Coming of age in the frontal cortex: The role of puberty in cortical maturation

Delevich, Kristen; Klinger, Madeline; Okada, Nana J.; Wilbrecht, Linda

doi:10.1016/j.semcdb.2021.04.021

Cited by 45 publications

(33 citation statements)

References 134 publications

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“…Because gonadectomy in adult animals alters PFC DA fiber distribution (Kritzer and Kohama, 1998;Kritzer, 1998Kritzer, , 2003Adler et al, 1999;Kritzer et al, 1999), the pubertal spike in sex hormones has been long posited to drive sex differences in adult PFC DA innervation. However, contrary to the maturation of other PFC neurotransmitter systems (Drzewiecki et al, 2016(Drzewiecki et al, , 2020Piekarski et al, 2017;Delevich et al, 2020Delevich et al, , 2021, evidence regarding a role for puberty in the development of mesocortical DA circuitry remains elusive. DA innervation to the PFC has been shown to increase along a similar timescale throughout adolescence in both male and female rats, with no apparent effect of puberty onset in this trajectory (Willing et al, 2017).…”

Section: Puberty As a Driver Of Dopamine Circuitry Developmentmentioning

confidence: 99%

Mesocorticolimbic Dopamine Pathways Across Adolescence: Diversity in Development

Reynolds

Flores²

2021

Front. Neural Circuits

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Mesocorticolimbic dopamine circuity undergoes a protracted maturation during adolescent life. Stable adult levels of behavioral functioning in reward, motivational, and cognitive domains are established as these pathways are refined, however, their extended developmental window also leaves them vulnerable to perturbation by environmental factors. In this review, we highlight recent advances in understanding the mechanisms underlying dopamine pathway development in the adolescent brain, and how the environment influences these processes to establish or disrupt neurocircuit diversity. We further integrate these recent studies into the larger historical framework of anatomical and neurochemical changes occurring during adolescence in the mesocorticolimbic dopamine system. While dopamine neuron heterogeneity is increasingly appreciated at molecular, physiological, and anatomical levels, we suggest that a developmental facet may play a key role in establishing vulnerability or resilience to environmental stimuli and experience in distinct dopamine circuits, shifting the balance between healthy brain development and susceptibility to psychiatric disease.

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Section: Puberty As a Driver Of Dopamine Circuitry Developmentmentioning

confidence: 99%

Mesocorticolimbic Dopamine Pathways Across Adolescence: Diversity in Development

Reynolds

Flores²

2021

Front. Neural Circuits

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“…Puberty, the transition to reproductive maturity, is a developmental stage when the ovaries begin to secrete increasing amounts of estrogens and progestins due to a rise in activity of the hypothalamic-pituitary-ovarian (HPO) axis ( Jost et al, 1973 ; Keating et al, 2019 ; Delevich et al, 2021 ). In addition, ALLO gradually increases before and rapidly drops off with pubertal onset in rodents and humans ( Fadalti et al, 1999 ; McCartney et al, 2007 ; Shen et al, 2007 ; Smith, 2013 ).…”

Section: Pubertymentioning

confidence: 99%

“…In addition, ALLO gradually increases before and rapidly drops off with pubertal onset in rodents and humans ( Fadalti et al, 1999 ; McCartney et al, 2007 ; Shen et al, 2007 ; Smith, 2013 ). Some evidence suggests that changes in estradiol, progesterone, and ALLO during puberty may play a key role in brain and behavioral maturation by altering inhibitory tone ( Schulz et al, 2009 ; Holder and Blaustein, 2014 ; Jones and Lopez, 2014 ; Juraska and Willing, 2017 ; Delevich et al, 2021 ).…”

Section: Pubertymentioning

confidence: 99%

“…Rodent studies have shown that the underlying mechanisms that contribute to the development of greater inhibitory tone in the brain following pubertal onset are multifaceted and due in part to increases in GAD expression, as well as increases in the production of inhibitory synapses and GABA transporters ( Kilb, 2012 ; Shen et al, 2020 ). As described below, growing inhibitory tone following pubertal onset also results from alterations in PV neurons within the medial prefrontal cortex (mPFC, analog to human PFC) and hippocampus ( Sisk and Zehr, 2005 ; Smith et al, 2009 ; Buzsáki and Wang, 2012 ; Kilb, 2012 ; Juraska et al, 2013 ; Caballero and Tseng, 2016 ; Zimmermann et al, 2019 ; Delevich et al, 2021 ). Inhibitory tone in these regions is further influenced by changes in subunit expression of GABA A Rs, which affect GABA A R activity ( Smith et al, 2009 ).…”

Section: Pubertymentioning

confidence: 99%

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GABA System Modifications During Periods of Hormonal Flux Across the Female Lifespan

Gilfarb

Leuner

2022

Front. Behav. Neurosci.

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The female lifespan is marked by periods of dramatic hormonal fluctuation. Changes in the ovarian hormones estradiol and progesterone, in addition to the progesterone metabolite allopregnanolone, are among the most significant and have been shown to have widespread effects on the brain. This review summarizes current understanding of alterations that occur within the GABA system during the major hormonal transition periods of puberty, the ovarian cycle, pregnancy and the postpartum period, as well as reproductive aging. The functional impacts of altered inhibitory activity during these times are also discussed. Lastly, avenues for future research are identified, which, if pursued, can broaden understanding of the GABA system in the female brain and potentially lead to better treatments for women experiencing changes in brain function at each of these hormonal transition periods.

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“…Gonadal hormones influence circuit regulation through both organizational effects in development as well as activational effects in adulthood. The importance of gonadal hormones for mPFC development, synapse formation, and pruning has been recently reviewed (Premachandran et al, 2020;Delevich et al, 2021). In adult rodents, estrogen receptors α and β (ERα and ERβ) are present in the male rodent mPFC (Figure 1), distributed broadly across cortical layers in both pyramidal and non-pyramidal putative interneurons (Montague et al, 2008).…”

Section: Gonadal Hormone Influencesmentioning

confidence: 99%

Effects of Biological Sex and Stress Exposure on Ventromedial Prefrontal Regulation of Mood-Related Behaviors

Wallace

Myers

2021

Front. Behav. Neurosci.

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The ventral portion of the medial prefrontal cortex (vmPFC) regulates mood, sociability, and context-dependent behaviors. Consequently, altered vmPFC activity has been implicated in the biological basis of emotional disorders. Recent methodological advances have greatly enhanced the ability to investigate how specific prefrontal cell populations regulate mood-related behaviors, as well as the impact of long-term stress on vmPFC function. However, emerging preclinical data identify prominent sexual divergence in vmPFC behavioral regulation and stress responsivity. Notably, the rodent infralimbic cortex (IL), a vmPFC subregion critical for anti-depressant action, shows marked functional divergence between males and females. Accordingly, this review examines IL encoding and modulation of mood-related behaviors, including coping style, reward, and sociability, with a focus on sex-based outcomes. We also review how these processes are impacted by prolonged stress exposure. Collectively, the data suggest that chronic stress has sex-specific effects on IL excitatory/inhibitory balance that may account for sex differences in the prevalence and course of mood disorders.

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Coming of age in the frontal cortex: The role of puberty in cortical maturation

Cited by 45 publications

References 134 publications

Mesocorticolimbic Dopamine Pathways Across Adolescence: Diversity in Development

Mesocorticolimbic Dopamine Pathways Across Adolescence: Diversity in Development

GABA System Modifications During Periods of Hormonal Flux Across the Female Lifespan

Effects of Biological Sex and Stress Exposure on Ventromedial Prefrontal Regulation of Mood-Related Behaviors

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