Depressed mothers' newborns are less responsive to animate and inanimate stimuli

Infant and Child DevelopmentInf. Child. Dev. 20: 94–105 (2011)

Published online 4 May 2010 in Wiley Online Library

(wileyonlinelibrary.com). DOI: 10.1002/icd.687

Depressed Mothers’ Newborns AreLess Responsive to Animate andInanimate Stimuli

Tiffany Fielda,b,�, Maria Hernandez-Reifc,a andMiguel Diegoa

aUniversity of Miami Medical School, Miami, FL, USAbFielding Graduate University, Santa Barbara, CA, USAcUniversity of Alabama, Tuscaloosa, AL, USA

Data from our research are reviewed showing limited attentive-ness and responsivity to animate stimuli in newborns ofdepressed mothers. These include face–voice stimuli of mothersand strangers, newborn cry sounds and instrumental and vocalmusic. Newborns of depressed mothers are also noted to be lessattentive and responsive when presented with inanimate stimuli,including different texture nipples, different temperature nipplesand different weight tubes. Potential underlying mechanisms aresuggested by research showing negative effects of prenataldepression, elevated prenatal cortisol and lower prenatal dopa-mine and serotonin on the newborns of depressed mothers.Additional risk factors are explored, including sleep disturbancesand other prenatal stressors. Early interventions, includingpregnancy massage, massage therapy for infants and demonstra-tion of the Brazelton Assessment, have been noted to enhance theneonates’ attentiveness and responsivity to animate and inani-mate stimuli. Limitations of these studies are discussed, includ-ing the sample being limited to lower SES women who havemany other problems that potentially affect newborns. Morecontrolled studies are needed to assess potential mediatingfactors for the inferior performance of these newborns onperceptual tasks such as limited attentiveness and/or greaterarousal as well as longitudinal follow-up studies to determinewhether these limited perceptual abilities continue into infancy.Copyright r 2010 John Wiley & Sons, Ltd.

Key words: newborns; prenatal depression

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*Correspondence to: Tiffany Field, Touch Research Institute, University of Miami School ofMedicine, P. O. Box 016820, Miami, FL 33101, USA. E-mail: [email protected]

Copyright r 2010 John Wiley & Sons, Ltd.

In this paper, data are reviewed on the limited attention and responsivity toanimate and inanimate stimuli by newborns of depressed mothers. This programof research from our lab also includes studies on potential underlyingmechanisms for these problems, including prenatal maternal comorbid anxietyand anger, prenatal sleep disturbances, elevated stress hormones and other riskfactors. Early intervention studies are also reviewed, including massage therapyand Brazelton Neonatal Behaviour Assessment demonstrations. All of thefindings presented were significant at least at po0.05 based on samples ofapproximately 20 infants divided equally by gender. Finally, several limitationsof the studies are discussed as well as suggested future directions.

RESPONSES TO ANIMATE STIMULI

Responses to Face/Voice Stimulus

Dysregulated physiological and biochemical profiles have been reported forprenatally depressed mothers and their newborns. These included: (1) rightfrontal EEG that usually accompanies withdrawn behaviour; (2) low vagalactivity typically associated with inattentiveness; (3) elevated cortisol levels thatoften suggest arousal or stress; and (4) lower levels of serotonin and dopaminewhich are activating neurotransmitters (Field et al., 2004). We expected that thisneonatal dysregulation would affect the perception of different stimuli by thesenewborns. In one study, neonates born to depressed versus non-depressedmothers were compared on the Brazelton Neonatal Behaviour Assessment Scale(NBAS) (Hernandez-Reif, Field, Diego, & Ruddock, 2006). The neonates ofdepressed mothers received lower scores on the orienting to the live face/voicestimulus and on the alertness items, suggesting that they were less alert and lessattentive to face/voice stimuli. They also scored less optimally on the cuddlinessand hand-to-mouth activity items, suggesting that they were more aroused.These data lent support to our model that infants of depressed mothers are morearoused and less attentive, although it is difficult to determine the degree towhich elevated arousal and inattentiveness contributed to these lower scores(Field, 2009).

In a similar study, both responsivity to different face stimuli and facial ex-pressivity were studied in newborns of depressed mothers (Lundy, Field, &Pickens, 1996). The facial expressions of newborns of depressed and non-de-pressed mothers were recorded during the NBAS and during the modeling ofhappy, sad, and surprised faces by an adult examiner. The newborns of de-pressed mothers once again demonstrated inferior performance on the orientingcluster of the Brazelton scale, and they showed fewer interest and more precryexpressions during the Brazelton exam. During the facial expression modeling,they showed less orienting towards the faces and fewer facial expressions.The lesser expressivity of those newborns may relate to their lesser attentivenessto the faces that were modeled for them.

In another study, we explored discrimination of mothers’ and strangers’faces (Hernandez-Reif, Field, Diego, & Largie, 2002). Depressed mothers’newborns showed inferior face discrimination. They required more time tohabituate their mother’s face, and afterwards they failed to show a visualpreference for their mother’s face or the stranger’s face, as compared with theinfants of non-depressed mothers who showed a novelty preference for thestranger’s face.

Depressed Mothers’ Newborns Are Less Responsive 95

Copyright r 2010 John Wiley & Sons, Ltd. Inf. Child. Dev. 20: 94–105 (2011)DOI: 10.1002/icd

Responses to Newborn Cry Sounds

In other studies, we investigated newborns’ responses to animate auditorystimuli. For example, in one study, depressed mothers’ newborns showed lessdiscrimination of other newborns’ cry sounds (Field, Diego, Hernandez-Reif, &Fernandez, 2007). Newborns’ crying in response to the cry of another newbornhas been called an empathetic response. The purpose of this study was todetermine whether newborns of depressed mothers also showed an empatheticresponse. Newborns of depressed and non-depressed mothers were presentedwith cry sounds of themselves or other infants, and their sucking and heart ratewere recorded. The newborns of non-depressed mothers responded to the crysounds of other infants with reduced sucking and decreased heart rate, suggestingthat they were attending to the cry sounds. Cessation of sucking and heart ratedeceleration have often been used as measures of newborns’ attentiveness tovarious stimuli. The newborns of depressed mothers did not show a change intheir sucking or heart rate to the cry sounds of other infants. This failure to attendand respond to other infants’ cry sounds may predict the lack of empathy thatchildren of depressed mothers have shown towards their mothers’ feigned crysounds at the preschool stage (Jones, Field, & Davalos, 2000).

Responses to Instrumental and Vocal Music

In another study, we explored instrumental and vocal music effects on EEG andEKG in neonates of depressed and non-depressed mothers (Hernandez-Reif,Diego & Field, 2006). Neonates born to depressed and non-depressed motherswere randomly assigned to hear an audiotaped lullaby of instrumental musicwith vocals or a lullaby of instrumental music without vocals. EEG and EKGwere recorded for 2 min of silence (baseline) from the neonates and for 2 min ofinstrumental music with or without vocals. The neonates of depressed mothersshowed greater relative right frontal EEG asymmetry to both types of music,suggesting withdrawal responses to music in general. The neonates of non-depressed mothers, on the other hand, showed greater relative left frontal EEGasymmetry to the instrumental without vocal music, suggesting an approachresponse, and greater relative right frontal EEG asymmetry to the instrumentalwith vocal music, suggesting a withdrawal response. Heart rate decelerationsoccurred following the music onset for both groups of infants. However, whencompared with infants of non-depressed mothers, the infants of depressedmothers showed delayed heart rate decelerations, suggesting a slower processingand/or a delayed attentiveness to the music.

RESPONSES TO INANIMATE STIMULI

Different Texture Nipples

Newborns of depressed mothers have also shown limited responsivity toinanimate stimuli. In one study, less exploring of different texture nipplesoccurred in newborns of depressed mothers (Hernandez-Reif, Field, Del Pino, &Diego, 2000). Newborns of depressed and non-depressed mothers werecompared on their perception of nubby and smooth nipples by mouth. Bothgroups of newborns discriminated these textures, and they showed a preferencefor the smooth texture nipples based on their sucking more on the smooth

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nipples. However, the newborns of depressed mothers spent on average 50% lesstime orally exploring the nipples, 33% less time exploring the more novel nubbynipple, and 59% less time mouthing the more familiar smooth nipple.

Different Temperature Nipples

Neonates of depressed versus non-depressed mothers have also shown differentsucking patterns on different temperature nipples (Hernandez-Reif, Field, &Diego, 2004). The newborns sucked on cold and warm nipples on alternatingtrials. Half the newborns received the cold nipple on the first of the eight trials,and the other half of the newborns received the warm nipple first. The neonatesof depressed mothers sucked twice as much as the neonates of non-depressedmothers, suggesting several possibilities, including that the neonates ofdepressed mothers were over-aroused or that they simply loved sucking onthe nipples. Although the newborns in both groups did not show a preference forthe cold or warm nipples, the neonates who received the cold nipple on the firsttrial sucked significantly more on the subsequent trials than those who receivedthe warm nipple on the first trial, suggesting that an initially cold nipple mightelicit more sucking.

Temperature perception was slower in newborns of depressed versus non-depressed mothers when they held different temperature tubes (warm versuscold) in their hands (Hernandez-Reif, Field, Diego, & Largie, 2003). Both groups ofinfants showed a decrease in holding the familiar temperature tube and showedan increase in holding a tube of the opposite temperature. However, the newbornsof depressed mothers required twice as long to notice the different temperature ofthe two tubes. That is perhaps not surprising because the infants of depressedmothers did not spend as much time ‘exploring’ the tube with their hands.

Different Weight Tubes

We also tested the perception of different weight tubes (Hernandez-Reif, Field,Diego, & Largie, 2002). A light-weight (2 g) or heavier-weight (8 g) tube of pelletswas placed in the right hand of neonates born to depressed or non-depressedmothers. After the infants habituated one weight tube (the light or heavy weighttube) by hand, they were tested with the opposite weight tube. The infants of thedepressed mothers did not respond to the novel weight tube, and only 15% ofthose infants showed hand movements that might have facilitated theirperception of the tube’s weight (e.g. hand-to-mouth or turning/moving of thewrist or hand). In contrast, 78% of the newborns of non-depressed mothersshowed hand activity that might have facilitated weight perception, and as agroup, they held the novel weight tube longer, suggesting that they hadperceived the weight change.

POTENTIAL UNDERLYING MECHANISMS

Prenatal Depression and Elevated Cortisol

Several potential underlying mechanisms for the inferior perceptual performanceof newborns of depressed mothers have been suggested, including the negativeeffects of prenatal depression and anxiety and associated elevated stress



hormones, sleep disturbances and other risk factors (Field, Hernandez-Reif, &Diego, 2006). We assessed the stability of cortisol and mood states acrosspregnancy (from 20 to 32 weeks gestation). Relationships were noted betweencortisol and depression and cortisol and anxiety. Significant stability was notedbetween the 20-week and the 32-week measures, including depression, anxietyand cortisol. These were, in turn, correlated with each other and with sleepdisturbances in the pregnant women.

Sleep Disturbances

Because sleep disturbances were highly correlated with elevated cortisol, thepregnant women were then given self-report measures on sleep disturbances(Field Diego, Hernandez-Reif, Figueiredo, et al., 2007). Their newborns were alsoobserved during sleep. During both the second and third trimesters, thedepressed women had more sleep disturbances and higher depression, anxietyand anger scores. They also had higher norepinephrine and cortisol levels.The newborns of the depressed mothers, in turn, had more sleep disturbances,including less time in deep sleep and more time in indeterminate (disorganized)sleep, and they were more active and cried/fussed more.

Chronicity of Depression Across Prenatal and Postnatal Periods

We also compared the impact of the prenatal onset versus the postnatal onset andthe chronicity (prenatal and postnatal) effects of maternal depression on neonatalbehaviour (Diego, Field, & Hernandez-Reif, 2005). Neonates born to mothersreporting symptoms of depression at any time point exhibited more indetermi-nate (disorganized) sleep than neonates of non-depressed mothers. Neonatesborn to mothers reporting prenatal depression also spent more time fussing andcrying, and they exhibited more stress behaviours than neonates born to non-depressed mothers or neonates born to mothers exhibiting symptoms ofdepression only during the postpartum period. The neonates born to motherswho reported symptoms of depression during both the prepartum andpostpartum periods received less optimal Brazelton Neonatal BehaviourAssessment scores than neonates of non-depressed mothers or neonates bornto mothers who exhibited symptoms of depression during only the prepartum oronly during the postpartum periods. Taken together, these findings suggest thatneonatal behaviour is influenced not just by the presence but also by the timingand duration of maternal depression symptoms.

Prenatal Dopamine Effects

In a study on the effects of prenatal dopamine, depressed pregnant women weredivided into high and low prenatal dopamine groups based on a tertile split ontheir dopamine levels at 20 weeks gestation (Field et al., 2008). The low dopaminegroup had higher CES-D scores at the 20-week gestational age assessment andlower dopamine and serotonin levels at both the 20- and the 32-week gestationalage assessments. The neonates of the mothers with low dopamine levels hadsimilarly low dopamine and serotonin levels as well as higher cortisol levels.And, the neonates in the low dopamine group had inferior autonomic stabilityand excitability scores on the NBAS. Thus, mothers with low prenatal maternal

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dopamine levels appear to have newborns who are more aroused (higher cortisollevels and excitability) and less regulated (autonomic stability), although theseeffects were confounded by low serotonin levels.

Prenatal Serotonin Effects

Serotonin has long been associated with depression (Cubala & Landwski, 2006;Neumeister, 2003; Neumeister, Young, & Stastny, 2004). Serotonin receptors andserotonin transporters are reduced in depression, suggesting that serotonin systemsplay a key role in the pathophysiology of depression (Neumeister et al., 2004).

In a study on relationships between prenatal serotonin levels and other bio-chemical variables during pregnancy as well as their relationships to neonatalbiochemical and behavioural variables, pregnant women were divided into thetop and bottom tertiles based on their serotonin levels at 20 weeks gestational age(Field, Diego, Hernandez-Reif, Fernandez et al., 2007; Field, Yando, Bendell,Hernandez-Reif, Diego et al., 2007). Both the depressed mothers and their neo-nates had low serotonin levels and the newborns had inferior scores on theBrazelton Scale.

Prenatal Anxiety and Comorbid Depression and Anqer Effects on the Foetus andNeonate

Because the pregnant women who were depressed also seemed to be anxious andangry, we assessed the combined effects of anxiety, anger and depression.Pregnant women were classified as experiencing high or low anxiety during thesecond trimester of pregnancy (Field et al., 2003). The high-anxiety women alsohad high scores on depression and anger scales. In a follow-up across pregnancy,the foetuses of the high-anxiety women were noted to be more active and toexperience growth delays. The high-anxiety mothers’ low dopamine levels werefollowed by their neonates having low dopamine and serotonin levels. The high-anxiety mothers’ newborns also had greater relative right frontal EEG activation(associated with withdrawal behaviour) and lower vagal tone (associated withinattentiveness). Finally, the newborns of these mothers spent more time in deepsleep and less time in quiet and active alert states and showed more state changesand less optimal performance on the NBAS.

Other Risk Factors

Because other risk factors emerged in our studies, we combined several samplesand explored multiple risk factors (Field, Hernandez-Reif, & Diego, 2006).The women were diagnosed as depressed based on the Center for Epidemio-logical Studies Depression Scale (CES-D) and the Structured Clinical Interviewfor Depression. They were interviewed on several demographic variables, riskfactors and stress questionnaires. On average, the depressed pregnant womenwere younger, they had less education and lower socioeconomic status, and theywere less often married. Fewer of the depressed women and their partners werehappy when they were told that they were pregnant, a greater number of thedepressed women experienced a stressful situation during pregnancy, more ofthe depressed women were prescribed antibiotics during pregnancy, and thedepressed women had less optimal obstetric complications scores, including a



greater incidence of prematurity. Finally, the scores of the depressedpregnant women on the stress questionnaires suggested greater depression(CES-D), anxiety (STAI), anger (STAXI), pregnancy anxieties (PAAS) and dailyhassles.

In another study on risk factors, depressed pregnant women reported moresubstance use, including cigarettes, caffeine and medications (primarily anti-biotics) (Field, Yando, Bendell, Hernandez-Reif, Diego et al., 2007). Their scoreson the Feelings About Pregnancy and Delivery Scale were lower, including thecoping, support, intimacy, and cultural effects scores. In addition, they reportedhaving more stressful situations during pregnancy, being less happy whenfinding out they were pregnant and their significant other being less happy whenfinding out about the pregnancy. Prenatal caffeine use, in particular, affectedneonatal outcomes (Diego et al., 2007). Newborns of mothers who consumedcaffeine (62% of mothers drank caffeine daily) were more often low birth weightand showed more stress behaviours.

Thus, there appeared to be several potential prenatal variables that con-tributed to the newborns of depressed mothers performing less optimally inneonatal perception studies. It is not clear from these data from multiple separatestudies which factors or which interactions of risk factors are making thestrongest contributions to neonatal performance. Longitudinal studies frompregnancy through the newborn period are needed to determine the relativecontributions of these predictor variables. Nonetheless, these prenatal risk factorshighlight the need for early interventions.

EARLY INTERVENTIONS

Massage Therapy Effects on Prenatal Depression

Various forms of stimulation have been noted to lower prenatal depression andcortisol levels, including yoga (Narendran, Nagarathna, Narendran, Gunasheela& Nagendra, 2005) and massage therapy (Field, Diego, Hernandez-Reif,Schanberg, & Kuhn, 2004). And, serotonin and dopamine levels are increasedfollowing massage therapy (Field, Hernandez-Reif, Diego, Schanberg, & Kuhn,2005) and after exercise (Struder et al., 1997). Vagal activity also increasesfollowing massage therapy (Diego & Field, 2008).

Vagal activity has been notably lower in depressed pregnant women and intheir newborns (Field et al., 2004; Jones et al., 1998). Low vagal activity is relatedto several developmental problems, including inattentiveness and behaviourproblems, in later childhood (Porges, Doussard-Roosevelt, Portales, & Green-span, 1996). In at least one study, the effects of massage therapy appeared to bemediated by increased vagal activity (Diego & Field, 2008).

Neonates born to depressed mothers have benefited from their mothers re-ceiving pregnancy massage. Those newborns whose mothers received moderatepressure massage versus those who received light pressure massage therapyduring pregnancy (month 5 through month 8) were compared on theirbehaviours during 15-min sleep–wake behaviour observations and on theirperformance on the NBAS (Field, Hernandez-Reif, & Diego, 2005). The group ofneonates whose mothers received moderate pressure massage spent a greaterper cent of the observation time smiling and vocalizing, and they receivedbetter scores on the orienting, motor, excitability and depression clustersof the NBAS.

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Massage Therapy for Infants of Depressed Mothers

Infants born to depressed mothers, themselves, can benefit from massagetherapy. In this study, the infants were given 15 min of either massage or rockingfor 2 days per week for a 6-week period (Field et al., 1996). The infants whoexperienced massage therapy compared with infants in the rocking group spentmore time in active alert and active awake states, they cried less, and they hadlower salivary cortisol levels, suggesting lower arousal levels. After the massageversus the rocking sessions, the infants spent less time in an active awake state,suggesting that massage may be more effective than rocking for inducing sleep.Over the 6-week period, the massage therapy infants showed greater improve-ment on emotionality, sociability and soothability temperament dimensions andthey had greater decreases in urinary stress catecholamines/hormones (norepi-nephrine, epinephrine and cortisol).

Depressed Mothers’ Neonates Improve Following a Brazelton Demonstration

To assess the effectiveness of a short-term intervention for improving theorienting behaviours of newborns of depressed mothers, the depressed mothersfirst observed the NBAS soon after delivery (Hart, Field, & Nearing, 1998).The mothers were then given a similar instrument, the Mother’s Assessment ofthe Behaviour of her Infant, to independently conduct Brazelton-like assessmentsat home. The control group mothers were not present when the Brazelton wasgiven, and they periodically completed questionnaires at home on theirparenting attitudes and their infants’ development. Brazelton assessments wererepeated at the end of the infants’ first month. The experimental group infantsperformed better than the control group infants on the orienting and stateorganization scales of the Brazelton. These findings suggested that this simpleand cost-effective intervention benefited infants of depressed mothers during theearly postpartum period.

LIMITATIONS OF THESE STUDIES

Several limitations of these studies should be noted. First, less than 3% of ourprenatal clinic population was receiving treatment for their prenatal depression,which is consistent with other samples (Flynn, Blow, & Marcus, 2006). Thesestudies were also limited to lower socioeconomic status women who, of course,have many other problems in addition to their depression, as was noted in ourstudy on multiple risk factors (Field et al., 2006).

Other comorbid risk factors like anxiety and anger were not assessed in all ofthe studies. In the studies that assessed comorbidity, the women with comorbiddepression and anxiety and their newborns fared worse (Field et al., 2008) and, ofcourse, the comorbid condition of depression and anxiety is more common thanprenatal depression alone (Hoffman & Hatch, 2000).

The prenatal assessments were limited to two time periods during pregnancy(16–20 weeks gestation and 30–34 weeks gestation), and different gestational agefoetuses may, of course, be differentially affected (Martin & Dombrowski, 2008).It is, however, difficult to recruit younger gestational age women because theytypically do not attend prenatal clinics at an earlier age, and late in gestation, theyare often delivering prematurely.



Our continuing focus on cortisol as a potential predictor is also limited.Although we have elsewhere referred to cortisol as the ‘culprit variable’(see Field & Diego, 2008 for a review), several other variables have been exploredand need further study, including uterine artery resistance (Copper et al., 1996;Tchirikov, Rybakowski, Huneke, Schoder, Schroder, 2002; Van den Bergh, Mulder,Mennes, & Glover, 2005), and other biochemical markers, including nor-epinephirine (Lundy et al., 1999), progesterone and estriol. For example, pro-gesterone/estriol ratios have predicted prematurity, which suggests that theymight also affect neonatal perception (Ruiz et al., 2008).

Immune factors have also been implicated in depression, including elevatedpro-inflammatory cytokines (most especially IL-1, IL-6 and TNF-alpha) and lowlevels of natural killer cell activity (Suarez, Lewis, Krishnan, & Young, 2004;Zorilla, Luporsky, McKay, Rosenthal, Houldin, et al., 2001). These models havenot yet been explored in prenatally depressed women.

Others (Wust, Federenko, van Rossum, Koper, & Hellhammer, 2005) havesuggested that genetic determinants could mediate the relationship betweendepression and elevated cortisol inasmuch as twin studies have shown highheritability of cortisol levels (Bartels, Van den Bergh, Sluyter, Boomsa, & de Geus,2003; Federenko, Nagamine, Hellhammer, Wadhwa, & Wust, 2004; Wust, Fed-erenko, Hellhammer, & Kirschbaum, 2000). In this way, according to the authors,genetic factors may influence the cortisol levels that the foetus is exposed to and,in turn, impact neonatal behaviour.

Lastly, developmental follow-ups are needed to determine any lasting effectsof prenatal depression. If the depression is chronic, one might expect that theprenatal depression effects would be compounded by the postpartum depressioneffects that have been reported into late childhood (Hay, Pawlby, Angold, Harold,& Sharp, 2003). Other prenatal depression effects may only emerge later in de-velopment (Martin & Dembrowski, 2008). It is also not clear which variables aremediating the inferior performance of these newborns on perceptual tasks, forexample, whether it’s elevated arousal, less attentiveness and/or other variablesyet to be considered. And, it is not known whether the limited perceptual abilitiesof these newborns continue into infancy. Again, more controlled studies areneeded as well as longitudinal and early intervention studies.

ACKNOWLEDGEMENTS

We would like to thank the mothers and infants who participated in these studiesand the research associates who assisted us. This research was supported by aMerit Award (MH46586), Senior Research Scientist Awards (MH00331 andAT001585) and a March of Dimes Grant (] 12-FYO3-48) to Tiffany Field andfunding from Johnson and Johnson Pediatric Institute to the Touch ResearchInstitutes.

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