NeuroImage (Apr 2020)

Smaller anterior subgenual cingulate volume mediates the effect of girls’ early sexual maturation on negative psychobehavioral outcome

  • Naohiro Okada,
  • Noriaki Yahata,
  • Daisuke Koshiyama,
  • Kentaro Morita,
  • Kingo Sawada,
  • Sho Kanata,
  • Shinya Fujikawa,
  • Noriko Sugimoto,
  • Rie Toriyama,
  • Mio Masaoka,
  • Shinsuke Koike,
  • Tsuyoshi Araki,
  • Yukiko Kano,
  • Kaori Endo,
  • Syudo Yamasaki,
  • Shuntaro Ando,
  • Atsushi Nishida,
  • Mariko Hiraiwa-Hasegawa,
  • Kiyoto Kasai

Journal volume & issue
Vol. 209
p. 116478

Abstract

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Early-maturing girls are relatively likely to experience compromised psychobehavioral outcomes. Some studies have explored the association between puberty and brain morphology in adolescents, while the results were non-specific for females or the method was a region-of-interest analysis. To our knowledge, no large-scale study has comprehensively explored the effects of pubertal timing on whole-brain volumetric development or the neuroanatomical substrates of the association in girls between pubertal timing and psychobehavioral outcomes. We collected structural magnetic resonance imaging (MRI) data of a subsample (N ​= ​203, mean age 11.6 years) from a large-scale population-based birth cohort. Tanner stage, a scale of physical maturation in adolescents, was rated almost simultaneously with MRI scan. The Strengths and Difficulties Questionnaire total difficulties (SDQ-TD) scores were rated by primary parents some duration after MRI scan (mean age 12.1 years). In each sex group, we examined brain regions associated with Tanner stage using whole-brain analysis controlling for chronological age, followed by an exploration of brain regions also associated with the SDQ-TD scores. We also performed mediation analyses. In girls, Tanner stage was significantly negatively correlated with gray matter volumes (GMVs) in the anterior/middle cingulate cortex (ACC/MCC), of which the subgenual ACC (sgACC) showed a negative correlation between GMVs and SDQ-TD scores. Smaller GMVs in the sgACC mediated the association between higher Tanner stages and higher SDQ-TD scores. We found no significant results in boys. Our results from a minimally biased, large-scale sample provide new insights into neuroanatomical correlates of the effect of pubertal timing on developmental psychological difficulties emerging in adolescence.

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