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Altered corticolimbic connectivity reveals sex-specific adolescent outcomes in a rat model of early life adversity.

ABSTRACT: Exposure to early-life adversity (ELA) increases the risk for psychopathologies associated with amygdala-prefrontal cortex (PFC) circuits. While sex differences in vulnerability have been identified with a clear need for individualized intervention strategies, the neurobiological substrates of ELA-attributable differences remain unknown due to a paucity of translational investigations taking both development and sex into account. Male and female rats exposed to maternal separation ELA were analyzed with anterograde tracing from basolateral amygdala (BLA) to PFC to identify sex-specific innervation trajectories through juvenility (PD28) and adolescence (PD38;PD48). Resting-state functional connectivity (rsFC) was assessed longitudinally (PD28;PD48) in a separate cohort. All measures were related to anxiety-like behavior. ELA-exposed rats showed precocial maturation of BLA-PFC innervation, with females affected earlier than males. ELA also disrupted maturation of female rsFC, with enduring relationships between rsFC and anxiety-like behavior. This study is the first providing both anatomical and functional evidence for sex- and experience-dependent corticolimbic development.

SUBMITTER: Honeycutt JA

PROVIDER: S-EPMC7010412 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Altered corticolimbic connectivity reveals sex-specific adolescent outcomes in a rat model of early life adversity.

Honeycutt Jennifer A JA Demaestri Camila C Peterzell Shayna S Silveri Marisa M MM Cai Xuezhu X Kulkarni Praveen P Cunningham Miles G MG Ferris Craig F CF Brenhouse Heather C HC

eLife 20200120

Exposure to early-life adversity (ELA) increases the risk for psychopathologies associated with amygdala-prefrontal cortex (PFC) circuits. While sex differences in vulnerability have been identified with a clear need for individualized intervention strategies, the neurobiological substrates of ELA-attributable differences remain unknown due to a paucity of translational investigations taking both development and sex into account. Male and female rats exposed to maternal separation ELA were analy ...[more]

PMID: 31958061

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Project description:BACKGROUND:Stunting affects more than 161 million children worldwide and can compromise cognitive development beginning early in childhood. There is a paucity of research using neuroimaging tools in conjunction with sensitive behavioral assays in low-income settings, which has hindered researchers' ability to explain how stunting impacts brain and behavioral development. We employed high-density EEG to examine associations among children's physical growth, brain functional connectivity (FC), and cognitive development. METHODS:We recruited participants from an urban impoverished neighborhood in Dhaka, Bangladesh. One infant cohort consisted of 92 infants whose height (length) was measured at 3, 4.5, and 6?months; EEG data were collected at 6?months; and cognitive outcomes were assessed using the Mullen Scales of Early Learning at 27?months. A second, older cohort consisted of 118 children whose height was measured at 24, 30, and 36?months; EEG data were collected at 36?months; and Intelligence Quotient (IQ) scores were assessed at 48?months. Height-for-age (HAZ) z-scores were calculated based on the World Health Organization standard. EEG FC in different frequency bands was calculated in the cortical source space. Linear regression and longitudinal path analysis were conducted to test the associations between variables, as well as the indirect effect of child growth on cognitive outcomes via brain FC. RESULTS:In the older cohort, we found that HAZ was negatively related to brain FC in the theta and beta frequency bands, which in turn was negatively related to children's IQ score at 48?months. Longitudinal path analysis showed an indirect effect of HAZ on children's IQ via brain FC in both the theta and beta bands. There were no associations between HAZ and brain FC or cognitive outcomes in the infant cohort. CONCLUSIONS:The association observed between child growth and brain FC may reflect a broad deleterious effect of malnutrition on children's brain development. The mediation effect of FC on the relation between child growth and later IQ provides the first evidence suggesting that brain FC may serve as a neural pathway by which biological adversity impacts cognitive development.

Dataset Information

Altered corticolimbic connectivity reveals sex-specific adolescent outcomes in a rat model of early life adversity.

Publications

Altered corticolimbic connectivity reveals sex-specific adolescent outcomes in a rat model of early life adversity.

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