Neural processing of infant and adult face emotion and maternal exposure to childhood maltreatment.
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ABSTRACT:
SUBMITTER: Olsavsky AK
PROVIDER: S-EPMC7058929 | biostudies-literature | 2019 Sep
REPOSITORIES: biostudies-literature
Publications
Neural processing of infant and adult face emotion and maternal exposure to childhood maltreatment.
Olsavsky Aviva K AK Stoddard Joel J Erhart Andrew A Tribble Rebekah R Kim Pilyoung P
Social cognitive and affective neuroscience 20190901 9
Face processing in mothers is linked to mother-infant social communication, which is critical for parenting and in turn for child development. Neuroimaging studies of child maltreatment-exposed (CME) mothers are sparse compared to studies of mothers with postpartum depression, which have suggested blunted amygdala reactivity to infant stimuli. We expected to see a similar pattern in CME mothers. Based on broader studies in trauma-exposed populations, we anticipated increased amygdala reactivity ...[more]
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Project description:BackgroundIndividuals with a history of maltreatment show altered amygdala reactivity to emotional stimuli, atypical frontal regulatory control, and differences in frontolimbic connectivity compared with nonmaltreated controls. However, despite early trauma, many individuals who experience maltreatment show resilience or adaptive functioning in adulthood including positive social, educational, and occupational outcomes.MethodsThe present study used a psychophysiological interaction model to examine the effect of adult adaptive functioning on group differences between maltreated and nonmaltreated adults in task-based amygdala functional connectivity. The task used was a facial emotion-matching paradigm. Functional magnetic resonance imaging scans were collected from 41 adults with a history of substantiated childhood maltreatment and 39 nonmaltreated adults who were well matched on demographic variables, all of whom had been studied since childhood. Adaptive functioning was measured with a composite score of success on stage-salient developmental tasks.ResultsConsistent with previous research, we found differences in task-related amygdala functional connectivity between the maltreated and nonmaltreated groups. Effects were seen in the left hippocampus, right dorsolateral prefrontal cortex, dorsomedial prefrontal cortex, and right thalamus. However, when adult functioning was included in the model, maltreatment-related differences in amygdala connectivity were observed only in the hippocampus. Adult adaptive functioning independently predicted task-related amygdala connectivity in frontal and parietal regions across the entire sample.ConclusionsThese results suggest that frontolimbic functional connectivity is predicted by positive developmental adaptation in this high-risk population, regardless of maltreatment history, whereas intralimbic connectivity (amygdala and hippocampus) is more specifically associated with maltreatment history.
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Project description:BackgroundCognitive models of post-traumatic stress disorder (PTSD) propose that trauma entails cognitive alterations of increased distrust and perceived threat from others. We tested whether these predictions also hold in individuals with varying levels of childhood maltreatment (CM), which is much more prevalent than traumatic events as required for a PTSD diagnosis. We hypothesized that higher levels of CM would entail greater distrust and perceived threat, and that distrust would be more change-resistant in participants with more CM.MethodsThe study was pre-registered; the pre-registration protocol, data, and code are available at https://osf.io/pufy2/ . We recruited 549 participants (M age = 29.2, 74.5% women) for an online study via websites related to CM, Borderline Personality Disorder, and via snowball method on social media. Participants self-reported their level of CM on the childhood trauma questionnaire (CTQ). Next, they played two rounds of a hypothetical distrust game, indicating the perceived trustworthiness of avatars by way of estimating expected monetary deductions from them (i.e. higher amounts indicating greater distrust). After the first round, we provided participants with the feedback that very little money was taken from them. We expected those with more CM to be less responsive to the positive feedback and to adapt their estimates less in the subsequent round. Following the distrust game, participants completed an emotion rating task in which they rated the emotional expressions of 60 faces on a scale from 'very negative' to 'very positive'. We included angry, fearful, and happy facial expressions, and expected individuals with higher CM levels to provide more negative ratings. We conducted linear mixed effects models with random intercepts for raters and stimuli (crossed), and modelled random slopes for all within-person predictors.ResultsAs hypothesized, higher levels of CM were associated with higher levels of distrust and a weaker decrease in distrust following positive feedback. Further supporting our hypotheses, individuals with higher levels of CM showed more negatively shifted emotion ratings.ConclusionsIncreased distrust and perceived interpersonal threat following trauma, as proposed in cognitive models of PTSD, likely also apply to individuals with CM, following a dose-response relationship. We discuss clinical implications of considering any level of CM as a potentially relevant treatment-factor, even when a trauma-related disorder is not the main diagnosis, and propose future research avenues.
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Project description:PurposeTo determine the association between maternal exposure to childhood maltreatment (CM) and risk of stillbirth (fetal death at or after 20 weeks' gestation).MethodsPopulation-based case-control study from the Stillbirth Collaborative Research Network (SCRN) conducted in 2006-2008, and the follow-up study, SCRN-Outcomes after Study Index Stillbirth (SCRN-OASIS), conducted in 2009 in the United States. Cases (n = 133) included women who experienced a stillbirth, excluding stillbirths attributed to genetic/structural or umbilical cord abnormalities and intrapartum stillbirths. Controls (n = 500) included women delivering a healthy term live birth (excluding births less than 37 weeks gestation, neonatal intensive care unit admission, or death). CM exposure was measured using the Childhood Trauma Questionnaire, administered during the SCRN-OASIS study. Dichotomized scores for five subscales of CM (physical abuse, physical neglect, emotional abuse, emotional neglect, and sexual abuse) and an overall measure of CM exposure were analyzed using logistic regression.ResultsGenerally, there was no association between CM and stillbirth, except for the emotional neglect subscale (OR: 1.93; 95% CI: 1.17, 3.19).ConclusionsChildhood neglect is understudied in comparison to abuse and should be included in the future studies of associations between CM and pregnancy outcomes, including stillbirth.
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Project description:Accumulating evidence suggests that childhood maltreatment (CM) confers risk for psychopathology later in life by inducing hypervigilance to social threat cues such as fearful faces. However, it remains unclear whether the modulatory impact of CM extents to the olfactory domain of social communication in humans. To address this question, we examined whether CM modulates the neural processing of chemosensory threat signals in sweat and whether CM affects the stress-reducing effects of oxytocin (OXT) in this context. In a randomized, double-blind within-subject functional MRI study design, 58 healthy participants (30 females) received intranasal OXT (40 IU) or placebo (PLC) and completed a forced-choice emotion recognition task with faces of varying emotion intensities (neutral to fearful) while exposed to sweat stimuli and a non-social control odor. Axillary sweat samples were collected from 30 healthy male donors undergoing an acute psychosocial stressor (stress) and ergometer training (sport) as control in a pre-study. CM was assessed by the 25-item Childhood Trauma Questionnaire (CTQ). The final fMRI analysis included 50 healthy participants (26 females). Regression analysis showed a stress-specific association of CTQ scores with amygdala hyperreactivity, hippocampal deactivation, and increased functional connectivity between the amygdala and the hippocampus, medial orbitofrontal cortex, and the anterior cingulate cortex (ACC) under PLC. Furthermore, we observed a positive association of CTQ scores and the dampening effects of OXT on stress-related amygdala responses. Our findings suggest that CM may induce hypervigilance to chemosensory threat cues in a healthy sample due to inefficient frontolimbic inhibition of amygdala activation. Future studies should investigate whether increased recruitment of the intralimbic amygdala-hippocampus complex reflects a compensatory mechanism that prevents the development of psychopathology in those who have experienced CM. Furthermore, the results reveal that the stress-specific effects of OXT in the olfactory domain are more pronounced in participants with increasing levels of CM exposure.
| S-EPMC7425696 | biostudies-literature
Project description:Although a growing literature describes the effects of negative childhood experiences on biological outcomes, it is difficult to compare results across studies because of differences in measures of childhood experiences, biological markers, sample characteristics, and included covariates. To ensure comparability across its analyses, this study used a single national survey of adults in the United States-the Midlife in the United States (MIDUS) study-to examine comprehensively the association between adverse childhood experiences, operationalized as childhood maltreatment (CM), and biological markers of risk for poor health and to assess whether these associations differ by type of maltreatment, sex, or race. The sample included 1254, mostly White (78%), adults aged 34-86 years (mean age 57 years), 57% of whom were female. We present incidence rate ratios (IRR) from negative binomial and Poisson regressions to examine the relationships between exposure to CM (emotional, physical, and sexual abuse; emotional and physical neglect; and a CM-index reflecting frequency across all five types of maltreatment) and four biological risk summary scores (overall physiological dysregulation, cardiometabolic risk, inflammation, and hypothalamic pituitary axis/sympathetic nervous system (HPA/SNS) function). We also tested whether the effect of each type of CM varied by sex and by race. The CM-index was associated with higher overall physiological dysregulation and inflammation, but the associations were weaker and not statistically significant for cardiometabolic risk and HPA/SNS function. With the exception of a possible sex difference in the association between sexual abuse and overall physiological dysregulation, there was little evidence that the associations varied systematically by type of CM or by sex or race. We conclude that exposure to CM predicts adult biological risk, particularly inflammation. Inconsistency with previous research suggests that additional research is needed to confirm findings regarding sex and race differences.
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Project description:UNLABELLED:Major depression has been repeatedly associated with amygdala hyper-responsiveness to negative (but not positive) facial expressions at early, automatic stages of emotion processing using subliminally presented stimuli. However, it is not clear whether this "limbic bias" is a correlate of depression or represents a vulnerability marker preceding the onset of the disease. Because childhood maltreatment is a potent risk factor for the development of major depression in later life, we explored whether childhood maltreatment is associated with amygdalar emotion processing bias in maltreated but healthy subjects. Amygdala responsiveness to subliminally presented sad and happy faces was measured by means of fMRI at 3 T in N = 150 healthy subjects carefully screened for psychiatric disorders. Childhood maltreatment was assessed by the 25-item childhood trauma questionnaire (CTQ). A strong association of CTQ-scores with amygdala responsiveness to sad, but not happy facial expressions emerged. This result was further qualified by an interaction of emotional valence and CTQ-scores and was not confounded by trait anxiety, current depression level, age, gender, intelligence, education level, and more recent stressful life-events. Childhood maltreatment is apparently associated with detectable changes in amygdala function during early stages of emotion processing which resemble findings described in major depression. Limbic hyper-responsiveness to negative facial cues could be a consequence of the experience of maltreatment during childhood increasing the risk of depression in later life. LIMITATION:the present association of limbic bias and maltreatment was demonstrated in the absence of psychopathological abnormalities, thereby limiting strong conclusions.
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Project description:Maternal childhood maltreatment experiences (CMEs) may influence responses to infants and affect child outcomes. We examined associations between CME and mothers' neural responses and functional connectivity to infant distress. We hypothesized that mothers with greater CME would exhibit higher amygdala reactivity and amygdala-supplementary motor area (SMA) functional connectivity to own infant's cries. Postpartum mothers (N = 57) assessed for CME completed an functional magnetic resonance imaging task with cry and white-noise stimuli. Amygdala region-of-interest and psychophysiological interaction analyses were performed. Our models tested associations of CME with activation and connectivity during task conditions (own/other and cry/noise). Exploratory analyses with parenting behaviors were performed. Mothers with higher CME exhibited higher amygdala activation to own baby's cries vs other stimuli (F1,392 = 6.9, P < 0.01, N = 57) and higher differential connectivity to cry vs noise between amygdala and SMA (F1,165 = 22.3, P < 0.001). Exploratory analyses revealed positive associations between both amygdala activation and connectivity and maternal non-intrusiveness (Ps < 0.05). Increased amygdala activation to own infant's cry and higher amygdala-SMA functional connectivity suggest motor responses to baby's distress. These findings were associated with less intrusive maternal behaviors. Follow-up studies might replicate these findings, add more granular parenting assessments and explore how cue processing leads to a motivated maternal approach in clinical populations.
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Project description:BackgroundChildhood maltreatment and peer victimisation are common sources of early-life interpersonal stress. Childhood maltreatment is associated with atypical frontolimbic emotion processing and regulation, and increased vulnerability for self-harm/suicide. However, few studies have compared the neurofunctional correlates between caregiver- versus peer-inflicted mistreatment.AimsWe compared the alterations of neurofunctional correlates of facial emotion processing in youths exposed to childhood maltreatment or peer victimisation, and explored their associations with self-harm.MethodFunctional magnetic resonance imaging data were collected from 114 age- and gender-matched youths (39 childhood maltreatment, 37 peer victimisation and 38 controls) during an emotion discrimination task. Region-of-interest (amygdala, insula) and whole-brain analyses were conducted.ResultsGroups differed significantly during disgust processing only. Both groups had lower activation in the right amygdala and bilateral posterior insula than controls; left insular underactivation was furthermore related to increased self-harm in maltreated youths. Compared with controls, at the whole-brain level, both groups also had underactivation in a cluster of bilateral limbic-thalamic-striatal, precuneus/posterior cingulate, temporal, fusiform/lingual and cerebellar regions, which was negatively associated with emotional problems in controls, as well as a cluster of somatosensory regions associated with increased self-harm in maltreated youths.ConclusionsEarly-life interpersonal stress from caregivers or peers is associated with common underactivation of limbic-thalamic-striatal, precuneus/posterior cingulate and somatosensory regions during disgust processing. The hypoactivation of key emotion and sensory processing and self-referential brain regions could be a potential suppressive mechanism to cope with the aversive emotion; however, it may also entail increased risk of affective psychopathology in seemingly healthy youths.
| S-EPMC11698183 | biostudies-literature
Project description:BackgroundChild maltreatment (CM) has severe effects on psychological and physical health. The hypothalamic-pituitary-adrenal (HPA) axis, the major stress system of the body, is dysregulated after CM. The analysis of cortisol and dehydroepiandrosterone (DHEA) in scalp hair presents a new and promising methodological approach to assess chronic HPA axis activity. This study investigated the effects of CM on HPA axis activity in the last trimester of pregnancy by measuring the two important signaling molecules, cortisol and DHEA in hair, shortly after parturition. In addition, we explored potential effects of maternal CM on her offspring's endocrine milieu during pregnancy by measuring cortisol and DHEA in newborns' hair.MethodsCM was assessed with the Childhood Trauma Questionnaire (CTQ). Cortisol and DHEA were measured in hair samples of 94 mothers and 30 newborns, collected within six days after delivery. Associations of maternal CM on her own and her newborn's cortisol as well as DHEA concentrations in hair were analyzed with heteroscedastic regression models.ResultsHigher CM was associated with significantly higher DHEA levels, but not cortisol concentrations in maternal hair. Moreover, maternal CM was positively, but only as a non-significant trend, associated with higher DHEA levels in the newborns' hair.ConclusionsResults suggest that the steroid milieu of the mother, at least on the level of DHEA, is altered after CM, possibly leading to non-genomic transgenerational effects on the developing fetus in utero. Indeed, we observed on an explorative level first hints that the endocrine milieu for the developing child might be altered in CM mothers. These results need extension and replication in future studies. The measurement of hair steroids in mothers and their newborns is promising, but more research is needed to better understand the effects of a maternal history of CM on the developing fetus.
| S-EPMC5461775 | biostudies-literature
Project description:BackgroundPrevention studies for perinatal depression rarely focus on the mother-infant dyad or consider the impact of maternal childhood maltreatment (CM).MethodsA secondary analysis of two combined randomized controlled trials of Practical Resources for Effective Postpartum Parenting (PREPP) examined the moderating role of CM on the efficacy of preventing perinatal depression and effects on infant behavior at six weeks.Results32% of 109 pregnant women endorsed CM (CM+). At six weeks postpartum, women who received PREPP compared to enhanced treatment as usual (ETAU) had significant reductions in depression and anxiety based on the observer-rated Hamilton Rating Scale for Depression (HRSD) and Hamilton Rating Scale for Anxiety (HRSA) (mean difference of M=-3.84 (SD= 0.14, p<0.01) and M=- 4.31 (SD= 0.32, p <0.001) respectively). When CM was added to the models, there no longer was a significant PREPP versus ETAU treatment effect on HRSD and HRSA outcomes in CM+ women though effects remained for CM- women. However, CM+ women who received PREPP vs ETAU reported a mean increase in infant daytime sleep of 189.8 min (SE= 50.48, p = 0.001).LimitationsSelf-report measures of infant behavior were used.ConclusionsCM+ women versus CM- had limited response to an intervention to prevent perinatal depression yet still reported an increase in infant daytime sleep. This study adds to the growing literature that prevention studies may need to incorporate approaches tailored to fit women with childhood trauma histories while also considering infant functioning as both may be treatment targets relevant to maternal mood.
| S-EPMC8217280 | biostudies-literature