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Original Investigation
June 26, 2019

Association of Prepubertal and Postpubertal Exposure to Childhood Maltreatment With Adult Amygdala Function

Author Affiliations
  • 1School of Psychology, South China Normal University, Guangzhou, China
  • 2Department of Psychiatry, Harvard Medical School, Boston, Massachusetts
  • 3Developmental Biopsychiatry Research Program, McLean Hospital, Belmont, Massachusetts
  • 4Brain Imaging Center, McLean Hospital, Belmont, Massachusetts
  • 5Equian, Woburn, Massachusetts
JAMA Psychiatry. 2019;76(8):843-853. doi:10.1001/jamapsychiatry.2019.0931
Key Points

Question  What is the association between exposure to childhood maltreatment at different ages and adult amygdala response to threatening faces?

Findings  In this cohort study of 202 young adults, self-reported exposure to maltreatment during early childhood was significantly associated with blunted amygdala response via functional magnetic resonance imaging, whereas early teen exposure was significantly associated with augmented amygdala response.

Meaning  The findings suggest that maltreatment may be a risk factor for disorders characterized by hyperactive amygdala response and disorders associated with hypoactive amygdala responses, which may be associated with differences in age at the time of exposure to specific types of adversity during childhood.

Abstract

Importance  Abnormalities 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.

Objective  To 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 Participants  Data 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.

Exposures  The Maltreatment and Abuse Chronology of Exposure (MACE) scale was used to retrospectively assess type and age of exposure to childhood maltreatment.

Main Outcomes and Measures  Activation 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).

Results  Of 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 Relevance  The 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.

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