INFANT BEHAVIOR AND DEVELOPMENT 20 (2), 1997, pp. 175-l 86 ISSN 01634383 Copyright 0 1997 ABLEX Publishing Corporation All rights of reproduction in any form reserved.
Infants of Intrusive and Withdrawn Mothers NANCY AARON JONES,TIFFANY FIELD, University of Miami School of Medicine
NATHAN A. Fox University of Maryland,
College Park
MARISABEL DAVALOS, JULIEMALPHURS, KIRSTENCARRAWAY University of Miami School of Medicine
SAUL SCHANBERG& CYNTHIA KUHN Duke University Medical School Two styles of mother-infant interactions have been observed in depressed mothers, including an intrusive style (overstimulating behavior) and a withdrawn style (understimulating behavior). To examine how these styles affect infants, we assessed 87 infants and their mothers, who had been assigned to “intrusive” or “withdrawn” profiles, based on their face-to-face interactive behaviors with their 3-month-old infants. Behavioral assessments were made at 3, 6, and 12 months. The results indicated that infants of withdrawn mothers showed less optimal interactive behavior, greater relative right frontal EEG asymmetry (due to decreased left frontal EEG activation and increased right frontal EEG activation), and lower Bayley Mental Scale scores at 1 year. Infants of intrusive mothers had higher catecholamine and dopamine levels, and their EEG patterns showed greater relative left frontal EEG asymmetry (due to increased left frontal EEG activation and decreased right frontal EEG activation). intrusive
withdrawn
physiology
Two styles of depressed mother behavior have been described during mother-infant interactions, including intrusive (overstimulating) and withdrawn (understimulating) behavior (Cohn, Matias, Tronick, Connell, & Lyons-Ruth, 1986; Field, Healy, Goldstein, & Guthertz, 1990). Similar profiles of maternal behavior had been reported in studies on the interactive behaviors infants and their mothers of premature (Bakeman & Brown, 1980; Field, 1977) and in the attachment literatures the presence of overstimulating and understimulating, insensitive mothering styles has also been studied (Belsky, Rovine, Taylor, 1984; Isabella, 1993; Isabella & Belsky, 1991; Pederson et al., 1990). The present study examined the differential effects of these behavior styles on infants’ behavior and development. Although infants of depressed mothers, in general, have shown social interaction problems and developmental delays, the infants of intrusive and withdrawn mothers Direct all correspondence to: Nancy Aaron Jones or Tiffany Field, Touch Research Institute, University of Miami School of Medicine, P.O. Box 016820 (D-820). Miami, FL 33101.
EEG
mother-infant
interaction
might also differ as a function of their mothers’ interaction styles. Behavior patterns displayed by intrusive and withdrawn mothers are different, and there are conflicting reports on the behavioral differences noted in the infants of intrusive versus withdrawn mothers. The attachment literature indicates that infants of insensitive and overstimulating mothers demonstrated avoidant behaviors, whereas the infants of insensitive and understimulating mothers demonstrated resistant behaviors and both groups were more likely to be insecurely attached to their mothers (Belsky et al., 1984; Isabella, 1993; Isabella & Belsky, 1991; Pederson et al., 1990). Specifically examining mothers labeled intrusive versus withdrawn, Cohn et al. (1986) reported that withdrawn mothers spent approximately 80% of their time disengaged from their infants and responded to their infants only when the infants were distressed. Intrusive mothers showed anger and irritation or roughly handled their infants 40% of the time. The infants of intrusive mothers protested less than 5% of the time but spent 55% of the time avoiding their mothers. On tk 175
176
Jones, Field, Fox, Davalos, Malphurs, Carraway, Schanberg, and Kuhn
other hand, infants of withdrawn mothers protested 30% of the time and watched their mothers less than 5% of the time. Alternatively, data from Field et al. (1990) indicated that infants of withdrawn mothers were inactive and spent a majority of their time looking around, whereas infants of intrusive mothers fussed a large proportion of the time. Knowing the differences between infants of intrusive and withdrawn mothers may suggest intervention strategies that correspond to the mother’s interaction profile. For example, a recent interaction coaching study demonstrated that coaching instructions given to depressed mothers were effective only when the mothers’ specific style of interaction was considered (Malphurs et al., 1996). Specifically, mothers showing a profile of overstimulating and intrusive behaviors elicited positive infant responses only when the instruction to “imitate your infant” (or to slow down and be less intrusive) was given. The overstimulating mothers did not elicit positive infant responses from the coaching instruction to “keep your infant’s attention.” In contrast, mothers who showed understimulating and withdrawn behaviors elicited positive infant responses from the coaching instruction asking them to get their infant’s attention and did not benefit from the instruction to imitate their infant. This study showed that specific intervention techniques tailored to the interaction profile of the mother elicited positive responses. Effective coaching behaviors were different when the mother was intrusive versus when the mother was withdrawn, indicating that infants of intrusive and withdrawn mothers show differential responses to specific elicitors. In addition to these differences in interactive behaviors, physiological differences might be expected in infants of intrusive versus withdrawn mothers. The model elaborated by Fox (1991) suggests that differences in brain electrical activity (as measured by an electroencephalogram [EEG]) have been shown to predict an individual’s tendency to approach or withdraw from novel situations. Although the specific cortical centers responsible for these differences in EEG activation are unknown, patterns of EEG activity may provide the basis for hypotheses regarding the neural substrates of certain patterns of motivated behavior. Measures of alpha suppression (less alpha power) have been used
as an index of relative cortical activation (Shagass, 1972). An asymmetry in cortical activation refers to the degree to which a specific hemisphere is differentially activated in comparison to the homologous region on the opposite side. Asymmetry scores that are positive indicate greater relative left hemisphere activation, whereas asymmetry scores that are negative indicate greater relative right hemisphere activation (Davidson, 1988). Resting EEG asymmetry has been shown to be related to depressive symptoms in adults (Tomarken & Davidson, 1989) and in infants of depressed mothers (Dawson et al., 1992; Field, Fox, Pickens, & Nawrocki, 1995; Jones, Field, Fox, Lundy, & Davalos, in press). Evidence from studies conducted by Davidson and his colleagues (Henriques & Davidson, 199 1; Sobotka, Davidson, & Senulis, 1992) have suggested that differences in EEG asymmetry scores in the right frontal region are due to reduced left hemisphere activation and associated with a deficit in approach-related processes. Infants of depressed mothers have shown greater relative right frontal EEG asymmetry (Dawson et al., 1992; Field et al., 1995). Field (1995) has suggested that this pattern of EEG activation may be a marker of physiological dysregulation in these infants. It is possible that infants will respond to differences in intrusive and withdrawn maternal styles. Similarly, infants of withdrawn mothers may adopt regulatory strategies including negative affect/distress or anger. In part, the behavioral outcome of infants of depressed mothers will be a function of the interaction of the infants’ temperament/ biological disposition and the mothers’ caregiving style. The purpose of the current study is to examine differences in behavior in interactive mothsymptoms. Different ers with depressive behaviors were expected in the infants because of the different interaction behaviors of the intrusive 2nd withdrawn mothers. Patterns of EEG activity in these infants were expected to covary with the different behaviors. Assuming that both overstimulating and understimulating maternal behavior would be stressful for the infant, elevated stress hormones (urinary cortisol and catecholamines) were also expected. Infants of depressed mothers have shown ele-
Intrusive and Withdrawn
vated cortisol and catecholamine levels in other studies (Field, 1995). In this study, we examined the interactive behavior, EEG, cortisol, and catecholamines in infants of intrusive versus withdrawn mothers. We expected that infants of intrusive mothers would be more active during interactions than infants of withdrawn mothers. We also expected that infants of intrusive mothers would show greater left frontal EEG asymmetry (increased left hemisphere EEG activation), whereas infants of withdrawn mothers would have greater right frontal EEG asymmetry (decreased left hemisphere EEG activation). Both groups of infants would have elevated urinary cortisol and catecholamine levels. METHOD Participants From a larger sample of mothers participating in an ongoing study on maternal depression and its effects on infant development, 87 mothers (6.5 who reported elevated depressive symptoms) were selected for having shown intrusive or withdrawn behavior styles during interactions with their infants at 3 months of age. During the 3-minute interaction, mothers were asked to play with their infants as they would at home. We defined intrusive behavior as: rough tickling, poking and tugging, using rapid, staccato actions, and tense or fake facial expressions. We defined withdrawn behavior as: flat maternal affect, rare touching, rare vocalizing, disengaged behaviors, and looking away from the infant. Mothers were classified into intrusive or withdrawn categories based
177
on their behavior during the face-to-face interactions af 3 months of age. Seventy-one (43 intrusive, 28 withdrawn) of the original 87 dyads returned at 6 months, and 55 (31 intrusive, 24 withdrawn) returned for the l-year visit. Demographic information and infant characteristics are shown in Table 1.
Three- and &Month Procedures Face-to-face Interaction. At both the 3- and 6-month assessments, mothers were instructed to play for 3 minutes with their infants as they would at home but without toys. Eight dyads from the withdrawn group had incomplete interactions, and two dyads from the intrusive group had incomplete interactions at the 3-month assessment At 6 months, two dyads from the intrusive and two dyads from the withdrawn group did not complete the interaction and were not included in the analysis. Also, because there was a disproportionately greater number of intrusive versus withdrawn participants, 15 randomly selected infants and their mothers were excluded from the intrusive group in the analyses. The videotaped interactions were coded by coders who were unaware of the mothers’ group status. The coders used the Interaction Rating Scale (IRS), which included ratings of both the mothers’ and infants’ behaviors (Field, 1980). The mothers’ behaviors included state, physical activity, head orientation, gaze, silence during infant gaze aversion, facial expressions, vocalizations, infantized behaviors, contingent responsivity, game-playing, and a summary score. The infants’ behaviors included state, physical activity, head orientation, gaze, facial expressions, fussiness, vocalizations, and a summary score. Coders were trained to 90% agreement on the IRS, and interobserver reliability was assessed on 30% of the videotaped interactions (K = .78). Mothers’ affect was also coded by research assistants blind to the mother’s group status. For the facial expression coding, only mothers who were videotaped directly facing
TABLE 1 Demographics of Intrusive and Withdrawn Mothers and their Infants Intrusive Group”
Birthweight
(g)
Withdrawn Groupb
M
SD
M
SD
3172
764
2879
655
Age at birth (wks)
38.1
3.6
37.9
3.5
Length
49.9
4.2
48.8
4.8
4.4
.7
4.3
.7
33.9
2.8
32.7
2.6
(cm)
SES (Hallingshead) Head Size (cm) Race (%) African-American
26
White,
Non-Hispanic
15
6
White,
Hispanic
59
70
Mother
24
BDI Scores:
3-Months
13.6
10.3
12.8
8.6
6-Months
11.1
7.8
11.6
9.0
7.6
7.4
12.4*
9.4
1 -year Nofe: Si nificance between On = 53. %n = 34. ‘p < .05 (two-tailed).
means is read across rows.
178
Jones, Field, Fox, Davalos, Malphurs, Carraway, Schanberg, and Kuhn
the camera were coded for the percentage of time they displayed sadness, anger, and anxiety. Using this strict criterion, only 12 intrusive mothers and 11 withdrawn mothers could be coded at 3 months, and two few could be coded at 6 months. The mothers who were scored using this criterion were no different from the remaining sample of mothers in their level of depression (as assessed by the Beck Depression Inventory [BDI]; Beck, Ward, Mendelson. Mach, & Erbaugh, 1961, F(1, 85) < I). The mothers were scored continuously for the 3-min interaction. No clear indications of sadness were obtained (only neutral expressions), so this category was not analyzed. Anxiety and anger were evident, and the percentage of time the mothers displayed these behaviors was used in the data analysis of the mothers’ affect. Anger was defined as any type of aggressive behavior, such as poking, prodding, grabbing, grinding teeth, or other rough interactive behaviors with the infant. It also included negative vocalizations, such as harsh tones and negative comments. Mothers were also considered angry if their facial expressions were forced and tense. Anxiety was coded when the mother was engaged in repetitive behaviors, such as snapping, clapping. repeatedly calling the infant’s name or nervous fidgeting. Mothers who paused for extended periods of time during the interaction and who looked around for the experimenter to indicate the end of the session were also coded as anxious. Coders were trained to 80% agreement on these scales, and interobserver reliability was assessed on 5% of the videotaped interactions (x = .69). EEG Recordings. A 3-min EEG recording was obtained from the mother and the infant. Mothers were told to sit very still during the recording. Infants were seated on their mothers’ lap and watched a rattle (Field et al., 1995). Thirty-four infants (20 with intrusive mothers and I4 with withdrawn mothers) and 35 mothers (20 intrusive, IS withdrawn) had usable EEG data at 3 months. Twenty-four infants (14 intrusive, 10 withdrawn) and 24 mothers (14 intrusive, 10 withdrawn) had usable EEG data at 6 months. A stretch lycra cap (Electra-Cap, Inc.) with the international IO-20 system was positioned on the participant’s head. Omni-prep gel and electrode gel were inserted into the midfrontal (F3 & F4) and parietal sites (P3 & P4) and into the vertex site (Cz). Although there is controversy about the appropriate reference location (Davidson, 1988), for the present study, the vertex reference was used because of its ease of use with infant subjects and because it has been shown to produce comparable data to other reference sites (Tomarken, Davidson, Wheeler, & Kinney, 1992). The Omni-prep gel is used to gently abrade the scalp, and the electrode gel is designed to provide good conductance. EOG was also obtained using two Beckman mini-electrodes, one placed at the outer canthus and the second placed at the supra orbit position of one eye. All electrode impedances were required to be less than 5K ohms, or the site was reabraded with the blunt end of a Q-tip until optimal impedances were obtained. The signal was passed through a Grass Model I2 Neurodata Acquisition System. The output from each amplifier was directed to a Dell 325D PC fitted with an Analog Devices RTI-815 A/D board. The sampling rate was 512 samples per second and streamed to a hard disk using data acquisition software (Snapstream, v. 3.21. HEM Data Corp., 1991).
EEG Analysis. Artifact in the EEG was underscored by using the EOG channel as a cue for eye movement artifact. The data containing eye or muscle artifact were eliminated from each channel. The data were submitted to a discrete Fourier Transform using a Hanning Window with 50% overlap (Long, 1990). This analysis provided power for each single hertz frequency bin in picowatt ohms (which is equal to a microvolt squared) for each channel. After spectral plots were made on a subsample of the infants, we determined that the 6-9 Hz band would be used. Previous research (Fox, Bell, & Jones, 1992; Tomarken & Davidson, 1989) has shown that the 69 Hz frequency band in infants of this age is similar to the characteristics of the alpha band in adults, thus we used this frequency band for the analyses. For the mother’s EEG data, we used the traditional alpha frequency band (8-13 Hz). For data obtained from both the mother and the infant, we computed frontal and parietal alpha EEG asymmetry scores using the natural log power of the scores in rhe frontal and parietal regions. The asymmetry score is a difference score, reflecting the power in one hemisphere relative to the power in the contralateral hemisphere (In[Right] minus In[Left]), with greater scores indicating more left hemisphere EEG activation. (lrine Collecfion. Immediately upon the arrival of the mother and the infant at the lab, we applied a urine bag to the infant. If the infant urinated during the lab session, we removed the bag and stored the single urine sample for later analysis. The mother was also asked to provide a single urine sample. At the 3-month visit, we were only able to obtain urine from 19 infants (10 intrusive, 9 withdrawn) and 37 mothers (20 intrusive, 17 withdrawn). At the 6-month visit, we obtained urine from 20 infants (IO intrusive, 10 withdrawn) and 35 mothers (I 8 intrusive, I7 withdrawn). The urine samples were subsequently assayed for catecholamines (norepinephrine, epinephrine, dopamine) and cortisol levels. Since these were single sample urine assays, the values were corrected using creatinine values for each subject. Volume corrections are not as precise as the creatinine correction with single samples, so the creatinine correction was used.
One-Year Procedure At the l-year assessment. we examined the child’s growth (height, weight, and head circumference) and development on the Bayley Mental and Motor Scales (Bayley, 1969).
RESULTS Three- and 6-month Interactions Infants of intrusive and withdrawn mothers were compared on their behavior ratings and affective behaviors using independent sample t test procedures. The results are presented in Table 2 and Table 3 of the 3- and 6-month interactions, respectively. At the 3-month visit, there were very few differences between the intrusive and withdrawn mothers. The withdrawn mothers received lower infantized behavior ratings, t(6 I ) = 1.95, p < .OS, and displayed more frequent anxious expressions, t(21) = 3.05, p < .Ol,
179
Intrusive and Withdrawn
whereas the intrusive mothers showed more frequent anger expressions, t(21) = 2.49, p < .02. The infants of withdrawn mothers received lower ratings on Activity, t(61) = 2.31, p < .05, Orientation, t(61) = 4.11, p < .Ol, Gaze, t(61) = 2.91, p c .Ol, and the overall Summary ratings, t(61) = 3.32,~ < .Ol. At 6 months, the withdrawn mothers had less optimal ratings on State ratings, t(49) = 2.57, p < .Ol, facial Expressions, t(49) = 2.44, p < .Ol, and the overall Summary ratings, t(49) = 2.70, p < .Ol. Their infants also received less optimal ratings on gaze t(49) = 2.97, p < .Ol, facial Expressions, t(49) = 2.66, p < .Ol, and the overall Summary ratings, t(49) = 2.88, p < .Ol. Summary of 3- and 6-Month Interaction
sions than withdrawn mothers. Withdrawn mothers also showed fewer facial expressions, a more depressed (less alert) state, less infantized behaviors, and a lower overall summary rating than intrusive mothers. Infants of withdrawn mothers showed fewer facial expressions, less gaze, less orientation toward their mothers, decreased physical activity, and a lower overall summary rating than infants of intrusive mothers. These data suggest that infants of withdrawn mothers showed lower levels of interactive behaviors than infants of intrusive mothers. Three- and 6-Month Physiological Variables
Data
The data suggest that intrusive mothers showed more angry and less anxious affective expres-
Group (intrusive versus withdrawn) x Region (frontal versus parietal) repeated-measures mul-
TABLE 2 Interactive Behavior for Infants of Intrusive and Withdrawn Mothers at 3 Months Intrusive Groupa M Mother
Interaction
Withdrawn Groupb
SD
M
SD
Ratings
State
2.6
.47
2.5
.69
Vocalizations
1.9
.72
1.9
.58
Activity
1.7
.77
1.7
.69
Orientation
3.0
.oo
2.9
.19
Gaze
2.9
.16
2.9
.19
Silence
1.5
.62
1.7
.71
Expressions
2.5
.65
2.3
.68
lnfantized
2.0
.59
1.7*
.60 .68
Contingent
1.7
.65
1.6
Gameplaying
1.4
.69
1.2
.50
Summary
2.1
.31
2.0
.29
Mother
Response
Affective
Behaviors
Anger Anxious Infant
Interaction
(% time) 40.4
23.0
6.4**
14.6
7.6
6.3
51.7**
13.4
Ratings
State
2.8
.42
2.7
.54
Activity
2.9
.31
2.6’
.56
Orientation
2.3
.68
1.8***
.77
Gaze
2.7
.52
2.0***
.67
Expressions
2.6
.54
2.4
.68
Fussiness
2.8
.42
2.6
.68
Vocalizations
2.0
.77
1.8
.73
Summary
2.6
.28
2.3’;’
.42
Note: Significance between means is read across rows. On = 36. n = 27. *p < .05, t test (two-tailed); **p < .Ol, using Bonferroni correction. ***p < ,006, using Bonferroni correction.
180
Jones, Field, Fox, Davalos, Malphurs, Carraway, Schanberg, and Kuhn TABLE 3 Interactive Behavior for Infants of intrusive and Withdrawn Mothers at 6 Months Intrusive Group0 M Mother
Interaction
Withdrawn Groupb
SD
M
SD
Ratings
State
2.6
.50
2.0**
.73
Activity
1.9
.74
1.6
.74
Orientation
3.0
.oo
2.9
.27
Gaze
2.9
.19
2.8
.33
Silence
1.5
.65
1.7
.70
Expressions
2.6
.49
2.2’
.70
Vocalizations
1.8
.63
1.6
.70
lnfantized
1.9
.68
1.6
.57
Contingent
1.8
.32
1.7
.61
Gameplaying
1.6
.80
1.4
.71
Summory
2.1
.26
1.9’
.31 .63
Infant
Response
Interaction
Ratings
State
2.7
.52
2.6
Activity
2.7
.52
2.5
.71
Orientation
2.2
.73
1.8
.88
Gaze
2.6
.49
2.1***
.72
Expressions
2.7
.48
2.2’
.77
Fussiness
2.6
.50
2.4
.76
Vocalizations
2.0
.90
1.6
.85
Summary
2.5
.26
2.2***
.50
Note: Significance between means is read across rows. On = 26. n = 25. *p c .05, t test (two-tailed), **p < .005, using Bonferroni l**p < ,006, using Bonferroni correction.
tivariate analyses of variance (MANOVAs) were conducted using the EEG asymmetry score as the dependent variable. The analysis of the mothers’ EEG revealed a main effect for region at 3 months, F( 1,33) = 4.92, p < .05, and at 6 months, F( 1,22) = 6.58, p < .05. Due to the significant differences between the frontal and parietal regions, data were analyzed separately for each region. Simple analyses of variance (ANOVA) revealed that withdrawn mothers showed greater relative right frontal EEG asymmetry, whereas intrusive mothers showed greater relative left frontal EEG asymmetry at 3 months, F( 1, 34) = 3.70, p < .05, and at 6 months, F(1, 23) = 6.00, p < .05, (see Figure 1). The analyses were not significant for the parieta1 region at 3-months F( 1, 34) < 1, or at 6 months, F(1, 23) < 1. Examination of the mothers who showed right frontal EEG asymmetry (score < 0) versus left frontal EEG asymmetry (score > 0) showed that 13 of the 20 intrusive
correction.
mothers (6 of the 15 withdrawn) had left frontal EEG asymmetry whereas 7 of the 20 intrusive mothers (9 of the 15 withdrawn) had right frontal EEG asymmetry at 3 months x2(1, N = 20) = 1.40, p > .05. At 6-months a similar pattern emerged, with 11 of the 14 intrusive mothers (4 of the 10 withdrawn) showing left frontal EEG asymmetry and 3 of the 14 intrusive mothers (6 of the 10 withdrawn) showing right frontal EEG asymmetry, x2( 1, N = 24) = 3.70, p < .05. Group (intrusive versus withdrawn) x region (frontal versus parietal) x Hemisphere (right versus left) repeated-measures MANOVAs were also conducted using the mothers’ power scores as the dependent variable. These analyses revealed a significant main effect for region at 3 months, F(1, 33) = 4.98, p < .05 and at 6 months,F(1,22)=8.10,p<.Ol.GroupxHemisphere MANOVAs were then conducted separately for the frontal and parietal regions. A significant Group x Hemisphere interaction was
Intrusive and Withdrawn
181
P-C .05. At 6 months, the infants of intrusive mothers showed significantly greater relative left frontal EEG asymmetry than the infants of the withdrawn mothers, F( 1, 23) = 3.20, p c .05 (see Figure 1). The parietal region analyses yielded no significant effects at 3 months, F(1,33) < 1, or at 6 months, F(1, 23) < 1. At 3 months, 6 of the 20 infants of intrusive mothers (8 of the 14 withdrawn) showed left frontal EEG asymmetry whereas 14 of the 20 infants of intrusive mothers (6 of the 14 withdrawn) showed right frontal EEG asymmetry, x2( 1, N = 20) < 1. At 6 months, the pattern was different, with 11 of the 14 infants of intrusive mothers (5 of the 10 withdrawn) showing left frontal EEG asymmetry and only 3 of the 14 infants of intrusive mothers (5 of the 10 withdrawn) showing right frontal EEG asymmetry, x2( 1, N = 24) = 2.1, p > .05. Group x Region x Hemisphere repeated measures MANOVAs were also conducted using the infants’ power scores as the dependent variable. These analyses revealed a significant main effect Figure 1. Frontal asymmetry of intrusive and withdrawn mothers and their infants.
obtained within the frontal region at 3 months, F(1, 33) = 4.00, p < .05, and at 6 months, F(1, 22) = 3.20, p c .05. Post hoc t tests showed that differences in the left hemisphere were significant at 3 months, t(33) = 2.40, p < .05, and at 6 months, t(22) = 2.20, p < .05 (see Figure 2). These analyses were not significant for the parieta1 region at 3 months, F( 1, 33) < 1, and at 6 months, F( I, 22) < 1. The Group x Region repeated-measures MANOVAs using the infants’ EEG asymmetry data yielded a main effect for region at 3 months, F( 1,32) = 6.5, p < .05, and at 6 months, F(1, 22) = 4.6, p c .05. Subsequent data were analyzed separately for the frontal and parietal regions. Simple ANOVAs showed that infants’ brain electrical patterns were nearly symmetrical for the infants of withdrawn mothers at both 3 and 6 months but switched for infants of intrusive mothers between the 3- and 6-month assessments. At 3 months, infants of intrusive mothers showed significantly greater relative right frontal EEG asymmetry, F( 1, 33) = 3.50,
Figure 2. Right and left frontal EEG activation of intrusive and withdrawn mothers.
182
Jones, Field, Fox, Dovalos, Malphurs, Carraway, Schanberg, and Kuhn TABLE 4 Urine Measures for Intrusive and Withdrawn Mothers Intrusive Group
3-month
urine
Withdrawn Group n
M
SD
16.0
20
45.3
17.5
17
3.2
20
6.8
1.9
17
M
SD
39.5 5.9
n
measures’
Norepinephrine Epinephrine Dopamine
330.6
69.2
20
315.1
66.2
17
Cortisol
133.3
36.4
20
135.8
31 .l
17
43.9
16.7
18
47.2
16.4
17
7.7
4.0
18
7.1
3.7
17
6-month
urine
measures’
Norepinephrine Epinephrine Dopamine Cortisol
352.1
122.0
18
343.9
88.0
25.0
18
115.8:
120.2
17
21.1
17
Note: Significance between means is read across rows. ‘p < .05, t test (two-tailed). ‘Units are nanograms per milligram (ng/mg), corrected using creatinine.
for region at 3 months, F( 1, 32) = 3.1, p < .05, and at 6 months, F( 1,22) = 8.6, p < .Ol. Group x Hemisphere MANOVAs were then conducted separately for the frontal and parietal regions. A significant Group x Hemisphere interaction was obtained within the frontal region at 3 months, F(1, 32) = 4.70, p < .05, and at 6 months, F( 1,22) = 3.90, p < .05. Post hoc t tests showed no significant group differences for either the right or the left hemisphere at 3 months, t(32) < 1. At 6 months, infants of intrusive and withdrawn mothers showed differences in left, t(22) = 6.00, p < .Ol, and in right EEG activation, t(22) = 6.20, p < .Ol, with greater left frontal EEG activation (less right frontal EEG activation) in infants of intrusive mothers (M = 56.7, SD = 26.1 versus M = 59.7, SD = 26.0, with lower power scores equal to greater activation) than in infants of withdrawn mothers (M = 40.2, SD = 11.6 versus M = 39.0, SD = 10.0). These analyses were not significant for the parietal region at 3-months, F( 1, 32) < 1, or at 6 months, F( 1, 22) < 1. Independent sample t tests were conducted on 3- and 6-month mother and infant urine samples. Although only one group difference was noted for the mothers’ data (intrusive mothers had lower urinary cortisol levels at 6 months), the infants of intrusive mothers had higher catecholamines (norepinephrine, t(18) = 2.63, p < .02, epinephrine, t( 18) = 2.29. p < .05 and higher dopamine levels, t( 18) = 3.02, p < .Ol, and tended to have higher cortisol levels,
t( 18) = 1.95, p = .06, at 6 months (see Tables 4 and 5). Summary of Physiological
Data
In general, the EEG indicate that intrusive mothers showed greater relative left frontal EEG asymmetry, whereas the withdrawn mothers showed greater relative right frontal EEG asymmetry. These findings are due to differences within the left hemisphere, with intrusive mothers showing greater left hemisphere activation and withdrawn mothers showing less left hemisphere activation. The withdrawn mothers showed higher urinary cortisol at the 6-month visit. No differences in catecholamines were obtained for intrusive and withdrawn mothers during the assessment periods. Infants of intrusive mothers showed greater relative left frontal EEG asymmetry at the 6month visit but not at the 3-month visit, whereas infants of withdrawn mothers showed greater relative right frontal EEG asymmetry at both 3 and 6 months. At 6 months, the differences ;n EEG patterns between the intrusive and withdrawn groups were in both the left and right hemispheres, with greater left hemisphere (less right) EEG activation in the infants of intrusive mothers and less left (greater right) hemisphere activation in the infants of withdrawn mothers. Infants of intrusive mothers showed higher catecholamines (epinephrine, norepinephrine), and higher dopamine levels at the 6-month visit.
Intrusive and Withdrawn TABLE 5 Urine Measures for Infants of Intrusive and Withdrawn Mothers Withdrawn Group
Intrusive Group
J-month
urine
n
M
SD
n
96.4
10
150.8
82.3
9
18.4
10
27.0
16.7
9
A
SD
171.4 26.1
measures’
Norepinephrine Epinephrine Dopomine
2817.8
1193.0
10
2347.8
1000.8
9
Cortisol
1359.4
855.0
10
683.9
619.0
9
119.8
76.8
10
49.1’;
47.3
10
19.1
9.6
10
9.4*
9.4
6-month
urine
measures’:
Norepinephrine Epinephrine Dopomine
10
1597.2
673.1
10
792.0**
622.1
10
557.4
230.0
10
270.2
178.3
10
Cortisol
Significance between means is read across rows. Note: ‘units are nanograms per milligram (ng/mg), corrected using creatinine *p c .05, t test (two-tailed), **p < .Ol , using Bonferroni correction.
1-Year Outcome Measures At the l-year assessment, mothers who were classified as withdrawn reported more depressive symptoms than the mothers who were classified as intrusive at the 3-month assessment, t(53) = 2.00, p < .05. In addition, an ANOVA revealed a significant difference between infants of intrusive versus withdrawn mothers on the Bayley Mental Development Scale, favoring the intrusive versus withdrawn group of infants (M= 108.5, SD= 15.1 versus M= 101.1, SD = 16.0), F(1, 52) = 3.70,~ < .05. There were no differences between the infants of intrusive and withdrawn mothers in their Bayley Motor scores (M = 116.4, Development Scale SD = 16.7 versus M= 117.8, SD = 15.2) F(1, 52
values.
drawn mothers, intrusive mothers showed more angry affect and withdrawn mothers showed more anxious affect. Withdrawn mothers also showed less infantized behavior at 3 months of age, and at 6-months the withdrawn mothers also exhibited a more depressed (less alert) state rating, fewer facial expressions, and overall inferior summary ratings. These data are important because early mother-infant interactions may be precursors to the infants’ interactions with other individuals later in development. Recent data, for example, have shown that intrusive mothering can lead to more aggressive and agonistic sibling interactions (Volling & Belsky, 1992). This effect may be mediated by the mothers’ angry affect during early interactions. In this study, the intrusive and withdrawn styles of the mothers were based on a 3-min interaction at 3 months of age. Other data have shown, in an independent sample of mothers and infants, that intrusive and withdrawn styles generalize to interactions with significant others (Hart, Field, Stem, & Jones, in press). The data in the present study also support the behavioral data on infants of intrusive and withdrawn mothers (Cohn et al., 1986; Field et al., 1990). Infants of withdrawn mothers versus infants of intrusive mothers showed less orientation toward the mother, more gaze aversion, less physical activity, and they received lower summary interactive ratings at 3 months of age. At the (j-month assessment, the infants of withdrawn mothers showed similar differences, but
184
Jones, Field, Fox, Davalos, Malphurs, Carraway, Schanberg, and Kuhn
also showed fewer facial expressions. These results suggest that infants of withdrawn mothers mirror their mothers’ depressive style of interaction much as in the model prepared by Field (1995). Physiological differences were also obtained between intrusive and withdrawn mothers and their infants. Research has shown that withdrawal behaviors versus approach behaviors may be related to EEG asymmetry, with greater relative right frontal EEG asymmetry associated with withdrawal and depression and greater relative left frontal EEG asymmetry associated with approach and angry/intrusive behaviors (Davidson, Schaffer, & Saron, 1985; Dawson et al., 1992; Field et al., 1995; Fox & Davidson, 1988; Henriques & Davidson, 1991; Schaffer, Davidson, & Saron, 1983; Sobotka et al., 1992). The greater relative right frontal EEG asymmetry of our withdrawn mothers is consistent with the previous studies (Davidson et al., 1983; Henriques & Davidson, 1991; Schaffer et al., 1985). The present data extend those in the literature to indicate that intrusive mothers and their infants showed greater relative left frontal EEG asymmetry. Further, the differences in EEG asymmetry were due to the differences in the left hemisphere, with greater left hemisphere EEG activation in intrusive mothers and their infants and less left hemisphere EEG activation in withdrawn mothers and their infants. The current findings provide additional evidence that there are individual differences in interactive behaviors for intrusive and withdrawn mothers which, in turn, influence the interactive behaviors of the infants. These individual differences in interactive behaviors also covary with the EEG patterns of the mothers and their infants. These behavioral patterns and their corresponding EEG patterns suggest that emotions and motivated behaviors are differentially associated with EEG activity in the frontal regions of the brain. Studies have shown that the emotions associated with approach-related motivated behaviors correspond to greater left frontal EEG activation (Sobotka et al., 1992), whereas emotions associated with withdrawalrelated motivated behaviors correspond to less left frontal EEG activation, as in the studies of depression and distress/disgust emotions (Hen-
riques & Davidson, 1991; Jones & Fox, 1992; Tomarken, Davidson, & Henriques, 1990). Infants of intrusive and withdrawn mothers also differed in their catecholamine and cortisol levels. The fact that the catecholamines and cortisol levels were greater in the infants of intrusive mothers suggests that the infants of the intrusive mothers may be experiencing more stress than the infants of the withdrawn mothers which would be consistent with the interpretation that the infants are experiencing angry feelings towards their mother. Because we did not code for angry facial expressions (using FACS criteria) in the infants of the intrusive mothers, we cannot at the present time conclude that the infants of the intrusive mothers are feeling anger. Alternatively, the withdrawn mothers and infants may simply be more depressed (as suggested by their higher CESD Scores). A recent study suggests that depression relatess more to depressed dopamine levels than to elevated norepinephrine, which could explain the data from the present study (Weiss, Demetrikopoulos, West, & Bonsall, in press). The elevated dopamine in the infants of intrusive mothers is consistent with the literature which suggests that dopamine is an activating neurotransmitter. Dopamine has been considered a pivotal neurotransmitter in the neurotransmitter model being investigated in children’s psychiatric disorders by Rogeness, Javors, and Pliszka (1992). In that model derived from a fairly extensive database on multiple kinds of children’s disorders, high norepinephrine and high dopamine are associated with normal, extroverted, high-energy traits, while high norepinephrine accompanied by low dopamine is associated with anxious inhibited, depressed behavior. In addition, the data suggest that children with elevated norepinephrine and dopamine and low serotonin levels (SHIAA) tend to have externalizing problems, suggesting that if the infants of intrusive mothers continue to have this neurotransmitter profile combined with low serotonin levels, they have externalizing problems. Although the present data show a neurotransmitter pattern that was consistent with the expectations for the infants of intrusive mothers (i.e., high norepinephrine and high dopamine), the infants of the withdrawn mothers did not have the increased norepinephrine patterns that would be expected. Within the
Intrusive and Withdrawn
present study, we did not compare the withdrawn infants to a normal control group. Thus, the withdrawn group may show elevated norepinephrine levels in comparison to a control group but not in comparison to the intrusive group. Children of withdrawn mothers demonstrated lower scores on the Bayley Mental Scale, perhaps because their mothers were showing more depressive symptoms at 1 year or because they received less stimulation during their early interactions. Less stimulation may contribute to slower language development which, in turn, would affect performance on the Bayley Mental Scale. Alternatively, the infants of intrusive mothers may be showing superior mental scores because of their higher stress levels. Thus, the infants of intrusive mothers would appear to be more “stressed” based on their biochemistry (elevated catecholamine levels and cortisol), and the infants of withdrawn mothers seem to have been disadvantaged by less stimulating interactions with their mothers and lower Bayley Mental Scale scores. More intensive longitudinal studies are needed to examine these patterns. AUTHORS’
NOTES
This research was supported by an NIMH Research Scientist Award (#MH00331) and an NIMH Research Grant (#MH46586) to Tiffany Field. We thank the mothers and infants who participated in this study. REFERENCES Bakeman, R., & Brown, J.V. (1980). Early interaction: Consequences for social and mental development at three years. Child Development, 51, 437-447. Bayley, N. (1969). Bayley Scales of Infant Development. New York: The Psychological Corporation. Beck, A.T., Ward, C.H., Mendelson, M., Mach, J.E., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561-571. Belsky, J., Rovine, M., & Taylor, D.G. (1984). The Pennsylvania infant and family development project, III: The origins of individual differences in infant-mother attachment: Maternal and infant contributions. Child Development, 55.718-728.
185
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. San Francisco, CA: Jossey-Bass. Davidson, R.J. (1988). EEG measures of cerebral asymmetry: Conceptual and methodological issues. International Journal of Neuroscience,
39,71-89. Davidson, R.J., Schaffer, C.E., & Saran, C. (1985). Effects of lateralized stimulus presentations on the self-report of emotion and EEG asymmetry in depressed and non-depressed subjects. Psychophysiology, 22, 353-364.
Dawson. G.. Klinger. L.. Pansgiotides. H.. Hill. D.. 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. Field, T. (1977). Effects of early separation, interactive deficits and experimental manipulation on infant-mother face-to-face interaction. Child Development, 48, 163-77 1. Field T. (1980). Interactions of preterm infants born ’ to lower class teenage mothers. In T. Field, S. Goldberg, D. Stem, & A. Sostek (Eds.), High risk infants and children: Adult andpeer interactions. New York: Academic. Field. T. (1995). Infants of depressed mothers. Infant Behavior and Development, 18, 1-13. Field T., Fox, N.A., Pickens, J., & Nawrocki, T. (1995). Right frontal EEG activation in 3- to 6month-old infants of depressed mothers. Developmental Psychology, 31, 358-363. Field, T., Healy, B., Goldstein, S., & Guthertz, M. (1990). Behavior state matching in motherinfant interactions of non-depressed versus depressed mother-infant dyads. Developmental Psychology, 26, 7-14. Fox, N.A. (1991). If it’s not left, it’s right: Electroencephalogram asymmetry and the development of emotion. American Psychologist, 46, 863872. Fox,N.A., Bell,M.A., & Jones,N.A. (1992). Individual differences in response to stress and cerebral asymmetry. Developmental Neuropsychology, 8, 161-184. Fox, N.A., & Davidson, R.J. (1984). Hemispheric specialization and the development of affect. In N.A. Fox & R.J. Davidson (Eds.), The psychology of affective development. Hillsdale, NJ: Erlbaum. Fox, N.A., & Davidson, R.J. (1988). Patterns of brain electrical activity during facial signs of emo-
186
Jones, Field, Fox, Davalos, Malphurs, Carraway, Schanberg, and Kuhn
tion in 10.month-old infants. Developmental Psychology, 24, 230-236. Hart, S., Field, T., Stem, M., & Jones, N.A. (in press). Depressed father’s stereotyping of infants labeled “depressed.” Infant Mental Health Journul. Henriques, J.B., & Davidson, R.J. (1991). Left frontal hypoactivation in depression. Journal of Abnormal Psychology, 100, 535-545. Hollingshead, A.B. (1975). Four-Factor index of Social Status. Unpublished Manuscript. Yale University. Isabella, R.A. (1993). Origins of attachment: Maternal interactive behavior across the first year. Child Development, 64, 605-62 1. Isabella, R.A., & Belsky, J. (1991). Interactional synchrony and the origins of infant-mother attachment: A replication study. Child Development, 62, 373-384. Jones, N.A.. Field, T., Fox, N.A., Lundy, B., & Davalos, M. (1997). EEG activation in lmonth-old infants of depressed mothers. Development & Psychopathology, 9,491-505. Jones, N.A., & Fox, N.A. (1992). Electroencephalogram asymmetry during emotionally evocative films and its relation to positive and negative affectivity. Bruin and Cognition, 20, 280-299. Long, J.M. (1990). EEG Analysis System. Caroga Lake, NY: James Long Inc. Malphurs, J.E., Larrain, C.M., Field, T., 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. Pederson, D.R., Moran, G., Sitko, C., Campbell, K., Ghesquire, K., & Acton, H. (1990). Maternal sensitivity and the security of infant-mother attachment: A Q-sort study. Child Development, 58, 1974-1983. Rogeness, G.A., Javors, M.A., & Pliszka, S.R. (1992). Neurochemistry and child and adolescent psychiatry. Journal of the American Academy of Child and Adolescent Psychiatry, 31, 765-781.
Schaffer, C.E., Davidson, R.J., & Saron, C. (1983). Frontal and parietal electroencephalogram asymmetry in depressed and nondepressed subjects. Biological Psychiatry, 18, 753-762. Shagass, C. (1972). Electrical activity of the brain. In N.S. Greenfield & R.A. Stembach (Eds.), Hundbook of psychophysiology. New York: Holt, Rinehart, & Winston. Sobotka, S.S., Davidson, R.J., & Senulis, J.A. (1992). Anterior brain electrical asymmetries in response to reward and punishment. Electroencephalography and Clinical Neurophysiology. 83, 236-247. Tomarken, A.J., & Davidson, R.J. (1989). Laterality emotion: An electrophysiological and approach. In F. Boller & J. Grafman (Eds.), Handbook of neuropsychology (Vol. 3). Elsevier Science Publishers. Tomarken, A.J., Davidson, R.J., & Henriques, J.B. (1990). Resting frontal brain asymmetry predicts affective responses to films. Journul of Personality and Social Psychology, 59, 791801. Tomarken, A.J., Davidson, R.J., Wheeler, R.E.. & Kinney, L. (1992). Psychometric properties of resting anterior EEG asymmetry: Temporal stability and internal consistency. Psychophysiology, 29, 576-592. Volling, B.L., & Belsky, J. (1992). The contribution of mother-child and father-child relationships to the quality of sibling interaction: A longitudinal study. Child Development, 63, 12091222. Weiss, J.M., Demetrikopoulos, M.K., West, C.H.K., & Bonsaii, R.W. (in press). An hypothesis linking the nonandrenergic and dopaminergic system in depression. Depression.
23 February 1996; Revised 27 September 1996 n