Depressed mothers who are “good interaction” partners versus those who are withdrawn or intrusive

Infant Behavior & Development 26 (2003) 238–252

Depressed mothers who are “good interaction” partners versus those who are withdrawn or intrusive Tiffany Field∗ , Miguel Diego, Maria Hernandez-Reif, Saul Schanberg, Cynthia Kuhn a

Department of Pediatrics (D-820), Touch Research Institutes, University of Miami School of Medicine, P.O. Box 016820, Miami, FL 33101, USA b Duke University School of Medicine, Durham, NC, USA Received 29 July 2002; received in revised form 18 December 2002; accepted 19 December 2002

Abstract The interactions of 3-month-old infants and their depressed mothers were classified as intrusive, withdrawn or good interactions. Analyses of retrospective data suggested that all depressed groups scored higher on depression (CES-D) and anxiety (STAI) scales and had similarly elevated cortisol, norepinephrine and epinephrine during pregnancy. The depressed mothers and their newborns also had greater relative right frontal EEG activation. Despite these group similarities, the infants of the “good interaction” mothers did not show high amounts of indeterminate sleep and they received better scores on the Brazelton scale. The more organized behaviors of these newborns may have contributed to the better interaction ratings of the “good interaction” depressed mothers. © 2003 Elsevier Science Inc. All rights reserved. Keywords: Depressed mothers; Good interactions; Interaction behavior; Withdrawn mothers; Intrusive mothers

Withdrawn and intrusive interaction styles were described for depressed mothers several years ago by Tronick, Cohn and by our research group (Cohn, Matias, Tronick, Connell, & Lyons-Ruth, 1986; Field, 1986; Tronick & Field, 1986), with the different style mothers showing different interaction behavior with their infants. Recently, these different style depressed mothers were noted to not only have different interaction styles with their infants but to also have different physiological and biochemical profiles that were partially mirrored by their infants (Field et al., 2001). The intrusive mothers’ depression seemed to have less severe effects, ∗

Corresponding author. Tel.: +1-305-243-6790; fax: +1-305-243-6488. E-mail address: [email protected] (T. Field). 0163-6383/03/$ – see front matter © 2003 Elsevier Science Inc. All rights reserved. doi:10.1016/S0163-6383(03)00020-1

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possibly because those women had normal dopamine levels which had behavior activation effects, paralleling the rat model developed by Jay Weiss and his colleagues (Weiss, Bonsall, Demetrikopoulos, Emery, & West, 1998). The withdrawn mothers, in contrast, corresponded to the Weiss model of more severe “depression” effects, possibly due to depleted dopamine and behavioral inactivation and anhedonia. Depressed mothers have typically been classified as intrusive or withdrawn based on videotapes of the mothers’ and infants’ face-to-face interactions usually when the infants were 3–6 months old (Jones, Field, Hart, Lundy, & Davalos, 2001). In the Jones et al.’s study 41% of the depressed mothers were identified as being intrusive (i.e., showing rough physical contact including tickling, poking, tugging, using rapid staccato actions and tense or fake facial expressions), 38% were identified as withdrawn (flat affect, rare touching, rare vocalizing, disengaged behavior and looking away from the infant) and 21% were classified as undefined or “good interaction” partners because they could not be classified as intrusive or withdrawn and their behaviors were more similar to those of non-depressed mothers (smiling, sensitive touching and contingently responsive behavior; Jones et al., 2001). The extremely withdrawn mothers behaved like statues with virtually no interaction with their infants. In contrast, the extremely intrusive mothers behaved like “wood–pecking, boxing machines” poking and “boxing” their infants’ faces and jerking their heads such that some sessions needed to be interrupted and referrals made to protective services. The two different style depressed mothers also have different EEG patterns (Diego et al., 2002; Diego, Field, & Hernandez-Reif, 2001; Jones et al., 2001). Withdrawn depressed mothers and their infants showed greater relative right frontal EEG activation patterns, while intrusive depressed mothers and infants showed greater relative left frontal EEG activation. According to Davidson (1998), these patterns may reflect left frontal hypoactivation in the withdrawn mothers and right frontal hypoactivation in the intrusive mothers. EEG researchers have documented associations between approach emotions such as happy and anger and greater relative left frontal EEG activation (Davidson & Fox, 1982, 1989). The same researchers reported an association between withdrawal emotions such as sadness and greater relative right frontal EEG activation. Right frontal EEG activation in depressed individuals appears to be explained by left frontal hypoactivation both in adults (Henriques & Davidson, 1990) and in infants of depressed mothers (Dawson et al., 1999; Dawson, Klinger, Panagitotides, Hill, & Spieker, 1992). The infants of withdrawn mothers appeared to be more affected, as was reflected in the lower interaction ratings of the withdrawn mothers and their infants when the infants were 3 months old (Jones et al., 2001). The infants of withdrawn mothers also had lower Bayley mental scale scores at 1 year (Hart, Jones, Field, & Lundy, 1999). Based on the intrusive/withdrawn classification made at 3–6 months postpartum we retrospectively compared the prenatal and neonatal data of these two groups (Field et al., 2001). The depressed mothers as a whole had higher cortisol and norepinephrine levels during pregnancy. Although the mothers from both groups had been diagnosed as dysthymic on the Diagnostic Interview Schedule and had equivalently high Beck Depression Inventory scores, the withdrawn mothers had lower dopamine levels. The neonates of these mothers had biochemical profiles similar to their different classification mothers. The newborns of the withdrawn mothers had lower dopamine levels, like their mothers, and the newborns of the intrusive mothers had higher dopamine levels, like their mothers. Otherwise the profiles were similar, with both

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groups of mothers and infants having similarly high norepinephrine and cortisol levels and similarly low serotonin levels. The neonates of the depressed mothers showed inferior performance on the orientation, motor, reflex, excitability, withdrawn and depression clusters of the Brazelton, with the newborns of the withdrawn mothers showing the least optimal performance, most particularly on the Brazelton orientation, motor and Lester depression scores. Stepwise regression analyses revealed that the depressed mothers’ prenatal norepinephrine and dopamine levels significantly predicted their newborns’ norepinephrine and dopamine levels as well as their Brazelton scores. Prenatal depression contributed to 35% of the variance in newborn cortisol, and prenatal anxiety and norepinephrine contributed to 44% of the variance in newborn norepinephrine levels. During the course of the previous studies we were able to explore various assessment procedures that might distinguish the intrusive and withdrawn depressed mothers prior to their interactions with their 3-month-old infants so that they could be identified during pregnancy. Earlier we had only been able to distinguish the mothers’ style by their interaction behaviors with their 3–6-month-old infants. However, in a comprehensive assessment study (Diego et al., 2001), we were able to document high correlations between the depressed mothers’ different interaction styles at 3–6 months and their EEG patterns and scores on the Behavioral Inhibition Scale/Behavioral Activation Scale (BIS/BAS) at the prenatal period. As might have been expected, the mothers with high BIS (behavioral inhibition) scores were those showing withdrawn interaction behavior and greater relative right frontal EEG in contrast to those with high BAS (behavioral approach) scores showing greater relative left frontal EEG activation and intrusive interaction patterns. Throughout the previous studies the depressed mothers who had “good interactions” (moderate amounts of smiling, touching and contingently responsive behavior) were not assessed. The purpose of the current study was to determine the behavioral/physiological/biochemical profiles of these mothers and their infants as compared to those depressed mothers who were intrusive or withdrawn and non-depressed mothers and their infants.

1. Methods 1.1. Participants Depressed and non-depressed women were recruited near the end of their second trimester (M = 24 weeks; R = 20–28 weeks) from obstetrician-gynecologists’ offices. The women’s medical charts were reviewed to screen out any women who showed drug use during pregnancy based on routine drug screens. Subsequently, when their infants were 3 months old, the pregnant women were assigned to a depressed or non-depressed group based on their scores on the Center for Epidemiological Studies Depression Scale (CES-D; Radloff, 1977). Those who had elevated scores (>16) were assigned to the depressed symptom group (M CES-D = 24.0), while women scoring in the normal range (<12) were assigned to the non-depressed group (M CES-D score = 8.0). At that time, they were also classified as having withdrawn, intrusive, or “good interaction” styles based on their interaction behaviors with their 3-month-old infants (see description at end of Section 1). The final sample included 140 pregnant women (100

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with elevated depressive symptom scores) of lower-middle socioeconomic status (M = 3.0 on the Hollingshead, 1975). The distribution of different style depressed mothers was similar to that of our previous studies. Of the 100 depressed women, 39% (N = 39) were classified as having intrusive, 36% withdrawn and 25% “good interaction” styles. The women averaged 27.7 years of age, 33% were single, and their ethnicity was distributed: 43% Hispanic-American, 34% African-American, 14% White Non-Hispanic and 9% Other. Eighty-four percent of the prenatally recruited sample were full-term (M = 37 weeks GA) and healthy. A significantly greater number of the infants born prematurely were infants of depressed mothers (25% vs. 7%, p < .01). Because of expected differences in their interaction patterns related to prematurity, these infants were excluded from the final sample. The newborns were tested within 2 days after birth (M = 1.9 days). Fifty-eight percent of the depressed group were female infants and 54% of the non-depressed group were female infants. The depressed and non-depressed groups did not differ on demographic variables. Similarly, the depressed intrusive, withdrawn and “good interaction” groups did not differ on demographic variables. Although only 4 of the mothers in the non-depressed group were classified as intrusive and only 2 as withdrawn, those mothers were excluded from the final sample. Also, 6 mothers who were not depressed prenatally but became depressed postpartum were omitted from the sample. 1.2. Procedure At their prescribed ultrasound session (M gestational age = 24 weeks) the mothers were given the CES-D (Radloff, 1977), the Spielberger Trait Anxiety Inventory (Spielberger, Gorsuch & Lushene, 1970), the BIS/BAS (Carver & White, 1994) and the Profile of Mood States (POMS; McNair, Lorr, & Droppleman, 1971). The ultrasound sessions were coded for fetal activity. First morning urine samples were obtained from the mothers during the prenatal visit and from them and their newborns within 24 hr after delivery. Shortly after the delivery the medical records were used to score the Obstetric Complications Scale (OCS; Littman & Parmelee, 1978), and the Brazelton Neonatal Behavior Assessment Scale (Brazelton, 1984) was also given within the first 2 days after birth. In addition, at that time, the mothers’ and newborns’ EEGs were recorded and the newborns’ sleep states and activity were coded. At 3 months the mothers were given the CES-D again for depression/non-depression group classification purposes, and mother–infant interactions were also classified as intrusive, withdrawn or “good interactions.” 1.3. Measures 1.3.1. The Center for Epidemiological Studies Depression Scale (CES-D) The CES-D (Radloff, 1977) is a 20-item self-report scale designed to measure depressive symptoms including depressed mood, feelings of guilt, worthlessness, helplessness and hopelessness, loss of energy, and sleep and appetite disturbances (Radloff & Teri, 1986). The 20 symptoms are rated for frequency (over the past week) from “rarely or none of the time” to “most or all of the time.” A summary score ranges from 0 to 60 by summing all items. Reliability and validity have been acceptable across a variety of demographic characteristics including age, education, geographic area, and racial, ethnic and language groups (Radloff & Teri, 1986).

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The CES-D was given to the mother at the time of prenatal recruitment, again within 24 hr following delivery and at the 3-month interaction assessment. 1.3.2. The Behavioral Inhibition System/Behavioral Approach System Scale (BIS/BAS) The BIS/BAS (Carver & White, 1994) is a 24-item questionnaire consisting of personal statements followed by four severity options ranging from very true to very false. The Behavioral Inhibition System Scale examines inhibited or withdrawn behavior and the Behavioral Approach System Scale examines approach behavior. Difference scores are obtained by subtracting z-transformed BIS scores from BAS scores. Positive scores denote greater BAS activity, while negative scores denote greater BIS activity. The BIS/BAS and EEG activity have been significantly related in non-depressed (Sutton & Davidson, 1997) and depressed (Diego et al., 2001) samples. 1.3.3. The State-Trait Anxiety Inventory The State-Trait Anxiety Inventory (Spielberger et al., 1970) was used to assess anxiety levels. This 20-question 4-point Likert scale forms a summed score from 20 to 80 for the trait subscale with higher scores indicating greater anxiety. The Trait Anxiety Scale is comprised of how the subject “typically feels.” Characteristic items include: “I feel nervous” and “I feel calm.” Research has demonstrated that the State-Trait Anxiety Inventory has adequate concurrent validity and internal consistency (r = .83). 1.3.4. Profile of Mood States (POMS) Anger Scale The POMS Anger Scale (McNair et al., 1971) consists of 12 items rated on 5-point scales ranging from (0) “not at all” to (4) “extremely.” The scale has adequate concurrent validity and good internal consistency (r = .95; McNair & Lorr, 1964). 1.3.5. Fetal activity This assessment was made at 20–28 weeks (M = 24 weeks). For this assessment the technician positioned the scanner to obtain a lateral view of the fetus. The observer who was blind to the mother’s group assignment then watched the fetus for five consecutive minutes. Every 3 s (a total of 100 samples), a tape-recorded cue (heard through an earphone) prompted the observer to record the fetal activity categories including: (a) single limb movement, (b) multiple limb movement, and (c) gross body movement. Inter-rater reliability, calculated on one third of the sample for two observers, yielded the following Kappa values: single limb movement = .82; multiple limb movement = .86; gross body movement = 1.00. For the data analyses, the total percent time the fetus engaged in movement was calculated (adding the above categories). No effort was made to discern fetal behavior states because they cannot be reliably identified prior to 36 weeks without confirmation through fetal heart rate monitoring. 1.3.6. First-morning urine samples First-morning urine samples were collected from the depressed and non-depressed women at their ultrasound visit and within 24 hr following delivery. Newborn first morning urine samples were collected in the nursery also within 24 hr following delivery. The samples were frozen

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and sent to Duke University to be analyzed by lab technicians who were “blind” to group assignment. The urines were assayed for norepinephrine, epinephrine, dopamine, serotonin and cortisol levels after correcting for creatinine levels. Norepinephrine, epinephrine, serotonin and cortisol levels were assessed because of their previously reported positive association with depression (Field, 1995) and dopamine because of a recent animal model implicating a negative association between dopaminergic activity and depression (Weiss, Demetrikopoulos, West, & Bonsall, 1996). 1.3.7. Obstetric complications Obstetric complications were assessed on the Obstetric Complications Scale (Littman & Parmelee, 1978) which is comprised of 41 items taken from the medical charts and rated as optimal or non-optimal. 1.3.8. Sleep/wake behavior Sleep/wake behaviors were continuously videotaped in compressed time (3 hr sleep coded in 1 hr using time lapse video) for an inter-feeding interval (2–3 hr) before the Brazelton was performed on the first afternoon after birth. Thoman’s studies of term infants’ sleep patterns suggest that an inter-feeding interval time frame can provide a representative sample (Thoman, 1975), and Sostek and Anders (1975) have used “nap” recordings of this duration. The videotapes were coded for all movements that occurred during that period onto a laptop computer according to the procedures we have used in our other sleep studies (Field et al., 1986). Prior to sleep state coding the examiner was trained to .90 reliability. An adaptation of Thoman’s Sleep State Criteria was used to define sleep/wake behavior and state categories (Thoman, 1975). Sleep was assessed because less quiet and more indeterminate (uncodable) sleep has been associated with greater relative right frontal EEG activation in newborns of depressed mothers (Jones et al., 1998). 1.3.9. The Brazelton Neonatal Behavior Assessment Scale The Brazelton Neonatal Behavior Assessment Scale (Brazelton, 1984) was given on the first afternoon after birth. The Brazelton assessments were performed by researchers who were trained to .90 reliability and were blind to the group classification of the mothers and infants. This neurobehavioral examination consists of 28 items, each scored on a 9-point scale, and 20 elicited reflexes, each scored on a 3-point scale. The infant’s performance was summarized according to the traditional Lester, Als, and Brazelton’s (1982) clusters, and Lester and Tronick’s (1992) depression, excitability and withdrawal factors. 1.3.10. EEG for a baseline measure of relative right or left frontal EEG activation At the neonatal stage the EEG was recorded while the infant was in a quiet alert state in a bassinet. The researcher was blind to the mother’s depression status. EEG and behavior were recorded for the typical 3 min period while the infant was awake and alert. We have reported significant 1–3 months stability of EEG asymmetry (r = .45; Jones, Field, Fox, Lundy, & Davalos, 1997) as well as significant 3-month to 3-year stability (Jones et al., 1997). At a separate time during the session the mother’s EEG was recorded while she sat quietly with her eyes open for 3 min.

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1.3.11. EEG recording The EEG for both the mother and infant were recorded using lycra stretchable caps (manufactured by Electro-Cap, Inc.) that were positioned on the subject’s head using anatomical landmarks (Bloom & Anneveldt, 1982). Electrode gel was injected into the electrodes at the following sites: F3, F4, P3, P4, T3, T4, O1, O2 and Cz for the mother and F3, F4, P3, P4 and Cz for the infant. Impedences were brought below 5 k. Additional electrodes were positioned on the external canthus and above the supra orbit of the right eye to record the subject’s EOG, which was used to determine horizontal and vertical eye movement artifacts. The EEG signals were obtained using a Grass Model 12 Neurodata Acquisition System with filters set at 1 Hz high pass and 100 Hz low pass and a gain of 20,000. Prior to data collection, the signal for each channel was calibrated. The output was directed to a Dell 325 D PC fitted with Analog Devices RTI-815 A/D board. The sampling rate was 512 samples per second, and the data were streamed across the computer screen and then saved to a hard disk using data acquisition software (Snapstream, v. 3.21, HEM Data Corp. 1991). 1.3.12. EEG analyses EEG data were analyzed using an EEG analysis software package (EEG Analysis System v. 5.3, James M. Long, 1987–1990). The first step of this process involves computing EEG off-line to derive a computer-averaged reference (mothers’ EEG only), followed by the manual elimination of sections of data that are unusable due to artifact (eye movements, muscle activity or technical difficulties). The remaining artifact-free data were spectrally analyzed using discrete Fourier transforms to yield power data for the 1–30 Hz frequency bands in 1 Hz bins. The infant EEG data were spectrally plotted, revealing that the majority of activity fell within the 3–13 Hz frequency bins. The 3–13 Hz frequency range has also been used in previous newborn EEG research (Jones et al., 1998, 1997). Data analyses were conducted on the natural log power data for both hemispheres in the frontal and parietal regions. Frontal alpha laterality ratios (FLR) were computed by obtaining the difference of the mean log power density scores of a right hemisphere site and its homologous left hemisphere site (LnRight − LnLeft; log power of F4 minus the log power of F3). A score of zero represents hemispheric symmetry, a negative score represents greater relative right frontal EEG activation and a positive score represents greater relative left frontal EEG activation. 1.3.13. Vagal tone For this measure, heart rate was recorded from the mothers and their infants for a 3 min period while the infant was in an infant seat and the mother was seated on a chair. Vagal tone was assessed by placing 3 EKG electrodes on the newborn’s chest and back and by placing 3 EKG electrodes on the mothers’ forearm and inner arms. The electrodes were connected to a Grass Model 12 Neurodata Acquisition system preamplifier with bandpass frequencies set at 1.0 and 100 Hz. and a gain of 2,000. The output was directed to a Dell 325 D PC fitted with Analog Devices RTI-815 A/D board. The data were streamed across the computer screen at a sampling rate of 512 samples per second and then saved to a hard disk using data acquisition software (Snapstream, v. 3.21, HEM Data Corp. 1991). After scoring for artifact, the EKG data were converted to inter-beat intervals (IBI) using an EKG analysis program (James Long

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Company, Caroga Lake, NY) and then to vagal tone using Delta-Biometrics, Inc., Mxedit software, which utilizes an algorithm developed by Porges (1991). 1.3.14. Classification interaction style At 3 months, each of the mother–infant dyads was videotaped for a total of 3 min during a spontaneous interaction in which the mother was to pretend that she was home playing with her infant. Three-minute interaction sessions have typically been used at the 3-month period because of the infants’ limited alertness and attention span at this age (Cohn, Campbell, Matias, & Hopkins, 1990; Field, Healy, Goldstein, & Guthertz, 1990; Tronick & Field, 1986). As is usual for these interaction sessions, the infant was placed in an infant seat on a tabletop, and the mother was seated in a chair facing the infant. Two video cameras and a split screen generator were used to simultaneously record the mother’s face and torso and the infant’s face during the interactions. The spontaneous interaction at 3 months was then used to classify the depressed mothers as intrusive or withdrawn as in our previous study (Field et al., 1990) and that by Cohn et al. (1990) on the different style depressed mothers. The classification used was as follows: (1) intrusive was defined as rough physical contact including tickling, poking, tugging, using rapid staccato actions and vocalizations and tense or fake facial expressions; (2) withdrawn was defined as flat affect, rare touching, rare vocalizing, disengaged behavior, looking away from the infant; and (3) “good interaction” classification was used when the mothers did not meet the criteria of intrusive or withdrawn and when they showed moderate amounts of smiling, touching and contingently responsive behavior as has been noted in studies on non-depressed mothers. As in our previous studies, the mothers were classified based on the simultaneous viewing of the videotapes by two researchers who classified the mothers after watching the 3-min interaction sample. Kappas averaged .84 for inter-rater reliability and test-retest reliability averaged .87. The first mothers who met criteria for these categories were entered into our data analyses until we met our sample size of 100 depressed mothers and 40 non-depressed mothers.

2. Results MANOVAs followed by ANOVAs if the MANOVAs were significant were performed for the following groups of variables: (1) prenatal self-report measures; (2) prenatal and postnatal biochemical data; (3) fetal activity and obstetric complications; (4) mother and infant physiological measures; (5) sleep–wake behaviors; and (6) Brazelton scale scores. 2.1. Group comparisons 2.1.1. Prenatal self-report data A significant MANOVA group effect (depressed intrusive, withdrawn or “good interaction” and non-depressed group assignment) for the set of prenatal self-report measures followed by ANOVAs on the individual measures suggested the following: (1) the “good interaction” depressed group versus the non-depressed group had lower approach (BAS) scores (F = 5.19, p < .05), higher depression (CESD) scores (F = 65.53, p < .001), higher anxiety (STAI)

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Table 1 Mean scores for prenatal self-report measures Variables

Approach (BAS) Inhibition (BIS) Depression (CES-D) Anxiety (STAI) Anger (POMS)

Groups Intrusive (N = 39)

Withdrawn (N = 36)

Good (N = 25)

Non-depressed (N = 40)

36.19 (10.35)a 16.67 (5.33)a 23.32 (9.06)a 44.77 (10.21)a 20.89 (9.46)a

30.43 (10.45)ab 21.21 (4.67)b 23.54 (6.79)a 44.31 (10.62)a 18.47 (9.74)a

27.96 (10.25)b 17.87 (5.04)a 19.07 (9.40)a 42.00 (11.09)a 13.07 (8.80)b

33.13 (9.65)a 17.18 (3.74)a 7.16 (3.92)b 31.42 (8.62)b 5.54 (5.35)c

Different superscripts (a, b, c, ab) denote significantly different means, for example, a is significantly different from b but ab is not significantly different from a or b.

scores (F = 18.87, p < .001) and higher anger (POMS) scores (F = 15.39, p < .001); (2) the “good interaction” depressed group as compared with the withdrawn group had lower inhibition (BIS) scores (F = 4.72, p < .05) and lower anger (POMS) scores (F = 6.31, p < .01); and (3) the “good interaction” depressed group as compared to the intrusive group had lower approach (BAS) scores (F = 4.28, p < .05) and lower anger (POMS) scores (F = 5.24, p < .05) (Table 1). 2.1.2. Biochemical data A MANOVA yielded a significant group effect. Subsequent ANOVAs on each of the biochemical variables suggested the following (Table 2): (1) the “good interaction” depressed group mothers as compared to the non-depressed group had higher prenatal cortisol (F = 4.84, p < .05), norepinephrine (F = 4.24, p < .05) and epinephrine levels (F = 4.42, p < .05) and higher postnatal norepinephrine levels (F = 4.31, p < .05), and their neonates had higher cortisol (F = 7.15, p < .001) and lower dopamine levels (F = 5.92, p < .005); (2) the “good interaction” depressed group as compared to the withdrawn group had higher dopamine levels (F = 4.99, p < .01) during the prenatal period; and (3) the “good interaction” depressed group mothers as compared to the intrusive group had higher norepinephrine levels (F = 4.24, p < .05), and their neonates had higher cortisol and lower dopamine levels (F = 3.08, p < .05). 2.1.3. Fetal activity, obstetric complications, EEG and vagal tone A significant MANOVA followed by ANOVAs on fetal activity and obstetric complications and another MANOVA on mother and infant EEG and vagal tone measures suggested the following (Table 3): (1) the “good interaction” depressed group as compared to the non-depressed group had greater fetal activity (F = 4.16, p < .05) and greater relative right frontal EEG activation in both the mothers (F = 8.23, p < .001) and newborns (F = 8.71, p < .001) and lower vagal tone in the mothers (F = 4.48, p < .05); (2) the “good interaction” depressed group as compared to the withdrawn group had less relative right frontal EEG activation in both the mothers (F = 6.21, p < .01) and newborns (F = 5.83, p < .01); and (3) the “good interaction” depressed group of newborns as compared to the intrusive group had less relative right frontal EEG activation (F = 7.38, p < .005).1

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Table 2 Means for prenatal and neonatal biochemical values (corrected for creatinine) Variables

Groups Intrusive (N = 35)

Withdrawn (N = 31)

Good (N = 22)

Mother prenatal Cortisol Norepinephrine Epinephrine Dopamine Serotonin

371.41 (188.40)a 49.79 (21.23)a 6.11 (3.34)a 332.41 (174.97)a 5336.30 (2351.22)a

374.98 (214.41)a 60.36 (25.76)ab 5.49 (4.65)a 217.51 (72.59)b 4027.28 (2923.90)a

306.65 (92.84)a 70.50 (20.77)b 6.32 (4.14)a 392.62 (139.36)a 3633.38 (1612.14)a

222.54 (97.09)b 49.11 (16.59)a 3.80 (2.45)b 373.79 (129.13)a 4813.78 (1416.35)a

Mother postnatal Cortisol Norepinephrine Epinephrine Dopamine Serotonin

200.01 (106.15)a 46.40 (21.17)a 5.27 (2.86)a 270.85 (40.47)a 4133.29 (1859.71)a

310.33 (249.99)a 54.90 (25.55)a 5.78 (2.18)a 247.16 (76.73)a 4532.70 (2259.27)a

174.25 (87.83)a 49.66 (20.94)a 3.24 (0.92)a 343.18 (157.42)a 3368.43 (1177.45)a

176.38 (93.27)a 36.07 (13.22)b 4.13 (2.91)a 315.08 (104.04)a 5279.83 (3798.20)a

Neonate

(N = 30)

(N = 26)

(N = 20)

(N = 31)

440.02 (210.45)a 97.46 (33.21)a 4.84 (2.83)a 505.62 (260.85)a 8525.78 (4578.74)a

611.48 (187.87)b 66.76 (32.67)a 4.21 (3.22)a 212.56 (160.22)b 4373.79 (3582.92)b

739.20 (255.44)b 85.23 (44.65)a 3.55 (2.88)a 234.60 (204.62)b 6921.81 (3994.41)ab

342.67 (159.50)a 81.92 (43.76)a 5.14 (3.08)a 564.62 (266.42)a 10633.37 (6745.80)a

Cortisol Norepinephrine Epinephrine Dopamine Serotonin

Non-depressed (N = 34)

Different superscripts (a, b, ab) denote significantly different means, for example, a is significantly different from b but ab is not significantly different from a or b.

Table 3 Means for fetal activity, obstetric complications and physiological measures Variables

Fetal activity Obstetric complications Frontal asymmetry mother Frontal asymmetry newborn Vagal tone mother Vagal tone newborn

Groups Intrusive (N = 32)

Withdrawn (N = 28)

Good (N = 20)

Non-depressed (N = 32)

39.12 (33.37)ab 95.04 (30.37)a −0.09 (0.16)a −0.06 (0.09)a 3.76 (0.18)a 4.36 (0.21)a

34.19 (27.94)ab 94.40 (23.20)a −0.23 (0.20)b −0.09 (0.12)a 3.89 (0.24)a 4.11 (0.24)a

43.90 (22.60)a 102.94 (19.52)ab −0.09 (0.18)a −0.02 (0.07)b 3.93 (0.16)a 4.22 (0.19)a

28.42 (18.69)b 106.34 (21.35)b 0.04 (0.10)c 0.06 (0.09)c 4.12 (0.49)b 4.76 (0.37)a

Different superscripts (a, b, c, ab) denote significantly different means, for example, a is significantly different from b but ab is not significantly different from a or b.

2.1.4. Sleep–wake behavior A significant MANOVA followed by univariate ANOVAs on the individual sleep–wake behaviors suggested (Table 4): (1) the “good interaction” depressed group as compared to the non-depressed group spent less time in the quiet alert state (F = 4.24, p < .05) and had a greater number of state changes (F = 4.39, p < .05); (2) the “good interaction” depressed group as compared to the withdrawn group spent less time in indeterminate sleep (F = 4.12,

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Table 4 Means (% time) for sleep states and activity level Variables

Deep sleep Active sleep Rem sleep Quiet alert Active alert Fussing Crying Indeterminate sleep Number of state changes Movement

Groups Intrusive (N = 29)

Withdrawn (N = 26)

Good (N = 18)

Non-depressed (N = 29)

30.31 (27.14)a 13.62 (14.00)a 21.69 (22.09)a 7.92 (14.71)a 6.08 (11.76)a 4.46 (10.01)a 5.46 (9.40)a 53.08 (22.15)a 48.51 (29.60)a 68.00 (11.00)a

42.77 (27.54)a 16.69 (12.66)a 10.31 (8.23)a 2.62 (6.29)b 4.54 (2.30)a 3.54 (5.59)a 3.08 (4.94)a 57.00 (19.09)a 58.08 (30.34)a 69.00 (13.00)a

24.83 (28.88)a 11.67 (16.61)a 6.67 (4.03)a 1.83 (4.49)b 8.00 (8.12)a 7.50 (6.66)a 9.00 (11.85)a 38.17 (18.27)b 57.83 (15.07)a 72.00 (19.00)a

25.61 (29.94)a 9.00 (10.57)a 13.70 (21.32)a 8.30 (10.88)a 6.61 (9.99)a 6.39 (10.52)a 5.09 (7.74)a 36.09 (25.53)b 32.30 (24.14)b 63.00 (18.00)a

Different superscripts (a, b) denote significantly different means, for example, a is significantly different from b.

p < .05); and (3) the “good interaction” depressed group as compared to the intrusive group spent less time in the quiet alert state (F = 5.19, p < .01) and less time in indeterminate sleep (F = 6.23, p < .005). 2.1.5. Brazelton scale scores A significant MANOVA followed by univariate ANOVAs on the individual scales suggested that (Table 5): (1) the newborns of the “good interaction” depressed group versus those of the non-depressed group had more depressive symptoms (F = 5.14, p < .01); (2) the newborns of the “good interaction” depressed group as compared to newborns of withdrawn mothers had higher scores on the Brazelton including (a) habituation (F = 4.99, p < .05), (b) orientation

Table 5 Mean Brazelton scale scores Variables

Brazelton scores Habituation Orientation Motor Range of state Regulation of state Autonomic stability Reflexes Withdrawal symptoms Excitability Depressive symptoms

Groups Intrusive (N = 30)

Withdrawn (N = 28)

Good (N = 19)

Non-depressed (N = 31)

4.87 (2.34)ab 4.09 (1.73)a 3.86 (1.39)a 3.59 (1.03)a 4.19 (1.35)a 5.60 (2.15)a 2.88 (1.96)a 3.18 (2.10)a 2.42 (1.41)a 4.47 (3.16)a

4.75 (2.38)a 3.42 (1.37)b 3.63 (1.26)a 2.97 (1.14)b 3.68 (1.62)a 5.43 (2.09)a 2.50 (1.73)a 3.80 (2.38)a 2.55 (1.57)a 4.43 (3.12)a

5.56 (1.02)b 4.01 (2.43)a 4.18 (1.28)b 3.83 (1.40)a 3.38 (2.17)a 5.54 (2.81)a 2.70 (1.39)a 3.39 (2.36)a 2.14 (1.12)a 3.88 (3.64)b

5.89 (1.74)b 4.79 (1.62)a 4.62 (1.01)b 3.97 (1.05)a 4.50 (1.44)a 6.50 (1.24)a 2.68 (2.52)a 2.56 (1.70)a 2.20 (1.84)a 2.30 (2.15)c

Different superscripts (a, b, c) denote significantly different means.

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(F = 4.20, p < .05), (c) motor (F = 4.85, p < .01), (d) range of state (F = 4.77, p < .01), and (e) less depressive symptoms (F = 6.18, p < .005); and (3) the newborns of the “good interaction” depressed mothers versus the intrusive mothers had higher Brazelton motor scale scores (F = 5.13, p < .01) and fewer depressive symptoms (F = 7.11, p < .001).

3. Discussion The profile of the “good interaction” depressed mothers and their infants is relatively complex. Like the intrusive and withdrawn mothers, the “good interaction” depressed mothers as compared to the non-depressed mothers scored higher on the depression scale (CES-D) and the anxiety scale (STAI). However, the “good interaction” depressed mothers had lower approach (BAS) scores as compared to the non-depressed group and the intrusive group, and they had lower inhibited (BIS) scores than the withdrawn group. That was not surprising inasmuch as the “good interaction” depressed group was partially defined as those who could not be classified as intrusive (low BAS scores) or withdrawn (low BIS scores). As compared to both the withdrawn and intrusive group, the “good interaction” depressed group had lower anger scores. In this sense, they are positioned somewhere between the non-depressed group and the two more traditionally recognized depressed groups, the withdrawn and the intrusive groups. But they appeared to differ more from the non-depressed than from the depressed groups at least on self-report measures. On their biochemical profile, the “good interaction” depressed group was similarly positioned between the non-depressed group and the two depressed groups. Like the other depressed groups, the mothers from the “good interaction” depressed group had a biochemical profile of elevated stress (elevated cortisol and epinephrine) during pregnancy, similar to earlier data showing elevated stress in prenatally depressed mothers (Field et al., 2001; Lundy et al., 1999). Their norepinephrine levels were unusually high, as were those of the withdrawn mothers. Unlike the withdrawn mothers however, they did not have low dopamine levels. At the neonatal stage the “good interaction” depressed mothers like the other depressed mothers had elevated norepinephrine levels, and their newborns, like the newborns of the withdrawn mothers, had elevated cortisol and lower dopamine levels. Greater relative right frontal EEG activation was noted in the “good interaction” depressed mothers and infants just as it has been noted in depressed mothers and infants in general in previous studies (Field, Fox, Pickens, Nawrocki, & Soutllo, 1995; Jones et al., 1998, 1997). However, the “good interaction” depressed mothers were less right than the withdrawn mothers, and their infants were less right than the infants of both the withdrawn and intrusive mothers. The “good interaction” depressed mothers, like the other depressed mothers, also had lower vagal tone as compared to the non-depressed mothers. Like the infants of withdrawn mothers, the infants of “good interaction” depressed mothers spent less time in the quiet alert state, and like the two other groups of newborns of depressed mothers they showed a greater number of state changes. They did not, however, show the high amounts of indeterminate sleep that were shown by the infants of the other two depressed groups. This variable was of interest because it had significantly predicted childhood IQ scores in another sample (Sigman & Parmelee, 1989).

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Despite all of the above which suggested that the “good interaction” depressed mothers and their newborns more closely matched the groups of depressed-withdrawn and depressedintrusive mothers and their newborns, the newborns of “good interaction” depressed mothers were very similar to the newborns of non-depressed mothers on the Brazelton scale. The only exception was that they showed more depressive symptoms than the newborns of non-depressed mothers, although they showed fewer depressive symptoms than the two groups of infants from the other types of depressed mothers. This behavior similarity and their lesser amounts of indeterminate sleep and their less relative right frontal EEG suggests that newborns born to the “good interaction” depressed mothers were less dysregulated. This, in turn, may have contributed to their mothers being “good interaction” partners or displaying behaviors that look more like those of non-depressed mothers. The “good interaction” depressed mothers’ interaction behaviors might also relate to their lower anger scores, their higher levels of dopamine (greater activation) and their relatively less right frontal EEG activation. Clinically, this group of infants would seem to be less at risk for developmental delays and thus in less need of early intervention than the infants of the two other depressed mother groups. However, longer interaction observations may need to be conducted for classification purposes even though 3 min has been a standard in the mother–infant face-to-face interaction literature. In addition, longer term outcome data may be needed, and more sophisticated statistical analyses such as path analyses may help determine underlying mechanisms. The data, nonetheless, highlight the importance of identifying different types of interaction styles in depressed mothers. As has been noted previously, the risk factors for the infant vary as a function of the mothers’ style of interaction. For example, infants of withdrawn mothers have been noted to have lower Bayley mental scale scores at 1 year (Hart et al., 1999). The different style mothers also appear to respond to different types of interventions. For example, intrusive depressed mothers’ frontal EEG shifts to symmetry following classical music unlike withdrawn depressed mothers (Martinez-Tornek, Field, Jones, Diego, & Hernandez-Reif, 2003). and their interactions improve especially after being asked to engage in imitative behavior (Malphurs et al., 1996). Thus, identifying the different interaction styles in depressed mothers not only enables an assessment of relative risk for the infants but also the type of intervention that might be most effective.

Note 1. Group by region (frontal vs. parietal) repeated measures MANOVAs conducted on mother and infant EEG asymmetry revealed group differences for only the frontal region.

Acknowledgments We would like to thank the mothers and infants who participated in this study. This research was supported by an NIMH Senior Research Scientist Award (MH#00331) and an NIMH merit award (MH#46586) to Tiffany Field and funding by Johnson and Johnson.

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References Bloom, J., & Anneveldt, M. (1982). An electrode cap tested. Electroencephalography and Clinical Neurophysiology, 54, 591–594. Brazelton, T. B. (1984). Neonatal Behavior Assessment Scale. Philadelphia: Lippincott. Carver, C. S., & White, T. L. (1994). Behavioral inhibition, behavioral activation and affective responses to impending reward and punishment: The BIS/BAS scales. Journal of Personality and Social Psychology, 67, 319–333. Cohn, J. E., Campbell, S. B., Matias, R., & Hopkins, J. (1990). Face-to-face interactions of postpartum depressed and non-depressed mother–infant pairs at two months. Developmental Psychology, 26, 12–23. Cohn, J. F., Matias, R., Tronick, E. Z., Connell, D., & Lyons-Ruth, K. (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. Davidson, R. J. (1998). Affective style and affective disorders: Perspectives from affective neuroscience. Cognition and Emotion, 12, 421–447. Davidson, R. J., & Fox, N. A. (1982). Asymmetrical brain activity discriminates between positive versus negative affect in human infants. Science, 218, 1235–1237. 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., Panagitotides, 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, 1058–1066. Dawson, G., Klinger, L. G., Panagitotides, H., Hill, D., & Spieker, S. (1992). Frontal lobe activity and affective behavior of infants of mothers with depressive symptoms. Child Development, 63, 725–737. Diego, M. A., Field, T., Hart, S., Hernandez-Reif, M., Jones, N., Cullen, C., Schanberg, S., & Kuhn, C. (2002). Facial expressions and EEG in infants of intrusive and withdrawn mothers with depressive symptoms. Depression and Anxiety, 15, 10–17. Diego, M. A., Field, T., & Hernandez-Reif, M. (2001). BIS/BAS scores are correlated with frontal EEG asymmetry in intrusive and withdrawn depressed mothers. Infant Mental Health Journal, 22, 665–675. Field, T. (1986). Models for reactive and chronic depression in infancy. In E. Tronick & T. Field (Eds.), Maternal depression and infant disturbance. San Francisco: Jossey-Bass. Field, T. (1995). Infants of depressed mothers. Infant Behavior and Development, 18, 1–13. Field, T., Diego, M., Dieter, J., Hernandez-Reif, M., Schanberg, S., Kuhn, C., Yando, R., & Bendell, D. (2001). Depressed withdrawn and intrusive mothers’ effects on their fetuses and neonates. Infant Behavior and Development, 24, 27–39. Field, T., Fox, N., Pickens, J., Nawrocki, T., & Soutllo, D. (1995). Relative right frontal EEG activation in 3-to-6 month old infants of depressed mothers. Developmental Psychology, 31, 358–363. Field, T., Healy, B., Goldstein, S., & Guthertz, M. (1990). Behavior state matching and synchrony in mother–infant interactions of nondepressed versus depressed dyads. Developmental Psychology, 26, 7–14. Field, T., Schanberg, S. M., Scafidi, F., Bauer, C. R., Vega-Lahr, N., Garcia, R., Nystrom, J., & Kuhn, C. M. (1986). Tactile/kinesthetic stimulation effects on preterm neonates. Pediatrics, 77, 654–658. Hart, S., Jones, N. A., Field, T., & Lundy, B. (1999). One-year-old infants of intrusive and withdrawn depressed mothers. Child Psychiatry and Human Development, 30, 111–120. Henriques, J. B., & Davidson, R. J. (1990). Regional brain electrical asymmetries discriminate between previously depressed and healthy control subjects. Journal of Abnormal Psychology, 99, 22–31. Hollingshead, A. (1975). Four-factor index of social status. New Haven, CT: Yale University. Jones, N. A., Field, T., Hart, S., Lundy, B., & Davalos, M. (2001). Maternal self-perceptions and reactions to infant crying among intrusive and withdrawn depressed mothers. Infant Mental Health Journal, 22, 576–586. Jones, N. A., Field, T., Fox, N. A., Davalos, M., Lundy, B., & Hart, S. (1998). Newborns of depressed mothers with depressive symptoms are physiologically less developed. Infant Behavior and Development, 21, 537–541. Jones, N., Field, T., Fox, N. A., Lundy, B., & Davalos, M. (1997). EEG activation in one-month-old infants of depressed mothers. Development and Psychopathology, 9, 491–505.

252

T. Field et al. / Infant Behavior & Development 26 (2003) 238–252

Lester, B., Als, H., & Brazelton, T. B. (1982). Regional obstetric anesthesia and newborn behavior: A reanalysis toward synergistic effects. Child Development, 53, 687–692. Lester, B., & Tronick, E. (1992). Neurodevelopmental battery. Unpublished scale. Littman, D., & Parmelee, A. (1978). Medical correlates of infant development. Pediatrics, 61, 470–482. Lundy, B. L., Jones, N. A., Field, T., Nearing, G., Davalos, M., Pietro, P., Schanberg, S., & Kuhn, C. (1999). Prenatal depression effects on neonates. Infant Behavior and Development, 22, 121–137. Malphurs, J., Field, T., Larrain, C. M., Pickens, J., Pelaez-Nogueras, M., Yando, R., & Bendell, D. (1996). Altering withdrawn and intrusive interaction behaviors of depressed mothers. Infant Mental Health Journal, 17, 152–160. Martinez-Tornek, A., Field, T., Jones, N., Diego, M., & Hernandez-Reif, M. (2003). Music–mood induction effect EEG in depressed, intrusive and withdrawn mothers. International Journal of Neuroscience, in press. McNair, D. M., & Lorr, M. (1964). An analysis of mood in neurotics. Journal of Abnormal Social Psychology, 69, 620–627. McNair, D. M., Lorr, M., & Droppleman, L. F. (1971). POMS profile—Profile of Mood States. San Diego, CA: Educational and Industrial Testing Services. Porges, S. W. (1991). Vagal tone: A mediator of affect. In J. A. Garber & K. A. Dodge (Eds.), The development of affect regulation and dysregulation. New York: Cambridge University Press. Radloff, L. S. (1977). The CES-D scale: A self-report depression scale for research in the general population. Journal of Applied Psychological Measures, 1, 385–401. Radloff, L. S., & Teri, L. (1986). Use of the center for epidemiological studies depression scale with older infants. Clinical Gerontologist, 5, 119–135. Sigman, Parmelee (1989, January). Longitudinal predictors of cognitive development. Paper presented at the meeting of the American Association for the Advancement of Science, San Francisco. Sostek, A. M., & Anders, T. S. (1975). Effects of varying laboratory conditions on behavioral-state organization of 2- and 8-week-old infants. Child Development, 46, 871–878. Spielberger, C., Gorsuch, R. L., & Lushene, R. E. (1970). The State Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press. Sutton, S. K., & Davidson, R. J. (1997). Prefrontal brain asymmetry: A biological substrate of the behavioral approach and inhibition system. Psychological Science, 8, 204–210. Thoman, E. B. (1975). Early development of sleeping behaviors in infants. In N.T. Ellis (Ed.), Behavior and development in infancy: Human and animal studies. New York: Wiley. Tronick, E. Z., & Field, T. (1986). Maternal depression and infant disturbance. San Francisco: Josey-Bass. Weiss, J. M., Bonsall, R., Demetrikopoulos, M. K., Emery, M. S., & West, C. H. (1998). Galantin: A significant role in depression. Annals of the New York Academy of Science, 21, 364–382. Weiss, J. M., Demetrikopoulos, M. K., West, C. H. K., & Bonsall, R. W. (1996). Hypothesis linking the noradrenergic and dopaminergic systems in depression. Depression, 3, 225–245.