Pubertal hormones organize the adolescent brain and behavior

Sisk, Cheryl L.; Zehr, Julia L.

doi:10.1016/j.yfrne.2005.10.003

Cited by 1,082Sexual Differentiation and DisordersHypothalamic control of reproductive hormonesNeuroendocrine regulation and behavior

Pubertal hormones organize the adolescent brain and behavior

Sisk, Cheryl L., Zehr, Julia L.·2005·Frontiers in Neuroendocrinology

DOI 10.1016/j.yfrne.2005.10.003

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Abstract

Maturation of the reproductive system during puberty results in elevated levels of gonadal steroid hormones. These hormones sculpt neural circuits during adolescence, a time of dramatic rewiring of the nervous system. Here, we review the evidence that steroid-dependent organization of the adolescent brain programs a variety of adult behaviors in animals and humans. Converging lines of evidence indicate that adolescence may be a sensitive period for steroid-dependent brain organization and that variation in the timing of interactions between the hormones of puberty and the adolescent brain leads to individual differences in adult behavior and risk of sex-biased psychopathologies.

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At least in adulthood, the anterior insular cortex participates in multiple brain networks and varies its functional involvement according to stimulus environment and task demands.
“That is, at least in adulthood, this region participates in multiple brain networks and varies its functional involvement with these networks according to the nature of the stimulus environment and task demands.”
From The role of the anterior insula in adolescent decision making (2014) · cites this paper as [10]
Theorists propose that the anterior insular cortex acts as an integrative hub coordinating recruitment of task- and context-relevant brain networks in response to arousal.
“More recently, theorists have proposed that AIC function goes beyond simply interpreting signals of arousal, and have argued that this region acts as an ‘integrative hub’ which is centrally involved in coordinating the recruitment of task- and context-relevant brain networks in response to arousal [10].”
From The role of the anterior insula in adolescent decision making (2014) · cites this paper as [10]
The anterior insular cortex is thought to act as a hub integrating cognitive and emotional information and to have structural and functional connections to regions prominent in developmental models, including lateral prefrontal cortex and striatum.
“This region is thought to act as a hub involved in the integration of cognitive and emotional information [10], and to have structural and functional connections to regions that feature prominently in current developmental models of adolescent decision making (e.g., the IPFC and striatum).”
From The role of the anterior insula in adolescent decision making (2014) · cites this paper as [10]
During adolescence there are hormonally-driven organizational and activational changes in the brain.
“During adolescence there are hormonally-driven organizational and activational changes in the brain”
From Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking (2013) · cites this paper as Sisk & Zehr, 2005
Recent studies demonstrate that organizational changes occur during adolescence and may be critical for activational changes to take place.
“recent studies have demonstrated that there are organizational changes occurring during adolescence as well, and, moreover, that these organizational changes may be critical for activational changes to take place”
From Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking (2013) · cites this paper as Sisk & Zehr, 2005

Activational changes are transient, and affected brain systems often return to their pre-activated state when hormone levels subside.
“Activational changes are considered transient, and the brain systems affected by them often return to their pre-activated state when hormone levels subside”
From Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking (2013) · cites this paper as Sisk & Zehr, 2005
Organizational changes are permanent changes in brain structure and organization initiated by hormone release but not dependent on continuing hormone release.
“organizational changes are permanent changes in the structure and organization of brain regions that are initiated by the release of hormones but not dependent on continuing hormone release”
From Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking (2013) · cites this paper as Sisk & Zehr, 2005
Restructuring in the pubertal brain is argued to be driven by hormonal changes and to carry functional consequences for higher-order functions such as executive functions and social cognition.
“These processes of restructuring in the pubertal brain are argued to be driven by hormonal changes (Sisk and Foster 2004;Sisk and Zehr 2005;Schulz et al. 2009) and to carry functional consequences on higher order brain functions such as executive functions and social cognition”
From Developmental Changes in Organization of Structural Brain Networks (2013) · cites this paper as Sisk and Zehr 2005
Sex hormones intensify adolescent behavioral and psychological changes.
“Sex hormones intensify adolescent behavioral and psychological changes (94–96), but in emerging adulthood and into adulthood, average rates of depression, anxiety, and risk-taking decline.”
From Emerging Adulthood, a Pre-adult Life-History Stage (2020) · cites this paper as [94]
Adolescence is often a time when various mental illnesses emerge, including mood disorders, drug abuse disorders, eating disorders, and psychoses.
“adolescence is often a time when various mental illnesses emerge such as mood disorders, drug abuse disorders, eating disorders, and psychoses (Pine 2002; Chambers, Taylor et al. 2003; Sisk and Zehr 2005; Paus, Keshavan et al. 2008)”
From Developmental imaging genetics: Linking dopamine function to adolescent behavior (2014) · cites this paper as Sisk and Zehr 2005
During preadolescence, the dopaminergic system experiences a restructuring that involves a reduction in the density of dopamine receptors in the striatum and prefrontal cortex, leading to an increased dopamine response.
“During preadolescence, the dopaminergic system experiences a restructuring that involves a reduction in the density of dopamine receptors in the striatum and prefrontal cortex, leading to an increased dopamine response (see review by Sisk and Zehr 2005).”
From Sleep Problems Across Development: A Pathway to Adolescent Risk Taking Through Working Memory (2015) · cites this paper as Sisk and Zehr 2005
The same hormones that contribute to the development of the secondary sex characteristics also play a critical role in reorganizing neural circuitry.
“The same hormones that contribute to the developmental of the secondary sex characteristics also play a critical role in reorganizing neural circuitry (Schulz and Sisk, 2016, Sisk, 2016, Sisk and Zehr, 2005).”
From Becoming a sexual being: The “elephant in the room” of adolescent brain development (2017) · cites this paper as Sisk and Zehr, 2005
Animal models suggest that the behavioral response to gonadal hormones differs between pre- and post-pubertal animals.
“Consistent with the idea that adolescence is a sensitive period for the behavioral effects of gonadal hormones, animal models suggest that the behavioral response to gonadal hormones differs between pre- and post-pubertal animals.”
From Becoming a sexual being: The “elephant in the room” of adolescent brain development (2017) · cites this paper as Sisk and Zehr, 2005
Unlike the pre-pubertal brain, the post-pubertal brain is primed for steroid hormones to activate reproductive behavior.
“Unlike the pre-pubertal brain, the post-pubertal brain is primed for steroid hormones to activate reproductive behavior (Sisk and Zehr, 2005).”
From Becoming a sexual being: The “elephant in the room” of adolescent brain development (2017) · cites this paper as Sisk and Zehr, 2005
Pubertal status is likely to modulate social fears and motivations, due to changing hormones and changing physical appearance.
“Furthermore, pubertal status is likely to modulate social fears and motivations, due to changing hormones and changing physical appearance (Forbes et al., 2010, Sisk and Zehr, 2005).”
From Gaining insight into adolescent vulnerability for social anxiety from developmental cognitive neuroscience (2014) · cites this paper as Sisk and Zehr, 2005

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Early puberty and early sexual activity are associated with bulimic-type eating pathology in middle adolescence11The full text of this article is available via JAH Online at http://www.elsevier.com/locate/ajpmonline.
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Peripubertal castration of male rats, adult open field ambulation and partner preference behavior
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Estrogen and progesterone do not activate Fos in AVPV or LHRH neurons in male rats
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Untitled work
Huttenlocher (1997) · doi:10.1002/(sici)1096-9861(19971020)387:2
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Andersen (2000) · doi:10.1002/1098-2396(200008)37:2
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(1996) · doi:10.1002/(sici)1096-9861(19961202)376:1

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A social neuroscience perspective on adolescent risk-taking
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Understanding adolescence as a period of social–affective engagement and goal flexibility
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The Teenage Brain: Sensitivity to Social Evaluation
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Consensus Statement on the Use of Gonadotropin-Releasing Hormone Analogs in Children
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Sex Differences in the Brain: The Not So Inconvenient Truth
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A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing
Tottenham, N. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.068.2009 · Cited by 651 · see citing works
The organizational–activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues
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Stress and the hypothalamic pituitary adrenal axis in the developmental course of schizophrenia
Walker, E., Mittal, V., & Tessner, K. (2008) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.4.022007.141248 · Cited by 615 · see citing works
Back to the future: The organizational-activational hypothesis adapted to puberty and adolescence
Schulz, K. M., Molenda-Figueira, H. A., & Sisk, C. L. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.03.010 · Cited by 587 · see citing works
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<scp>N</scp> icotine and the adolescent brain
Yuan, M., Cross, S. J., Loughlin, S. E., & Leslie, F. M. (2015) · The Journal of Physiology · doi:10.1113/jp270492 · Cited by 582 · see citing works
Sex differences, gender and addiction
Becker, J. B., McClellan, M. L., & Reed, B. G. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23963 · Cited by 570 · see citing works
Sex differences in the adolescent brain
Lenroot, R., & Giedd, J. N. (2009) · Brain and Cognition · doi:10.1016/j.bandc.2009.10.008 · Cited by 563 · see citing works
Neural circuit mechanisms of social behavior
Chen, P., & Hong, W. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.026 · Cited by 527 · see citing works
Sex differences in the physiology of eating
Asarian, L., & Geary, N. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00446.2012 · Cited by 513 · see citing works
Why Interventions to Influence Adolescent Behavior Often Fail but Could Succeed
Yeager, D. S., Dahl, R. E., & Dweck, C. S. (2018) · Perspectives on Psychological Science · doi:10.1177/1745691617722620 · Cited by 512 · see citing works
White matter development in adolescence: A DTI study
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Pubertal development and behavior: hormonal activation of social and motivational tendencies
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Age differences in affective decision making as indexed by performance on the Iowa gambling task
Cauffman, E., Shulman, E. P., Steinberg, L., Claus, E., Banich, M. T., Graham, S., & Woolard, J. (2010) · Developmental Psychology · doi:10.1037/a0016128 · Cited by 488 · see citing works
Drivers of human development: How relationships and context shape learning and development <sup>1</sup>
Osher, D., Cantor, P., Berg, J., Steyer, L., & Rose, T. (2020) · Applied Developmental Science · doi:10.1080/10888691.2017.1398650 · Cited by 484 · see citing works
“A remodeling of the brain’s dopaminergic system occurs around the time of puberty, in which amounts of dopamine fall sharply from levels in the early developmental phases (e.g., Sisk & Zehr, 2005).”
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Authors: Sisk, C. L., & Zehr, J. L.
Affiliations: Michigan State University (US)
Corresponding author: Sisk, Cheryl L.
ORCID: Sisk, Cheryl L.
Venue: Frontiers in Neuroendocrinology
Publisher: Elsevier BV
Published: 2005-10
Volume: 26
Issue: 3-4
Pages: 163-174
ISSN: 0091-3022 (ISSN-L)
DOI: 10.1016/j.yfrne.2005.10.003
OpenAlex: W2152591277
Cited by: 1,082
References: 159
Citations by year: 2026: 41 · 2025: 36 · 2024: 48 · 2023: 42 · 2022: 48 · 2021: 48 · 2020: 62 · 2019: 63 · 2018: 67 · 2017: 59 · 2016: 72 · 2015: 75 · 2014: 68 · 2013: 99 · 2012: 54
FWCI: 1.57
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Frontiers in Neuroendocrinology (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation
National Institutes of Health
National Institute of Mental Health (MH-068764, MH-068975, R01MH068764, F32MH068975)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: puberty, sex steroids, adolescent brain development, sensitive period, neural circuit maturation
MeSH terms: Adolescent, Animals, Brain, Critical Period, Psychological, Female, Gonads, Humans, Hypothalamo-Hypophyseal System, Male, Neuronal Plasticity, Puberty, Sex Characteristics, Sex Factors, Gonadal Steroid Hormones, Sexual Maturation, Adolescent Development, Mice, Rats

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Pubertal hormones organize the adolescent brain and behavior

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