scores as the dependent variable revealed significant main 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 security interaction (F(2, 112) ⫽ 2.73, p ⫽ .07). On average, infants of mothers with major depression had lower frontal EEG asymmetry scores than infants of subthreshold and nondepressed mothers, and insecurely attached infants had lower frontal EEG asymmetry scores than securely attached infants (see Figs. 1 and 2). When securely and insecurely attached infants were examined separately, it was revealed that, among insecurely attached infants, infants of mothers with major depression had lower frontal EEG asymmetry scores than 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 results remained essentially the same. Analyses of the parietal EEG revealed no main effects of maternal depression or attachment security. 3.2.2. Maternal depression, infant attachment security, and infant autonomic activity 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 measures ANOVA with infant heart rate (beats/min) as the dependent variable revealed significant main 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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Fig. 1. Infant frontal EEG asymmetry (ln right minus ln left EEG power) in infants of nondepressed, subthreshold, and depressed mothers.

mothers with major depression had higher heart rates than infants of mothers with subthreshold depression or no depression (see Fig. 3). Analyses were conducted with and without covariates 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 measures ANOVA with infant vagal tone as the dependent variable revealed a significant main effect of condition (F(2, 250) ⫽ 6.83, p ⫽ .001). Infants had lower vagal tone during the interaction conditions compared to the baseline condition. Analyses were conducted with and without covariates and the results remained essentially the same. Recent research suggests that disorganized attachment may be associated with increased heart rate during separation from mother (Willemsen-Swinkels, Bakermans-Kranenburg,

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

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

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

4. Discussion In this sample, infants of mothers with subthreshold depression were more likely to be insecurely attached than infants of mothers with major depression. This finding supports previous research indicating that the relation between maternal depression and attachment security is not straightforward, and that some types of depression may place a child at greater risk for insecure attachment than others (DeMulder & Radke-Yarrow, 1991). Furthermore, in the present sample, mothers experiencing subthreshold depression were less likely to be married. Indeed, mothers with subthreshold depression who also were unmarried were more likely to have infants who were insecurely attached. This finding supports the notion advanced by previous researchers that maternal depression is one of a number of risk factors that 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 such as that conveyed by single parenthood are less likely to be sensitive and responsive in their interactions with their children. Less sensitive and responsive parenting might then result in insecure attachment status. Alternatively, since single mothers may spend more time away from their infants (e.g. working), their increased absence might contribute to the infant’s insecure attachment. However, the findings do not support this contention because unmarried and married mothers in this study spent equal amounts of time working away from home. That subthreshold depression was more strongly associated with insecure attachment than major depression corroborates recent research which suggests that the effects of maternal depression on infant attachment are diverse, even among studies such as this one that attempt to minimize confounding factors, such as poverty and family discord (Martins & Gaffan,

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2000). Martins & Gaffan (2000) speculate that some of this variability may relate to either the age of the infant at assessment or the presence of protective factors in the lives of the depressed mothers. In this sample, the middle-class mothers with major depression may have had protective influences that buffered the effects of maternal depression on the infants. For example, mothers with major depression may have had greater access to treatments for depression, such as supportive psychotherapy and medications. The presence of alternative caretakers (e.g. fathers, grandparents) might also have buffered infants from the effects of maternal depression. It will be important for future research to examine the influence of such protective 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 brain activation compared to infants of nondepressed mothers and mothers with subthreshold depression. And, as reported earlier, this pattern of reduced left frontal activation was apparent 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 frontal brain activation compared to securely attached infants. It was also found that the reduced relative left frontal brain activity exhibited by infants of depressed mothers was accentuated for 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 approach emotions, while the right prefrontal cortex is specialized for the expression of withdrawal emotions (Davidson & Fox, 1988, 1989; Dawson, Panagiotides et al., 1992). It is possible that reduced left frontal brain activity in infants of depressed mothers may index a greater propensity to use withdrawal-type emotion regulatory strategies, such as turning away from the external environment, in order to cope with negative arousal. Such an explanation is consistent with the model proposed by Tronick & Gianino (1986). The novel finding that insecurely attached infants also exhibit this atypical pattern of frontal brain activity raises the question of whether an insecure attachment may reflect a failure to use appropriate approachtype regulatory strategies, such as adaptive approach of the mother during reunion episodes. This study extends previous research by examining the relation among maternal depression, attachment, and infant autonomic activity. The primary finding was that infants of mothers with major depression exhibited elevated heart rate across all conditions indicating that these infants were generally more aroused. Thus, for both psychophysiological measures, infants of mothers with major depression were more likely to show altered psychophysiological responses as compared to mothers with subthreshold depression and those without depression. However, contrary to our predictions, infants who displayed insecure attachment did not show increases in heart rate across the conditions relative to securely attached infants. The absence of an effect of attachment security on heart rate was somewhat surprising, 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 the relation between maternal depression and infant psychophysiological responses may be mediated 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 interactions, 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 in an additive fashion or interact with the infant’s own temperament to affect the child’s development. Given the correlational nature of this study, it is impossible to determine the mechanism or mechanisms underlying the association between maternal depression and altered infant psychophysiological responses. Further research is needed to elucidate the factors that might account for these findings. Future research should also address the long-term consequences of atypical psychobiology among infants of depressed mothers, as well as among insecurely attached infants. Longitudinal research will be helpful in determining whether such psychobiological measures index increased risk for negative outcomes in childhood and adolescence. Maternal depression 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 and protective factors may operate to increase or decrease the risk for negative outcomes in children of depressed mothers. It also is currently unknown whether these psychophysiological patterns are relatively stable, or likely to change given decreases in maternal depression 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 in this 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, and numerous student research assistants. References Baxter, L. R., Schwartz, J. M., Phelps, M. E., Mazziotta, J. C., Guze, B. H., Selin, C. E., Gerner, R. H., & Sumida, R. M. (1989). Reduction in prefrontal cortex glucose metabolism common to three types of depression. Archives of General Psychiatry, 46, 243–250. Cohn, J. F., Matias, R., Tronick, E. Z., Connell, D., & Lyons-Ruth, D. (1986). Face-to-face interactions of depressed mothers and their infants. In E. Z. Tronick & T. Field (Eds.), Maternal depression and infant disturbance (pp. 31– 45). San Francisco: Jossey-Bass. Cohn, J. F., & Tronick, E. Z. (1989). Specificity of infants’ response to mothers’ affective behavior. Journal of the American Academy of Child and Adolescent Psychiatry, 28, 242–248. Davidson, R. J., & Fox, N. A. (1988). Cerebral asymmetry and emotion: Development and individual differences. In S. Segalowitz & D. Molfese (Eds.), Developmental implications of brain lateralization (pp. 191–206). New York: Guilford. Davidson, R. J., & Fox, N. A. (1989). Frontal brain asymmetry predicts infants’ response to maternal separation. Journal of Abnormal Psychology, 98, 127–131. Dawson, G., Frey, K., Panagiotides, H., Osterling, J., & Hessl, D. (1997). Infants of depressed mothers exhibit atypical frontal brain activity: A replication and extension of previous findings. Journal of Child Psychology and Psychiatry, 38(2), 179 –186.

148

G. Dawson et al. / Infant Behavior & Development 24 (2001) 135–149

Dawson, G., Frey, K., Panagiotides, H., Yamada, E., Hessl, D., & Osterling, J. (1999). Infants of depressed mothers exhibit atypical frontal electrical brain activity during interactions with mother and with a familiar, nondepressed adult. Child Development, 70(5), 1058 –1066. Dawson, G., Frey, K., Self, J., Panagiotides, H., Hessl, D., Yamada, E., and Rinaldi, J. (1999). Frontal electrical brain activity in infants of depressed mothers: Relation to variations in infant behavior. Development and Psychopathology, 11, 589 – 605. Dawson, G., Grofer Klinger, L., Panagiotides, H., Spieker, S., & Frey, K. (1992). Infants of mothers with depressive symptoms: Electroencephalographic and behavioral findings related to attachment status. Development and Psychopathology, 4, 67– 80. Dawson, G., Hessl, D., & Frey, K. (1994). Social influences on early developing biological and behavioral systems related to risk for affective disorder. Development and Psychopathology, 6, 759 –779. Dawson, G., Panagiotides, H., Grofer Klinger, L., & Hill, D. (1992). The role of frontal lobe functioning in the development of self-regulatory behavior in infancy. Brain and Cognition, 20, 152–175. DeMulder, E. K., & Radke-Yarrow, M. (1991). Attachment and affectively ill and well mothers: Concurrent behavioral correlates. Development and Psychopathology, 3, 227–242. Donovan, W. L., & Leavitt, L. A. (1985). Physiologic assessment of mother-infant attachment. Journal of the American Academy of Child Psychiatry, 24, 65–70. Donovan, W. L., Leavitt, L. A., & Walsh, R. O. (1998). Conflict and depression predict maternal sensitivity to infant cries. Infant Behavior and Development, 21(3), 505–517. Downey, G., & Coyne, J. (1990). Children of depressed parents: An integrative review. Psychological Bulletin, 108, 50 –76. Field, T. (1986). Models for reactive and chronic depression in infancy. In E. Z. Tronick & T. Field (Eds.), Maternal depression and infant disturbance (pp. 47– 60). No. 34. San Francisco: Jossey-Bass. Field, T. (1995). Infants of depressed mothers. Infant Behavior and Development, 18, 1–13. Field, T., Healy, B., Goldstein, S., Perry, S., Bendall, D., Schanberg, S., Zimmerman, E., & Kuhn, C. (1988). Infants of depressed mothers show “depressed” behavior even with non-depressed adults. Child Development, 59, 1569 –1579. Fox, N. A. (1991). If it’s not left, it’s right: Electroencephalograph asymmetry and the development of emotion. American Psychologist, 46, 863– 872. Goodman, S. H., & Gotlib, I. H. (1999). Risk for psychopathology in the children of depressed mothers: A developmental model for understanding mechanisms of transmission. Psychological Review, 106(3), 458 – 490. Hart, S., Field, T., del Valle, C., Pelaez-Nogueras, M. (1998). Depressed mothers’ interactions with their one-year-old infants. Infant Behavior and Development, 21(3), 519 –525. Henriques, J. B., & Davidson, R. J. (1990). Regional brain electrical asymmetries discriminate between previously depressed subjects and healthy controls. Journal of Abnormal Psychology, 99, 22–31. Hollingshead, A. B. (1975). Form Factor Index of Social Status. New Haven, CT: Yale University. Izard, C. E., Porges, S. W., Simons, R. F., Haynes, O. M., Hyde, C., Parisi, M., & Cohen, B. (1991). Infant cardiac activity: Developmental changes and relations with attachment. Developmental Psychology, 27(3), 432– 439. Jones, N. A., Field, T., Fox, N. A., Davalos, M., Malphurs, J., Carraway, K., Schanberg, S., & Kuhn, C. (1997). Infants of intrusive and withdrawn mothers. Infant Behavior and Development, 20(2), 175–186. LeDoux, J. E. (1987). Emotion. In F. Plum (Eds.), Handbook of physiology: I. The nervous system. Vol. V. Higher functions of the brain (pp. 419 – 460). Bethesda, MD: American Physiological Society. Lundy, B. L., Jones, N. A., Field, T., Nearing, G., Davalos, M., Pietro, P. A., Schanberg, S., & Kuhn, C. (1999). Prenatal depression effects on neonates. Infant Behavior and Development, 22(1), 119 –129. Luria, A. R. (1966). Higher cortical functions in man. New York: Basic Books. Lyons-Ruth, K., Connell, D. B., Grunebaum, H. U., & Botein, S. (1990). Infants at social risk: Maternal depression and family support services as mediators of infant development and security of attachment. Child Development, 61, 85–98. Main, M., & Solomon, J. (1990). Procedure for identifying infants as disorganized/disoriented during the Ainsworth

G. Dawson et al. / Infant Behavior & Development 24 (2001) 135–149

149

strange situation. In M. T. Greenberg, D. Cicchetti, & E. M. Cummings (Eds.), Attachment in the preschool years: Theory, research, and intervention (pp. 121–160). Chicago: The University of Chicago Press. Martins, C., & Gaffan, E. A. (2000). Effects of early maternal depression on patterns of infant-mother attachment: A meta-analytic investigation. Journal of Child Psychology and Psychiatry, 41(6), 737–746. Murray, L., & Cooper, P. J. (1997). Postpartum depression and child development. Psychological Medicine, 27, 253–260. Nauta, W. J. H. (1971). The problem of the frontal lobes: A reinterpretation. Journal of Psychiatric Research, 8, 167–187. Nurnberger, J., Goldin, L. R., & Gershon, E. S. (1986). Genetics of psychiatric disorders. In G. Winokur & P. Clayton (Eds.), The Medical Basis of Psychiatry (pp. 486 –521). Philadephia: Saunders. Radke-Yarrow, M. (1998). Children of Depressed Mothers: From Early Childhood to Maturity. Cambridge, UK: Cambridge University Press. Radke-Yarrow, M., Cummings, E. M., Kuczynski, L., & Chapman, M. (1985). Patterns of attachment in two- and three-year-olds in normal families and families with parental depression. Child Development, 56, 884 – 893. Radke-Yarrow, M., McCann, K., DeMulder, E., Belmont, B., Martinez, P., & Richardson, D. T. (1995). Attachment in the context of high-risk conditions. Development and Psychopathology, 7, 247–265. Radloff, L. S. (1977). The CES-D scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1, 385– 401. Rosenblum, O., Mazet, P., & Be´ nony, H. (1997). Mother and infant affective involvement states and maternal depression. Infant Mental Health Journal, 18(4), 350 –363. Shaw, D. S., & Vondra, J. I. (1993). Chronic family adversity and infant attachment security. Journal of Child Psychology and Psychiatry, 34(7), 1205–1215. Spangler, G., & Grossman, K. E. (1993). Biobehavioral organization in securely and insecurely attached infants. Child Development, 64, 1439 –1450. Spitzer, R. L., Williams, J. B., Gibbon, M., & First, M. (1989). Structured Clinical Interview for DSM-III-R (with psychotic screen). Biometric Research Department, New York State Psychiatric Institute, New York. Teti, D. M., Gelfand, D. M., Messinger, D. S., & Isabella, R. (1995). Maternal depression and the quality of early attachment: An examination of infants, preschoolers, and their mothers. Developmental Psychology, 31(3), 364 – 376. Teti, D. M., & Nakagawa, M. (1990). Assessing attachment in infancy: The Strange Situation and alternate systems. In E. D. Gibbs & D. M. Teti (Eds.). Interdisciplinary assessment of infants: A guide for early intervention professionals (pp. 191–214). Baltimore: Paul H. Brookes. Tronick, E. Z., & Gianino, A. F. (1986). The transmission of maternal disturbances to the infant. In E.Z. Tronick & T. Field (Eds.), Maternal depression and infant disturbance (pp.5–11). San Francisco: Jossey-Bass. Tsuang, M. T., & Faraone, S. V. (1990). The genetics of mood disorders. Baltimore: Johns Hopkins University Press. Willemsen-Swinkels, S. H. N., Bakermans-Kranenburg, M. J., Buitelaar, J. K., van IJzendoorn, M. H., & van Engeland, H. (2000). Insecure and disorganised attachment in children with a pervasive developmental disorder: Relationship with social interaction and heart rate. Journal of Child Psychology and Psychiatry and Allied Disciplines, 41(6), 759 –767.