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Separable Effects of Childhood Maltreatment and Adult Adaptive Functioning on Amygdala Connectivity During Emotion Processing.

ABSTRACT: BACKGROUND:Individuals 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. METHODS:The 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. RESULTS:Consistent 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. CONCLUSIONS:These 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.

SUBMITTER: Demers LA

PROVIDER: S-EPMC5851478 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Separable Effects of Childhood Maltreatment and Adult Adaptive Functioning on Amygdala Connectivity During Emotion Processing.

Demers Lauren A LA McKenzie Kelly Jedd KJ Hunt Ruskin H RH Cicchetti Dante D Cowell Raquel A RA Rogosch Fred A FA Toth Sheree L SL Thomas Kathleen M KM

Biological psychiatry. Cognitive neuroscience and neuroimaging 20170918 2

<h4>Background</h4>Individuals 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.<h4>Methods</h4>The present study used a psychophysiological interac ...[more]

PMID: 29529406

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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.

Project description:ImportanceAbnormalities in amygdala response to threatening faces have been observed in anxiety disorders, autism, bipolar disorder, depression, posttraumatic stress disorder, and schizophrenia. Abnormally hyperactive and hypoactive responses have typically been associated with anxiety and inhibition vs risk taking and inappropriate social behaviors. Maltreatment is a major risk factor for most of these disorders and is associated with abnormal amygdala function.ObjectiveTo identify the type and age of exposure to childhood maltreatment that are associated with hyperactive and hypoactive amygdala responses in young adulthood.Design, setting, and participantsData collection for this retrospective cohort study took place from November 8, 2010, to August 23, 2012. Data analyses were conducted from September 20, 2012, to June 27, 2018. Participants were recruited from the urban and suburban Boston vicinity without diagnostic restrictions based on exposure history.ExposuresThe Maltreatment and Abuse Chronology of Exposure (MACE) scale was used to retrospectively assess type and age of exposure to childhood maltreatment.Main outcomes and measuresActivation and pattern information functional magnetic resonance imaging were used to assess bilateral amygdala response to angry and fearful faces vs neutral faces or shapes, and sensitive exposure periods were identified using cross-validated artificial intelligence predictive analytics (50 averaged randomized iterations with training on 63.3% and testing on 36.7% of the sample).ResultsOf the 202 participants (mean [SD] age, 23.2 [1.7] years; 118 [58.4%] female), 52 (25.7%) reported no exposure to maltreatment and 150 (74.3%) reported exposure to 1 or more maltreatment types. Eight participants (15.1%) with a MACE score of 0 and 51 (34.2%) with a MACE score of 1 or higher had a history of major depression (odds ratio, 2.40; 95% CI, 1.05-6.06; P = .03); 8 unexposed participants (15.1%) and 46 with MACE scores of 1 or higher (30.9%) had a history of 1 or more anxiety disorders (odds ratio, 2.45; 95% CI, 1.03-6.50; P = .03). Retrospective self-report of physical maltreatment between 3 and 6 years of age and peer emotional abuse at 13 and 15 years were associated with amygdala activation to emotional faces vs shapes. Early exposure was associated with blunted response (β = -0.17, P < .001), whereas later exposure was associated with augmented response (β = 0.16, P < .001). Prepubertal vs postpubertal maltreatment was associated with an opposite response on the voxelwise response pattern in clustering stimuli of the same type (eg, mean [SD] emotional ellipse areas for physical maltreatment at age 4 years vs nonverbal emotional abuse at 13 years: 1.41 [1.05] vs 0.25 [0.10], P < .001) and in distinguishing between stimuli of different types (eg, mean [SD] emotional vs neutral faces distance for peer emotional abuse at age 6 years vs 13 years: 1.89 [0.75] vs 0.80 [0.39], P < .001).Conclusions and relevanceThe findings suggest that prepubertal vs postpubertal developmental differences in the association between maltreatment and amygdala response to threatening or salient stimuli exist. Understanding the role of adversity in different sensitive exposure periods and the potential adaptive significance of attenuated vs enhanced amygdala response may help explain why maltreatment may be a risk factor for many different disorders and foster creation of targeted interventions to preempt the emergence of psychopathology in at-risk youths.

Dataset Information

Separable Effects of Childhood Maltreatment and Adult Adaptive Functioning on Amygdala Connectivity During Emotion Processing.

Publications

Separable Effects of Childhood Maltreatment and Adult Adaptive Functioning on Amygdala Connectivity During Emotion Processing.

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