The role of puberty on physical and brain development: A longitudinal study in male Rhesus Macaques

• Type of Material: Article
• Authors: ZA Kovacs-Balint, Emory University; Jessica Raper, Emory University; R Richardson, Emory University; A Gopakumar, Emory University; KP Kettimuthu, Emory University; Melinda Higgins, Emory University; E Feczko, University of Minnesota; E Earl, Oregon Health and Science University; Kelly Ethun, Emory University; Longchuan Li, Emory University; M Styner, University of North Carolina; D Fair, University of Minnesota; Jocelyne Bachevalier, Emory University; Maria Sanchez, Emory University
• Language: English
• Date: 2023-04-07
• Publisher: ELSEVIER SCI LTD
• Publication Version: Final Published Version
• Copyright Statement: © 2023 The Authors
• License: Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1016/j.dcn.2023.101237
• Title of Journal or Parent Work: DEVELOPMENTAL COGNITIVE NEUROSCIENCE
• Volume: 60
• Start Page: 101237
• End Page: 101237
• Grant/Funding Information: This work was supported by the National Institutes of Health (NIH) grant numbers HD090925, MH100029, MH078105-01S1, MH078105-04S1, MH096773, MH086633, MH091645, P50 HD103573, U54 HD079124, K99/R00 MH091238, T15LM007088 and the NIH’s Office of the Director, Office of Research Infrastructure Programs (ORIP) OD P51OD011132 (ENPRC Base Grant); both the Imaging Center and the Biomarkers Core Laboratory are facilities supported by the ENPRC Base Grant P51OD011132. The funders had no role in review design, data collection and analysis, decision to publish, or preparation of the manuscript. The content is solely the responsibility of the authors and does not represent the official views of the NICHD, NIMH, or the NIH. The ENPRC is fully accredited by AAALAC International.
• Keywords: MRI; ELEMENT-BINDING PROTEIN; PUBERTAL DEVELOPMENT; FUNCTIONAL CONNECTIVITY; Adolescence; PREFRONTAL CORTEX; Science & Technology; Testosterone; MACACA-MULATTA; DEVELOPMENTAL TRAJECTORIES; Psychology, Developmental; Life Sciences & Biomedicine; RHESUS-MONKEY; Social Sciences; Amygdala; POSTNATAL-DEVELOPMENT; Hippocampus; Neurosciences; ANDROGEN RECEPTORS; Prefrontal cortex; Neurosciences & Neurology; Psychology; BRAIN-DEVELOPMENT
• Research Categories: Psychology, Developmental; Biology, Neuroscience

Abstract

This study examined the role of male pubertal maturation on physical growth and development of neurocircuits that regulate stress, emotional and cognitive control using a translational nonhuman primate model. We collected longitudinal data from male macaques between pre- and peri-puberty, including measures of physical growth, pubertal maturation (testicular volume, blood testosterone -T- concentrations) and brain structural and resting-state functional MRI scans to examine developmental changes in amygdala (AMY), hippocampus (HIPPO), prefrontal cortex (PFC), as well as functional connectivity (FC) between those regions. Physical growth and pubertal measures increased from pre- to peri-puberty. The indexes of pubertal maturation -testicular size and T- were correlated at peri-puberty, but not at pre-puberty (23 months). Our findings also showed ICV, AMY, HIPPO and total PFC volumetric growth, but with region-specific changes in PFC. Surprisingly, FC in these neural circuits only showed developmental changes from pre- to peri-puberty for HIPPO-orbitofrontal FC. Finally, testicular size was a better predictor of brain structural maturation than T levels -suggesting gonadal hormones-independent mechanisms-, whereas T was a strong predictor of functional connectivity development. We expect that these neural circuits will show more drastic pubertal-dependent maturation, including stronger associations with pubertal measures later, during and after male puberty.