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Patterns of brain electrical activity in


infants of depressed mothers who
breastfeed and bottle feed: the mediating
role of infant temperament.

ARTICLE in BIOLOGICAL PSYCHOLOGY NOVEMBER 2004


Impact Factor: 3.47 DOI: 10.1016/j.biopsycho.2004.03.010 Source: PubMed

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Biological Psychology 67 (2004) 103124

Patterns of brain electrical activity in infants of


depressed mothers who breastfeed and bottle feed:
the mediating role of infant temperament
Nancy Aaron Jones , Barbara A. McFall, Miguel A. Diego
Florida Atlantic University at Jupiter, 5353 Parkside Drive, Jupiter, FL 33458, USA

Abstract

Successful breastfeeding involves a dyadic interaction between a mother and her infant. The present
study was designed to examine the association between breastfeeding and temperament in infants of
depressed mothers. Seventy-eight mothers, 31 who were depressed, and their infants participated.
Depressed mothers who had stable breastfeeding patterns were less likely to have infants with highly
reactive temperaments. Multivariate analyses of variances (MANOVAs) showed that infants of de-
pressed mothers who breastfed did not show the frontal asymmetry patterns, i.e., left frontal hypoac-
tivity, previously reported. Moreover, breastfeeding stability, even in depressed mothers, was related
to more positive dyadic interactions. Finally, a model was supported, in which the effects of maternal
depression on infant feeding are mediated by infant frontal EEG asymmetry and infant tempera-
ment. These findings could provide a foundation for developing intervention techniques, employing
breastfeeding promotion and support, directed toward attenuating the affective and physiological
dysregulation already noted in infants of depressed mothers.
2004 Elsevier B.V. All rights reserved.

Keywords: Frontal EEG asymmetry; Emotion; Breastfeeding; Temperament; Infancy

1. Introduction

In 1997, the American Academy of Pediatrics recommended that women breastfeed their
infants for the first year of life (Gartner, 1998) increasing interest and rates of breastfeeding.
However, a substantial portion of women, especially depressed women, do not choose to

Corresponding author. Tel.: +1-561-799-8632; fax: +1-561-799-8535.


E-mail address: njones@fau.edu (N.A. Jones).

0301-0511/$ see front matter 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.biopsycho.2004.03.010
104 N.A. Jones et al. / Biological Psychology 67 (2004) 103124

breastfeed or do so for relatively short periods of time (Field et al., 2002a; Galler et al.,
1999). Investigators are now compelled to examine the factors that are associated with the
benefits of sustained breastfeeding and to examine whether breastfeeding can benefit the
physiological and affective development of infants. Moreover, it is important to investigate
whether breastfeeding has positive or negative effects on the affective development of in-
fants of depressed mothers. Previous research has consistently demonstrated that infants of
depressed mothers are at increased risk for physiological and affective dysregulation (Field,
1995; Jones et al., 1998) necessitating further inquiry into the benefits of breastfeeding for
these infants. In this study, we attempted to examine whether the dysregulated affective
and physiological development, noted in infants of depressed mothers, was also evident in
infants of depressed mothers with sustained breastfeeding patterns.
Little is know about patterns of breastfeeding in depressed mothers, and it is likely that
what may be true of other adults who breastfeed does not hold for breastfeeding depressed
mothers. Depressed mothers have been less likely than other adults to choose to breast-
feed (Galler et al., 1999; Milligan et al., 1990), making it unclear whether breastfeeding
can benefit depressed mothers and their infants. Until recently, inquiry into the benefits
of breastfeeding to infants of depressed mothers was largely precluded by a scarcity of
research participants since breastfeeding has been more prevalent among psychologically
non-symptomatic, college-educated, middle-class women whose infants are at low risk for
adverse outcomes. However, due to the resurgence of cultural acceptance of breastfeed-
ing and the enhanced understanding of the physiological importance (Newman, 1995),
depressed mothers are now choosing to breastfeed.
Besides the wealth of research that has touted the physiological benefits of breastfeeding
on infant health, a number of studies have also assessed the emotional benefits of breastfed
compared to bottle fed motherinfant pairs. In parallel with earlier findings highlighting
greater reciprocity and affection during breastfeeding (Bernal and Richards, 1970; Dunn
and Richards, 1977), recent research has also demonstrated (Lavelli and Poli, 1998) that
breastfeeding mothers provide their neonates with less auditory stimulation, but more visual
gaze and tactile stimulation. In addition, investigations probing whether the experiences
entailed by breastfeeding extend beyond the feeding context have been addressed only
rarely. One study compared dyadic interactions of breastfeeding versus bottle-feeding adult
mothers in play situation (Kuzela et al., 1990) and reported that breastfeeding mothers
touched their infants more frequently, suggesting the benefits of breastfeeding extend to
other contexts.
Previous research has typically focused on the characteristics of the mother and her likeli-
hood for continued breastfeeding (Mezzacappa and Katkin, 2002; Mezzacappa et al., 2002;
Pugh, 1998) while relative few studies have examined the effects of infant characteristics
on breastfeeding. Of those studies that have measured infant behavior, researchers have
reported that breastfed newborns are more irritable but show more optimal physiological
organization (Dipietro et al., 1987; Zeskind et al., 1992). However, later in infancy, breast-
fed infants are reported to be more active, temperamentally easier, less irritable, more
positive, and more sociable (Field et al., 2002a; VanDiver, 1997; Worobey, 1992, 1998).
These data suggest that breastfeeding may be beneficial to the infant, yet the newborn may
not manifest overt behavioral signs that promote continued breastfeeding. This issue is
even more important for depressed mothers because these mothers are less likely to feel
N.A. Jones et al. / Biological Psychology 67 (2004) 103124 105

competent in caring for their infants (Field et al., 2002a). Therefore, if their newborn re-
sponds with elevated distress to breastfeeding, depressed mothers are more likely to dis-
continue breastfeeding.
Examination of the factors that promote breastfeeding and those that act as barriers to
sustained breastfeeding should also focus on the role of infant temperament. We adhere to
a definition of temperament that involves behavioral reactivity and regulation as a function
of tonic biological and/or physiological patterns. Moreover, we contend that we are able
to understand variations in temperament by analyzing the manner in which emotions are
expressed and regulated during infancy (Calkins et al., 1996; Fox, 1994; Fox et al., 1994;
Goldsmith et al., 1987). Our own studies, and those of others (Dawson et al., 1997), have
suggested that newborns and infants of depressed mothers demonstrate greater dysregulated
affective and physiological patterns (Jones et al., 1997a, 1998; Lundy et al., 1999). Findings
from these studies have consistently found that infants of depressed mothers show greater
right frontal EEG asymmetry, lower vagal tone, more dysregulated biochemical patterns,
more disorganized behavioral, and sleep patterns. Collectively, these data suggest that infant
bio-behavioral regulation patterns, associated with maternal depression, may lead to a neg-
ative temperamental bias that is likely to influence later development and may predispose
the child for later affective disorders (Field, 1995).
Early in infancy, parental behaviors are primarily focused on care taking. Opportuni-
ties for breastfeeding benefits are likely warranted to ameliorate the negative behavioral
and physiological patterns already identified in infants of depressed mothers. However, we
know of no other studies that have examined infants of depressed mothers and the potentially
positive outcomes that may be garnered by exposing them to stable breastfeeding patterns
during infancy. Within the present study, we examined whether stable breastfeeding patterns
in depressed mothers were associated with attenuated negative developmental patterns in
their infants. We also examined additional factors that may be related to the positive out-
comes, whether affective bonding was increased as a result of stable breastfeeding, whether
infants were physiologically benefited by breastfeeding, and whether mothers perceptions
of their infants temperament and their behaviors were associated with feeding stability and
depression status.
The purpose of the present study was to examine breastfeeding in infants of depressed
mothers. Specifically, we examined individual differences in infant temperament (positive
and negative) that may be related to stable breastfeeding patterns in depressed mothers,
including infants physiological and behavioral reactivity, and the dyads socio-emotional
interaction patterns. Our goal was to determine whether each factor was associated with
breastfeeding stability and whether stable breastfeeding in depressed dyads was associ-
ated with attenuated negative outcomes. We hypothesized that maternal depression and
more negatively reactive infant temperament would be associated with a shorter duration
of breastfeeding. Second, we expected that depressed mothers who discontinued breast-
feeding by 3 months of age (or never breastfed) would have infants who show the greatest
dysregulation, in affective regulation and physiological activity. Third, we expected that
depressed mothers who continued breastfeeding would report more positive perceptions
of their infants temperament and would demonstrate greater mutual interactive behaviors
with their infants. Finally, we tested a model that examined the direct and indirect effects
of maternal depression on infant temperament, infant EEG activity, and feeding behaviors.
106 N.A. Jones et al. / Biological Psychology 67 (2004) 103124

Infant
Infant EEG Temperament
(positive
asymmetry
responsive-ness
during interaction)

Maternal
Depression
Score Duration
Breastfeeding

Fig. 1. Hypothesized model.

We hypothesized that the effects of maternal depression on feeding patterns are mediated
by infant frontal EEG activity and infant temperament (Fig. 1).

2. Method

2.1. Prescreening

Initially, hospital intake information (documenting demographic, feeding, and infant


health information) was used to obtain a sample of new mothers who fit the predefined
criteria. For the present study, we concentrated our efforts on obtaining middle class (mean
of 23 on Hollingshead scale (Hollingshead, 1975), adult (age: 2039 years) women with
healthy (>9 on 5 min APGAR), full-term (>37 weeks gestation) infants. We choose to re-
cruit a middle-class, healthy infant sample to rule out other possible confounds (Buxton
et al., 1991; Cooper et al., 1993). In order to expedite recruitment of depressed participants,
only mothers who received high scores (>16) or low scores (<12) on the Center for Epi-
demiological Studies Depression Scale (CES-D; Radloff, 1977) were asked to participate in
laboratory assessments. Mothers who were eligible at the newborn period were interviewed
over the phone at 1 month on the CES-D to confirm their depression status and to schedule
a laboratory session. The mothers and infants who participated in this study were drawn
from 232 hospital and telephone questionnaires conducted.

2.2. Participants

Seventy-eight mothers and their infants participated in the laboratory assessments at 1


month and 62 (77.5%) returned for the 3-month visit. Families were predominantly White
(four African Americans, two Hispanic and one Asian American), middle to upper-middle
class (Hollingshead mean = 2.32, S.D. = 0.80, range = 13). Mothers were adult (mean
age = 32.20 years, S.D. = 5.04 years) and married (93.5%), with one to three children.
Approximately half of the mothers were employed outside the home (44.2%). Infants (39
females and 39 males) were assessed at 1 month (mean = 35.99 days, S.D. = 5.70 days)
N.A. Jones et al. / Biological Psychology 67 (2004) 103124 107

Table 1
Mother and infant demographics
Measure Depressed Non-depressed

Breastfeedinga Bottle feedingb Breastfeedingc Bottle feedingd

Infant variables
Female (%) 26.7 68.8 51.7 55.6
Age (days)
One month 36.80 (5.87) 32.62 (4.63) 36.69 (6.23) 36.83 (4.82)
Three months 93.78 (8.32) 94.00 (2.24) 91.87(10.64) 95.30(11.05)
Maternal variables
Age (years) 33.60 (5.99) 31.06 (5.43) 32.37 (4.97) 31.78 (7.78)
SES (Hollingshead) 2.67 (0.79) 2.43 (0.81) 2.14 (0.84) 2.55 (0.70)
Marital status (percentage 93.3 93.8 96.4 94.4
of married)
Parity (percentage of 66.7 75.0 66.3 66.6
multiparous)
CES-D
One month 19.00 (2.53) 19.27 (6.11) 5.07 (3.28) 6.50 (3.45)
Three months 7.50 (4.32) 16.90 (6.48) 4.54 (3.44) 3.73 (3.39)
Note. Values represent mean scores. Standard deviations are in the parentheses.
a n = 15.
b n = 16.
c n = 29.
d n = 18.
P < 0.001.

and at 3 months (28 females and 34 males, mean = 92.66 days, S.D. = 9.19 days) of age.
There were no differences between the depression and feeding groups on their demographic
characteristics (Table 1).

2.3. Measures

The CES-D is a 20-item questionnaire used to assess depressive symptoms in a community


sample. Scores range from 0 to 60 and a score of greater than 16 has been shown to differ-
entiate clinical depression from non-depressed status. The CES-D has a 6.1% false-positive
rate and a 36% false-negative rate (Myers and Weissman, 1980), however, we obtained ad-
ditional information on maternal depression status from the Diagnostic Interview Schedule
(DIS; Robins et al., 1981). The DIS was used to screen out participants who were mildly
depressed. Extensive testing has shown that the DIS has good psychometric properties
(Costello et al., 1984, 1985) and it can be used by lay persons to assess depressive symp-
toms. Participants who received high scores on the CES-D and who had elevated symptoms
(consistent with dysthymia or major depressive disorder) on the DIS were assigned to the
depressed group. Approximately 20 mothers (22% of those contacted) had elevated CES-D
scores but were not assigned a diagnosis on the DIS. These mothers were not included in
the data analyses for the present study. Non-depressed mothers were chosen based on their
low CES-D scores (<12) and a negative personal and family history of depression.
108 N.A. Jones et al. / Biological Psychology 67 (2004) 103124

Feeding status was also assessed at the newborn, 1- and 3-month assessments. Mothers
were queried about their plans to use a specific feeding technique (and for how long), their
current manner of feeding their infant, and their rational for using that feeding technique.

2.4. Laboratory procedures at 1 and 3 months

Upon arrival at the lab, mothers signed a consent form, and completed a demographic and
feeding inventory, a CES-D, the DIS (if appropriate), and an infant temperament inventory
(Infant Behavior Questionnaire (IBQ); Rothbart, 1981). During this time, a research assistant
administered the Brazelton Neonatal Behavioral Assessment Scale (BNBAS; Brazelton and
Nugent, 1995) to examine the infants behavioral abilities during environmental interaction.
The Brazelton examiners were trained to 0.90 reliability. Seven infants did not complete the
entire Brazelton assessment. Following this assessment, mothers were asked to play with
her infant as she would at home. This face-to-face interaction lasted for 3 min and both
mothers and infants were videotaped during this procedure.
Baseline EEG activity was recorded from infant participants during a quiet, alert state.
The EEG activity was recorded while the infant was held by his/her mother or sitting in an
infant seat. EEG recordings were for 56 min in duration. Five infants (three at 1 month and
two at 3 months) would not tolerate the cap placement. In addition, five infants at 1 month
and four infants at 3 months had unusable data. Thus, a final sample of 70 infants had 1
month EEG data and 53 infants had EEG data at both 1 and 3 months.
Identical assessments were obtained at the 3-month visit, except the Infant Neurological
International Battery (Infinib; Ellison et al., 1985) was used as the developmental assessment
and an arm restraint procedure was performed at 3 months. The Infinib is designed to assess
the neurological integrity of infants based on 20 items with 5 factors (spasticity, vestibular
function, head and trunk ability, French angles, and leg function). This test is easy to
administer and has sufficient reliability for clinical and research purposes (Ellison et al.,
1985). For this study, the total score was computed and then standardized. This score used
to verify normal neurological function across groups. All groups were similar in their scores
(P > 0.05) and all infants were in above the above the abnormal cut-off score of 48.
The arm restraint task is modeled after the one described by Stifter and Braungart (1995)
and Stifter and Jain (1996). Stifter and her colleagues have used this task to examine tem-
peramental reactivity and the infants ability to regulate during a mildly frustrating task.
Infants are seated in an infant seat. Mothers sit in a chair facing her infant. Mothers are
instructed restrain their infants arms by the sides of their body for approximately 2 min.
The arm restraint is discontinued if the infant was distressed for 20 s. Mothers are also
instructed to maintain a neutral facial expression (or to look away from their infant if they
cannot remain neutral) and to remain silent during the procedure. Afterward the mother is
instructed to hold or sooth her infant. Three mothers and their infants did not complete this
task during the lab session.

2.5. Coding of mother and infant behaviors

Video recordings of 3 min, motherinfant interactions were coded on a second-by-second


basis. We modeled our coding schemes for the play interaction after ones described by
N.A. Jones et al. / Biological Psychology 67 (2004) 103124 109

Kuzela et al. (1990). During the play interaction, both mothers and infants, were coded
separately for affect, attention, and vocalization. The scales were scored on a seven-point
graduated scale, with lower scores indicating more non-optimal affect, attention, and vo-
calizations and higher scores indicating more optimal affect, attention, and vocalizations.
Percentage of time within each scaled score was weighted and summed to obtain an index
of the infants and the mothers interactive behaviors, with higher scores indicating more
positive facial affect, more directed attention, and more positive vocalizations.
An index of motherinfant mutuality was also coded on a seven-point graded scale and
coded on a second-to-second basis. The purpose of this coding was to obtain measures
of mutually responsive play behaviors, employing similar coding systems described by
Field et al. (1990). A low score on this scale indicated fewer and more negative mutually
responsive behaviors and a high score indicated more optimal/positive interactive behaviors.
The total percentage of time spent in mutual gaze and affective state (combining facial and
vocal expressions) was obtained by observing the mother and infant interactive behaviors
simultaneously. Descriptions of the behaviors used to index the behaviors during the play
and mutuality coding can be found in Table 2.
Finally, infant behavioral responses during the arm restraint were coded to assess in-
fant reactivity using similar scales as those described by Stifter and Braungart (1995) and
Stifter and Jain (1996). This task was also scored on second-by-second basis using scales to
measure facial affect, attention and vocalization. Three, five-point scales, with low scores
associated with low behavioral responses and high scores indicating maximum behavioral
responses, were coded. Percentage scores were used to compute an index of negative re-
activity, using higher scores on vocal and facial affect. Using descriptive statistics, we
separated the infants into low, middle, and high reactive groups, using the equal percent-
ages of 33.33% to form the groups. Descriptions of the behaviors coded for this task are
also found in Table 2.

2.6. Physiological recordings at 1 and 3 months

A stretch lycra cap (Electro Cap Inc.) with the international 1020 system was positioned
on the infants head to obtain a measure of EEG activity at each age. Electrode gel, used
to conduct, and Omni Prep gel, used to gently abrade, was inserted into eight sites. The
mid-frontal (F3 and F4), central (C3 and C4), parietal (P3 and P4), and occipital (O1 and
O2) sites were chosen in order to remain consistent with previous research in this area
(Jones et al., 1997a). Each site was referenced to the vertex (Cz).
Although there has been controversy concerning the appropriate reference location, the
vertex reference was used for three reasons. First in one study, this site has been shown
to be comparable to other reference sites (Tomarken et al., 1992). Although other studies
question the use of this reference with adult participants (Hagemann et al., 1998; Reid
et al., 1998) no study has resolved this issue with infant participants (Pivik et al., 1993).
Second recordings, using this site as a reference for infant participants, are more feasible
given the ease of preparing the Cz site and the possible attrition of infant participants
when employing more invasive and/or more numerous recording sites (Pivik et al., 1993).
Third, the literature on infant EEG activity has used the vertex as the reference site almost
exclusively (Field et al., 2002b; Fox et al., 1992; Jones et al., 1998). Thus, we choose to
110 N.A. Jones et al. / Biological Psychology 67 (2004) 103124

Table 2
Mother and infant codes, descriptors, and inter-rater reliability
Coded behavior Description

Mother and infant affect, attention and vocalization ( = 0.86 for infant and 0.89 for mother)
7 Participant shows strong interest, smiling, positive intonation of vocalizations, and positive
touch
6 Participant moderate shows interest, pleasant positive attitude, positive intonation of
vocalizations, and positive touch
5 Participant shows some interest but no variability in intonation of vocalizations, variable
stimulation, little touch or heightened physical activity or physical contact. Participant is
reactive but with little facial affect
4 Participant shows varied positive, no, and/or negative affect, no consistency in responsiveness
or attention. Mothers touch is for grooming rather than stimulating. Infant is non-reactive or
neutral
3 Mother speaks to child but her face and voice are flat in affect, directs conversation without
being responsive. Infant displays escape motor activities and may attend but briefly,
occasionally frets
2 Mother losing interest, shows some self-interest (i.e., self-grooming). Infant is not attentive,
vocalizations are fussy in tone. Infant may achieve full cry temporarily but reverts back to a
fret or neutral affect
1 Mother shows varied interest in infant, possibly negative facial expressions or vocalizations.
Infant is crying or is negatively responsive
Motherinfant mutuality ( = 0.91)
7 Positive mutuality: mother and child attending. Mother attending and allowing for infant
response, positive intonation in vocalization in both mother and infant smiling, mother
possibly singing
6 Intermittent positive mutuality: mother and child attending, varied intonation of vocalization,
infants eyes are attending but smiling is varied
5 Varied mutuality: mother attends most of the time with varied positive and some neutral
affect. Infant attends more than half of the time but with neutral affect
4 Neutral mutuality: mother and child attend but with little or no affect by either. Some
grooming behaviors may be present but little stimulus/response interaction
3 Mother attending/infant not responsive or negatively responsive: mother stimulating but infant
shows little interest. Mother possibly over-stimulating, infant my show negative response,
infant clearly not enjoying the interaction and mother not changing her behavior in response
2 Mother attending/infant not attending or escaping: mother attends but no response from
infant. Infant showing intermittent negative vocalization or full cry. Infant is showing signs
that clearly indicate distress at interacting and mother not responding to infant distress
1 No mutuality: neither attending to each other nor interacting negatively
Infant reactivity during arm restraint ( = 0.92)
5 Infant in full, continuous cry and twisting, stretching and kicking is observed
4 Infant showing no positive vocalizations, steady cry, with escape-type behaviors
3 Infant showing escalated fussing, may have brief neutral tone but infant reverts to fretting
2 Infant showing brief fussing and facial negativity (frown, pout)
1 No negative vocalizations or facial expressions are observed

use the vertex as the reference site in order to compare our results to similar findings in the
literature.
Electrode impedances were brought down to less than 5 k or the sites were re-abraded.
EOG was also be obtained, to aid artifact scoring, using two mini-electrodes, one at the
N.A. Jones et al. / Biological Psychology 67 (2004) 103124 111

outer canthus and one at the supra orbit position of one eye. The electrical signal was am-
plified at each site using SA Instrumentation Bioamps and bandpassed from 1 to 100 Hz.
EEG activity from each electrode lead was displayed on a computer acquisition mon-
itor. The EEG was digitized on-line at a rate of 512 samples/s and saved to the com-
puter hard disk using data acquisition software (Snapstream, v. 3.21, HEM Data Corp.,
1991).
EEG data were examined and scored for eye and motor movement artifact using the
EOG channel as cues. Using software developed by James Long Inc., artifact was si-
multaneously eliminated from all channels. Then data were then submitted to a discrete
Fourier transform using a Hanning window with 50% overlap. This analysis produced
power for the specified frequency band in pW  (1 V squared) for each channel. Pre-
vious research suggested that the commonly used (adult) frequency bands are not appro-
priate for infant EEG activity analyses (Bell, 2002). Moreover, research has shown that
there is a shift in the alpha frequency band across development (Matousek and Petersen,
1973).
EEG were analyzed in two ways: (1) using single hertz frequency bands in order to
examine the spectral characteristics of the data; and (2) using the frequency bands commonly
used for infants (36 Hz for 1-month olds and 69 Hz for the 3-month olds; Jones et al.,
1997a, 1998). To normalize the distribution, power scores for each region were submitted
to a natural log transformation (ln). Finally, EEG asymmetry scores were computed to
determine the relative contribution of each hemisphere (ln(right) ln(left)), with negative
scores reflecting greater relative right hemisphere EEG activity and positive scores reflecting
greater relative left hemisphere EEG activity.

2.7. Data reduction and analyses

Chi-square analyses were used to examine the incidence of stable feeding patterns
across development for infants of depressed and non-depressed mothers. In addition, in-
fants were assigned to a highly reactive, mid-level reactive, and low reactive groups based
on their responses to the 3-month arm restraint procedure. Infants who were in the up-
per 33.33% of negative facial and vocal responses were classified as high reactive whereas
infants in the lower 33.33% of facial and vocal responses were classified as low
reactive.
To examine the association between mother and infant behaviors and physiology related
to depression status and feeding patterns, four groups were examined. These groups were
composed of the following: (1) depressed mothers with stable breastfeeding patterns from
newborn to 3 months of age; (2) depressed mothers with little breastfeeding and mostly
bottle feeding from newborn to 3 months; (3) non-depressed mothers with stable breastfeed
patterns across age; and (4) non-depressed mothers with little breastfeeding and mostly
bottle feeding across age.
Infant data were examined using multivariate analyses of variances (MANOVAs) for EEG
activity and dyad data were examined for their behavioral responses during interactions
(positive, neutral, negative, and mutual/synchronous responses). Follow-up analyses were
conducted using separate univariate ANOVAs for depressed versus non-depressed groups
and/or for stable breastfeeding versus bottle-feeding (and non-stable breastfeeding) groups.
112 N.A. Jones et al. / Biological Psychology 67 (2004) 103124

3. Results

3.1. Maternal depression and infant temperament

In an attempt to determine whether reactive infant temperament and maternal depression


were related to the earlier cessation of breastfeeding, we conducted several chi-square
analyses. Infants classified as high in reactive during the arm restraint procedure were
compared to those low in reactive on the stability of their breastfeeding patterns to 3 months
of age. Results showed that 77.8% of the infants who were high reactive and had a depressed
mother were predominately bottle fed whereas only 22.2% were breastfed (2 (3, N =
59) = 13.45, P < 0.05). Moreover, 70% of infants of non-depressed mothers who were
reactive were stable in their breastfeeding whereas only 30% of these infants were bottle
fed, suggesting that infant temperament is associated with breastfeeding stability in infants
of depressed mothers. These results were not found when examining infants with low or
mid-level reactive groups.
Feeding patterns were related to depressed mothers plans to breastfeed at the new-
born period and their actual feeding duration during the first 3 months. Depressed mothers
planned to breastfed for shorter periods of time, with 94.2% planning to breastfed for less
than 6 months than non-depressed mothers, 27.6% of whom were planning to breastfed
for less than 6 months (2 (3, N = 78) = 45.92, P < 0.05). Further, a one-way ANOVA
comparing depressed to non-depressed mothers on their feeding duration during the course
of the study yielded a significant effect (F(1, 76) = 5.68, P < 0.05), with depressed moth-
ers breastfeeding their infants a shorter duration of time (mean = 43.81 days, S.D. =
38.20 days) compared to non-depressed mothers (mean = 64.13 days, S.D. = 35.95
days).

3.2. EEG patterns for infants of depressed who breastfeed

A group (four levels; depressed/breastfed, depressed/bottle fed, non-depressed/breastfed,


non-depressed/bottle fed) region (four levels; frontal, central, parietal, occipital) age
(two levels; 1 and 3 months) repeated-measures MANOVA was conducted using the infants
EEG asymmetry score as the dependent variable. Results yielded a significant three-way
interaction (F(9, 147) = 2.06, P < 0.05). Analyses of each region separately showed
group differences in frontal EEG asymmetry (F(3, 49) = 3.14, P < 0.05) across age but
no differences in central, parietal and occipital regions (all P > 0.05) (Fig. 2). Univariate
ANOVAs showed that frontal EEG asymmetry differed between groups at 1 month of age
(F(3, 66) = 6.48, P < 0.05) and were only marginally significant at 3 months (F(3, 55) =
2.90, P = 0.09).
In addition, an overall group (four levels) region (four levels) hemisphere (two
levels; right versus left) age (two levels) MANOVA was conducted using the infants
ln-transformed EEG power values as the dependent variable. Results yielded several mul-
tivariate main effects and interactions, with an overall significant four-way interaction
(F(9, 147) = 2.34, P < 0.05). In order to interpret the interactions and due to the spe-
cific hypotheses about frontal region EEG activity, we confined our subsequent analyses to
examining frontal EEG activity.
N.A. Jones et al. / Biological Psychology 67 (2004) 103124 113

Fig. 2. EEG asymmetries.

A subsequent group hemisphere age analysis for the infants frontal region, ln-
transformed power scores yielded a significant main effect for group (F(3, 49) = 2.88,
P < 0.05) and a significant group hemisphere interaction (F(3, 49) = 3.26, P <
0.05), with less left hemisphere activity in the frontal region in the depressed bottle-feeding
group than in the other three groups, post-hoc significance (P = 0.04) (Fig. 3). The de-
pressed/breastfeeding group and the non-depressed groups did not show differences in
hemispheric EEG activity in the frontal region (P > 0.05).

3.3. Infant developmental assessments

Infant neurobehavioral responses were assessed on the Brazelton exam at 1 month and on
the Infinib at 3 months of age. Multivariate analyses were conducted to determine whether
Brazelton scores differed for feeding and depression groups. Results showed a multivariate
interaction for Brazelton items between groups (F(21, 189) = 3.60, P < 0.05). Follow-up
univariate analyses between groups showed differences between groups for habituation
(F(3, 67) = 7.66, P < 0.05), orientation (F(3, 67) = 2.70, P < 0.05), motor maturity
(F(3, 67) = 3.98, P < 0.05), regulation of state (F(3, 67) = 2.82, P < 0.05), and abnormal
reflexes (F(3, 67) = 6.32, P < 0.05). Mean scores for each measure can be found in
Table 3. Overall, results showed early benefits for infants of non-depressed mothers and
114 N.A. Jones et al. / Biological Psychology 67 (2004) 103124

Fig. 3. EEG power (ln-transformed) scores for the frontal region.

infants of depressed mothers who were breastfed, with this latter group exhibiting increased
habituation abilities and decreased abnormal reflexes.
An ANOVA comparing scores on the Infinib for depression and feeding groups did not
reach significance, with both all groups showing similar developmental capabilities at 3
months of age (P > 0.05).

Table 3
Infant Brazelton scores
Measure Depressed Non-Depressed

Breastfeedinga Bottle feedingb Breastfeedingc Bottle feedingd

Habituation 7.73 (0.57) 6.76 (1.20)+ 7.76 (0.30) 7.10 (0.74)


Orientation 6.44 (1.06)+ 6.69 (0.93) 7.17 (0.58) 6.78 (0.74)
Motor maturity 5.60 (0.31) 6.07 (0.66)+ 5.44 (0.70) 5.61 (0.40)
Range of state 3.07 (1.18) 3.86 (0.82) 3.38 (1.16) 3.34 (0.96)
Regulation of state 5.45 (1.24) 5.58 (0.90) 6.38 (1.38) 6.20 (0.78)
Autonomic stability 6.19 (1.17) 6.29 (1.01) 6.70 (0.96) 6.57 (1.18)
Abnormal reflexes 1.00 (1.04) 2.25 (1.06)+ 0.92 (1.15) 1.00 (0.84)
Note. Values represent mean scores. Standard deviations are in the parentheses. Different superscripts denote
significantly different post-hoc comparisons, P < 0.05.
a n = 12.
b n = 16.
c n = 25.
d n = 18.
P < 0.05.
N.A. Jones et al. / Biological Psychology 67 (2004) 103124 115

3.4. Maternal reports of infant temperament

MANOVAs were conducted on the mothers reports of positive and negative (activity
level, smiling and laughter, distress latency, distress to limitations, soothability and du-
ration of orienting) behaviors on the six scales of the Infant Temperament Questionnaire
(IBQ) for the four groups. Results showed that all mothers reported differences in infant
temperament on the six scales (F(5, 53) = 86.50, P < 0.05), with more reports of positive
behaviors and fewer reports of negative behaviors. In addition, maternal reports of infant
behaviors on the temperament scales increased across age (F(1, 57) = 116.52, P < 0.05).
However, no meaningful group differences in the types of behaviors reported by depressed
and non-depressed mothers nor for breastfeeding and bottle-feeding groups were apparent
from ratings of maternal perceived infant temperament.

3.5. Mother and infant behaviors during play

A group affect (three levels; positive, neutral, negative) age MANOVA showed that
infants were exhibiting more positive and less negative and neutral interactive behaviors
at 3 months than at 1 month (F(2, 110) = 13.88, P < 0.05) (Fig. 4 illustrates the data).
Follow-up univariate ANOVAs revealed that the infants of depressed, bottle-feeding mothers
showed more negative affect at 1 month (F(3, 72) = 2.80, P < 0.05) and these infants also
showed the least positive affect at 3 months (F(3, 55) = 3.22, P < 0.05), than the other
three groups.
A repeated-measures group age MANOVA was conducted on the percentage of time in
mutually responsive interactions as the dependent variables. Result showed no significant
interaction effects. However, a significant main effect for age was evident (F(1, 55) = 27.80,
P < 0.05). As expected, the dyads demonstrated more mutually interactive behaviors at 3
months than at 1 month.
Examination of mutually interactive behaviors separately for the maternal depression
groups versus the feeding groups were conducted at 3 months of age. This univariate
ANOVA yielded a significant between-subjects effect for feeding group (F(1, 57) = 4.24,
P < 0.05), with mean scores indicating that dyads who did not have stable breastfeeding
patterns had less mutually interactive behaviors at the 3-month visit (mean = 61.23, S.D. =
7.04) than infants who had stable breastfeeding patterns (mean = 66.14, S.D. = 7.04).

3.6. Path analysis

Finally, a path analysis was conducted using EQS (EQS v. 5.7b, Multivariate Software,
Inc, 1998) in order to evaluate the role of infant frontal EEG asymmetry and temperament
in mediating maternal depression effects on feeding behaviors. Missing data for nine sub-
jects were replaced with mean values. Based on previous findings, we hypothesized that
maternal depression would negatively affect feeding behavior. Similarly, we hypothesized
that infant temperament would be related to feeding behavior. Furthermore, we predicted
that maternal depression would be related to infant temperament via its effects on the de-
velopment of the underlying structures of emotion and emotion regulation, reflected by
frontal EEG asymmetry patterns. As such the hypothesized model examined the direct and
116
N.A. Jones et al. / Biological Psychology 67 (2004) 103124
Fig. 4. Infant behavioral responses during motherinfant interactions at 1 and 3 months.
N.A. Jones et al. / Biological Psychology 67 (2004) 103124 117

Table 4
Correlations
Infant feeding Depression Frontal EEG Infant temperament
score asymmetry (positive during
interaction)
Infant feeding
N 78 78 78 78
Covariance 1637.722 64.786 3.074 149.491
Pearson correlation 1 0.221 0.338 0.366
Significance (two-tailed) 0.052 0.003 0.001
Depression score
N 78 78 78 78
Covariance 64.786 52.529 0.487 22.102
Pearson correlation 0.221 1 0.299 0.302
Significance (two-tailed) 0.052 0.008 0.007
Frontal EEG asymmetry
N 78 78 78 78
Covariance 3.074 0.487 0.051 0.801
Pearson correlation 0.338 0.299 1 0.352
Significance (two-tailed) 0.003 0.008 0.002
Infant temperament (positive during interaction)
N 78 78 78 78
Covariance 149.491 22.102 0.801 102.093
Pearson correlation 0.366 .302 0.352 1
Significance (two-tailed) 0.001 0.007 0.002
Correlation is significant at the 0.01 level (two-tailed).

indirect effects of maternal depression on both infant temperament and feeding behaviors
(Fig. 1).
Analyses were conducted using the maximum likelihood estimation procedure on the
variance/covariance matrix (Table 4). The hypothesized model was tested revealing an
adequate fit for the model (2 (1, N = 78) = 3.81, P < 0.05), comparative fit index
(CFI) of 0.91, RMSEA of 0.19 (Fig. 5). Post-hoc modifications were then performed in an

R2 =0.09
Infant
Infant EEG .29* Temperament
(positive R2 =0.17
asymmetry
responsive-ness
during interaction)
-.30* -.22

.33*

Maternal
Depression .12
Score Duration
R2 =0.15
Breastfeeding

Chi Square=3.81,p=0.05, CFI=0.91, RMSEA=0.19

Fig. 5. Initial model.


118 N.A. Jones et al. / Biological Psychology 67 (2004) 103124

R2 =0.09

Infant EEG
asymmetry
-.24*
-.30*

-.29* Duration
Maternal R2 =0.18
Breastfeeding
Depression
Score

Infant
-.28*
Temperament
-.22*
(positive
responsiveness during
interaction)

R2 =0.17

Chi Square=0.46, p=0.50, CFI=1.00, RMSEA=0.00


Fig. 6. Final model.

attempt to develop a better fitting model. The Wald test indicated that eliminating the path
between maternal depression and feeding behaviors would improve the fit of the model.
A path between infant frontal EEG asymmetry and feeding behavior was added following
results of the Lagrange multiplier test. The model was re-estimated revealing an excellent
fit (2 (1, N = 78) = 0.46, P = 0.50, CFI = 1.0, RMSEA = 0.0), suggesting an
improvement from the hypothesized model (Fig. 6).
This final model suggests that the effects of maternal depression on feeding are mediated
by infant frontal EEG asymmetry and temperament. Furthermore, this model suggests that
maternal depression was strongly predictive of infant frontal EEG asymmetry (standard-
ized coefficient for direct effect = 0.30, t = 2.73, P < 0.05) and infant temperament
(standardized coefficient for indirect effect = 0.30, t = 2.76, P < 0.001). Furthermore,
maternal depression effects on infant temperament (standardized coefficient for indirect
effect = 0.09, t = 1.89, P < 0.1) were marginally mediated by frontal EEG asymmetry
and the effects of frontal EEG asymmetry on feeding (standardized coefficient for indirect
effect = 0.08, t = 1.83, P < 0.1) were marginally mediated by infant temperament.

4. Discussion

The goal the present investigation was to examine the factors that promote breastfeeding
stability and to examine the physiological and affective development in infants of depressed
mothers who breastfed compared to those who bottle fed. Previous research has suggested
that depressed mothers are less likely to breastfeed (Galler et al., 1999; Milligan et al., 1990)
and infants of depressed mothers demonstrate dysregulated physiological and behavioral
patterns as early as the newborn period (Jones et al., 1997a, 1998; Lundy et al., 1996,
N.A. Jones et al. / Biological Psychology 67 (2004) 103124 119

1999). Within the present study, we documented that maternal depression is associated
with less stable breastfeeding, that greater negative infant temperament is associated with
less stable breastfeeding in depressed dyads, and that more positive dyadic interaction is
associated with infants of non-depressed mothers and infants of depressed mothers with
a stable breastfeeding relationship than for infants of depressed mothers who bottle feed.
Our final model showed that infant temperament and frontal EEG asymmetry mediated the
association between maternal depression and feeding patterns. As a caveat to these results we
must note that this study is correlational in nature, as we could not assign dyads to depression
and feeding groups, yet these data point to potentially important future intervention studies.

4.1. Maternal depression and breastfeeding patterns

That depressed mothers in this study were less likely to intend to maintain an extended
duration of breastfeeding at the newborn period is discouraging given that numerous health
care agencies are working to increase breastfeeding rates across infancy (Department of
Health and Human Services, Blueprint for Action on Breastfeeding, 2000). However, these
data are consistent with previous research showing lower rates of breastfeeding in depressed
women (Field et al., 2002a; Galler et al., 1999). Typically studies have examined the char-
acteristics of the parents and the likelihood of breastfeeding continuity across infancy. This
is one of the few studies to show an association between infant temperament and breastfeed-
ing stability across the early months of development. Specifically, we showed that greater
negative infant reactivity was associated with more variable feeding patterns in depressed
mothers compared to non-depressed mothers. While our data are confounded, as we cannot
separate situational variables (mothers plans for breastfeeding or bottle feeding and moth-
ers depression status) and individual difference variables (infant temperament and EEG
activity patterns), this study points several important future studies that may be beneficial
to conduct. For example, breastfeeding support and promotion could be employed, using
random assignment, as a clinical intervention for depressed mothers during the prenatal
period. The findings of this study could determine more directly whether breastfeeding
can benefit the affective and physiological functioning of the dyad even though exposed to
maternal depression.
Moreover, there are many reasons that the depressed mothers may fail to establish stable
breastfeeding patterns with their infants. The more simplistic explanation is that depressed
mothers are more concerned about their own emotional state than the feeding status of their
infants. While this explanation is possible, we are suggesting that depressed mothers may
show lower rates of breastfeeding due to their lack of understanding of normative tempera-
mental changes across infancy. As noted by previous studies, newborns who breastfed are
more temperamentally irritable and more difficult to sooth (Dipietro et al., 1987). Bottle
feeding, on the other hand, has a depressive effect on infant behavior (Dipietro et al., 1987).
Therefore, newborn behavioral responses, as a result of breastfeeding, may confuse and
tax the already depleted resources of the depressed mother. However, several studies have
noted that breastfed newborns demonstrate more optimal physiological organization (e.g.,
Zeskind et al., 1992) and, later in development, mothers who maintain stable breastfeeding
patterns report that their infants exhibit easier temperaments (VanDiver, 1997) and more
socially responsive behaviors (Kuzela et al., 1990; Worobey, 1992, 1998), suggesting posi-
120 N.A. Jones et al. / Biological Psychology 67 (2004) 103124

tive outcomes later in development for breastfed dyads. Therefore, depressed mothers must
be educated about the numerous benefits of breastfeeding stability and must be encouraged
to continue breastfeeding, despite the seemingly more challenging behaviors displayed by
their newborns. Moreover, these parents should be counseled that the seemingly more taxing
newborn behaviors are normative and not due to inadequate parenting skills. Currently de-
pressed mothers are discontinuing breastfeeding within the first 2 months and therefore fail
to experience the potential benefits associated with the more positive infant physiological
and behavioral responses that are the result of stable breastfeeding patterns.
Although we did demonstrate that infant temperament is related to breastfeeding sta-
bility in the depressed group, the sample size for this study is small and is limited to the
first 3 months of development. The findings presented here, however, remain an important
area for future work, primarily due to the increasing evidence that breastfeeding stability
benefits overall infant health and development. Ultimately supporting mothers during the
breastfeeding months will likely have long lasting benefits for depressed mothers and their
infants.

4.2. Physiological patterns in infants of depressed mothers who breastfeed

Our study also suggests that infant EEG activity is associated with maternal depression
and breastfeeding stability. The final path model showed a strong association between
maternal depression and infant EEG patterns and infant temperament. Specifically, infants
of depressed mothers who had been breastfed until their third month of life were less likely
to show the right frontal EEG asymmetry patterns previously associated with maternal
depression (Dawson et al., 1999, 1997; Jones et al., 1998) and linked to risk for depression in
adults (Davidson, 1994; Henriques and Davidson, 1990). Alternatively, infants of depressed
mothers who were bottle fed exhibited a bilateral decrease in frontal EEG activity that was
especially pronounced on the left side. Although the difference in EEG asymmetry scores
decreased with age, this may be due, in part to the declining depressive symptoms in both
depression groups or it may be due to the resiliency of these infants. Nonetheless, future
studies should examine the stability of EEG patterns across development and the situational
factors that may attenuate these seemingly dysregulated EEG patterns in infants of depressed
mothers.
The EEG findings related to feeding patterns are intriguing in light of the fact that previous
investigations have only rarely assessed neurophysiological patterns associated with infant
feedings. One recent study by Lehtonen et al. (2002) examined EEG activity in 3- and
6-month-old infants during feeding. While their goal was to examine EEG patterns during
normative infant feeding session, they found undifferentiated theta (similar frequency
band to the band we called alpha) responses to feeding and did not establish organized
EEG activity patterns associated with feeding until 6 months of age. The authors speculate
that the development of the frontal regions and the emotional arousal inherent in feeding
was directly related to their findings. While their findings are later in development than
our own, the findings do parallel our associations between emotional responses and EEG
activity. Of interest, they did not find distinct patterns of EEG activity for bottle fed and
breastfed groups, most likely due to the small number of bottle fed participants in their
study. Collectively this study and our own findings suggest that further research should
N.A. Jones et al. / Biological Psychology 67 (2004) 103124 121

focus on feeding patterns in the infant and the association between emotional processing
and frontal lobe development.

4.3. Neurobehavioral assessments of infants of depressed mothers who breastfed

Consistent with previous studies, infants of depressed mothers also showed fewer op-
timal behaviors on the Brazelton Scales (Abrams et al., 1995; Jones et al., 1997a, 1998;
Lundy et al., 1996). Specifically infants of depressed mothers who bottle fed showed less
habituation and more abnormal reflexes. Although these results may be transitory, as these
infants did not differ on developmental assessments at 3 months of age, the findings suggest
that subtle differences in early neurobehavioral abilities are affected by maternal depression
and feeding status.

4.4. Motherinfant interactive behavior for depression and feeding groups

In separate analyses, we also demonstrated that motherinfant interactions were less


negative at 1 month of age and more positive by 3 months of age in the depressed group
with stable breastfeeding patterns but not in the depressed group who were bottle fed.
While previously we have established that infants of depressed mothers displayed greater
negative affect during interaction (Jones et al., 1997b) and Field et al. (1990) demonstrated
more negatively matched and fewer positively matched interactive patterns in depressed
groups, in the present study, infants of breastfeed, depressed mothers seemed to display
reduced dysregulated interaction patterns than the infants of depressed mothers who bottle
fed. Although these results could be due to other factors that motivate a depressed mother
to breastfeed, the fact that the depressed-breastfeeding dyads appeared to interact with
their infants like the non-depressed groups suggests that breastfeeding may benefit the
socio-emotional interactions of depressed dyads.
Breastfeeding patterns have also been examined retrospectively as a potential factor that
differentiates depressed and non-depressed groups. For example, Allen and his colleagues
(Allen et al., 1998) have also investigated the prenatal and perinatal risk factors for psy-
chopathologies in children and adolescents. Their study concluded that major depression
in childhood and adolescence was associated with not having been breastfed and having a
mother with an affective disorder during pregnancy. Given these data and the data presented
here, it may be beneficial to support breastfeeding patterns in depressed mothers to possibly
reduce the negative outcomes and the increased risk factors for affective problems noted in
previous studies (Allen et al., 1998; Field, 1995).
In conclusion, our previous research has demonstrated that infants of depressed moth-
ers exhibit risk factors that are associated with physiological and affective dysregulation
(Field, 1995; Jones et al., 1998). However, within this study we were able to demonstrate
that infants of depressed mothers who are stable in their breastfeeding patterns showed a
reduced association between physiological and affective dysregulation resulting from ex-
posure to maternal depression. Specifically, infants of depressed mothers who breastfed
did not demonstrate the greater relative right frontal EEG asymmetry (nor the left frontal
hypoactivity) compared to the bottle fed group. Moreover, increased positive affect was ap-
parent in 3-month-old infants of breastfed compared to the bottle-feeding/depressed group,
122 N.A. Jones et al. / Biological Psychology 67 (2004) 103124

suggesting that breastfeeding should be examined further as a potential intervention factor


for depressed mother and their infants.

Acknowledgements

We would like to thank the mothers and infants who participated in this study. We would
also like to thank all the students at Florida Atlantic University at Jupiter who helped with
data collection. This research was supported by a NIMH grant (MH61888) and a FAU
Research Initiation Award to Nancy Aaron Jones, Ph.D.

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