J. Cliihl Pmhi'l. P.\y<hiiii. Viil. .18, No. 2, p, 174-186, 1497Cambridge University Press

(£; 1'''''' Assodation lur Child Psychology and PsychiairyPrimed in Greal Britain, Alt righls reser\ed

0021

Infants of Depressed Mothers Exhibit Atypical Frontal Brain ActivityA Replication and Extension of Previous Findings

Geraldine Dawson. Karin Frey, Heracles Panagiotides. Julie Osterling and David HessIUniversity of Washington. Seattle, U.S.A.

The left frontal brain region is specialized for expression of positive emotions (e.g. joy)whereas the right frontal region is specialized forncgative emotions (e.g, sadness). Depressedadults have been found to exhibit rediieed left frontal electroencephalographic- activity. Inthis study, baseline frontal and parietal EEG activity was measured in l3-l5-month-oldinfants of depressed and nondepres.sed mothers who were of middle income with no othermajor psychiatric problems. Compared lo infant.s of nondepressed mothers, infants ofdepressed mothers exhibited reduced left frontal EEG activity. Infants of mothers withmajor depression exhibited lower levels of left frontal EEG activity than those of motherswith stibthreshold depression.

Keywords: Maternal depression. HEG activity, infants, emotion,

Ahhrcriafions: BSI: Brief Symptom Inventory: CHS D: Center for Hpidemiological Studies-Depression Queslionnaire; EEG: elcelroencephalogram: LIFE: Eongiludinal IntervalFollow-up Evaluation: SCID: Structured Clinical Interview for DSM IIIR,

IntroductionChildren of mothers experiencing depression are al risk

for a variety of behavioral and emotional difficulties,including problems in self-control, poor peer relation-ships, academic difficulties, attention problems andaffective disorder (Coghill, Caplan. Alexandra, Robson& Kumar. 1986; Downey & Coyne, 1990; Erickson,Sroufe & Egeland. 1985; Ghodsian, Zajicek & Wolkind.1984; Grun'ebaum, Cohler. Kaufman & Gallant. 1978;Orvaschel, Welsh-Allis & Weijai. 1988; Redditig,Harmon & Morgan. 1990). Indications of emotionaldifficulties can be seen as early as infancy, with infants ofniolhers experiencing depressive symptoms tending lo bewithdrawn and less aclive, and to express positive affectless frequently as compared to infants of nondepressedmothers (Field, 1992; Field el al.. 1985, 1988; Field,Healy. Goldstein & Guthertz, 1990).

The mechanisms underlying the association betweenmaternal depression and children's emotional andbehavioral difticulties are not well understood. Hypoth-eses regarding such mechanisms have focused on themother's pattern of interaction with her child and onprenatal and genetic faclors. The role of the motherinlani interaction has been supported by observationalstudies, which have consistently found that a motherexperiencing depressive symptoms is less likely to interactin an adaptive way with her infant. Mothers with elevated

Requests for reprints: Professor Geraidine Dawson, Depart-ment of Psychology, Box 351525, University of Washington,Seattle, WA 98195, U S A ,

depressive symptoms tend to have difficulty providingoptimal levels of stimulation, and display less positiveand more negative affect when interacting wiih theirinfants (Cohn, Campbell, Matias & Hopkins. 1990;Cohn, Matias. Tronick, Connell & Lyons-Ruth, 1986;Cohn&Troniek. 1989: Field et al.. 1985. 1988, 1990). Asa consequence, infants of such mothers are likely to havedifficulty in developing adequate strategies for regulatingemotional arousal (Tronick & Gianino, 1986). Also.given the contagious nature of affective responses inmother-infant inleraclion, the infant is likely to mimicthe mother's depressive affect (Field et al,, 1985. 1988).Support for other hypothesized mechanisms of trans-mission, which include factors related to the maternaldepression during the prenatal period and geneticinfluences, comes from studies of neonates born lomothers with depressive symptoms. These newborns tendto be less active and socially responsive and more irritablethan the newborns of nondepressed mothers (Field et al..1985; Whiffen & Gottlib. 1989; Zuckerman. Als.Bauchner. Parker & Cabral, 1990).

Infants of mothers with elevated depressive symptomshave also been found to exhibit atypical physiologicalpatterns, including elevated heart rates and salivarycortisol levels {Dawson. HessI & Frey. 1994; Field el al,.1988). Furthermore, Dawson and her colleagues foundthat toddlers of mothers experiencing depressivesymptoms exhibited reduced left frontal electro-eneephalographic (EEG) activity (Dawson. GroferKlinger, Panagiotides. Hill & Spieker. 1992a; Dawson.Grofer Klinger. Panagiotides. Spieker& Frey, 1992b), Inthe 1992 study. EEG recordings were taken from frontaland parietal sites during a baseline and other conditions

179

180 G, DAWSON et al.

designed to elicit positive and negative emotions. Com-pared to infants of nondepressed mothers., infants ofmothers with depressive symptoms showed reduced leftfrontal EEG activity during a baseline condition andwhile interacting with the mother. Similar findings weresubsequently reported for 3-6-month-infants of motherswith elevated depressive symptoms (Field, Fox, Pickens&Nawrocki, 1995).

Studies of normal adults (Davidson, 1984a. b, 1987;Davidson, Ekman, Saron, Senulis & Friesen, 1990;Silberman & Weingartner. 1986; Tucker, 1981) indicatethat the left and right frontal brain regions are specializedfor the expression of different emotions. Activity in theleft frontal region increases during emotions associatedwith approach toward the environment (e.g. joy, interest),whereas activity in the right frontal region increasesduring emotions associated with withdrawal (e.g. distress,sadness and disgust) (see Davidson et al., 1990; Fox,1991, for reviews). These frontal brain asymmetriesappear to be present early in life. Several studies of infantshave found increased right frontal EEG activity duringthe expression of "withdrawal" emotions, such as dis-gust, crying and sadness, and increased left frontal EEGactivity during the expression of "approach" emotionssuch as happiness (Bell & Fox, 1994; Davidson, 1994;Davidson & Fox, 1982, 1988, 1989; Dawson, 1994a, b;Dawson, Panagiotides, Grofer Klinger & Hill, 1992;Fox & Davidson, 1986, 1987, 1988; Heller, 1993).

Furthermore, adult depression has been linked to theleft hemisphere, particularly to the left frontal region.Robinson and his co-workers found that left-hemispherelesions were associated with depressive symptoms inbrain-damaged patients (Robinson & Benson, 1981;Robinson, Kubos, Starr, Reo & Price, 1984; Robinson &Stetela, 1981). Using measures of brain glucose metab-olism, Baxter et al. (1989) reported reduced left frontalactivity in depressed patients. In contrast, in a study ofregional cerebral blood flow in depressed patients,Drevets and his colleagues (Drevets et al., 1992) foundincreased activity of the left prefrontal cortex in depressedpatients. However, an analysis of individual patientsindicated that higher levels of depressive symptoms wereassociated with decreased activity in the left prefrontalcortex and increased activity of the left amygdala,Davidson and his colleagues (Schaffer, Davidson &Saron, 1983) examined patterns of EEG activity in adultswho reported elevated levels of depressive symptoms.They also found lowered levels of left mid-frontal FFGactivity in depressed subjects. Henriques and Davidson(1990) later reported that these atypical patterns offrontal EEG persisted during periods of remission insubjects with a past history of depression.

The purpose of the present study was to replicateprevious EEG findings from our laboratory indicatingreduced left frontal EEG activity in infants of depressedmothers. In the previous study, mothers were adolescentsof low income who reported depressive sytnptoms. butwho were not screened for other risk factors such assubstance abuse. The current study was based on aprimarily middle-income sample of mothers who werescreened to exclude subjects with other major risk factors.Depressed and nondepressed mothers were also matchedon a wide range of demographic variables. Maternal

depression was measured using both psychiatric diag-nostic criteria and standardized self-report questionnairesof depressive symptoms. The mother's course of illnesswas chronicled monthly from the infant's conception.Mothers were also administered a questionnaire thatassessed two emotional features that are often associatedwith depression, anxiety and hostility. In this paper, wereport on BEG data taken when the infant was in a quiet,alert state..

Method

ParticipantsRecruitment and exciusionary criteria. Mothers were

recruited from the Psychology Department infant subject pool,newspaper advertisements, and a variety of communityhospitals and clinics. Mothers were excluded if they reporteduse of street drugs (e.g. marijuana, cocaine), other drug oralcohol abuse, serious medical conditions, attendance in specialeducation classes, diagnosis of bipolar disorder, mania orpsychosis (based on the Structured Clinical Interview of theDSM-III-R), immanent suicide, significant pregnancy or birthcomplications and/or contact by Child Protective Services,Infants were excluded if they weighed less than 5 lbs at birth,were born more than 3 weeks early or late, had a history ofchronic seizures, central nervous system infection, head injury,prolonged hospitalization or chronic medical condition, sur-gery, physical malformations, sensory or motor problems,prenatal exposure to maternal drug use, foster care and/or weretaking any medication.

The final sample for the present study consisted of 117mothers and their 13-15-month-old infants (Mean infant age —13,74 months; SD = 0.5; 65 males and 52 females). The samplewas primarily European-American (93.7 Vo). The remainder ofparticipants were mixed race (3.6%), Native American (1,7%)or Asian-American (1,0%).

Diag,fwsis of depression, assessment of anxiety and hostilityand group matching variables. Fifty-four women werediagnosed as currently depressed based on the StructuredClinical Interview for the DSM-MI-R (SCID: Spitzer,Williams. Gibbon & First, 1989) and with a score of 16 andabove on the Center for Epidemiological Studies-DepressionQuestionnaire (CES-D; Radlofl", 1977). A diagnosis of de-pression was based on the presence of major depression(48,1%), double depression (3.7%), depression in partialremission (33.3%) or subthreshold depression (14,8%), Sixty-three mothers qualified for the nondepressed group. Thesemothers had scores on the CES-D below 9 and reported nocurrent or lifetime diagnosis of major depression on the SCID.In addition, mothers were administered an adapted version ofthe Longitudinal Interval Follow-up Evaluation (LIFE: Keller,Shapiro, Lavori & Wolfe. 1982: Keller et al,. 1987). which wasdesigned to assess, on a month-to-month basis, the longitudinalhistory of the mother's depression since the infant's conception.

In order to explore the role of anxiety and hostility, two otheraffective symptoms that are often associated with depression,mothers were administered the Brief Symptom Inventory (BSI,Derogatis & Melisaratos, 1983), This questionnaire has beenfound to have good test-rctcst reliability and internal cons-istency for the assessment of anxiety and hostility.

The groups of depressed and nondepressed mothers did notsignificantly differ in terms of SES level on the Hollingshead(1975) (the majority were middle class) or on maternal andpaternal education levels. Depressed mothers were, on average,2 years older (Ms = 32 and 29,9 yrs,) and less likely to bemarried (12% of depressed mothers and 1 % of nondepressed

INFANTS OF DEPRESSED MOTHERS 181

mothers were not married); these variables were used ascovariates when appropriate. Infant groups did not significantlydifferin terms ofage. gender, birth order (A/ = 1,71) or averageamount of time spent per week in daycare (M = 12.82 hours).

Procechire

EEG recording. Psychophysiologiea! testing took place inthe Developmental Psychophysiology Laboratory located inthe Child Development and Mental Retardation Center al theUniversity of Washington, While the infant was being preparedfor EEG testing, an assistant entertained the infant with toys.The infant was seated in a high chair across from a black curtainbehind which a video camera for recording infanl behavior waslocated. The EEG was recorded during a 1 min period, duringwhiL'h bubbles cascaded from behind the curtain in order tomaintain the infant's interest. The mother was seated behind herinfant: she was asked to minimize interaction and to display aneutral face if her infant looked at her.

Omni-prep was used as an abrading compound beforeattaching individual silver-silvcr-chloride electrodes to the scalpwith Grass EEG cream. Active EEG leads were at four scalplocations; left and right frontal and parietal (E3. F4, P3. P4:International 10-20 system). Parietal activity was recorded inorder to assess whether EEG dilTerences were specific to thefrontal region. Active EEG leads were referenced to linkedmastoid electrodes (identical impedances were obtained for theright and left mastoid; the mastoid with the lower Impedancewas matched to the higher one by means of a potentiometer), Aforehead electrode served as ground, EOG was recorded for off-line removal of ocular artifact via electrodes placed on theexternal canthus and supra orbit positions. All impedances werebelow 5 K£2,

Grass Neurodata Acquisition System (Model 12) was used torecord EEG. The high pass active filter was set at 1 Hz and thelow pass filter at 30 Hz. Analog-to-digital conversion was basedon a 512 points/sec sampling rate. Digitized data were storedcontinuously on an IBM PC-AT.

EEG records were edited for motor artifacts, including EOG,based on visual inspection using James Long Co, (Caroga Lake,New York) EEGEDIT software. Infants of depressed vs.nondepressed mothers did not differ in terms of the amount ofartifact-free EEG data available, A minimum of 15 sec ofartiiact-free EEG was required for inclusion in the analyses,

EEG iinalysis and measures. Discrete Fourier analyses wereperformed based on one-second epochs using custom-madesoftware developed by James Long Co. (Caroga Lake, NewYork), A Hanning window of one second, with half-secondoverlapping windows, was used. Fourier analyses were per-formed on artifact-free EHG to yield spectral power in the 3-5,6-9 and 10 12 Hz bands. Consistent with most ofthe previousresearch on EEG activity in infants (see review by Fox. 1991),analyses focused solely on the 6-9 Hz range. The 6-9 Hz bandis the dominant high-frequency band at this age and is believedto reflect infant "alpha" because its pattern of oscillation issimilar to the adult 8-13 Hz alpha rhythm (Bell & Fox. 1994:Mizuno ct al. 1970), EEG spectral power was natural log-transformed to normalize the distribution. Asymmetry scores(log right EEG power minus log left EEG power) were thencomputed to reflect relative activity of homologous right- andleft-hemisphere regions. This approach allows each subject toserve as its own control for individual differences in generallevels of FFG alpha power. Because reduced EEG alpha powerindicates increased brain activity (Steriade, 1981), negativeasymmetry scores indicate relative right-hemisphere activitywhereas positive asymmetry scores indicate relative left-hemi-sphere activity.

Behavioral coding

Infants" affective behavior during FEG recorded was codedfrom videotapes by raters blind to the mothers' diagnosticstatus. Affect ratings were based on facial expression and vocalquality. For each 10 sec period, coders made separate ratings ofnegative and positive atfect using 6-point scales adapted fromOsofsky (personal communication). The positive affect scaleranged from positive interest to squeals of laughter. Thenegative affect scale ranged from negative interest (e.g. furrowedbrow) to marked distress with screaming. Inter-rater agreementbased on double coding of 25 % of the tapes was .96 for positiveaffect and .92 for negative affect. Kappa values were ,76 and .81,respectively.

Results

Infant Affect as a Function of Mother's Diagnosis ofDepression

Between-group comparisons of infant positive andnegative affect during EEG recording indicated thatinfants of depressed and nondepressed mothersdisplayed similar affective behavior during this situ-ation. In fact, infants of nondepressed mothers had anonsignificant tendency to display slightly more negativeaffect than infants of depressed mothers [mean negativeaffect ratings = 1.18 and 1.04, respectively, ;(62.88) =1.87. p < .07], Levels of negative affect were somewhatmore variable among infants of nondepressed mothers{SD = .57) as compared to infants of depressed mothers{SD = .13), which required the use of a Mest for unequalvariances. Infants in the two groups did not differ in theamount of positive affect displayed [mean affect ratings= 2.18 and 2.27, respectively, /(104) - - . 64 , n.s.]. Theseresults suggest that it is unlikely that any physiologicaldifferences found between infants of depressed andnondepressed mothers are related to gross differences inaffective behavior during the time of EEG recording.

Infant EEG Activiiy as a Function of Mother'sDiagnosis

Figure 1 displays the mean frontal and parietal EEGasymmetry scores for infants of depressed and non-depressed mothers. A 2 {diagnostic group) by 2 (brainregion: frontal vs. parietal) analysis of variance(ANOVA) with EEG asymmetry scores as the dependentvariable yielded a significant group by region interaction[F{\, 115) - 5.18, ;7 < .025] and no main effects of groupor region.' When frontal and parietal EEG asymmetry

' Although sex differences were not predicted, exploratoryanalyses did yield a significant group x region x sex interaction(/•-= 6.16,p < .01). Separateanalyscsofthefrontaland parietalEEG asymmetry scores indicated that the sex difference wasconfined to the parietal region, Male infants of nondepressedmothers exhibited relative right parietal activity, whereas femaleinfants of nondepressed mothers exhibited relative left parietalactivity. For infants of depressed mothers, the pattern wasreversed: female infants of depressed mothers exhibited relativeright parietal activity whereas male infants exhibited relativeleft parietal activity. Because these differences were notpredicted or easily intcrpretable, we have chosen not toemphasize them until future studies replicate this finding.

182 G. DAWSON ct al.

Loo (RiflhO - Log (Lett) EEG Power Log (Right) - Log (Left) EEG Power

-0,02 •

-0.04

-0,06Nondepressed DepresBed

I Frontal Parietal

Figure I. Mean frontal atid parietal EEG asytnmetry scoresbased on EEG recordings taken from 13-15-month-old infantsof moihers with and without clinical depression. Lower asym-metry scores indicate relative right-hemisphere activation andhigher scores indicate relative left-hemisphere activatioti.

Frontal EEG Power {microvolts squared)4.3

4,25

4,15

4,1

4,05

4

- ^^mNondepresa

••1ed Depressed

Hemisphere

^ Right i ^ Left

Figure 2. Mean levels of left and right frontal and parietalEEG power exhibited by 13-15-month-old infants of motherswith and without clinical depression. Lower levels of EEGpower indicate increased levels of brain activation.

scores were analyzed separately, infants of depressedversus nondepressed mothers were found to differ signifi-cantly in their frontal EEG asymmetry scores [F(l. 115)= 8.52, p < .004] but not in their parietal EEG asym-metry scores ( F < 1.0, n.s,). Infants of depressed mothersshowed significantly lower frontal asymmetry scores thandid infants of nondepressed mothers. This effect remainedsignificant even after mother's age and marital statuswere entered as covariates in the analysis [/-(1,113) =11.29, /j<.001]. An identical pattern of" results isobtained by analyzing absolute levels of EEG power (i.e.without creating asymmetry scores). Such an analysisyields a significant group by region by hemisphereinteraction [f( 1,115) ^ 5.18,/? < .025]. As can be seen inFig. 2, which displays absolute levels of left and rightfrontal EEG power, the infant groups difter primarily interms of left frontal power.

-0.1Absent Subthreshold

Level of depression

Major

Figure 3. Mean frontal EEG asymmetry scores based on EEGrecordings taken from 13-15-month-old infants of motherswith varying levels of depression: (1) Absent no or fewdepressive symptoms; (2) Subthreshold depression ordepression in partial remission; and (3) Major depression.Lower asymmetry scores indicate relative right-hemisphereaetivation and higher scores indicate relative left-hemisphereactivation.

Subgroup Analyses Based on the Severity of MaternalDepression

Subsequent analyses examined infant EEG as a func-tion of the severity of maternal depression. According toSCID criteria, the severity of current symptoms for adiagnosis of double depression (i.e. dysthymia with majordepression) is identical to that for major depression. Adiagnosis of depression in partial remission or sub-threshold depression is given when the current symptomsare less severe or less extensive. Based on this diagnosticdistinction, two subgroups were created that reflected theseverity of depression. Group comparisons indicated thatthe three subgroups of mothers did not differ on any ofthe demographic matching variables. Interestingly, thetwo depressed subgroups also did not differ significantlyin terms of their self-report of depressive symptoms asassessed by the CES-D.

Figure 3 displays mean frontal EEG asymmetry scoresfor infants of nondepressed mothers and for the twosubgroups of infants of depressed mothers. As can beseen in Fig. 3, infants of mothers with more severedepression showed more extreme negative asymmetryscores as compared to infants of mothers with less severedepression. A trend analysis indicated a significant linearrelationship between infant frontal EEG and the severityof mother's depression [/"(I, 114) - 11.15,/?< .001].

Individual Differences in Infant Frontal EEGActivity

Figure 4 displays individual infants' frontal EEGasymmetry scores that fell one standard deviation aboveor below the mean. Positive scores are indicative of

INFANTS OF DEPRESSED MOTHERS 183

0.50 n

0.40 -

t r 0.30 -

o

S 0-22

ef

o -0.12

•^ -0.20

-0.30 -

-0.40 -

A Nondepressed

D Depressed

DD

DD

D

-0.50 -I

Eifiwe 4. Individual infants' frontal EEG asymmetry scoresfalling one standard deviation above or below the mean. Tenpercent of the infants with highly positive scores are infants ofdepressed mothers, whereas 75% of the infants with highlynegative scores are infants of depressed mothers. Lowerasymmetry scores indicate relative right-hemisphere cictivationand higher scores indicate relative left-hemisphere activation.

Infant EFG Activity a.s a Function of Timing ofMaternal Depression

Infant EEG activity was also examined as a function ofwhether mother met SCID criteria for depression duringthe prenatal and postnatal periods based on the LIFE.Three groups of mothers—nondepressed (A' = 63), post-natal only (A'= 23) and prenatal and postnatal {A =3!)—were compared using a one-way ANOVA andfrontal EEG asymmetry score as the dependent variable.This analysis yielded a significant main effect of group[F{2,]14) — 4.54. p<.0\: Mean frontal asymmetryscores were .05, —.02 and —.05 for the nondepressed,postnatal only, and prenatal and postnatal groups.respectively]. T-test comparisons between the groupsyielded a significant difference between the nondepressedgroup and the prenatal and postnatal group (/ = 2.81,;? < .01, 2-tailed) and a marginally significant differencebetween the nondepressed group and the postnatal onlygroup (/ = 1.72, p < .09, 2-tailed). The two depressedgroups did not differ significantly. Similar analysesconducted for the parietal EEG data indicated that thethree groups of infants did not differ significantly in theirpatterns of parietal EEG [F{2, 114) -0 .20 , n.s.).

The effect ofthe timing of the mothers' depression oninfants" EEG activity was impossible to separate from theeffects of the chronicity and severity of mothers' de-pression, however. Mothers who were depressed duringthe prenatal period also reported being depressed for agreater number of months during the postnatal period, ascompared to mothers who reported being depressedduring the postnatal period only. A multiple regressionanalysis showed that, after accounting for the eftect ofnumber of postpartum months of maternal depression( F = 11.81. /3 < .001), Ihc number of prepartum monthsof maternal depression was not predictive of infant frontalEEG patterns at 14 tnonlhs (F=O,I6, n.s). When theorder ofthese two variables was reversed in the regressionanalysis, the number of prenatal months of maternaldepression was marginally predictive of infant frontalEEG {F = 2.83, p < .10) and the number of postnatalmonths of maternal depression remained a significantpredictor of infant frontal EEG ( f - 8.86, p < .004).Thus, the number of postpartum months of depressionwas clearly the strongest predictor of infant frontal EEGat 14 months of age.

relatively high levels of left frontal activity and negativescores are indicative of relatively low levels of left frontalactivity. We anticipated that infants ofdepressed motherswould be under-represented in the group with highlypositive scores and over-represented in the group withhighty negative scores. This prediction was born out.Based on a sample of 54 depressed mothers and a totalsample of 117 mothers, chance alone predicted that 46%of the scores above or below one standard deviationwould represent infants ofdepressed mothers. However.only 10% (1 out oflO) of the infants wilh highly positivescores were infants ofdepressed mothers, whereas 75%(21 out of 28) ofthe infants with highly negative scoreswere infants ofdepressed mothers.

Infant EEG Activity as a Function of Mothers'' Reportof An.xiety and Hostility

Depressed and nondepressed mothers were found todiffer significantly in the levels of depression, anxiety andhostility they reported on the Brief Symptom Inventory(BSD (Depression: t = -12.58,/? < ,0001; Anxiety: t =-8 .05, / j< .0001: Hostility: ; - - 8 . 5 O , /?<.OOO1. 2-tailed). Eor the anxiety subscale. 20 of the depressedmothers and none of the nondepressed mothers hadscores in the clinically significant range. Eor the hostilitysubscale, 33 of the depressed mothers and I of thenondepressed mothers had scores in the clinically signifi-cant range.

184 G. DAWSON et al.

A series of multiple regression analyses was nextconducted in order to determine the relative influences onfrontal EEG of a diagnosis of depression vs. mother'sself-report of anxiety and hostility symptoms on the BSI.When BSI anxiety scores were entered first in a regressionanalysis, this variable was not found to be related toinfant frontal EEG asymmetry scores (r^ = .025, F =2,64, n.s.): furthermore, afteraccountingfor the variancein infant EEG attributed to anxiety, maternal depressionremained significantly related to infant frontal EEG {r'^Change = .04, F = 4.38, p < .05). Similar results wereobtained when BSI hostility scores were examined. Whenhostility scores were entered first in a regression analysis,this variable also was not found to be related to infantfrontal EEG asymmetry scores ( r = .024, F = 2.47, n.s.);again, after accounting for the variance in infant EEGattributed to hostility, maternal depression remainedsignificantly related to infant frontal EEG {r- Change =.04, F = 4 . 6 1 , /? < .05). These results suggest that theatypical patterns of infant frontal EEG were specificallyrelated to maternal depression, rather than more gen-erally related to maternal mental health problems or toother psychiatric symptoms frequently associated withdepression.

Discussion

EEG recordings taken during a quiet, alert staterevealed that infants of depressed mothers exhibitedreduced left frontal EEG activity. This pattern was mostpronounced in infants whose mothers currently metcriteria for major depression; infants whose mothers werein partial remission or who had subthreshold depressionalso displayed the atypical EEG pattern, albeit to a lesserdegree. When individual infants' patterns of frontal EEGwere examined, it was found that infants of depressedmothers were much more likely to have highly negativescores (indicative of reduced left frontal activity) andmuch less likely to have highly positive scores (indicativeof increased left frontal activity) than expected by chance.

These results replicate and extend previous findingsobtained with a different sample of mothers experiencingdepressive symptoms and their toddlers (Dawson et al.,1992a, b). The previous study was based on a ethni-cally diverse sample of low-income, adolescent motherswho were experiencing depressive symptoms. Theseyoung women were largely unmarried and were likely tobe experiencing multiple serious mental health problems,such as substance abuse, as well as the environmentalstressors that are often associated with low-incomestatus. Thus, it is possible that the atypical pattern offrontal EEG activity found in their infants was associatedwith factors other than maternal depression.This possibility is less tenable now that we have identifiedthe same pattern of brain activity in infants of adultwomen diagnosed with major depressive disorder, pri-marily of middle income and married, with no reportedalcohol, drug or other serious psychiatric condition (psy-chosis or manic-depressive disorder). Maternaldepression remains the factor common to these twodifierent samples. Moreover, the finding in the presentstudy that infant frontal EEG activity was not related to

mothers' report of symptoms of anxiety or hostilitysuggests that reduced left frontal EEG activity may bespecifically related to maternal depression, rather thanmore broadly to maternal psychopathology or othermental health symptoms often associated withdepression.

As in our previous study, infants of depressed andnondepressed mothers did not show observabledifferences in their emotional behavior during the timethe EEG recordings were made. Behavioral coding ofinfant emotional behavior indicated that the two groupsof infants displayed similar behavior during testing.Thus, the group differences in frontal EEG activity arenot easily attributable to infant emotional state at thetime the EEG recordings were made. In this context, thephysiological measures had greater sensitivity than thebehavioral measures in detecting differences betweeninfants of depressed and nondepressed mothers. It re-mains to be determined whether such measures of frontalEEG activity, taken from infants who are at risk foremotional difi^culties, index individual dififerences instable patterns of emotional behavior. Davidson and Fox(1988) have proposed that individual differences in frontalEEG asymmetry are related to differences in the basictendency to either withdraw from or approach theenvironment and in thresholds for experiencing emotionsassociated with withdrawal vs. approach. It is possiblethat the extreme patterns of reduced left frontal EEGactivity found in some of the infants of depressed mothersare related to early patterns of emotional withdrawaland other early depressive symptoms, but this remains tobe demonstrated empirically.

It is important to keep in mind that a diagnosis ofmaternal depression may comprise more than one riskfactor for the infant, including factors such as agenetically tran.smitted vulnerability to depression, bio-chemical factors related to the prenatal period, a post-natal environment with a surfeit of negative affect,disrupted social attachments and a variety of otherpsychosocial factors, such as marital conflict. Infantsmay be exposed to one or all of these factors. In fact,maternal depression following the birth of the child oftenis a continuation of prenatal maternal depression. Resultsof the present research, however, have indicated that theseverity and chronicity of postpartum maternaldepression were the strongest predictors of infant frontalEEG at 14 months; once the presence, severity andchronicity of postpartum depression were taken intoaccount, the presence of prenatal depression was notfound to be predictive of infant EEG patterns at 14months. In general, it is reasonable to expect that themore chronic and severe the mother's depression, thegreater will be the child's vulnerability lo developingpsychobiological and behavioral disturbances.

Euture research may allow us to determine whethermaternal depression during specific periods of infantdevelopment is particularly disruptive. There is evidence,for example, that maternal depression during the periodfrom 6-18 months is associated with enduring disruptionsin children's emotional development (Alpern & Lyons-Ruth, 1993; Coghill et al., 1986; Dawson et al.. 1994;Field, 1992; Wolkind, Zajicek-Coleman & Ghodsian,1980). This is a period of especially rapid emotional

INFANTS OF DEPRESSED MOTHERS 185

growth when social attachments are formed. Further-more, this is a period of accelerated growth of the frontallobe, a factor that could increase the infant's sensitivityto environmental influences on brain development(Chugani, 1994. Chugani & Phelps. 1986; Chugani.Phelps & Mazziotta, 1987; Huttenlocher. 1979. 1994).

If the atypical EEG pattern observed here arises as aconsequence of disruptions during sensitive developmen-tal periods, or due to getietic transmission, this patterncould have enduring and prognostic significance. At thistime, we do not know whether such EEG patternsexhibited by infants of depressed mothers have any long-term stability or clinical significance. Furthermore.although an association between reduced left frontalactivity and depression in adults has been found, it isunknown whether a similar relation exists during child-hood. We are currently evaluating the sample of childrenw ho participated in the present study at 3 | years of age. todetermine whether the EEG patterns observed at 14months are stable despite remission of maternal de-pressive symptoms. We are also exploring whether thereexists any relation between infant brain activity andbehavioral disturbances in infancy or later childhood.

s This work was supported by a grantfrom the National Institute of Mental Health (No. MH47I17).We wish to express our gratitude to the women and infants whoparticipated in this study and to acknowledge several peoplewho made essential conlributions: Paul Castelloe, JanSt, John.Dick McDonald and Al Ross.

References

Alpern, L. & Lyons-Ruth. K. (1993). Preschool children atsocial risk: Chronicity and timing of maternal depressivesymptoms and child behavior at school and at home.Development and Psychopalhology, 5. 371 387.

Baxter, L. R.. Schwartz, J. M.. Phelps. M. E., Mazziotta, J. C .Guzc. B. H., Selin. C. E., Gcrner, R. H. & Sumida, R. M.(1989). Reduction in prefrontal cortex glucose metabolismcommon to three types of depression. Archives of GeneralPsychialry. 46. 243-250,

Bell, M. A. & Fox. N. A. (1994). Brain development over thefirst year of life: Relations between EEG frequency andcoherence and cognitive and affective behaviors. In G.Dawson & K. Fischer (Eds.), Hunum heliavior and thedeveloping brain (pp. 314-345). New York: Guilford.

Chugani, H. T. (1994). Development aspects of regional brainglucose metabolism, behavior and plasticity. In G. Dawson& K. Fischer (Eds.). Human hetiavior and ihe developing brain(pp. 153-175). New York: Guilford Press,

Chugani, H, T, & Phelps. M, E, (1986). Maturational changesin cerebral function in infunts determined by 18FDG positronemission tomography. Science. 231, 840-843,

Chugani, H, T.. Phelps, M, E, & Mazziotta, J, C, (1987),Positron emission tomography study of human brain func-tional development. Annals of Neurology. 22. 487-497,

Coghill, S, R.. Caplan, H. L.. Alexandra, H., Robson, K, &Kumar, R, (1986), Impact of maternal postnatal depressionon cognitive development of young children, British MedicalJournal. 292. 1165-1167,

Cohn, J, F,, Campbell, S, B,. Matias. R. & Hopkins. J, (1990).Face-to-face interactions of postpartum depressed and non-

depressed mother-infant pairs at 2 months. DevelopmentalPsychology. 26, 15-23,

Cohn, J, F., Matias, R.. Tronick, E. Z,, Conncll. D, & Lyons-Ruth. D, (1986), Face-to-face interactions of depressedmothers and their infants. In E. Z. Tronick &T. Field (Eds,),Maternal depression and infant disturbance (pp, 31^5), SanFrancisco. CA: Josscy-Bass,

Cohn. J. F, & Tronick, E, Z, (1989), Specificity of infants'response to mothers' affective behavior. Journal of theAmerican Academv of Child and Adolescent Psychiatry. 28.242-248,

Davidson. R. J, (1984a), Affect, cognition and hemisphericspecialization. In C, E, Izard, J, Kagan & R, Zajonc (Eds,),Emotion, cognition and behavior (pp. 320 365), New York:Cambridge University Press.

Davidson, R, J, (1984b)- Hemispheric asymmetry and emotion,lnK, Schercr&P, Ekm-dn{E^s.). Approaches to emotion {pp.39-57), Hillsdalc. NJ: Eribaum,

Davidson, R, J, (1987). Cerebral asymmetry and the nature ofemotion: Implications for Ihe study of individual differencesand psychopathology. In R, Takahashi, P, Flor-Hcnry, J,Gruzclicr&S. Niwa(Eds,), Cerebral dynamics, laterality. andpsychopathology (pp. 71-83). New York: Elsevier.

Davidson, R. J. (1994), Temperament, affective style, andfrontal lobe asymmetry. In G, Dawson & K, Fischer (Eds,),Human behavior and the developing brain. New York:Guilford,

Davidson, R, J,. Ekman. P.. Saron, C . Senulis. R, & Friesen,W, V, (1990). Approach-withdrawal and cerebral asym-metry: Emotional expression and brain physiology 1. Journalof Personality and Social Psychology. 58. 330 341,

Davidson, R. J. & Fox. N, A. (1982). Asymmetrical brainactivity discriminates between positive versus negativeaffective stimuli in human infants. Science. 218, 1235- 1237.

Davidson. R, J, & Fox. N. A, (1988), Cerebral asymmetry andemotion: Development and individual differences. In S.Segalowitz & D, Molfcsc (Eds.). Developmental implicationsof brain laterali=ation (pp, 191-206), New York: Guilford,

Davidson, R. J, & Fox, N, A. (1989). Frontal brain asymmetrypredicts infants" response to maternal separation. Journal ofAbnormal Psychology. 98. 127-131.

Dawson. G. (1994a), Frontal electroenccphalographic corre-lates of individual differences in emotional expression ininfants: A brain systems perspective on emotion. In N. A,Fox (Ed.), Emotion regulation: Behavioral and biologicalconsiderations. Society for Research In Child DevelopmentMonographs. 59 (2-3), 135-151,

Dawson. G. (1994b), Development of emotional expression andemotion regulation in infancy: Contributions of the frontallobe, !nG. Dawson &K, Fischer (Eds.), Human behavior andthe developing brain (pp. 346-379), New York: GuilfordPress,

Dawson. G., Grofcr Klinger, L.. Panagiotides, H,. Hill, D, &Spieker, S. (1992a). Frontal lobe activity and alTectivebehavior of infants of mothers with depressive symptoms,Child Development, 63. 725 737,

Dawson, G,, Grofer Klinger, L,, Panagiotides. H,. Spieker. S,& Frey. K, (1992b), Infants of mothers with depressivesymptoms: Electrophysiologica! and behavioral findingsrelated to attachment status. Development and Psyeho-pathotogv. 4, 67-80.

Dawson. G,. Hessl. D. & Frey. K. (1994). Social influences onearly developing biological and behavioral symptoms relatedto risk for affective disorder. Development and Psychopath-ology. 6. 159-119.

Dawson, G.. Panagiotides, H,, Grofer Klinger, L, & Hill, D,(1992), The role of rrontal lobe functioning in the devel-opment of self-regulatory behavior in infancy. Brain andCognition. 20, 152-175.

186 G. DAWSON et al.

Derogatis. L. R, & Melisaratos. N. (1983). The Brief SymptomInventory: An introductory report. Psychological Medicine.!3. 595-605,

Downey, G. & Coyne. J. (1990). Children of depressed parents:An intcgrative review. Psychological Bulletin, 108. 50-76.

Drcvcts, W, C . Videen. T. O., Price, J. L,, Preskorn. S. H.,Carmichael, S. T, & Raichle. M. E, (1991), A functionalanatomical study of unipolar depression. The Journal ofNeuroscience. 12. 3628-3641,

Erickson, M,, Sroufe. L. A, & Egeland. B. (1985) The re-lationship between quality of attachment and behaviorproblems in preschool in a high-risk sample. In 1. Brcthcrton& E, Waters (Eds,), Growing points of attachment theoryand research. Society for Research in Child DevelopmentMonographs, 50 (1-2), 147-166.

Field, T, (1992). Infants of depressed mothers. Development andPsvchopathology. 4, 49 66,

Field. T.. Fox, N,'. Pickens. J. & Nawrocki, T, (1995), Relativeright frontal EEG activation in 3-6-month-oid infants of"depressed" mothers. Developmental Psychology 31.358-363,

Field, T.. Hcaly, B., Goldstein. S, & Guthertz, M. (1990).Behavior-state matching and synchrony in mother-infantinteractions of nondepressed versus depressed dyads. De-velopmental Psychology. 26. 7-14.

Field. T,, Healy. B,, Goldstein. S., Perry, S,, Bendall. D,.Schanberg, S,, Zimmerman, E, & Kuhn. C, (1988), Infants ofdepressed mothers show "depressed" behavior even withnondepressed adults. Child Development, 59. 1569-1579.

Field, T., Sandberg. D,. Garcia, R,, Vega-Lahr, N.. Goldstein,S. & Guy, L. (1985), Prenatal problems, postpartum de-pression, and early mother-infant interactions. Developmen-tal Psychology. 12, 11 52-1156,

Fox. N, A, (1991), If it's not left, it's right: Elcctro-encephalograph asymmetry and the development ofemotion, American Psychologist. 46. 863-872,

Fox, N, A. & Davidson, R, J. (1986). Taste-elicited changes infacial signs of emotion and the asymmetry of brain electricalactivity in human newborns, Neuropsychologia. 24. 417-422,

Fox, N. A, & Davidson, R, J, (1987). Electroencephalogramasymmetry in response to the approach of a stranger andmaternal separation. Developmental Psychology. 23, 233-240.

Fox, N, A. & Davidson, R. J. (1988). Patterns of brain electricalactivity during facial signs of emotion in lO-month-oldinfants. Developmental Psychology. 24. 230-236.

Ghodsian, M,. Zajicek. E, & Woikind, S, (1984), A longitudinalstudy of maternal depression and child behavior problems.Journal of Child Psychology and Psychiatry. 25. 91 109,

Grunebaum. H. U., Cohler, B, J,. Kaufman," C. & Gallant. D,H. (1978). Children of depressed and schizophrenic mothers.Child Psychiatry and Human Development. H, 219-228,

Heller. W, (1993). Neuropsychological mechanisms of indi-vidual differences in emotion, personality, and arousal.Neuropsychology. 7, 476-489,

Henriques, J, B, & Davidson. R. J, (1990). Regional brainelectrical asymmetries discriminate between previously de-pressed subjects and healthy controls. Journal of AbnormalPsychology. 99. 22-31,

Hollingshcad, A, B, (1975). Form factor index of social status.Unpublished manuscript, Yale University,

Huttenlocher. P, R. (1979). Synaptic density in human frontalcortex—developmental changes and effects oi aging. BrainResearch. 163. 195-205,

Huttenlocher, P, R. (1994). Synaptogenesis in human cerebralcortex. In G. Dawson & K, Fischer (Eds,), Human behaviorand the developing brain (pp, 137-152), New York: Guilford,

Keller, M. B,. Lavori. P.. Friedman, B., Nielsen. E.. Endicott,

J,, McDonald-Scott, P, & Andreasen, N. C, (1987). Thelongitudinal interval follow-up evaluation: A comprehensivemethod for assessing outcome in prospective longitudinalstudies. Archives of General Psychiatry, 44, 540-548.

Keller, M B , , Shapiro. R. W, Lavori. P. W, & Wolfe, N.(1982), Recovery in major depressive disorder: Analysis withthe life table and regression models. Archives of GeneralPsychiatry, 39, 905-9] 5.

Mizuno. T.. Yamauchi, N., Watanabe. A.. Komatsushiro, M,,Takagi, T., Iinumi, K, & Arakawa, T, (1970), Maturation ofpatterns of EEG: Basic waves of healthy infants under 12months of age. Tohoku Journal of Experimental Medicine.102. 91-98.

Orvaschel, H., Welsh-Allis. G, & Weijai. Y, (1988), Psycho-pathology in children of parents with recurrent depression.Journal of Abnormal Child Psychology, 16, 17-28,

Radloff, L. S. (1977). The CES-D scale; A self-report depressionscale for research in the general population. Applied Psvclio-logical Measurement, I. 385-401,

Redding, R, E,, Harmon. R, J, & Morgan. G, A. (1990),Relationships between maternal depression and infants'mastery behaviors. Infant Behavior and Development. 13,391-395.

Robinson. R. G, & Benson, D, F, (1981), Depression in aphasicpatients: Frequency, severity and clinical-pathological corre-lations. Brain and Language. 14. 282-291,

Robinson. R. G., Kubos, K. L., Starr, L, B.. Reo, K, & Priee.T. R, (1984), Mood disorders in stroke patients: Importanceof location of lesion. Brain. 107, 81 93.

Robinson. R, G, & Stetela, B. (1981), Mood change followingleft hemispherie brain injury. Annals of Neurology, 9,447^53,

Schaffer. C, E.. Davidson. R, V, & Saron, C. (1983), Frontaland parietal electroencephalogram asymmetry in depressedand nondepressed subjects. Biological Psychiatry. 18.753-762.

Silberman, E, K, & Wdngartner. H. (1986). Hemisphericlateralization of functions related to emotion. Brain andCognition, 5. 322-353.

Spitzer, R, L.. Williams. J. B,, Gibbon, M. & First. M. (1989).Structured Clinical Interview for DSM-HI-R {with psychoticscreen). Biometric Research Department, New York StatePsychiatric Institute. New York,

Steriade, M. (1981). EEG desynchronization is associated withcellular events that are prerequisites for active behavioralstates. Commentary on " Reticulo-cortical activity andbehavior. A critique of the arousal theory and a newsynthesis" by C. H. Vanderwolf & T, E, Robinson. TheBehavioral and Brain Sciences, 4. 489—492,

Tronick, E, Z, & Gianino. A. F. (1986). The transmission ofmaternal disturbances to the infant. In E. Z. Tronick & T,Field (Eds.), Maternal depression and infant disturbance (pp.5-11). San Francisco. CA: Jossey-Bass.

Tucker, D. M. (1981). Lateral brain function, emotion andconceptualization. Psychological Bulletin. 89. 19-46.

WhifTen, V, E, & Gottlib, 1. M, (1989), Infant of postpartumdepressed mothers: Temperament and cognitive status.Journal of Abnormal Psychology. 98. 274-279,

Wotkind. i. N,. Zajicek-Coleman, E. & Ghodsian, M, (1980).Continuities in maternal depression. International Journal ofFamily Psychiatry, 1. 167 182,

Zuckerman, B,, Als, H,, Bauchncr. H,. Parker, S, & Cabral, H.(1990), Maternal depressive symptoms during pregnancy andnewborn irritability. Developmental and Behavioral Pedi-atrics, II, 190-194,

Accepted manuscript received 28 June 1996