The neural basis of puberty and adolescence
Abstract
The pubertal transition to adulthood involves both gonadal and behavioral maturation. A developmental clock, along with permissive signals that provide information on somatic growth, energy balance and season, time the awakening of gonadotropin releasing hormone (GnRH) neurons at the onset of puberty. High-frequency GnRH release results from disinhibition and activation of GnRH neurons at puberty onset, leading to gametogenesis and an increase in gonadal steroid hormone secretion. Steroid hormones, in turn, both remodel and activate neural circuits during adolescent brain development, leading to the development of sexual salience of sensory stimuli, sexual motivation, and expression of copulatory behaviors in specific social contexts. These influences of hormones on reproductive behavior depend in part on changes in the adolescent brain that occur independently of gonadal maturation. Reproductive maturity is therefore the product of developmentally timed, brain-driven and recurrent interactions between steroid hormones and the adolescent nervous system.
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Increases in reward-seeking are coincident with pubertal maturation in animal studies.
“animal studies indicate that increases in reward-seeking are coincident with pubertal maturation”
From A dual systems model of adolescent risk‐taking (2010) · cites this paper as Sisk & Foster, 2004
The results for self-reported pubertal changes concur with prior research on pubertal development showing that puberty starts earlier in girls than boys.
“The results for selfreported pubertal changes concur with prior research on pubertal development showing that puberty starts earlier in girls than boys (Carskadon and Acebo, 1993;Sisk and Foster, 2004;Shirtcliff et al., 2009).”
From Longitudinal Changes in Adolescent Risk-Taking: A Comprehensive Study of Neural Responses to Rewards, Pubertal Development, and Risk-Taking Behavior (2015) · cites this paper as Sisk and Foster, 2004
Animal research indicates that some dopaminergic changes during puberty are indirectly attributable to gonadal hormonal shifts, in that gonadal hormones may catalyze other processes.
“that some are indirectly attributable to them (in that the presence of gonadal hormones may catalyze other processes)”
From A behavioral scientist looks at the science of adolescent brain development (2010) · cites this paper as Sisk & Foster, 2004
Animal research indicates that other dopaminergic changes may only coincide with puberty, possibly following a timetable set well before adolescence.
“that some are merely coincident with them, perhaps programmed to unfold along a developmental schedule established long before adolescence”
From A behavioral scientist looks at the science of adolescent brain development (2010) · cites this paper as Sisk & Foster, 2004
Animal research indicates that certain dopaminergic changes during puberty result directly from gonadal hormonal shifts.
“Animal studies suggest that some of the changes in dopaminergic activity are directly attributable to the hormonal changes of puberty”
From A behavioral scientist looks at the science of adolescent brain development (2010) · cites this paper as Sisk & Foster, 2004
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 Foster 2004
Sexual behavior develops according to a species-specific, genetically controlled, maturational plan in which the age at first reproduction occurs within a specific age range.
“Sexual behavior develops according to a species-specific, genetically controlled, maturational plan in which the age at first reproduction occurs within a specific age range (87).”
From Emerging Adulthood, a Pre-adult Life-History Stage (2020) · cites this paper as [87]
Puberty is defined as the process leading to the attainment of sexual maturation, beginning with the activation of the HPG axis and ending with reproductive competency.
“Traditionally, puberty is defined as the process leading to the attainment of sexual maturation [181], beginning with the activation of the HPG axis, and ending with reproductive competency [153, 178].”
From The neuroendocrine control of the circadian system: Adolescent chronotype (2012) · cites this paper as [178]
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Wilson, M. E. (1992) · Handbook of behavioral neurobiology · doi:10.1007/978-1-4899-2453-7_9 · Cited by 13 · see citing works
Hormonal control of sex differences in ultrasound production by hamsters
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Gonadotropin-Releasing Hormone
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Andersen (2000) · doi:10.1002/1098-2396(200008)37:2
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Our future: a Lancet commission on adolescent health and wellbeing
Patton, G. C., Sawyer, S. M., Santelli, J. S., Ross, D. A., Afifi, R., Allen, N. B., Arora, M., Azzopardi, P., Baldwin, W., Bonell, C., et al. (2016) · The Lancet · doi:10.1016/s0140-6736(16)00579-1 · Cited by 3,785 · see citing works
A social neuroscience perspective on adolescent risk-taking
Steinberg, L. (2008) · Developmental Review · doi:10.1016/j.dr.2007.08.002 · Cited by 3,644 · see citing works
“…at around 9 or 10 years of age, a subsequent reduction of dopamine receptor density in the striatum and prefrontal cortex, a transformation that is much more pronounced among males than females (at least in rodents) (Sisk & Foster, 2004; Sisk & Zehr, 2005; Teicher, Andersen, & Hostetter, 1995).”
BackgroundWhy do many psychiatric disorders emerge during adolescence?
Paus, T., Keshavan, M., & Giedd, J. N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2513 · Cited by 3,123 · see citing works
“The most-obvious outward physical manifestations of puberty are caused by changing levels of hormone”
BackgroundMolecular, spatial, and functional single-cell profiling of the hypothalamic preoptic region
Moffitt, J. R., Bambah-Mukku, D., Eichhorn, S. W., Vaughn, E., Shekhar, K., Perez, J. D., Rubinstein, N. D., Hao, J., Regev, A., Dulac, C., et al. (2018) · Science · doi:10.1126/science.aau5324 · Cited by 1,365 · see citing works
Steinberg, L., Albert, D., Cauffman, E., Banich, M., Graham, S., & Woolard, J. (2008) · Developmental Psychology · doi:10.1037/a0012955 · Cited by 1,542 · see citing works
“A growing literature, derived primarily from rodent studies, but with implications for human development, indicates that the remodeling of the dopaminergic system within the socioemotional network involves an initial postnatal rise and then, starting in preadolescence, a subsequent reduction of dopamine receptor densi…”
BackgroundResultSexual dimorphism of brain developmental trajectories during childhood and adolescence
Lenroot, R. K., Gogtay, N., Greenstein, D. K., Wells, E. M., Wallace, G. L., Clasen, L. S., Blumenthal, J. D., Lerch, J., Zijdenbos, A. P., Evans, A. C., et al. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.053 · Cited by 1,309 · see citing works
“Work in rodent models has shown that exposure to pubertal hormones during adolescence has effects on behavior which persist after the hormones are removed, providing evidence for a long term effect which could be related to changes in brain structure (Schulz and Sisk, 2006; Sisk and Foster, 2004).”
Maturation of the adolescent brain
SHARMA, S. K., Arain, Mathur, Rais, Nel, Sandhu, Haque, & Johal (2013) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s39776 · Cited by 1,339 · see citing works
“During adolescence, white matter increases in the corpus callosum, the bundle of”
BackgroundA dual systems model of adolescent risk‐taking
Steinberg, L. (2010) · Developmental Psychobiology · doi:10.1002/dev.20445 · Cited by 1,187 · see citing works
Pubertal hormones organize the adolescent brain and behavior
Sisk, C. L., & Zehr, J. L. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.10.003 · Cited by 1,082 · see citing works
“Puberty is proximally timed by internal and external stimuli that serve as permissive signals for reproductive maturation [18,28,36,111,133].”
BackgroundSelf-citationThe role of puberty in the developing adolescent brain
Blakemore, S., Burnett, S., & Dahl, R. E. (2010) · Human Brain Mapping · doi:10.1002/hbm.21052 · Cited by 1,011 · see citing works
“These effects are hypothesized to occur via two relatively distinct processes: organization and activation [Schulz et al., 2009; Sisk and Foster, 2004].”
BackgroundInfluentialBoehm, U., Bouloux, P.-M., Dattani, M. T., de Roux, N., Dodé, C., Dunkel, L., Dwyer, A. A., Giacobini, P., Hardelin, J.-P., Juul, A., et al. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.112 · Cited by 874 · see citing works
Consilience and Life History Theory: From genes to brain to reproductive strategy
FIGUEREDO, A., VASQUEZ, G., BRUMBACH, B., SCHNEIDER, S., SEFCEK, J., TAL, I., HILL, D., WENNER, C., & JACOBS, W. (2006) · Developmental Review · doi:10.1016/j.dr.2006.02.002 · Cited by 793 · see citing works
“(Sisk & Foster, 2004, p. 1045) Risk taking and novelty seeking are hallmarks of typical adolescent behavior.”
BackgroundPregnancy leads to long-lasting changes in human brain structure
Hoekzema, E., Barba-Müller, E., Pozzobon, C., Picado, M., Lucco, F., García-García, D., Soliva, J. C., Tobeña, A., Desco, M., Crone, E. A., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4458 · Cited by 788 · see citing works
Triadic model of the neurobiology of motivated behavior in adolescence.
ERNST, M., PINE, D. S., & HARDIN, M. (2006) · Psychological Medicine · doi:10.1017/s0033291705005891 · Cited by 718 · see citing works
“Pubertal changes depend on developmental alterations in the function of the hypothalamo–pituitary–gonadal (HPG) axis (Romeo, 2003; Sisk & Foster, 2004).”
BackgroundImaging brain development: The adolescent brain
Blakemore, S.-J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.11.080 · Cited by 649 · see citing works
“Evidence from animal studies indicates that the hormonal events of puberty exert profound effects on brain maturation and behaviour (Cahill, 2006; Sisk and Foster, 2004; Spear, 2000).”
BackgroundA 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
“These fi ndings are consistent with the notion that the transition into adolescence potentially marks another period when the environment can exert large effects on the brain (Sisk and Foster, 2004; Schulz et al., 2009).”
Braams, B. R., van Duijvenvoorde, A. C. K., Peper, J. S., & Crone, E. A. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.4764-14.2015 · Cited by 617 · see citing works
“The results for selfreported pubertal changes concur with prior research on pubertal development showing that puberty starts earlier in girls than boys (Carskadon and Acebo, 1993; Sisk and Foster, 2004; Shirtcliff et al., 2009).”
ResultSherman, L. E., Payton, A. A., Hernandez, L. M., Greenfield, P. M., & Dapretto, M. (2016) · Psychological Science · doi:10.1177/0956797616645673 · Cited by 627 · see citing works
“Subcortical regions functionally associated with emotion processing and reward undergo considerable changes and reorganization during puberty (Brenhouse & Andersen, 2011; Sisk & Foster, 2004).”
The role of nutrition in children's neurocognitive development, from pregnancy through childhood
Nyaradi, A., Li, J., Hickling, S., Foster, J. K., & Oddy, W. H. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00097 · Cited by 575 · see citing works
“…developmental period, with research indicating that structural reorganization, brain and cognitive maturation and—in particular—major developments in the prefrontal cortex take place during puberty (Luna and Sweeney, 2001; Sisk, 2004; Peper et al., 2009; Asato et al., 2010; Blakemore et al., 2010).”
BackgroundFrontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents
Somerville, L. H., Hare, T., & Casey, B. J. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21572 · Cited by 523 · see citing works
“…circulating gonadal hormones affect both organizational and activational mechanisms to influence brain function across development (Steinberg, 2008; Sisk & Foster, 2004; Romeo & Sisk, 2001) and has shown a predictive relationship between pubertal status and such appetitive behaviors as sensation…”
InfluentialWhite matter development in adolescence: A DTI study
Asato, M. R., Terwilliger, R., Woo, J., & Luna, B. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp282 · Cited by 512 · see citing works
“Cerebral Cortex September 2010;20:2122--2131 doi:10.1093/cercor/bhp282 Advance Access publication January 5, 2010”
InfluentialPubertal Development: Correspondence Between Hormonal and Physical Development
Shirtcliff, E. A., Dahl, R. E., & Pollak, S. D. (2009) · Child Development · doi:10.1111/j.1467-8624.2009.01263.x · Cited by 614 · see citing works
“For these reasons, biobehavioral researchers increasingly seek to examine measures of puberty to clarify studies of emotion-related neural circuitry (Nelson, Leibenluft, McClure, & Pine, 2005; Sisk & Foster, 2004 ), psychopathology (Angold & Worthman, 1993; Cyranowski, Frank, Young, & Shear, 2000), cognition (Steinber…”
BackgroundModulation of appetite by gonadal steroid hormones
Asarian, L., & Geary, N. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1860 · Cited by 506 · 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
Using Network Analysis to Identify Central Symptoms of Adolescent Depression
Mullarkey, M. C., Marchetti, I., & Beevers, C. G. (2018) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2018.1437735 · Cited by 496 · see citing works
“This may be especially true as adolescents move further through puberty, as neural and hormonal changes associated with puberty also appear to drive a need for affiliation with others (Sisk & Foster, 2004).”
BackgroundStress and the developing adolescent brain
Eiland, L. R., & Romeo, R. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.048 · Cited by 491 · see citing works
“Although the terms puberty and adolescence are often used interchangeably, and have some chronological overlap, these terms have separate meanings (Sisk and Foster, 2004).”
BackgroundAge 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
“…‘‘gonadal maturation and behavioral maturation are two distinct brain-driven processes with separate timing and neurobiological mechanisms, but they are intimately coupled through iterative interactions between the nervous system and gonadal steroid hormones” (Sisk & Foster, 2004, p. 1040).”
BackgroundInfluentialMedia use and brain development during adolescence
Crone, E. A., & Konijn, E. A. (2018) · Nature Communications · doi:10.1038/s41467-018-03126-x · Cited by 464 · see citing works
Simmonds, D. J., Hallquist, M. N., Asato, M. R., & Luna, B. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.12.044 · Cited by 443 · see citing works
“, 2011; Sisk and Foster, 2004), as puberty onset in females occurs 2–3 years earlier than in males (Sisk and Foster, 2004).”
Changes in Sleep as a Function of Adolescent Development
Colrain, I. M., & Baker, F. C. (2011) · Neuropsychology Review · doi:10.1007/s11065-010-9155-5 · Cited by 452 · see citing works
“Puberty occurs within the broader scope of adolescence and refers to the activation of the previously dormant hypothalamic-pituitary-gonadal axis that culminates in gonadal maturation (Sisk and Foster 2004).”
BackgroundOlfactory Inputs to Hypothalamic Neurons Controlling Reproduction and Fertility
Yoon, H., Enquist, L. W., & Dulac, C. G. (2005) · Cell · doi:10.1016/j.cell.2005.08.039 · Cited by 435 · see citing works
“the onset of puberty (Silverman et al., 1994; Sisk and Foster, 2004).”
BackgroundThe role of GABAA receptors in the acute and chronic effects of ethanol: a decade of progress
Kumar, S., Porcu, P., Werner, D. F., Matthews, D. B., Diaz‐Granados, J. L., Helfand, R. S., & Morrow, A. L. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1562-z · Cited by 432 · see citing works
“Puberty refers to gonadal maturation, while adolescence refers to a gradual period of maturation of social and cognitive behaviors (Powell 2006; Sisk and Foster 2004).”
Sex Differences and the Impact of Steroid Hormones on the Developing Human Brain
Neufang, S., Specht, K., Hausmann, M., Güntürkün, O., Herpertz‐Dahlmann, B., Fink, G. R., & Konrad, K. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn100 · Cited by 421 · see citing works
Puberty and the human brain: insights into adolescent development
Vijayakumar, N., Op de Macks, Z., Shirtcliff, E. A., & Pfeifer, J. H. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.06.004 · Cited by 437 · see citing works
Brain maturation in adolescence: concurrent changes in neuroanatomy and neurophysiology
Whitford, T. J., Rennie, C. J., Grieve, S. M., Clark, C. R., Gordon, E., & Williams, L. M. (2007) · Human Brain Mapping · doi:10.1002/hbm.20273 · Cited by 391 · see citing works
“While the most dramatic structural changes in the healthy human brain are thought to occur in the perinatal period [Huttenlocher and Dabholkar, 1997], there is a growing body of evidence suggesting that adolescence is also a period of substantial neurodevelopment [Sisk and Foster, 2004].”
BackgroundDavey, C. G., Yücel, M., & Allen, N. B. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.04.016 · Cited by 377 · see citing works
“Puberty starts in the brain—with the release of gonadotrophin-releasing hormone from the hypothalamus under the influence of neural mechanisms that are still opaque (Sisk and Foster, 2004).”
BackgroundLinked Sex Differences in Cognition and Functional Connectivity in Youth
Satterthwaite, T. D., Wolf, D. H., Roalf, D. R., Ruparel, K., Erus, G., Vandekar, S., Gennatas, E. D., Elliott, M. A., Smith, A. C. W., Hakonarson, H. H., et al. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu036 · Cited by 377 · see citing works
Sex differences in anxiety and emotional behavior
Donner, N. C., & Lowry, C. A. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1271-7 · Cited by 379 · see citing works
“neural, and behavioral events of sexual maturation [336], and is”
BackgroundO'Doherty, D. C. M., Chitty, K. M., Saddiqui, S., Bennett, M. R., & Lagopoulos, J. (2015) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2015.01.002 · Cited by 375 · see citing works
“The inclusion of paediatric data in neural morphological studies is potentially problematic given the growth and development typically occurring in the brains of children and adolescents (Sisk and Foster, 2004; Hedges et al., 2007; Whitford et al., 2007).”
BackgroundMcCormick, C. M., & Zovkic, I. B. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.07.012 · Cited by 373 · see citing works
Somerville, L. H., Bookheimer, S. Y., Buckner, R. L., Burgess, G. C., Curtiss, S. W., Dapretto, M., Elam, J. S., Gaffrey, M. S., Harms, M. P., Hodge, C., et al. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.08.050 · Cited by 356 · see citing works
“Despite the importance of hormones in neurodevelopmental processes (Giedd et al., 2006; Goddings et al., 2014; Romeo, 2003; Sisk and Foster, 2004; Spear, 2000), the relationship between puberty and brain connectivity changes remains poorly understood.”
Ernst, M., & Fudge, J. L. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.10.009 · Cited by 358 · see citing works
Brenhouse, H. C., & Andersen, S. L. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.04.013 · Cited by 340 · see citing works
“Definitions of adolescence can also be reasonably based on gonadal changes as they are relevant to sexual maturation (Sisk and Foster, 2004).”
BackgroundA behavioral scientist looks at the science of adolescent brain development
Steinberg, L. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.11.003 · Cited by 342 · see citing works
“... there is not much of one to tell.) Animal studies suggest that some of the changes in dopaminergic activity are directly attributable to the hormonal changes of puberty, that some are indirectly attributable to them (in that the presence of gonadal hormones may catalyze other processes), and that some are merely c…”
Impulsive and Self-Conscious: Adolescents' Vulnerability to Advertising and Promotion
Pechmann, C., Levine, L. J., Loughlin, S. E., & Leslie, F. M. (2005) · Journal of Public Policy & Marketing · doi:10.1509/jppm.2005.24.2.202 · Cited by 334 · see citing works
The Impact of Sex, Puberty, and Hormones on White Matter Microstructure in Adolescents
Herting, M. M., Maxwell, E. C., Irvine, C., & Nagel, B. J. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr246 · Cited by 331 · see citing works
“Adolescence is the transition between childhood and adulthood , during which significant physical, social, and behavioral changes occur (Sisk and Foster 2004; Sisk and Zehr 2005).”
BackgroundMartel, M. M. (2013) · Psychological Bulletin · doi:10.1037/a0032247 · Cited by 329 · see citing works
Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure
Schneider, M. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00110.x · Cited by 330 · see citing works
“Because the most important adolescent behavioral changes and many important neuronal maturational processes are closely linked to pubertal development ( Sisk & Foster 2004 ), the more exact time window of puberty (around pd 38 to pd 60 in males and pd 28 to ~pd 40 in females) (Fig. 1) might be the better choice for st…”
BackgroundInfluentialBell, M. R. (2018) · Endocrinology · doi:10.1210/en.2018-00220 · Cited by 308 · see citing works
Roles of Sex Hormones and Gender in the Gut Microbiota
Yoon, K., & Kim, N. (2021) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm20208 · Cited by 305 · see citing works
Sex differences in the gut microbiome–brain axis across the lifespan
Jašarević, E., Morrison, K. E., & Bale, T. L. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0122 · Cited by 295 · see citing works
Adolescent Development and Juvenile Justice
Steinberg, L. (2009) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.032408.153603 · Cited by 294 · see citing works
“…network involves an initial postnatal rise and then, starting in preadolescence, a subsequent reduction of dopamine receptor density in the striatum and prefrontal cortex; this pattern is more pronounced among males than females (Sisk & Foster 2004, Sisk & Zehr 2005, Teicher et al. 1995).”
BackgroundVijayakumar, N., Allen, N. B., Youssef, G. J., Dennison, M., Yücel, M., Simmons, J. G., & Whittle, S. (2016) · Human Brain Mapping · doi:10.1002/hbm.23154 · Cited by 273 · see citing works
“The most common explanation for potential sex differences in cortical development is the sexually dimorphic effects of puberty, with support coming from experimental studies on animal and more recently observational studies in humans [Bramen et al., 2011; Peper et al., 2009; Raznahan et al., 2010; Sisk and Foster, 200…”
ResultPuberty and adolescence as a time of vulnerability to stressors that alter neurobehavioral processes
Holder, M. K., & Blaustein, J. D. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.10.004 · Cited by 279 · see citing works
“, 1989), their secretory activity is quiescent during the prepubertal period (Sisk and Foster, 2004).”
BackgroundInfluentialMcCormick, C. M., Smith, C. L., & Mathews, I. Z. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.09.005 · Cited by 278 · see citing works
Family Rearing Antecedents of Pubertal Timing
Belsky, J., Steinberg, L. D., Houts, R., Friedman, S. L., DeHart, G. B., Cauffman, E. E., Roisman, G. I., Halpern‐Felsher, B. L., & Susman, E. J. (2007) · Child Development · doi:10.1111/j.1467-8624.2007.01067.x · Cited by 277 · see citing works
McCormick, C. M., Mathews, I. Z., Thomas, C., & Waters, P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.06.003 · Cited by 276 · see citing works
“It is a time of maturation of social and cognitive behaviour in preparation for adulthood, with adolescents showing significant increases in exploratory behaviour, in social play, and in risktaking (Doremus-Fitzwater et al., 2009; Sisk & Foster, 2004; Spear, 2000a).”
GnRH and GnRH receptors in the pathophysiology of the human female reproductive system
Maggi, R., Cariboni, A. M., Marelli, M. M., Moretti, R. M., Andrè, V., Marzagalli, M., & Limonta, P. (2015) · Human Reproduction Update · doi:10.1093/humupd/dmv059 · Cited by 272 · see citing works
“Finally, the timing of the reactivation of the GnRH pulse could be due to both internal and external sources (Sisk and Foster, 2004); the existence of an hypothalamic pubertal clock or of brain sensors, which is also able to monitor circulating signals of somatic development, may co-ordinate the…”
BackgroundPuberty and Its Measurement: A Decade in Review
Dorn, L. D., & Biro, F. M. (2011) · Journal of Research on Adolescence · doi:10.1111/j.1532-7795.2010.00722.x · Cited by 378 · see citing works
“There are likely numerous permissive signals that trigger pubertal onset, including the hormones leptin and ghrelin as well as body composition (Sisk & Foster, 2004).”
BackgroundUllsperger, J. M., & Nikolas, M. A. (2017) · Psychological Bulletin · doi:10.1037/bul0000106 · Cited by 293 · see citing works
“…influencing risk in multiple domains of psychopathology, such as greater susceptibility to peer influence, heightened sensitivity to social cues and negative facial expressions, as well as increased risk-taking/novelty-seeking behaviors (Dumontheil, 2016; Sisk & Foster, 2004; Steinberg, 2010).”
BackgroundHormonal influences on sexually differentiated behavior in nonhuman primates.
Wallen, K. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.02.001 · Cited by 305 · see citing works
Adolescence as a vulnerable period to alter rodent behavior
Schneider, M. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1581-2 · Cited by 266 · see citing works
“…has been subsequently extended to the first acquisition of reproductive competence in all mammalian and nonmammalian vertebrates and in invertebrates (Sisk and Foster 2004; Perfito and Bentley 2009; Taranger et al. 2010), thereby representing a universal process of vital importance among various…”
BackgroundInfluentialPubertal maturation and programming of hypothalamic–pituitary–adrenal reactivity
Romeo, R. D. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.02.004 · Cited by 258 · see citing works
“Indeed, adolescent development is increasingly being viewed as an additional period of hormone-dependent organization of the brain and behavior [95,118,115,124,125].”
Panksepp, J. B., Jochman, K. A., Kim, J. U., Koy, J. J., Wilson, E. D., Chen, Q., Wilson, C. R., & Lahvis, G. P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000351 · Cited by 295 · see citing works
“While adolescence includes the pubertal stages of development, it also encompasses the more gradual acquisition of psychosocial skills that precede, accompany and follow the capacity to produce offspring [18,34,36].”
BackgroundDevelopmental programming and endocrine disruptor effects on reproductive neuroendocrine systems
Gore, A. C. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.02.002 · Cited by 251 · see citing works
“Furthermore, not only is puberty important for activational effects of steroid hormones on neonatally imprinted circuits [12,153,16, 116,119], but the brain may be sensitive to the organizational effects of steroid hormones during this developmental stage [119,129,39,144].”
BackgroundSocial reward among juvenile mice
Panksepp, J. B., & Lahvis, G. P. (2007) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2006.00295.x · Cited by 248 · see citing works
“Adolescent development entails bodily, cognitive and emotional changes (Sisk & Foster 2004; Spear 2000) that usually co-occur with major transitions in social relationships (Douglas et al. 2003; Smetana et al. 2006).”
BackgroundNegriff, S., & Susman, E. J. (2011) · Journal of Research on Adolescence · doi:10.1111/j.1532-7795.2010.00708.x · Cited by 241 · see citing works
Developmental Changes in Organization of Structural Brain Networks
Khundrakpam, B. S., Reid, A., Brauer, J., Carbonell, F., Lewis, J., Ameis, S., Karama, S., Lee, J., Chen, Z., Das, S., et al. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs187 · Cited by 234 · see citing works
“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 (Blake-more and…”
BackgroundSilk, J. S., Siegle, G. J., Lee, K. H., Nelson, E. E., Stroud, L. R., & Dahl, R. E. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst175 · Cited by 231 · see citing works
“Thus, it is possible that the effects of pubertal development on brain response could differ for males and females based on differences in both the timing of puberty and the levels of different pubertal hormones (Sisk and Foster, 2004).”
BackgroundBurke, A. R., McCormick, C. M., Pellis, S. M., & Lukkes, J. L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.018 · Cited by 225 · see citing works
“While puberty takes place during adolescence, these are different constructs because puberty is a discrete measurable event, while adolescence is a gradual brain and behavioral maturation process that encompasses a more extensive portion of ontogeny (Sisk and Foster, 2004).”
Wachs, T. D., Georgieff, M., Cusick, S. E., & McEwen, B. S. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12314 · Cited by 236 · see citing works
Dadds, M. R., Moul, C., Cauchi, A., Dobson-Stone, C., Hawes, D. J., Brennan, J., & Ebstein, R. E. (2014) · Development and Psychopathology · doi:10.1017/s0954579413000497 · Cited by 230 · see citing works
“In terms of the psychopathy phenotype, a wealth of evidence indicates that levels and the nature of aggression, antisocial behavior, and related traits, such as empathy and risk taking, undergo dramatic changes at puberty (Moffitt, 1993; Sisk & Foster, 2004).”
BackgroundMcCormick, C. M., & Mathews, I. Z. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.09.019 · Cited by 230 · see citing works
Dickerson, S. M., & Gore, A. C. (2007) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-007-9048-y · Cited by 220 · see citing works
“Moreover, puberty itself may be associated with further organizational or reorganizational changes in the nervous system and is beginning to be considered a second critical period for brain sexual differentiation [32].”
BackgroundFemale reproductive maturation in the absence of kisspeptin/GPR54 signaling
Mayer, C., & Boehm, U. (2011) · Nature Neuroscience · doi:10.1038/nn.2818 · Cited by 213 · see citing works
“2818" language="eng" relation="no"> Puberty, in humans and mice, is a transition period of gonadal and behavioral maturation that occurs between juvenile stages and adulthoo”
BackgroundSmith, A. R., Chein, J., & Steinberg, L. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.03.006 · Cited by 214 · see citing works
“…one line of research has focused on the pattern of proliferation and pruning of dopamine receptors in the striatum and prefrontal cortex (PFC) during adolescence as an underlying mechanism of increased functional activation of the reward-related system during this period (Sisk & Foster, 2004).”
BackgroundMeyer, U., Nyffeler, M., Schwendener, S., Knuesel, I., Yee, B. K., & Feldon, J. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301413 · Cited by 215 · see citing works
“These two developmental stages are largely comparable between mice and rats, and roughly correspond to a period between 11–16 year and B20 years onward, respectively, in humans (Spear, 2000; Sisk and Foster, 2004; Rasier et al, 2006).”
BackgroundInfluence of photoperiod on hormones, behavior, and immune function
Walton, J. C., Weil, Z. M., & Nelson, R. J. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.12.003 · Cited by 207 · see citing works
“tive feedback leads to increased secretion of LH and FSH and activation of the reproductive system [285].”
Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis
Burke, A. R., & Miczek, K. A. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3369-1 · Cited by 207 · see citing works
“Although many rodent neural systems mature during adolescence (Brenhouse and Andersen 2011; McCutcheon and Marinelli 2009; Sisk and Foster 2004; Spear 2000), the maturation of DA neurons in the ventral tegmental area (VTA) that project to the medial prefrontal cortex (mPFC) and NAc is perhaps the…”
BackgroundInfluentialEmerging Adulthood, a Pre-adult Life-History Stage
Hochberg, Z., & Konner, M. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00918 · Cited by 204 · see citing works
“Sexual behavior develops according to a species-specific, genetically controlled, maturational plan in which the age at first reproduction occurs within a specific age range (87).”
BackgroundA brain circuit that synchronizes growth and maturation revealed through Dilp8 binding to Lgr3
Vallejo, D. M., Juarez-Carreño, S., Bolı́var, J., Morante, J., & Domínguez, M. (2015) · Science · doi:10.1126/science.aac6767 · Cited by 203 · see citing works
“It is possible that the release of PTTH at the larval-pupal transition might additionally require disinhibition of inhibitory input(s), as proposed for the secretion of GnRH from hypothalamic neurons at the onset of puberty (5, 10).”
BackgroundMichaud, P., Suris, J., & Deppen, A. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2006.04.037 · Cited by 206 · see citing works
Study Characteristics and Recidivism Base Rates in Juvenile Sex Offender Recidivism
Caldwell, M. F. (2009) · International Journal of Offender Therapy and Comparative Criminology · doi:10.1177/0306624x08330016 · Cited by 200 · see citing works
Adewale, H. B., Jefferson, W. N., Newbold, R. R., & Patisaul, H. B. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.109.078261 · Cited by 198 · see citing works
“The primary mechanism for pubertal onset remains unclear [37, 38] but in rats DOV is a hallmark of puberty and was therefore used as the physiological indicator of puberty.”
Neuroendocrine regulation of Drosophila metamorphosis requires TGFβ/Activin signaling
Gibbens, Y., Warren, J. T., Gilbert, L. I., & O’Connor, M. B. (2011) · Development · doi:10.1242/dev.063412 · Cited by 194 · see citing works
“(Mauras et al., 1996; Sisk and Foster, 2004; Gilbert et al., 1997; Gilbert et al., 2002).”
Impacts of stress and sex hormones on dopamine neurotransmission in the adolescent brain
Sinclair, D., Purves-Tyson, T. D., Allen, K. M., & Weickert, C. S. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3415-z · Cited by 191 · see citing works
“Defining adolescence Adolescence is regarded as “the gradual period of transition from childhood to adulthood” (Spear 2000), which encompasses puberty, the period during which sexual maturity is attained [for detailed reviews, see also Schneider (2008, 2013) and Sisk and Foster (2004)].”
BackgroundNeuronal migration in the adult brain: are we there yet?
Ghashghaei, H. T., Lai, C., & Anton, E. S. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2074 · Cited by 192 · see citing works
“Remnants of gonadotropin-releasing hormone (GnRH + ) neurons, which are essential for autonomic functions relating to sexual behaviou”
BackgroundMRI atlas of the human hypothalamus
Baroncini, M., Jissendi, P., Balland, É., Besson, P., Pruvo, J., Francke, J.-P., Dewailly, D., Blond, S., & Prévot, V. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.07.013 · Cited by 190 · see citing works
“…for the integration and coordination of various brain functions, and as such, it is prone to involvement in several major brain disorders (Saper, 1990; Overeem et al., 2002; Sisk and Foster, 2004; Swaab, 2006; Aziz et al., 2007; Bao et al., 2008; Willis, 2008; Gordon, 2010; Kalsbeek et al., 2010).”
BackgroundBecker, S. P., Langberg, J. M., & Byars, K. (2015) · Journal of Youth and Adolescence · doi:10.1007/s10964-014-0248-y · Cited by 197 · see citing works
“synaptic pruning (Sisk and Foster 2004).”
BackgroundSibley, M. H., Kuriyan, A. B., Evans, S. W., Waxmonsky, J. G., & Smith, B. H. (2014) · Clinical Psychology Review · doi:10.1016/j.cpr.2014.02.001 · Cited by 190 · see citing works
“…changes in the reproductive system, puberty is characterized by a period of rapid reorganization of neural circuitry, which is thought to influence regions of the brain associated with planning, drug sensitivity, response to reward, decisionmaking, and risk-taking (Sisk & Foster, 2004).”
BackgroundFrom the stressed adolescent to the anxious and depressed adult: Investigations in rodent models
McCormick, C. M., & Green, M. R. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.063 · Cited by 180 · see citing works
“Adolescence is a transitional phase between childhood and adulthood in which puberty is a defining characteristic, although adolescence encompasses a wider range of developmental changes than does puberty (Sisk and Foster, 2004; Blakemore et al., 2010).”
Animal Models of Depression: What Can They Teach Us about the Human Disease?
Becker, M., Pinhasov, A., & Ornoy, A. (2021) · Diagnostics · doi:10.3390/diagnostics11010123 · Cited by 185 · see citing works
Emergence of sex differences in the development of substance use and abuse during adolescence
Kuhn, C. M. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.06.003 · Cited by 182 · see citing works
“…respectively causes further sexual differentiation of behaviors including aggression in males and feeding-related behaviors in females (Juraska, Sisk, & DonCarlos, 2013; Schulz, Molenda-Figueira, & Sisk, 2009; Schulz et al., 2004; Schulz & Sisk, 2006; Sisk & Foster, 2004; Sisk & Zehr, 2005).”
BackgroundPrasad, P. K., Hardy, K. K., Zhang, N., Edelstein, K., Srivastava, D. K., Zeltzer, L. K., Stovall, M., Seibel, N. L., Leisenring, W. M., Armstrong, G. T., et al. (2015) · Journal of Clinical Oncology · doi:10.1200/jco.2014.57.7528 · Cited by 178 · see citing works
“throughout adolescence and into early young adulthood, with accelerated development of higher-order skills such as executive functions.(9,10) The full extent of executive dysfunction may only become evident in adolescence and adulthood, with the onset of expectations to act more independently and use advanced planning…”
BackgroundRegulation of Body Size and Growth Control
Texada, M., Koyama, T., & Rewitz, K. (2020) · Genetics · doi:10.1534/genetics.120.303095 · Cited by 129 · see citing works
Reward-related brain function and sleep in pre/early pubertal and mid/late pubertal adolescents
Holm, S. M., Forbes, E. E., Ryan, N. D., Phillips, M. L., Tarr, J. A., & Dahl, R. E. (2009) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2009.04.001 · Cited by 174 · see citing works
“were Tanner stage three, four, or five on the Tanner scale that assesses breast/genital development, an index reflecting changes in levels of gonadal steroids, which influence neural development and affect-related brain function [33].”
BackgroundEarly Cannabis Use, Polygenic Risk Score for Schizophrenia and Brain Maturation in Adolescence
French, L., Gray, C., Leonard, G. T., Perron, M., Pike, G. B., Richer, L., Séguin, J. R., Veillette, S., Evans, J., Eric Artiges, A., et al. (2015) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.1131 · Cited by 175 · see citing works
Neurodevelopmental changes of reading the mind in the eyes
Moor, B. G., de Macks, Z. A. O., Güroğlu, B., Rombouts, S. A. R. B., van der Molen, M. W., & Crone, E. A. (2011) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr020 · Cited by 171 · see citing works
“Further, there is increasing evidence that pubertal hormones could have an impact on structural and functional brain maturation, as well as on behavior (Sisk and Foster, 2004; Blakemore et al., 2010).”
The relationship between puberty and social emotion processing
Goddings, A., Burnett Heyes, S., Bird, G., Viner, R. M., & Blakemore, S. (2012) · Developmental Science · doi:10.1111/j.1467-7687.2012.01174.x · Cited by 169 · see citing works
“Many of these changes have been linked with puberty, the biological process that culminates in reproductive competence and a defining event of adolescence (Sisk & Foster, 2004).”
BackgroundResultBramen, J. E., Hranilovich, J. A., Dahl, R. E., Chen, J. Z.-J., Rosso, C., Forbes, E. E., Dinov, I. D., Worthman, C. M., & Sowell, E. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033850 · Cited by 169 · see citing works
“Animal studies have shown that the brain’s response to both sensory and steroidal stimulation differs in juveniles, adolescents and adults [8].”
Background
- Authors
- Sisk, C. L., & Foster, D. L.
- Affiliations
- Michigan State University (US)
- University of Michigan (US)
- Corresponding author
- Sisk, Cheryl L
- ORCID
- Sisk, Cheryl L
- Venue
- Nature Neuroscience
- Published
- 2004-09-27
- Volume
- 7
- Issue
- 10
- Pages
- 1040-1047
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2094109313
- Cited by
- 1,085
- References
- 109
- Citations by year
- 2026: 40 · 2025: 37 · 2024: 50 · 2023: 46 · 2022: 60 · 2021: 58 · 2020: 59 · 2019: 50 · 2018: 75 · 2017: 43 · 2016: 59 · 2015: 62 · 2014: 56 · 2013: 74 · 2012: 57
- FWCI
- 4.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Keywords
- puberty, adolescence, GnRH neurons, steroid hormones, adolescent brain development, sexual motivation, sexual behavior, reproductive maturation, neural circuits, gonadal maturation
- MeSH terms
- Adolescent, Animals, Biological Clocks, Brain, Gonads, Humans, Hypothalamo-Hypophyseal System, Gonadotropin-Releasing Hormone, Puberty, Sexual Behavior, Sex Characteristics, Sexual Maturation
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