Elsevier

Psychoneuroendocrinology

Volume 51, January 2015, Pages 307-317
Psychoneuroendocrinology

Neonatal amygdala lesions advance pubertal timing in female rhesus macaques

https://doi.org/10.1016/j.psyneuen.2014.09.028Get rights and content

Highlights

  • Neonatal amygdala lesions result in earlier menarche and first ovulation.

  • Neonatal amygdala lesions do not decrease the length of the pubertal period.

  • Greater body weight cannot account for the effects of earlier puberty onset.

  • The effects of social rank on menarche in amygdala-lesioned females are unclear.

  • Social rank did not alter the timing of first ovulation.

Summary

Social context influences the timing of puberty in both humans and nonhuman primates, such as delayed first ovulation in low-ranking rhesus macaques, but the brain region(s) mediating the effects of social context on pubertal timing are unknown. The amygdala is important for responding to social information and thus, is a potential brain region mediating the effects of social context on pubertal timing. In this study, female rhesus macaques living in large, species-typical, social groups received bilateral neurotoxic amygdala lesions at one month of age and pubertal timing was examined beginning at 14 months of age. Pubertal timing was affected in neonatal amygdala-lesioned females (Neo-A), such that they experienced significantly earlier menarche and first ovulation than did control females (Neo-C). Duration between menarche and first ovulation did not differ between Neo-A and Neo-C females, indicating earlier first ovulation in Neo-A females was likely a consequence of earlier menarche. Social rank of Neo-A females was related to age at menarche, but not first ovulation, and social rank was not related to either event in Neo-C females. It is more likely that amygdalectomy affects pubertal timing through its modulation of GABA-ergic mechanisms rather than as a result of the removal of a social-contextual inhibition on pubertal timing.

Section snippets

Subjects

Subjects were female rhesus macaques (N = 16; born March–June) living with their mothers and siblings in large, species-typical social groups at the Yerkes National Primate Research Center (YNPRC) Field Station (Lawrenceville, GA). Subjects were selected from high-, middle-, and low-ranking matrilines, excluding the highest- and lowest-ranking matrilines, so that females had comparable social contexts, with all females having matrilines ranked above and below their matriline. Social groups

Results

Neither age at menarche (t(7) = 1.33, p = .224) nor age at first ovulation (t(7) = 0.73, p = .487) differed between surgical (Neo-C) and behavioral sham (Neo-BC) control females and these two groups were combined as one control group (Neo-C) for all analyses.

Discussion

Age at menarche typically occurs at 2.5 years of age in rhesus macaques (Resko et al., 1982, Wilson et al., 1988). Neonatal amygdalectomy resulted in menarche in all Neo-A females at approximately 1.5 years of age, one year earlier than menarche is typically observed. The proportion of females reaching first ovulation each season did not differ between amygdala-lesioned and control females, possibly because, opposite to our prediction, the variation in age at first ovulation was greater in

Conclusion

The current study demonstrates the amygdala can influence the HPG axis and that damage to the amygdala early in life can result in earlier pubertal onset and reproductive maturity.

Role of the funding sources

This project was funded by the National Institute of Mental Health (MH050268). The Yerkes National Primate Research Center is supported by The National Center for Research Resources (P51 RR00165; YNPRC Base grant) and is currently supported by the Office of Research Infrastructure Programs (OD P51OD11132). The funding sources were not involved in the study design, data collection, analysis, or writing of the manuscript. The decision to submit the article for publication was at the discretion of

Conflict of interest

The authors declare no competing financial interests.

Acknowledgements

The YNPRC is fully accredited by the Association for the Assessment and Accreditation of Laboratory Animal Care International. The authors thank Trina Villarreal, Amy Henry, Sara Dicker, Rebecca Roberts, M.A, Daniela Sanchez, M.A., Maurand Cappelletti, M.A., Casie Lyons, and Patrick MacFarland for their assistance with data collection, the Bachevalier lab for their work in completing the amygdala lesion surgeries and estimation of the lesion extent, and Dr. Mark Wilson and Dr. Mar Sanchez for

References (41)

  • F. Döcke

    Differential effects of amygdaloid and hippocampal lesions on female puberty

    Neuroendocrinology

    (1974)
  • F. Döcke et al.

    Studies on the puberty-controlling function of the mediocortical amygdala in the immature female rat

    Neuroendocrinology

    (1976)
  • F. Döcke et al.

    Evidence for direct central nervous inhibition of LH secretion during sexual maturation of female rats

    Endokrinologie

    (1980)
  • B. Ersoy et al.

    The factors affecting the relation between menarcheal age of mother and daughter

    Child Care Health Dev.

    (2005)
  • D.L. Foster

    Luteinizing hormone and progesterone secretion during sexual maturation of the rhesus monkey: short luteal phases during initial menstrual cycles

    Biol. Reprod.

    (1977)
  • R.E. Frisch et al.

    Height and weight at menarche and a hypothesis of critical body weights and adolescent events

    Science

    (1970)
  • J.A. Graber et al.

    The antecedents of menarcheal age: heredity, family environment, and stressful life events

    Child Dev.

    (1995)
  • M.M. Grumbach et al.

    Puberty: ontogeny, neuroendocrinology physiology and disorders

  • M.E. Herman-Giddens

    Recent data on pubertal milestones in United States children: the secular trend toward earlier development

    Int. J. Androl.

    (2006)
  • K.L. Keen et al.

    Effects of pulsatile infusion of the GABAA receptor blocker bicuculline on the onset of puberty in female rhesus monkeys

    Endocrinology

    (1999)
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