Cited by 175Hypothalamic control of reproductive hormonesNeurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology Research

Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?

Open access
Piekarski, David J., Johnson, Carolyn M., Boivin, Josiah R., Thomas, A. Wren, Lin, Wan Chen, Delevich, Kristen, M. Galarce, Ezequiel, Wilbrecht, Linda·2017·Brain Research

Abstract

Postnatal brain development is studded with sensitive periods during which experience dependent plasticity is enhanced. This enables rapid learning from environmental inputs and reorganization of cortical circuits that matches behavior with environmental contingencies. Significant headway has been achieved in characterizing and understanding sensitive period biology in primary sensory cortices, but relatively little is known about sensitive period biology in associative neocortex. One possible mediator is the onset of puberty, which marks the transition to adolescence, when animals shift their behavior toward gaining independence and exploring their social world. Puberty onset correlates with reduced behavioral plasticity in some domains and enhanced plasticity in others, and therefore may drive the transition from juvenile to adolescent brain function. Pubertal onset is also occurring earlier in developed nations, particularly in unserved populations, and earlier puberty is associated with vulnerability for substance use, depression and anxiety. In the present article we review the evidence that supports a causal role for puberty in developmental changes in the function and neurobiology of the associative neocortex. We also propose a model for how pubertal hormones may regulate sensitive period plasticity in associative neocortex. We conclude that the evidence suggests puberty onset may play a causal role in some aspects of associative neocortical development, but that further research that manipulates puberty and measures gonadal hormones is required. We argue that further work of this kind is urgently needed to determine how earlier puberty may negatively impact human health and learning potential.

AI snapshot

Written from the paper’s full text.

TL;DR

This review argues that puberty onset may causally contribute to some developmental shifts in associative neocortex, but the evidence remains largely correlational. It proposes that pubertal gonadal steroids may regulate sensitive-period plasticity via ERbeta-expressing PV+ interneurons and calls for experimental manipulation and hormone measurement.

Key findings

  • The review concludes that the evidence suggests puberty onset may play a causal role in some aspects of associative neocortical development, but further research that manipulates puberty and measures gonadal hormones is required.
  • Across language, reading/math, autobiographical memory, executive function, stress, and drug-related behaviors, many changes have inflection points near pubertal milestones; however, many studies did not assess pubertal status or hormones.
  • The proposed model is that pubertal steroids may influence the timing and/or duration of the juvenile sensitive period in cortical circuits primarily through PV+ inhibitory interneurons; ERbeta is expressed almost exclusively in PV+ interneurons (about 96% of ERbeta cells, representing 15–27% of total PV+ interneurons).
  • Earlier puberty is advancing and is associated with increased risk for psychopathology and substance abuse; if puberty closes sensitive periods, earlier onset may truncate juvenile learning plasticity.

Methods

  • Narrative review with no primary data; it synthesizes human, rodent, macaque, and songbird literature on associative neocortex, puberty milestones, gonadal steroids, and sensitive periods.
  • Main analysis is qualitative synthesis and proposal of a speculative biological model; no systematic search strategy or meta-analysis is described.
  • The paper compares pubertal milestones in humans and rodents and reviews neurobiological changes including gray/white matter, synapses, cell bodies/dendrites, excitatory/inhibitory transmission, and steroid receptor expression.

Limitations

  • Stated: little evidence causally links puberty onset with loss of plasticity; most studies do not manipulate puberty or assess pubertal markers; cross-sectional age-group studies lack resolution because puberty onset is variable.
  • Stated: the proposed model is speculative and has yet to be tested; further work must manipulate puberty and measure gonadal hormones, ideally longitudinally.
  • Evident: as a narrative review, it does not systematically quantify evidence or assess risk of bias; many cited findings are from animal models and may not translate directly to humans.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.brainres.2016.08.042

Cites

Statistics

Nothing to recompute.

Claims the paper makes

0 of 357 cited sources checked · 0 supported · 0 flagged

  • Findingcitation

    Pre-pubescent juvenile mice (P26) more quickly update their choice behavior when the reward unexpectedly shifts to a different odor in a reversal phase of the task.

    “and that they more quickly update their choice behavior when the reward unexpectedly shifts to a different odor in a reversal phase of the task (Johnson and Wilbrecht, 2011).”
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    • cites Johnson and Wilbrecht, 2011

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  • Findingcitation

    Pre-pubescent juvenile mice (P26) learn odor associations more rapidly than adults.

    “We observe that pre-pubescent juvenile mice (P26) learn the odor associations more rapidly than adults”
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    • cites Johnson and Wilbrecht, 2011

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  • Premisecitation

    In both sexes, circulating gonadal steroids rise across puberty until reaching adult concentrations.

    “In both sexes, circulating gonadal steroids (predominately estradiol and progesterone in girls and testosterone in boys, although both sexes experience rises in all three hormones at puberty) rise across puberty until reaching adult concentrations”
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    • cites Boswell, 2014

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    • cites Rilling et al., 1996 source

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  • Interpretationreasoning

    Development is likely studded with a series of sensitive periods in which experience-dependent plasticity in specific circuits, including those in associative regions of neocortex, is timed to coincide with access to important information.

    “Thus, development is likely studded with a series of sensitive periods in which experience-dependent plasticity in specific circuits, including those in associative regions of neocortex, is timed to coincide with access to important information.”
    Quote in the paperSubstantial claim
  • Interpretationreasoning

    Overall, there is an intriguing array of changes in the neurobiology and function of associative neocortex with inflection points near the ages of pubertal milestones.

    “Overall, we uncover an intriguing array of changes in the neurobiology and function of associative neocortex with inflection points near the ages of pubertal milestones.”
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    Findingown data

    Behavioral flexibility declines with age and is adult-like after P40, about 10 days after the onset of puberty in mice.

    “Behavioral flexibility declines with age and is adult-like after P40, just ~10 days after the onset of puberty in mice (Fig. 4).”
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    Premisecitation

    During the peripubertal period, plasticity attuned to information from parents or the natal environment may close, while plasticity related to social opportunities and sampling the wider environment may peak.

    “During this period, plasticity attuned to information from parents or the natal environment may close, while plasticity related to social opportunities and sampling the wider environment may peak”
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    • cites Crone and Dahl, 2012 source

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    Premisecitation

    During childhood and adolescence relatively more energy may be allocated toward somatic growth, while in adulthood growth is restricted so that more energy can be allocated toward reproductive ends.

    “during childhood and adolescence relatively more energy may be allocated toward somatic growth, while in adulthood growth is restricted so that more energy can be allocated toward reproductive ends”
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    • cites Ellis et al., 2009 source

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    Premisecitation

    Earlier puberty is associated with vulnerability for substance use, depression and anxiety.

    “earlier puberty is associated with vulnerability for substance use, depression and anxiety”
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    • cites Deardorff et al., 2007 source

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    • cites Graber et al., 2004

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    • cites Stice et al., 2001 source

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    Interpretationreasoning

    The sequence of pubertal milestones is similar in humans and rodents, suggesting that rodents may serve as a valid model for human pubertal development.

    “The sequence of pubertal milestones is similar in humans and rodents, suggesting that rodents may serve as a valid model for human pubertal development”
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    Premisenone given

    Puberty onset correlates with reduced behavioral plasticity in some domains and enhanced plasticity in others.

    “Puberty onset correlates with reduced behavioral plasticity in some domains and enhanced plasticity in others”
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    Premisecitation

    The importance assigned to each behavioral or physiological endpoint varies by age and stage of development.

    “The importance assigned to each behavioral or physiological endpoint varies by age and stage of development”
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    • cites Hochberg and Belsky, 2013

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    Premisecitation

    Pubertal onset is occurring earlier in developed nations, particularly in unserved populations.

    “Pubertal onset is also occurring earlier in developed nations, particularly in unserved populations”
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    • cites Aksglaede et al., 2009 source

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    • cites Biro et al., 2013 source

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    • cites Herman-Giddens, 2006 source

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    Premisecitation

    In boys, the first external indicator of puberty onset occurs with testosterone-induced increase in testicular volume along with a change in the color and texture of the scrotal skin.

    “In boys, milestones are more difficult to observe; the first external indicator of puberty onset occurs with testosterone-induced increase in testicular volume along with a change in the color and texture of the scrotal skin”
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    • cites Marshall and Tanner, 1970

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    Premisecitation

    Life history theory posits that an animal has finite time and resources and thus must selectively allocate these resources toward various evolutionary endpoints.

    “Life history theory posits that an animal has finite time and resources and thus must selectively allocate these resources toward various evolutionary endpoints”
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    • cites Ellis et al., 2009 source

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    • cites Roff, 2002

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    • cites Stearns, 1992

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    Premisenone given

    Puberty onset in animals, including humans, is initiated by an increase in pulsatile release of gonadotropin releasing hormone (GnRH) from the hypothalamus, which signals the pituitary to release lutenizing hormone and follicle stimulating hormone that mature the gonads and increase production and release of gonadal steroids.

    “Puberty onset in animals, including humans, is initiated by an increase in pulsatile release of gonadotropin releasing hormone (GnRH) from the hypothalamus, which signals the pituitary to release lutenizing hormone and follicle stimulating hormone that mature the gonads and increase production and release of gonadal steroids.”
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    Interpretationreasoning

    Juveniles may allocate their time and energy toward exploring and learning about their natal environment because their basic needs are provided by their parents.

    “because their basic needs (e.g. nutrition and protection) are provided by their parents, juveniles may allocate their time and energy toward exploring and learning about their natal environment”
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    Interpretationreasoning

    Once initiated, puberty likely exerts its broad effects on brain and body through the rise in gonadal steroids.

    “Once initiated, puberty likely exerts its broad effects on brain and body through the rise in gonadal steroids.”
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    Premisecitation

    Numerous factors may accelerate puberty in humans and animals including a stressful early environment or absence of a father in the household, early exposure to endocrine disruptors, or childhood obesity.

    “numerous factors may accelerate puberty in humans and animals including a stressful early environment or absence of a father in the household (Belsky, 2012), early exposure to endocrine disruptors (Meeker, 2012), or childhood obesity (Ahmed et al., 2009)”
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    Premisecitation

    Over the last decades, the average age at puberty onset in girls has advanced by multiple years.

    “Over the last decades, the average age at puberty onset in girls has advanced by multiple years”
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    • cites Aksglaede et al., 2009 source

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    • cites Biro et al., 2013 source

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    Premisecitation

    Infants and children exposed to a second language showed overlapping BOLD signal patterns when processing both languages in adulthood, but adults who became fluent in a second language after the first decade of life recruited different neural networks to process their second language.

    “Another study demonstrated that infants and children exposed to a second language showed overlapping BOLD signal patterns when processing both languages in adulthood, but adults who became fluent in a second language after the first decade of life (mean age 11.2 years old) recruited different neural networks to process their second language”
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    • cites Kim et al., 1997 source

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    Interpretationreasoning

    If this biological limit comes earlier in already disadvantaged groups, then it may enhance disparities in learning and future potential for achievement.

    “Further, if this biological limit comes earlier in already disadvantaged groups, then it may enhance disparities in learning and future potential for achievement.”
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    Premisecitation

    In zebra finches, pre-pubertal exposure to testosterone impairs song learning by inducing early song crystallization, consistent with the idea that hormones are sufficient to close a sensitive period of song flexibility.

    “In zebra finches, pre-pubertal exposure to testosterone impairs song learning by inducing early song crystallization, consistent with the idea that hormones are sufficient to close a sensitive period of song flexibility”
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    • cites Korsia and Bottjer, 1991

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    Premisecitation

    Studies of language-specific learning problems show that complex sensory processing is delayed in subjects diagnosed with dyslexia and other language-specific impairments, but improvements can be observed until age 10; after age 10, improvement stalls and subjects never 'catch up' with typically developing individuals.

    “studies show that complex sensory processing is delayed in subjects diagnosed with dyslexia and other language-specific impairments, but improvements can be observed until age 10. After age 10, improvement stalls and subjects never ‘catch up’ with typically developing individuals”
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    • cites Wright and Zecker, 2004

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    Premisecitation

    From a life history theory standpoint, earlier sexual maturation may reflect an adaptive developmental response and distinct life history strategy that maximizes reproductive fitness in a harsh environment.

    “From a life history theory standpoint, earlier sexual maturation may reflect an adaptive developmental response and distinct life history strategy that maximizes reproductive fitness in a harsh environment”
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    • cites Belsky, 2012 source

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    Premisecitation

    Gonadal steroids can affect cell physiology over the long term by acting as transcription factors to regulate gene expression or rapidly through non-genomic second messenger cascades.

    “can affect cell physiology over the long term by acting as transcription factors to regulate gene expression (Heldring et al., 2007) or rapidly through non-genomic second messenger cascades (Micevych and Dominguez, 2009)”
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    • cites Heldring et al., 2007 source

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    Premisecitation

    Puberty onset is associated with enhanced risk for psychopathology and behavior problems, including anxiety and depression, and substance abuse.

    “it is clear that puberty onset is associated with enhanced risk for psychopathology and behavior problems, including anxiety and depression, (Deardorff et al., 2007; Deardorff et al., 2013; Ge et al., 1996; Ge et al., 2001; Graber et al., 2004; Graber et al., 2006; Hayward et al., 1997; Silberg et al., 1999), and substance abuse (Graber et al., 1997; Stice et al., 2001)”
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    • cites Deardorff et al., 2007 source

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    Premisecitation

    Song motor plasticity is reduced after sexual maturation in species that learn one song for life (zebra finches), but in species that learn each season (canaries), plasticity is regulated by seasonal changes in gonadal steroids.

    “Song motor plasticity is reduced after sexual maturation in species that learn one song for life (zebra finches), but in species that learn each season (canaries), plasticity is regulated by seasonal changes in gonadal steroids”
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    • cites Doupe and Kuhl, 1999 source

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  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Interpretationreasoning

    If puberty onset closes sensitive periods in associative neocortex, then advanced puberty onset may truncate the juvenile period of early learning and enhanced plasticity.

    “If puberty onset closes sensitive periods in associative neocortex, then advanced puberty onset may truncate the juvenile period of early learning and enhanced plasticity.”
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    Premisecitation

    There is biological evidence that the location of language centers in the neocortex is highly plastic, but this plasticity is decreased in groups measured at postpubertal ages.

    “There is biological evidence that the location of language centers in the neocortex is highly plastic, but this plasticity is decreased in groups measured at postpubertal ages.”
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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Earlier puberty may be partly caused by increases in food intake and body mass index, but racial differences may also be independent of differences in body mass index.

    “Earlier puberty may be partly caused by increases in food intake and body mass index, but racial differences may also be independent of differences in body mass index”
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    • cites Rosenfield et al., 2009 source

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    Study design and conductcitation

    The relative roles that biology and social factors play in the development of puberty-related psychopathology is difficult to determine from studies in humans.

    “Unfortunately, the relative roles that biology and social factors play in the development of puberty-related psychopathology is difficult to determine from studies in humans”
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    Premisecitation

    In female rodents, vaginal opening is followed some days later by first estrus and a few days later by onset of regular cyclicity.

    “This is followed some days later by first estrus and a few days later by onset of regular cyclicity”
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    Premisecitation

    The associative cortices are thought to develop later than sensory cortices.

    “The associative cortices are thought to develop later than sensory cortices”
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    • cites Huttenlocher and Dabholkar, 1997

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    Premisecitation

    Gonadectomy combined with androgen receptor blockade during adolescence disrupts the development of crystallized adult song, suggesting that hormones are necessary for normal song crystallization.

    “gonadectomy combined with androgen receptor blockade during adolescence disrupts the development of crystallized adult song, suggesting that hormones are necessary for normal song crystallization”
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    • cites Bottjer and Hewer, 1992

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    Premisecitation

    In males, increased testosterone at puberty induces separation of the prepuce from the glans penis accompanied by increasing testicular volumes and eventual attainment of fertility.

    “In males, increased testosterone at puberty induces separation of the prepuce from the glans penis (preputial separation; (Korenbrot et al., 1977) accompanied by increasing testicular volumes and eventual attainment of fertility.”
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    • cites Korenbrot et al., 1977 source

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    Premisecitation

    In female rodents, the first indicator of the pubertal rise in estradiol is vaginal opening, during which increased circulating estradiol induces apoptosis in cells that form a thin sheath over the vaginal opening.

    “In female rodents, the first indicator of the pubertal rise in estradiol is vaginal opening, during which increased circulating estradiol induces apoptosis in cells that form a thin sheath over the vaginal opening”
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    • cites Ito et al., 2014 source

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    Premisecitation

    In North American boys and girls, earlier maturation is more common in black, Hispanic and low socioeconomic status children.

    “In North American boys and girls, earlier maturation is more common in black, Hispanic and low socioeconomic status children”
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    • cites Biro et al., 2010

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    • cites Biro et al., 2013 source

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    • cites Herman-Giddens, 2006 source

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    Premisecitation

    Age clearly affects prospects for recovery of executive function after focal injury in rat models; rats recover poorly from lesions made in the first week of life, but lesions made during the second week of life often result in full recovery of executive function in adulthood.

    “Age clearly affects prospects for recovery of executive function after focal injury in rat models; rats recover poorly from lesions made in the first week of life, but lesions made during the second week of life—roughly analogous to the first year of life in humans (Kolb and Cioe, 2000)—often results in full recovery of executive function in adulthood”
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    • cites Kolb, 1987 source

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    Interpretationnone given

    Changes to associative neocortex during the transition to adolescence may contribute to the altered executive function observed between juveniles and adolescents.

    “Changes to associative neocortex during the transition to adolescence may contribute to the altered executive function observed between juveniles and adolescents.”
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    Premisecitation

    Autobiographical memories related to important life events and life decisions peak after puberty and coincide with the time of important stages of early independent decision making.

    “In contrast, autobiographical memories related to important life events and life decisions peak after puberty and coincide instead with the time of important stages of early independent decision making”
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    • cites Koppel and Berntsen, 2015

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    • cites Rubin, 2015 source

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    Premisecitation

    More recent studies show that earlier maturation is still associated with positive effect for boys in terms of academic performance, but earlier maturation is now associated with worse academic performance in girls.

    “More recent studies of academic performance show that earlier maturation is still associated with positive effect for boys in terms of academic performance, but earlier maturation is now associated with worse academic performance in girls”
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    • cites Dubas et al., 1991 source

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    Premisecitation

    Early maturers of both sexes showed superior performance at age 8, 11 and 15, and this appeared to be independent of social class.

    “they found that early maturers of both sexes showed superior performance at age 8, 11 and 15, and this appeared to be independent of social class”
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    • cites Douglas and Ross, 1964

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    Premisecitation

    Developmental changes in spatial cognition may be driven by organizational effects of steroid hormones.

    “Schulz et al. (2009a) suggest developmental changes in spatial cognition may be driven by organizational effects of steroid hormones.”
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    • cites Schulz et al., 2009a

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    Interpretationnone given

    Subdomains of executive function develop along different trajectories, resulting in a complex pattern of maturation.

    “However, subdomains of executive function develop along different trajectories, resulting in a complex pattern of maturation.”
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    Premisecitation

    Relative pubertal timing (compared to grade level peers) rather than pubertal status (independent of grade level) drives these effects, suggesting that extrinsic social factors play a role in the effects of pubertal maturation on academic performance more than intrinsic biological factors.

    “Dubas et al. (1991) also find that relative pubertal timing (compared to grade level peers) rather than pubertal status (independent of grade level) drives these effects suggesting that extrinsic social factors play a role in the effects of pubertal maturation on academic performance more than intrinsic biological factors.”
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    • cites Dubas et al., 1991 source

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    Premisecitation

    Higher or lower levels of androgens due to idiopathic hypogonadotropic hypogonadism in men or congenital adrenal hyperplasia in women alters spatial cognition after puberty.

    “Schulz et al. (2009a) review a number of studies that show higher or lower levels of androgens due to idiopathic hypogonadotropic hypogonadism in men or congenital adrenal hyperplasia in women alters spatial cognition after puberty.”
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    • cites Schulz et al., 2009a

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    Interpretationcitation

    Across development, memories are differentially encoded or encoded in a way that they can be differentially later retrieved.

    “These data suggest that across development, memories are differentially encoded or encoded in a way that they can be differentially later retrieved”
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    • cites Rubin, 2015 source

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    Premisecitation

    Olfactory-related autobiographical memories are more readily retrieved from the time prior to puberty, and more general autobiographical memories are retrieved from around the peripubertal period than at later times in life.

    “Olfactory-related autobiographical memories are more readily retrieved from the time prior to puberty (Chu and Downes, 2000; Rubin, 2015; Willander and Larsson, 2008), and more general autobiographical memories are retrieved from around the peripubertal period than at later times in life”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Chu and Downes, 2000

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    • cites Janssen et al., 2011 source

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    Premisecitation

    Basic reading and mathematics skills are thought to depend on associative neocortex and are typically established in the prepubertal period from age 4-9.

    “Basic reading and mathematics skills are thought to depend on associative neocortex and are typically established in the prepubertal period from age 4–9 (by grade 3)”
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    • cites Blank, 2006

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    • cites Hernandez, 2011

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    Premisecitation

    Androgen receptor blockade enhances and testosterone reduces the capacity for adult song flexibility after nerve injury.

    “although androgen receptor blockade enhances and testosterone reduces the capacity for adult song flexibility after nerve injury”
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    • cites Williams et al., 2003 source

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    Interpretationreasoning

    Recovery capacity peaks during the second week of life before gradually declining across the juvenile period, and recovery potential becomes adult-like around the onset of puberty.

    “These data suggest that recovery capacity peaks during the second week of life before gradually declining across the juvenile period. Recovery potential then becomes adult-like around the onset of puberty.”
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    Premisecitation

    Prepubertal reading and math skills are thought to predict later outcomes.

    “Prepubertal reading and math skills are also thought to predict later outcomes”
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    • cites Hernandez, 2011

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    • cites Jordan et al., 2009

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    • cites Jordan and Levine, 2009

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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Premisenone given

    Associative neocortex is thought to be the site of memory storage, and a wealth of evidence suggests autobiographical memory storage changes with age.

    “Associative neocortex is thought to be the site of memory storage, and a wealth of evidence suggests autobiographical memory storage changes with age.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Studies from the 70s-80s find a decrement in spatial cognition at puberty onset or in earlier maturing children.

    “Petersen (1983) reviews a number of studies from the 70s-80s that find a decrement in spatial cognition at puberty onset or in earlier maturing children.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Petersen, 1983

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  • May combine two claims.

    Premisecitation

    The frontal association cortex is the seat of executive function and continues its development into the third decade of life in humans.

    “The frontal association cortex is the seat of executive function and continues its development into the third decade of life in humans”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Gogtay et al., 2004 source

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  • May combine two claims.

    Premisecitation

    Studies of complex switching report inconsistent developmental trajectories, including a plateau at age 10 or 11-12, gradual improvement across the teenage years, or an inverted U in the teenage years.

    “with other studies suggesting a plateau at age 10 (Chelune and Baer, 1986; Chevalier et al., 2013; De Luca et al., 2003) or 11–12 (Huizinga et al., 2006; Huizinga and van der Molen, 2007; Somsen, 2007), gradual improvement across the teenage years (Crone et al., 2006; Crone et al., 2008), or an inverted U in the teenage years (van der Schaaf et al., 2011).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Chelune and Baer, 1986 source

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    • cites Chevalier et al., 2013 source

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    • cites De Luca et al., 2003 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationnone given

    There are considerable individual differences in response inhibition performance across studies that may reflect age-independent factors.

    “however there are considerable individual differences in performance across studies that may reflect age independent factors.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    A growing body of studies suggests that flexibility in goal-directed behavior increases during adolescence.

    “A growing body of studies suggests that flexibility in goal-directed behavior increases during adolescence.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim.

    Interpretationreasoning

    Increased neural capacity to represent rules of the task and multiple actions may drive age-related increases in task performance.

    “Increased neural capacity to represent rules of the task and multiple actions may drive age related increases in task performance.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Pubertal stage and hormone concentrations were not significantly associated with delay discounting in either boys or girls.

    “Pubertal stage and hormone concentrations were not significantly associated with delay discounting in either boys or girls, but prepubertal children were not included in these studies, so the effect of puberty onset could not be determined (Bromberg et al., 2015; de Water et al., 2014).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Bromberg et al., 2015 source

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    • cites de Water et al., 2014 source

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  • May combine two claims.

    Premisecitation

    In 14-year-old adolescents, higher testosterone levels were associated with greater control over emotional actions and increased recruitment of the anterior prefrontal cortex.

    “Higher testosterone levels were associated with greater control over emotional actions and increased recruitment of the anterior prefrontal cortex.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Tyborowska et al., 2016 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    An accelerated longitudinal study of antisaccade performance in humans showed that accuracy improved most steeply between ages 10-14, but the authors did not track pubertal status.

    “An accelerated longitudinal design study of antisaccade performance in humans showed that accuracy improved most steeply between ages 10–14, but the authors did not track the pubertal status of participants (Paulsen et al., 2015).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Paulsen et al., 2015 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The ability to switch between sets of simple stimuli emerges by age 5.

    “The ability to switch between sets of simple stimuli emerges by age 5 (Espy, 1997).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Espy, 1997 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Delay discounting generally decreases between young childhood and adulthood, meaning children tend to choose a smaller immediate reward over a larger delayed reward.

    “Delay discounting generally decreases between young childhood and adulthood, meaning children tend to choose a smaller immediate reward over a larger delayed reward (Christakou et al., 2011; de Water et al., 2014; Green et al., 1994; Olson et al., 2007; Scheres et al., 2006; Steinberg et al., 2009).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Christakou et al., 2011 source

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    • cites de Water et al., 2014 source

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    • cites Green et al., 1994 source

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  • May combine two claims.

    Premisecitation

    Performance in a feedback learning task increased from age 8-12 before reaching adult levels, but was not explained by pubertal stage, estradiol, or testosterone levels.

    “Additionally, performance in a feedback learning task increased from age 8–12 before reaching adult levels, but was not explained by pubertal stage, estradiol, or testosterone levels”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Peters et al., 2014 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Early life stress can induce early vaginal opening in female rats.

    “Further, early life stress can induce early vaginal opening in female rats (Grassi-Oliveira et al., 2016)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Grassi-Oliveira et al., 2016 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In a follow up, Petersen (1983) finds null effects of pubertal status and grade (6-8) in a sample of high performing children.

    “However, in follow up Petersen (1983) finds null effects of pubertal status and grade (6–8) in a sample of high performing children.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Petersen, 1983

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In postpubertal rats, older adolescents were less cognitively flexible in reversal and set-shift phases of training than adults, but juveniles were not studied.

    “A similar task in postpubertal rats (but with 2 rather than 4 choices in the task) instead found that older adolescents were less cognitively flexible in reversal and set-shift phases of training than adults, but juveniles were not studied (Newman and McGaughy, 2011).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Newman and McGaughy, 2011

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  • May combine two claims.

    Premisecitation

    Stressors occurring during sensitive periods may have profound effects on development of brain, cognition, and behavior by altering the organization of neural circuits, which may lead to increased risk for psychopathology and negative health outcomes.

    “Stressors occurring during sensitive periods may have profound effects on development of brain, cognition, and behavior by altering the organization of neural circuits, which in turn may lead to increased risk for psychopathology and negative health outcomes (Gilbert et al., 2009; Heim and Nemeroff, 2001; Sánchez et al., 2001).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Gilbert et al., 2009 source

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    • cites Heim and Nemeroff, 2001 source

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    • cites Sánchez et al., 2001 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    A digging-based foraging task is a naturalistic method to test behavioral flexibility and is rapidly learned by mice and rats.

    “A digging-based foraging task is a naturalistic method to test behavioral flexibility and is rapidly learned by mice and rats (Birrell and Brown, 2000; Garner et al., 2006; Kim and Ragozzino, 2005).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Birrell and Brown, 2000 source

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    • cites Garner et al., 2006 source

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    • cites Kim and Ragozzino, 2005

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Children (age 6-12) and adolescents (age 13-17) excel at learning rules through experience, whereas adults were biased to learn more from explicit instruction.

    “A recent behavioral study showed that children (age 6–12) and adolescents (age 13–17) excel at learning rules through experience, whereas adults were biased to learn more from explicit instruction”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Decker et al., 2015 source

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  • May combine two claims.

    Interpretationcitation

    Although specific patterns of pubertal drug preference and intake differ between drugs, pubertal hormones regulate drug-related behaviors for a variety of drugs of abuse.

    “Thus, although specific patterns of pubertal drug preference and intake differ between drugs, pubertal hormones regulate drug-related behaviors for a variety of drugs of abuse.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Dopamine receptor expression peaks around the age of puberty, though only for specific receptor subtypes in specific neuronal populations.

    “Dopamine receptor expression also peaks around the age of puberty, though only for specific receptor subtypes in specific neuronal populations (reviewed in (Wahlstrom et al., 2010)).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Wahlstrom et al., 2010 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Prepubertal (p25) gonadectomy produces opposite effects on cocaine-induced locomotion in adult (p65) male and female rats, suggesting that pubertal hormones play a role in regulating sex-specific responses to cocaine.

    “In addition, prepubertal (p25) gonadectomy produces opposite effects on cocaine-induced locomotion in adult (p65) male and female rats, suggesting that pubertal hormones play a role in regulating sex-specific responses to cocaine (Parylak et al., 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Parylak et al., 2008 source

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  • May combine two claims.

    Premisecitation

    Gonadectomy at either pre-pubertal or adult timepoint increases both ethanol preference and intake in male rats, and testosterone replacement in adulthood lowers ethanol preference to control levels.

    “In contrast, gonadectomy at either timepoint increases both ethanol preference and intake in male rats (Vetter-O’hagen and Spear, 2011), and testosterone replacement in adulthood (p77–93) lowers ethanol preference to control levels (Vetter-O’Hagen et al., 2011).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Vetter-O’hagen and Spear, 2011

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    • cites Vetter-O’Hagen et al., 2011 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    p30-50 female rats show higher levels of cocaine self-administration than p30-p50 male rats, with higher levels of estradiol correlating with higher levels of cocaine self-administration in females.

    “For example, p30–50 female rats show higher levels of cocaine self-administration than p30-p50 male rats, with higher levels of estradiol correlating with higher levels of cocaine self-administration in females (Lynch, 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Lynch, 2008 source

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  • May combine two claims.

    Premisecitation

    Social isolation from P20-40 in mice disrupts medial PFC function and myelination, but later isolation from P40-60 does not.

    “Social isolation from P20–40 in mice disrupts medial PFC function and myelination, but later isolation from P40–60 does not (Makinodan et al., 2012).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Makinodan et al., 2012 source

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  • May combine two claims.

    Premisecitation

    In nicotine, sex differences in self-administration emerge at the time of puberty (p30-45), with females self-administering more than males and high estradiol to progesterone ratios correlating with higher rates of self-administration in females.

    “In the case of nicotine, sex differences in self-administration emerge at the time of puberty (p30–45), with females self-administering more than males and high estradiol to progesterone ratios correlating with higher rates of self-administration in females (Lynch, 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Lynch, 2009 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Adolescence, more than early life or adulthood, is a sensitive period for stress-induced programming of the brain.

    “Some reviews suggest that adolescence, more than early life or adulthood, is a sensitive period for stress-induced programming of the brain (Mccormick et al., 2010)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Mccormick et al., 2010 source

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  • May combine two claims.

    Premisecitation

    The dopamine system that innervates the frontal association cortex changes in complex ways around puberty, with distinct components showing distinct developmental trajectories.

    “The dopamine system that innervates the frontal association cortex changes in complex ways around puberty, with distinct components showing distinct developmental trajectories (Benes et al., 1996; Kuhn et al., 2010; McCutcheon and Marinelli, 2009; Sinclair et al., 2014; Wahlstrom et al., 2010).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Benes et al., 1996 source

      Not checked in the free run.

    • cites Kuhn et al., 2010 source

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    • cites McCutcheon and Marinelli, 2009

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationnone given

    There is growing evidence that early life stress alters development and perhaps accelerates the development of the brain and body.

    “There is growing evidence that early life stress alters development and perhaps accelerates the development of the brain and body.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationnone given

    The extent to which peripubertal vulnerability to long-term effects of drug exposure is mediated by pubertal hormones remains largely unknown.

    “While many studies point to ages surrounding puberty as a vulnerable time for the long-term effects of drug exposure, the extent to which this vulnerability is mediated by pubertal hormones remains largely unknown.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Parvalbumin positive fast spiking and non-fast spiking interneurons in frontal cortex dramatically increase in excitation in response to the D2 agonist quinpirole between p36 and p50, while non fast spiking interneurons increase in their response to a D1 receptor agonist.

    “For example, parvalbumin positive (PV+) fast spiking and non-fast spiking interneurons in frontal cortex dramatically increase in excitation in response to the D2 agonist quinpirole between p36 and p50, while non fast spiking interneurons increase in their response to a D1 receptor agonist (Tseng and O’donnell, 2007).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Tseng and O’donnell, 2007

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Animal models of drug abuse reveal unique patterns of drug-related behaviors and heightened sensitivity to the long-term effects of drug exposure during the peripubertal period.

    “it is not surprising that animal models of drug abuse reveal unique patterns of drug-related behaviors (Schramm-Sapyta et al., 2009) and heightened sensitivity to the long-term effects of drug exposure during this period (reviewed below).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Schramm-Sapyta et al., 2009 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Social isolation may result in stunted social learning from lack of play behavior, which itself peaks between P28-P35 in rats.

    “This may result in stunted social learning from lack of play behavior, which itself peaks between P28-P35 in rats (Meaney and Stewart, 1979; Thor and Holloway, 1984; Vanderschuren et al., 1997).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Meaney and Stewart, 1979

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    • cites Thor and Holloway, 1984

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    • cites Vanderschuren et al., 1997 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationnone given

    The onset of puberty may change individuals' needs and expectations as well as sensitivity to different forms of stress, resulting in different responses to stress between juveniles and adolescents.

    “The onset of puberty may change individuals’ needs and expectations as well as sensitivity to different forms of stress, resulting in different responses to stress between juveniles and adolescents.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    For ethanol, pre-pubertal (p23) or adult (p70) gonadectomy does not affect intake in adult female rats, though pre-pubertal gonadectomy increases ethanol preference in adult females.

    “For ethanol, pre-pubertal (p23) or adult (p70) gonadectomy does not affect intake in adult female rats, though pre-pubertal gonadectomy increases ethanol preference in adult females (Vetter-O’hagen and Spear, 2011).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Vetter-O’hagen and Spear, 2011

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Early life adversity may accelerate maturation of fear extinction/recovery behavior, attachment and avoidance learning, reversal learning, and maturation of frontal-amygdala connectivity.

    “maturation of fear extinction/recovery behavior (Callaghan and Richardson, 2011), attachment and avoidance learning (Moriceau et al., 2009), reversal learning (Thomas et al., 2015), and maturation of frontal-amygdala connectivity (Gee et al., 2013).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Callaghan and Richardson, 2011 source

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    • cites Moriceau et al., 2009 source

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    • cites Thomas et al., 2015

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    A greater number of accumbens-projecting PFC neurons express D1 receptors at p44 compared to p27 and p105 in male rats, a pattern that may directly relate to drug-seeking behavior in adolescent (p44) animals.

    “For example, a greater number of accumbens-projecting PFC neurons express D1 receptors at p44 compared to p27 and p105 in male rats—a pattern that may directly relate to drug-seeking behavior in adolescent (p44) animals (Brenhouse et al., 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Brenhouse et al., 2008 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In the prefrontal cortex, reduction in global synapse density occurs later than in sensory neocortex and declines at its steepest rate around the time of pubertal milestones.

    “In the prefrontal cortex, reduction in global synapse density occurs later than in sensory neocortex and declines at its steepest rate around the time of pubertal milestones (Huttenlocher and Dabholkar, 1997).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Huttenlocher and Dabholkar, 1997

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Peripubertal peaks in dopamine neuron firing and dopamine receptor expression suggest a period of enhanced motivation, reinforcement/reward sensitivity, and peripubertal changes in neuronal responses to dopamine receptor activation may be crucial for developing cognitive strategies appropriate for late adolescent and adult life stages.

    “Peripubertal peaks in dopamine neuron firing and dopamine receptor expression suggest a period of enhanced motivation, reinforcement/reward sensitivity, and peripubertal changes in neuronal responses to dopamine receptor activation may be crucial for developing the cognitive strategies appropriate for late adolescent and adult life stages.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Frontal white matter increases in volume in a linear fashion in male rats but jumps in females from P25-35 and then again from p45-60, suggesting specific regulation during the peripubertal period.

    “Frontal white matter increases in volume in a linear fashion in male rats but jumps in females from P25–35 and then again from p45–60, suggesting specific regulation during the peripubertal period (Willing and Juraska, 2015).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Willing and Juraska, 2015

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  • May combine two claims.

    Premisecitation

    The stimulatory effects of estradiol on dopaminergic function are well-established for adult female rodents, while evidence in pubertal females comes largely from effects of prepubertal ovariectomy on responses to dopaminergic drugs such as cocaine.

    “While the stimulatory effects of estradiol on dopaminergic function are well-established for adult female rodents (Kuhn et al., 2010), evidence in pubertal females comes largely from the effects of prepubertal ovariectomy on responses to dopaminergic drugs such as cocaine (reviewed above; Parylak et al., 2008).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Kuhn et al., 2010 source

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    • cites Parylak et al., 2008 source

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  • May combine two claims.

    Premisecitation

    In rats, gonadectomy results in no change in white matter volume in male rats but does increase white matter volume in female rats in the frontal cortex.

    “In rats, gonadectomy results in no change in white matter volume in male rats but does increase white matter volume in female rats in the frontal cortex (Koss et al., 2015).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Koss et al., 2015 source

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  • May combine two claims.

    Premisecitation

    Castration or testosterone injections during mid to late adolescence (p45-p60) alter various markers of dopaminergic function in male rats, though gonadal hormones are not necessary for male-specific peaks in striatal dopamine receptor expression.

    “For example, castration or testosterone injections during mid to late adolescence (p45-p60) alter various markers of dopaminergic function in male rats (Purves-Tyson et al., 2014), though gonadal hormones are not necessary for male-specific peaks in striatal dopamine receptor expression (Andersen et al., 2002).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Purves-Tyson et al., 2014 source

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    • cites Andersen et al., 2002 source

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  • May combine two claims.

    Premisecitation

    Androgen receptor expressing cells in the frontal cortex project to the VTA, providing the potential for puberty to initiate changes in bidirectional regulation of dopaminergic function.

    “Further, androgen receptor expressing cells in the frontal cortex project to the VTA (Aubele and Kritzer, 2012), providing the potential for puberty to initiate changes in bidirectional regulation of dopaminergic function.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Aubele and Kritzer, 2012

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  • May combine two claims.

    Premisecitation

    Castration in a very small sample of male monkeys did not clearly impact the general pattern of synapse density decline in the prefrontal principal sulcus, but there were too few samples to draw strong conclusions.

    “Castration in a very small sample of male monkeys did not clearly impact the general pattern of synapse density decline in the prefrontal principal sulcus (Anderson et al., 1995); however, there were too few samples to draw strong conclusions.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Anderson et al., 1995 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Many cells in the ventral tegmental area also express tyrosine hydroxylase, suggesting they produce dopamine.

    “Many of these cells also express tyrosine hydroxylase, suggesting they produce dopamine.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Frye et al., 2013 source

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    • cites Willing and Wagner, 2016

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    • cites Kritzer, 1997 source

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  • May combine two claims.

    Interpretationreasoning

    Correlational data suggest that synapse pruning and pubertal milestones may be co-regulated, but some experimental data suggest otherwise.

    “These correlational data suggest that synapse pruning and pubertal milestones may be co-regulated, but some experimental data suggest otherwise.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    When controlling for age, both pubertal hormones and stage of puberty correlate with changes in gray matter across adolescent development in disparate regions of cortex, including frontal cortex.

    “When controlling for age, both pubertal hormones and stage of puberty correlate with changes in gray matter across adolescent development in disparate regions of cortex (De Bellis et al., 2001), including in the frontal cortex (Bramen et al., 2011; Gogtay et al., 2004; Herting et al., 2014; Herting et al., 2015; Koolschijn et al., 2014; Neufang et al., 2009; Peper et al., 2009a; Raznahan et al., 2”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites De Bellis et al., 2001 source

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    • cites Bramen et al., 2011 source

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    • cites Gogtay et al., 2004 source

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  • May combine two claims.

    Premisecitation

    In frontal and parietal cortex, the gray matter peak occurs around 10-11 years of age in girls, while the peak in boys is shifted about one year later.

    “In frontal and parietal cortex, this peak occurs around 10–11 years of age in girls, while the peak in boys is shifted about one year later (Giedd et al., 1999)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Giedd et al., 1999 source

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  • May combine two claims.

    Premisecitation

    In macaques, the GABA alpha 2 subunit declines during postnatal development while the GABA alpha 1 subunit increases in the frontal cortex, resulting in a faster decay of inhibitory currents in pyramidal cells after puberty.

    “In another study of macaques, the GABA alpha 2 subunit declined during postnatal development while the GABA alpha 1 subunit increased in the frontal cortex, resulting in a faster decay of inhibitory currents in pyramidal cells after puberty (Hashimoto et al., 2009).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Hashimoto et al., 2009 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    These changes could significantly alter information processing and plasticity in the frontal cortex.

    “These changes could significantly alter information processing and plasticity in the frontal cortex.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    A similar pattern is observed in certain subtypes of dendrite in the human prefrontal cortex, which decline in arborization starting between ~10-15 years old, though it is unknown if there is a sex difference.

    “A similar pattern is observed in certain subtypes of dendrite in the human prefrontal cortex, which decline in arborization starting between ~10–15 years old, though it is unknown if there is a sex difference (Petanjek et al., 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Petanjek et al., 2008 source

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  • May combine two claims.

    Premisecitation

    Lower turnover that comes with age means that neurons come to sample information from fewer potential partners and exhibit fewer long thin spines that have greater potential to undergo significant Hebbian strengthening.

    “Lower turnover that comes with age means that neurons come to sample information from fewer potential partners (Stepanyants and Chklovskii, 2005) and exhibit fewer long thin spines that have greater potential to undergo significant Hebbian strengthening (Bourne and Harris, 2007; Kasai et al., 2010).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Stepanyants and Chklovskii, 2005

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    • cites Bourne and Harris, 2007

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    • cites Kasai et al., 2010 source

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  • May combine two claims.

    Interpretationcitation

    Peripubertal development is more strongly associated with maturation of inhibition, implicating changes to inhibition as one mechanism underlying peripubertal changes to cortical plasticity and function.

    “These data suggest that peripubertal development is more strongly associated with maturation of inhibition, which implicates changes to inhibition as one mechanism underlying peripubertal changes to cortical plasticity and function.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    In humans, mRNA for GABA receptor subunits and markers of inhibitory cell bodies change substantially across postnatal development, with some specific subunits and markers showing either positive or negative inflections around 10 years of age.

    “In humans, mRNA for GABA receptor subunits (Duncan et al., 2010; Fillman et al., 2010) and markers of inhibitory cell bodies (Fung et al., 2010) change substantially across postnatal development, with some specific subunits and markers showing either positive or negative inflections around 10 years of age.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Duncan et al., 2010 source

      Not checked in the free run.

    • cites Fillman et al., 2010 source

      Not checked in the free run.

    • cites Fung et al., 2010 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Manipulating ovarian hormone availability has no effect on cell number in the frontal cortex in 12 month old rats, suggesting that the frontal cortex is more sensitive to gonadal steroids earlier in life.

    “Manipulating ovarian hormone availability has no effect on cell number in the frontal cortex in 12 month old rats, suggesting that the frontal cortex is more sensitive to gonadal steroids earlier in life (Chisholm et al., 2012).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Chisholm et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    PV+ interneurons may be most affected by puberty onset and thus may underlie the changes in inhibition onto pyramidal cells.

    “It appears that PV+ interneurons may be most affected by puberty onset and thus may underlie the changes in inhibition onto pyramidal cells.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    In rats, AMPA/Kainate receptor binding sites and GluR2 protein begin to decline between ~P24-P30 and P60.

    “In rats, AMPA/Kainate receptor binding sites (Insel et al., 1990) and GluR2 protein (Murphy et al., 2012) begin to decline between ~P24-P30 and P60.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Insel et al., 1990 source

      Not checked in the free run.

    • cites Murphy et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Many measures of excitatory transmission in cortical pyramidal cells do not change across adolescence, while some measures of inhibition show marked peripubertal changes.

    “While many measures of excitatory transmission in cortical pyramidal cells do not change across adolescence, some measures of inhibition show marked peripubertal changes (reviewed below).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    There is no age related decline in frontal cortex neuron numbers in males, nor does removing the testes before puberty result in any changes to neuron number.

    “There is no age related decline in frontal cortex neuron numbers in males, nor does removing the testes before puberty result in any changes to neuron number (Koss et al., 2015; Willing and Juraska, 2015).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Koss et al., 2015 source

      Not checked in the free run.

    • cites Willing and Juraska, 2015

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    BDNF signaling in the cortex is modulated by puberty and directly affected by gonadal steroid availability.

    “BDNF signaling in the cortex is modulated by puberty and directly affected by gonadal steroid availability (Hill et al., 2012)”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Hill et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    AR and both ERs are expressed sparsely in axons and dendrites in the frontal cortex, including on both pre and postsynaptic sites, where they may directly alter synaptic signaling.

    “AR and both ERs are expressed sparsely in axons and dendrites in the frontal cortex, including on both pre and postsynaptic sites (DonCarlos et al., 2003; Wang et al., 2010) where they may directly alter synaptic signaling.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites DonCarlos et al., 2003 source

      Not checked in the free run.

    • cites Wang et al., 2010

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given

    Data describing developmental changes in the various steroid receptors in cortex during peripubertal development is relatively sparse, particularly in association cortex.

    “Unfortunately, data describing developmental changes in the various steroid receptors in cortex during peripubertal development is relatively sparse, particularly in association cortex.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    PR is unambiguously expressed in the rat frontal cortex at birth and rises in both males and females until it peaks during the second week of life, after which it significantly declines and is maintained at lower levels into adulthood.

    “It is unambiguously expressed in the rat frontal cortex at birth and rises in both males and females until it peaks during the second week of life, after which it significantly declines and is maintained at lower levels into adulthood (Hagihara et al., 1992; Kato and Onouchi, 1981; Kato and Onouchi, 1983; Kato et al., 1984; Lopez and Wagner, 2009; Shughrue et al., 1991; Shughrue et al., 1992).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Hagihara et al., 1992 source

      Not checked in the free run.

    • cites Kato and Onouchi, 1981

      Not checked in the free run.

    • cites Lopez and Wagner, 2009

      Not checked in the free run.

  • May combine two claims. The quote only partly states this claim.

    Interpretationcitation

    These neurons are more easily recruited by excitatory input but may be less plastic after puberty.

    “suggesting that these neurons are more easily recruited by excitatory input but may be less plastic.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    One mRNA labeling study found low and diffuse expression of ERalpha mRNA in human temporal cortex and restricted expression in deep layers of entorhinal cortex.

    “but one mRNA labeling study found low and diffuse expression of ERalpha mRNA in temporal cortex and restricted expression in deep layers of entorhinal cortex (Osterlund et al., 2000).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Osterlund et al., 2000 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Prior to weaning (~P18), ERalpha expression declines precipitously and shortly after ERbeta rises, resulting in higher ERbeta expression in neocortex in adults.

    “Prior to weaning (~P18), ERalpha expression declines precipitously and shortly after ERbeta rises (Prewitt and Wilson, 2007; Wilson et al., 2011; Zsarnovszky and Belcher, 2001), resulting in higher ERbeta expression in neocortex in adults (Kritzer, 2002; Shughrue et al., 1997)”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Prewitt and Wilson, 2007

      Not checked in the free run.

    • cites Wilson et al., 2011 source

      Not checked in the free run.

    • cites Kritzer, 2002 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In one study of mRNA from homogenized tissue, expression of the PR B isoform peaked at P8 and then declined to basal values before weaning, while the A isoform rose, resulting in total PR expression in the cortex remaining into adulthood.

    “They found that expression of the B isoform peaked at P8 and then declined to basal values before weaning, while the A isoform rose, resulting in total PR expression in the cortex remaining into adulthood (Kato et al., 1993).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Kato et al., 1993 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The maintenance of excitation coupled with the rise in inhibition in frontal cortex likely results in altered excitatory to inhibitory balance within frontal networks, which has been associated with regulation of sensitive period plasticity.

    “The maintenance of excitation coupled with the rise in inhibition demonstrated in frontal cortex likely results in altered excitatory to inhibitory balance within frontal networks, which has been associated with regulation of sensitive period plasticity.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationreasoning

    Cortical expression of steroid receptors is developmentally regulated, suggesting changing function with development.

    “2. Cortical expression of these receptors is developmentally regulated, suggesting changing function with development.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    There is an increase in calcium-permeable AMPA receptors in adolescent PV+ interneurons in frontal cortex, which is associated with altered short term synaptic plasticity.

    “Finally, there is also an increase in calcium-permeable AMPA receptors in adolescent PV+ interneurons in frontal cortex, which is associated with altered short term synaptic plasticity (Wang and Gao, 2010).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Wang and Gao, 2010

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The shift in inhibition is likely mediated by PV+ interneurons, which are also thought to regulate sensitive period plasticity in sensory cortex, making them attractive candidates for pubertal regulation of association cortex plasticity.

    “This shift in inhibition is likely mediated by PV+ interneurons, which are also thought to regulate sensitive period plasticity in sensory cortex (Davis et al., 2015; de Villers-Sidani et al., 2008; Hensch, 2005; Le Magueresse and Monyer, 2013; Werker and Hensch, 2015), and therefore are attractive candidates for pubertal regulation of association cortex plasticity.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Davis et al., 2015 source

      Not checked in the free run.

    • cites de Villers-Sidani et al., 2008 source

      Not checked in the free run.

    • cites Hensch, 2005 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    A general theme in the literature is that PR binding decreases before weaning and is maintained at mid to low levels into adulthood; this general pattern emerges in mRNA experiments as well.

    “However, a general theme in the literature is that PR binding decreases before weaning and is maintained at mid to low levels into adulthood (Kato and Onouchi, 1981; Kato and Onouchi, 1983; Kato et al., 1984; Parsons et al., 1982); this general pattern emerges in mRNA experiments as well (Hagihara et al., 1992; Intlekofer and Petersen, 2011).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Kato and Onouchi, 1981

      Not checked in the free run.

    • cites Kato and Onouchi, 1983

      Not checked in the free run.

    • cites Hagihara et al., 1992 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    PR is likely only expressed in neurons in rat cortex.

    “and it is likely only expressed in neurons (Lopez and Wagner, 2009; Hagihara et al., 1992).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Lopez and Wagner, 2009

      Not checked in the free run.

    • cites Hagihara et al., 1992 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In mice, while ERalpha mRNA transcript levels decrease through life, protein expression remains stable.

    “These studies mirror a study in mice that found that while ERalpha mRNA transcript levels decrease through life, protein expression remains stable (Dietrich et al., 2015).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Dietrich et al., 2015 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Very few studies have attempted to causally relate the pubertal rise in gonadal steroids to cortical sensitive period plasticity.

    “However, as we’ve discussed, very few studies have attempted to causally relate the pubertal rise in gonadal steroids to cortical sensitive period plasticity.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    Collectively, these changes could increase inhibition in association cortex and mediate transient enhancement and developmental reduction of plasticity in a manner similar to sensory cortex.

    “Collectively, these changes could increase inhibition in association cortex and mediate transient enhancement and developmental reduction of plasticity (Dorrn et al., 2010; Froemke et al., 2007; Gandhi et al., 2008; Hensch, 2005; Southwell et al., 2010) in a manner similar to sensory cortex (Levelt and Hubener, 2012) .”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Dorrn et al., 2010 source

      Not checked in the free run.

    • cites Froemke et al., 2007 source

      Not checked in the free run.

    • cites Hensch, 2005 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Early puberty is associated with increased risk for depression, anxiety, negative self-body image, drug use, and symptoms of eating disorders, conduct disorder, and schizophrenia.

    “but early puberty is associated with increased risk for depression, anxiety, negative self-body image, drug use, and symptoms of eating disorders, conduct disorder, and schizophrenia (Burt, 2006; Copeland et al., 2010; Ge et al., 2003; Graber et al., 2004; Kaiser and Gruzelier, 1996; Kaiser and Gruzelier, 1999; Obeidallah et al., 2009; Tschann et al., 1994; Whittle et al., 2012; Zehr et al., 2007)”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Burt, 2006 source

      Not checked in the free run.

    • cites Copeland et al., 2010 source

      Not checked in the free run.

    • cites Ge et al., 2003

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    During postnatal development, the brain gradually becomes less sensitive to the organizing effects of circulating steroids, such that earlier puberty may have greater effects on neural circuits than on-time or late puberty.

    “They have proposed that during postnatal development, the brain gradually becomes less sensitive to the organizing effects of circulating steroids, such that earlier puberty may have greater effects on neural circuits than on-time or late puberty (Fig. 8).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationreasoning

    There are dramatic changes in the function of the associative neocortex at ages overlapping with pubertal milestones, and these changes are accompanied by neurobiological changes in the associative neocortex itself.

    “It is clear from our survey of the literature that 1) there are dramatic changes in the function of the associative neocortex at ages overlapping with pubertal milestones, and 2) these changes are accompanied by neurobiological changes in the associative neocortex itself.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Steroid derivatives can act as neuromodulators; progesterone and androgen metabolites, all of which can be synthesized in the brain, are known to regulate GABA and NMDA neurotransmission, myelination, and neurite growth, many of which are independent of steroid receptor binding.

    “It is also important to appreciate that steroid derivatives can act as neuromodulators; progesterone and androgen metabolites, all of which can be synthesized in the brain, are known to regulate such diverse systems as GABA and NMDA neurotransmission, myelination, and neurite growth (Compagnone and Mellon, 2000), many of which are independent of steroid receptor binding.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Compagnone and Mellon, 2000 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Interpretationreasoning

    Changes in inhibitory neurotransmission of PV+ cells can potentially be explained by genomic alterations within PV+ interneurons themselves, which may feasibly be linked to activation of ERbeta receptors on PV+ interneurons.

    “Changes in inhibitory neurotransmission of PV+ cells can potentially be explained by genomic alterations within PV+ interneurons themselves, which may feasibly be linked to activation of ERbeta receptors on PV+ interneurons.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisenone given

    Many neural systems shift their developmental trajectories around the time of puberty onset, but only a handful of studies have sought to causally relate the rise in pubertal steroids with these changes to development.

    “Many neural systems shift their developmental trajectories around the time of puberty onset, but only a handful of studies have sought to causally relate the rise in pubertal steroids with these changes to development.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisenone given

    The age of puberty onset is advancing in developed nations, and there are possible connections between earlier puberty, decreased plasticity, and psychopathology.

    “This question is particularly urgent given clear evidence that the age of puberty onset is advancing in developed nations, and the possible connections between earlier puberty, decreased plasticity, and psychopathology.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationcitation

    The rise in either androgens or estrogens at puberty in both sexes may activate frontal cortex ERbeta, which may act as a transcription factor to alter gene expression that may then regulate the physiological properties of PV+ interneurons and change network inhibition.

    “Thus, the rise in either androgens or estrogens at puberty in both sexes may activate frontal cortex ERbeta where it may act as a transcription factor (Heldring et al., 2007) to alter gene expression that may then regulate the physiological properties of PV+ interneurons and change network inhibition.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Heldring et al., 2007 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Estrogen receptors in frontal cortex are specifically localized to PV+ interneurons: ERbeta, the predominant nuclear estrogen receptor expressed in cortex during puberty and adulthood, is expressed almost exclusively in PV+ interneurons.

    “Estrogen receptors in frontal cortex are specifically localized to PV+ interneurons: ERbeta, the predominant nuclear estrogen receptor expressed in cortex during puberty and adulthood (Kritzer, 2002; Pérez et al., 2003; Shughrue et al., 1998), is expressed almost exclusively in PV+ interneurons.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Kritzer, 2002 source

      Not checked in the free run.

    • cites Pérez et al., 2003 source

      Not checked in the free run.

    • cites Shughrue et al., 1998 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In mice, puberty may overlap with the decline in ocular dominance plasticity, but this is not true for many other species, including ferrets, monkeys, and humans.

    “In mice, puberty may overlap with the decline in ocular dominance plasticity, but this is not true for many other species, including ferrets (Issa et al., 1999) monkeys (LeVay et al., 1980), and humans (Sengpiel, 2014).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Issa et al., 1999 source

      Not checked in the free run.

    • cites LeVay et al., 1980 source

      Not checked in the free run.

    • cites Sengpiel, 2014 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Premisenone given

    Some studies link these processes and changes to pubertal steroids, while others do not find relationships.

    “Some studies link these processes and changes to pubertal steroids, while others do not find relationships.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    Based on reports of steroid receptor expression, PV+ interneurons are very likely to be affected by the pubertal rise in circulating steroids, which could affect pubertal changes to cortical function.

    “In all, this model has yet to be tested, but based on reports of steroid receptor expression we can surmise that PV+ interneurons are very likely to be affected by the pubertal rise in circulating steroids, which could affect pubertal changes to cortical function.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    PV+ interneuron axons branch extensively and provide dense inhibition to nearby pyramidal neurons in cortical circuits.

    “PV+ interneuron axons branch extensively (Karube, 2004) and provide dense inhibition to nearby pyramidal neurons in cortical circuits (Packer and Yuste, 2011).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Karube, 2004 source

      Not checked in the free run.

    • cites Packer and Yuste, 2011

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Activation of D2 receptors enhances excitability in PV+ interneurons, but only after puberty.

    “In these same cells, activation of D2 receptors enhances excitability, but only after puberty (Tseng and O’donnell, 2007).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Tseng and O’donnell, 2007

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The age and timing of sensitive period plasticity varies substantially throughout the cortex, and while mechanisms underlying these sensitive periods are similar, their triggers, and thus timing, vary substantially.

    “This suggests that the age and timing of sensitive period plasticity varies substantially throughout the cortex, and while mechanisms underlying these sensitive periods are similar, their triggers, and thus timing, vary substantially.”
    Quote in the paperSubstantial claim
140 of 140
  • The paper relies on this without support.

    Relatively little is known about sensitive period biology in associative neocortex.

    “relatively little is known about sensitive period biology in associative neocortex”
  • The paper relies on this without support.

    There is little evidence, either positive or negative, to causally link puberty onset with loss of plasticity.

    “However, there is little evidence, either positive or negative, to causally link puberty onset with loss of plasticity.”
  • The paper relies on this without support.

    The mechanism that determines the age at puberty onset is unknown.

    “The mechanism that determines the age at puberty onset is unknown”
  • The paper relies on this without support.

    It is unknown what is causing the trend of advancing puberty.

    “It is unknown what is causing this trend of advancing puberty”
  • The paper relies on this without support.

    It is not well understood if the associative cortices have sensitive periods for plasticity of function equivalent to those found in sensory regions.

    “it is not well understood if the associative cortices have sensitive periods for plasticity of function equivalent to those found in sensory regions”
  • The paper relies on this without support.

    It is unclear if age 9 (grade 3) is a cutoff for biological reasons or if there are also important curricular changes at this time.

    “It is unclear if age 9 (grade 3) is a cutoff for biological reasons or if there are also important curricular changes at this time”
  • The paper relies on this without support.

    No study of which the authors are aware has measured the effects of teaching or interventions before and after puberty to establish if puberty onset regulates sensitivity to teaching or intervention.

    “No study of which we are aware has measured the effects of teaching or interventions before and after puberty to establish if puberty onset regulates sensitivity to teaching or intervention.”
  • The paper relies on this without support.

    The causal role of puberty onset as the trigger closing the juvenile period and opening the adolescent period is unknown.

    “The causal role of puberty onset as the trigger closing the juvenile period and opening the adolescent period is unknown.”
  • The paper relies on this without support.

    Language, reading, mathematics, autobiographical memory, and executive function are regulated, at least in part, by the plasticity of associative cortex.

    “Language, reading, mathematics, autobiographical memory, and executive function are presumably regulated, at least in part, by the plasticity of associative cortex.”
  • The paper relies on this without support.

    Studies have not directly addressed the relationship between the onset of puberty and behavioral flexibility in humans.

    “To our knowledge, studies have not directly addressed the relationship between the onset of puberty and behavioral flexibility in humans.”
  • The paper relies on this without support.

    There is no published evidence to date that examines the impact of pubertal status or gonadal steroids on in vivo spine dynamics.

    “To our knowledge, there is no published evidence to date that examine the impact of pubertal status or gonadal steroids on in vivo spine dynamics.”
  • The paper relies on this without support.

    The peripubertal period is a time of exploration outside the home/nest in both humans and rodents, during which animals learn crucial information about the rewards available in their environment.

    “The peripubertal period is a time of exploration outside the home/nest in both humans and rodents, during which animals learn crucial information about the rewards (e.g. food, social contact, drugs) available in their environment.”
12 of 12

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Collectively, neuroimaging studies demonstrate consistent evidence of engagement in subgenual ACC, vlPFC, posterior midline regions, and ventral striatum during social exclusion; paradigms looking at anticipation/receipt of social evaluative feedback additionally elicit responses in amygdala and medial orbitofrontal cortex.

    “Collectively, these studies demonstrate consistent evidence of engagement in subgenual ACC (sgACC), vlPFC, posterior midline regions, and ventral striatum (for a meta-analysis, see (124)); the paradigms that look at anticipation/receipt of social evaluative feedback additionally elicit responses in amygdala and medial orbitofrontal cortex.(39,122,123,125)”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Same reference is dated 1997 and 2006

    Minor

    These entries list the same authors, title, journal volume, pages, and identifier, but give different publication years.

1 of 1

The citation lists haven’t been fetched yet

References 393 · Cited by 175

Research works printed but not linked: 3

  1. Graber, 2006, Is psychopathology associated with the timing of pubertal, Development?, 36, 1768
  2. Schulz-Wilson, 2002, Gonadal steroid hormones during puberty influence the social, submissive, and aggressive behaviors of adult male Syrian hamsters, Horm. Behav., 41, 477
  3. Wanzek, J., Vaughn, S., 2013. Research-Based-Implications from extensive early reading interventions. pp. 1–21.

Authors
Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L.
Affiliations
  • University of California, Berkeley (US)
  • University of California, San Francisco (US)
Corresponding author
Wilbrecht, Linda
Venue
Brain Research
Publisher
Elsevier BV
Published
2017-01
Volume
1654
Issue
Pt B
Pages
123-144
ISSN
0006-8993 (ISSN-L)
OpenAlex
W2510195464
Cited by
175
References
393
Citations by year
2026: 18 · 2025: 15 · 2024: 14 · 2023: 21 · 2022: 23 · 2021: 19 · 2020: 22 · 2019: 14 · 2018: 17 · 2017: 11 · 2016: 1
FWCI
2.06
Type
journal article
Language
en
Open access
Locations
  • Brain Research (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • NIH grants (R01MH087542 and R01DA029150 (LW)
  • Center on the Developing Adolescent at UC Berkeley
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
puberty, sensitive period, experience-dependent plasticity, adolescent brain development, gonadal hormones, pubertal hormones, precocious puberty, cortical development
MeSH terms
Animals, Humans, Neuronal Plasticity, Puberty, Sexual Maturation, Neocortex

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

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