The DOI matches its Crossref record; 110 of the 111 references it cites were found in a registry or an index.
Puberty and the maturation of the male brain and sexual behavior: recasting a behavioral potential
Abstract
The pubertal transition from the juvenile to adult state requires significant changes in behavior to meet the demands for success and survival in adulthood. These behavioral changes during puberty must be mediated by changes in the structure and/or function of the central nervous system. Despite the profound consequences of puberty on an animal's behavioral repertoire, the mechanisms underlying pubertal maturation of the nervous system remain largely unknown. In this review, we provide a synthesis of neural development during puberty as it relates to maturation of male reproductive behavior. We first outline neuroendocrine events associated with puberty and review work from our laboratory that identifies pubertal changes in the neural substrate controlling male reproduction by comparing the neural responses of prepubertal and adult males to steroids and female chemosensory cues. We then raise the question of whether puberty is a sensitive period in which gonadal hormones influence the structural and functional organization of neural circuits underlying male reproductive behavior. The central thesis of this review is that the development of the nervous system during puberty alters the way in which the male responds to social stimuli, involving the restructuring of neural circuits that integrate steroidal and sensory information and ultimately mediate steroid-dependent social behaviors in adulthood.
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“For instance, in male Syrian hamsters, it is well-established how pubertal hormones influence the structure and function of neural circuits that integrate steroidal and sensory information, and how these changing neural circuits alter the way males respond to social stimuli and engage in mating behaviors (Romeo et al., 2002).”
From Becoming a sexual being: The “elephant in the room” of adolescent brain development (2017) · cites this paper as Romeo et al., 2002
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Sisk, C. L., & Foster, D. L. (2004) · Nature Neuroscience · doi:10.1038/nn1326 · Cited by 1,085
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“The regions that make up the affective node are densely innervated by gonadal steroid receptors and undergo both functional and anatomical reorganization during puberty (Geidd et al. 1997; McEwen, 2001; Osterlund & Hurd, 2001; Romeo et al. 2002; Stevens, 2002).”
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Strategies and Methods for Research on Sex Differences in Brain and Behavior
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“In some cases, for example, steroids acting during puberty may have persistent effects on traits measured later in life (45, 46).”
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Eiland, L. R., & Romeo, R. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.048 · Cited by 539
“…is during this time that social behaviors, such as play, mating, and aggression, as well as alterations in brain gray and white matter volumes, change to their adult-like patterns (Spear, 2000, Romeo et al., 2002, Gogtay et al., 2004, Juraska and Markham, 2004, Markham et al., 2007, Spear, 2010).”
BackgroundSexual behavior in male rodents
Hull, E. M., & Dominguez, J. M. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.03.030 · Cited by 467
“NE antagonists − (Clark and Smith, 1990)”
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Adolescence: A central event in shaping stress reactivity
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“During this phase a multitude of hormonal and behavioural changes as well as alterations in neurobiological structures occur together with a substantial remodelling of cortical and limbic circuits [75].”
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Romeo, R. D. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.02.004 · Cited by 273
“hypothalamic–pituitary–gonadal (HPG) axis and the physiological and behavioral alterations that ensue [83,100,125].”
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“These results indicate that although the critical window during perinatal development is vitally important for early sexual differentiation of the brain, the pubertal period also plays a large role in “fine-tuning” the organizational effects of steroid hormones [119].”
BackgroundPuberty and adolescent sexuality
Fortenberry, J. D. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.03.007 · Cited by 200
“Affective brain centers – for example, the nucleus accumbens and amygdala – play key roles in social information processing brain networks that are extensively reorganized during puberty (Nelson, Leibenluft, McClure, & Pine, 2005) These brain regions have large populations of gonadal steroid receptors and are linked t…”
BackgroundTestosterone Cannot Activate an Adult-Like Stress Response in Prepubertal Male Rats
Romeo, R. D., Lee, S. H., Chhua, N., McPherson, C. R., & McEwen, B. S. (2004) · Neuroendocrinology · doi:10.1159/000077270 · Cited by 197
“The difference in stress responsiveness before and after pubertal development may be mediated by changes in neural maturation that occur during puberty. Indeed, in addition to perinatal maturation, puberty serves as another key period of neural development during which the central nervous system is further shaped and…”
BackgroundJuraska, J. M., Sisk, C. L., & DonCarlos, L. L. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.05.010 · Cited by 192
“Evidence began accumulating in the 1990s that testicular hormones, acting during puberty, masculinizemale social behaviors (Bloch and Mills, 1995; Primus and Kellogg, 1990; Romeo et al., 2002; Schulz and Sisk, 2006).”
Emergence of sex differences in the development of substance use and abuse during adolescence
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McCormick, C. M., Robarts, D., Kopeikina, K. J., & Kelsey, J. E. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.01.008 · Cited by 165
“There is growing evidence that adolescence is a time of heightened plasticity and may indeed be a sensitive period of development similar to the perinatal period (Romeo et al., 2002; Spear, 2000).”
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Haller, S. P., Kadosh, K. C., Scerif, G., & Lau, J. Y. F. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.02.002 · Cited by 144
Adolescents and androgens, receptors and rewards
Sato, S. M., Schulz, K. M., Sisk, C. L., & Wood, R. I. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.01.010 · Cited by 124
“This turns out not to be the case (Meek et al., 1997; Romeo et al., 2001; Romeo et al., 2002b), in spite of the fact that the number and distribution of AR and ER throughout the mating circuit are similar in hormone-treated prepubertal and adult castrates (Meek et al., 1997; Romeo et al., 1999;…”
BackgroundSex matters: repetitive mild traumatic brain injury in adolescent rats
Wright, D. K., O'Brien, T. J., Shultz, S. R., & Mychasiuk, R. (2017) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.441 · Cited by 119
The emergence of gonadal hormone influences on dopaminergic function during puberty
Kuhn, C., Johnson, M., Thomae, A., Luo, B., Simon, S. A., Zhou, G., & Walker, Q. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.10.015 · Cited by 113
“Several recent reviews of how gonadal steroids contribute to the development of reproductive function and sexual behaviors during puberty have been published (Romeo et al. 2002; Romeo 2003; Sisk et al. 2003; Sisk and Zehr 2005; Schulz and Sisk 2006).”
BackgroundMcCormick, C. M., Robarts, D., Gleason, E., & Kelsey, J. E. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.05.004 · Cited by 105
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“166 Nakajo et al Evolutionally Conserved Function of Kisspeptin Endocrinology, January 2018, 159(1):163–183”
BackgroundMethodInfluentialThornton, J., Zehr, J. L., & Loose, M. D. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.03.015 · Cited by 105
“…that there may be additional times after the perinatal period that are periods of ‘organization’ as steroid hormone exposure during adolescence may further shape the expression of a variety of adult behaviors (for review, Romeo et al., 2002; Sisk and Zehr, 2005; Schulz et al., 2009 this issue).”
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The Developing Brain and Adolescent-Typical Behavior Patterns
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Steroid hormones, stress and the adolescent brain: A comparative perspective
Brown, G. R., & Spencer, K. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.016 · Cited by 88
“While 2 most research has focused on the effects of steroid hormone exposure during prenatal or early 3 postnatal life, adolescence has been hypothesised to be another highly sensitive period of neural 4 development (Spear, 2000; Romeo et al., 2002; Andersen, 2003; Sisk and Zehr, 2005; 5 McCormick and Mathews, 2010).”
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Newly proliferated cells in the adult male amygdala are affected by gonadal steroid hormones
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“…humans, gonadal hormones are involved in the development, differentiation, and protection of the central nervous system (Garcia-Segura et al., 1994; Romeo et al., 2002), and the amygdala has been implicated in a variety of cognitive and behavioral functions (Albert and Walsh, 1984; Cahill et al.,…”
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Romeo, R. D. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.12.003 · Cited by 63
“The increase in motivated behaviors, such as mating and aggressive behaviors, and the decrease in social behaviors, such as play, are a few examples (Spear, 2000; Romeo et al., 2002; Pellis and Pellis, 2007).”
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“Since both testosterone and estrogen are vital for normal pubertal development [13] this has critical implications for adolescent humans.”
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“…and adolescence as vulnerable periods of development Puberty and adolescence are critical periods of development for reproductive behaviors (Romeo et al., 2002a,b; Schulz et al., 2004), social, emotional, and cognitive changes (Spear, 2000; Sisk and Foster, 2004; Schneider, 2008), and for…”
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“Puberty is a period of neural maturation during which the organization of the brain, that began in the perinatal period, is completed and when the pubertal rise in steroid hormones can further affect the development of adult behaviours [25,26].”
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“Although similar behavioral effects of AAS abuse have been reported in the adolescent and adult populations, it is highly disconcerting that adolescents are abusing AAS, especially since adolescence is a critical time period involving gonadal steroidmediated brain remodeling (Bakker et al., 2003; Keenan et al., 1993;…”
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“INTRODUCTION Puberty is a very important developmental period which is characterized by profound changes in an individual’s brain (Romeo et al., 2002), physiology (Romeo, 2003, 2005), and behavior (Romeo, 2005).”
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Adolescence, stress and cortisol in autism spectrum disorders
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“Initially, corticosterone levels decrease, reaching the lowest levels when the rats are around sexual maturity, and thereafter start to rise again [5,69].”
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Testosterone, puberty, and the pattern of male aggression in Syrian hamsters
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“For example, low doses of testosterone inhibit gonadotropin secretion in juveniles, but not in adults (Richardson, Gore, Venier, Romeo, & Sisk, 2001; Sisk & Turek, 1983) whereas doses of testosterone that activate reproductive behavior in adults fail to do so in juveniles (Meek, Romeo, Novak, & Sisk, 1997; Romeo et al…”
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“mating behavior) in pre-pubertal male rodents (Romeo et al. 2002).”
BackgroundInfluentialSexual arousal and masculinity-femininity of women.
Rieger, G., Savin‐Williams, R. C., Chivers, M. L., & Bailey, J. M. (2015) · Journal of Personality and Social Psychology · doi:10.1037/pspp0000077 · Cited by 43
Salas-Ramirez, K. Y., Montalto, P. R., & Sisk, C. L. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.11.004 · Cited by 42
“Previous work from this laboratory has demonstrated that male reproductive behavior cannot be activated by gonadal steroids in prepubertal animals (Meek et al., 1997; Romeo et al., 2002) and that the pubertal rise in testosterone organizes (further masculinizes and defeminizes) neural circuits to enhance or maximize t…”
InfluentialPubertal Development of Sex Differences in Circadian Function: An Animal Model
Lee, T. M., Hummer, D. L., Jechura, T. J., & Mahoney, M. M. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.031 · Cited by 40
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“However, there was no effect of treatment on either SVL or mass, nor were there treatment SVL or treatment mass interactions, in either females or males.”
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“The adolescent developmental period is particularly vulnerable to both biological and environmental factors, since perturbations in nervous system development during this time will affect mature adult behaviors, such as reproduction (Romeo et al., 2002).”
BackgroundSocial Anxiety in Children and Adolescents: Biological, Developmental, and Social Considerations
Detweiler, M. F., Comer, J. S., Crum, K. I., & Albano, A. M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-394427-6.00010-8 · Cited by 40
The endogenous androgen-regulated sialorphin modulates male rat sexual behavior
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Testosterone and the Brain: From Cognition to Autism
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“…recognized as a critical period for the development of hypothalamic–pituitary–adrenal (Romeo et al., 2005, 2006) and hypothalamic–pituitary–gonadal axis regulation (Meek et al., 1997), as well as the establishment of some reproductive behaviors (Romeo et al., 2002a, 2002b; Schulz et al., 2004).”
Zipser, B., Schleking, A., Kaiser, S., & Sachser, N. (2014) · Frontiers in Zoology · doi:10.1186/1742-9994-11-30 · Cited by 32
“This important phase of ontogeny - called adolescence - comprises extensive alterations in anatomy, endocrine systems, neuronal circuits and behaviour [15,17-19].”
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Gonadotropin-induced testosterone response in peripubertal male alligators
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“At puberty, internal and external signals that initiate reproductive maturation are processed by the brain and relayed to the GnRH pulse generator in the hypothalamus, inducing it to secrete GnRH in a pulsatile rhythm with a particular frequency and amplitude (Klein, 1999; Romeo et al., 2002).”
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Impact of neonatal hypothyroidism on reproduction in the male hamster, Mesocricetus auratus
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Anabolic steroids have long-lasting effects on male social behaviors
Salas-Ramirez, K. Y., Montalto, P. R., & Sisk, C. L. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.11.026 · Cited by 25
Early-Life Experiences: Enduring Behavioral, Neurological, and Endocrinological Consequences
Romeo, R. D., Tang, A. C., & Sullivan, R. M. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00062-0 · Cited by 25
“Adolescence is clearly marked by profound changes in an individual’s nervous system, physiology, and behavior (Andersen, 2003; Dahl, 2004; Romeo, 2003, 2005; Romeo et al., 2002; Spear, 2000, 2007).”
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Testosterone Modulates Status-Specific Patterns of Cooperation in a Social Network
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The social modulation of behavioural development
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“Afterwards, starting around puberty, they activate sexually dimorphic behaviors, such as the reproductive one, by acting on the same circuitries they had previously shaped [8,9].”
BackgroundSocial Anxiety in Children and Adolescents
Detweiler, M. F., Comer, J. S., & Albano, A. M. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-375096-9.00009-2 · Cited by 24
Oxidative stress in the brain of reproductive male rats during aging
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Pubertal BPA exposure changes central ERα levels in female mice.
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Cambios en el cerebro adolescente y conductas agresivas y de asunción de riesgos
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The anxiogenic effects of adolescent psychological stress in male and female mice
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“While puberty-related hormones are one possible contributor to the behavioural differences between juveniles and adults, they do not completely explain the differences [2], as early experimental exposure to these hormones before natural puberty does not result in rodents performing sexually mature behaviours [36].”
Neural Circuits Underlying Sexually Dimorphic Innate Behaviors
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Mouse Age Matters: How Age Affects the Murine Plasma Metabolome
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Neurochemistry of Male Sexual Behavior
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Determination of oxprenolol, methandienone and testosterone in meat samples by UHPLC-Q-ToF
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Metadata
- Authors
- Romeo, R. D., Richardson, H. N., & Sisk, C. L.
- Affiliations
- Michigan State University (US)
- Corresponding author
- Sisk, Cheryl L.
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2002-05
- Volume
- 26
- Issue
- 3
- Pages
- 381-391
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2095232389
- Cited by
- 152
- References
- 111
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 5 · 2023: 3 · 2022: 4 · 2021: 4 · 2020: 2 · 2019: 6 · 2018: 6 · 2017: 3 · 2016: 12 · 2015: 9 · 2014: 10 · 2013: 13 · 2012: 4
- FWCI
- 1.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-26483, R01HD026483)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Sexual Differentiation and Disorders
- Keywords
- puberty, male reproductive behavior, brain maturation, neuroendocrine regulation, sex steroids, neural circuits, sensitive period, social behavior, prepubertal males
- MeSH terms
- Androgens, Animals, Brain, Hormones, Humans, Male, Puberty, Sexual Behavior, Sexual Behavior, Animal
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