The relationship between pubertal hormones and brain plasticity: Implications for cognitive training in adolescence

Corinna Laube, Wouter van den Bos, Yana Fandakova, Corinna Laube, Wouter van den Bos, Yana Fandakova

Abstract

Adolescence may mark a sensitive period for the development of higher-order cognition through enhanced plasticity of cortical circuits. At the same time, animal research indicates that pubertal hormones may represent one key mechanism for closing sensitive periods in the associative neocortex, thereby resulting in decreased plasticity of cortical circuits in adolescence. In the present review, we set out to solve some of the existing ambiguity and examine how hormonal changes associated with pubertal onset may modulate plasticity in higher-order cognition during adolescence. We build on existing age-comparative cognitive training studies to explore how the potential for change in neural resources and behavioral repertoire differs across age groups. We review animal and human brain imaging studies, which demonstrate a link between brain development, neurochemical mechanisms of plasticity, and pubertal hormones. Overall, the existent literature indicates that pubertal hormones play a pivotal role in regulating the mechanisms of experience-dependent plasticity during adolescence. However, the extent to which hormonal changes associated with pubertal onset increase or decrease brain plasticity may depend on the specific cognitive domain, the sex, and associated brain networks. We discuss implications for future research and suggest that systematical longitudinal assessments of pubertal change together with cognitive training interventions may be a fruitful way toward a better understanding of adolescent plasticity. As the age of pubertal onset is decreasing across developed societies, this may also have important educational and clinical implications, especially with respect to the effects that earlier puberty has on learning.

Keywords: Episodic memory; Executive function; Hormones; MRI; Puberty onset; Working memory.

Conflict of interest statement

Declaration of Competing Interest The authors declare no conflict of interest.

Copyright © 2020 The Author(s). Published by Elsevier Ltd.. All rights reserved.

Figures

Fig. 1
Fig. 1
A. Hypothesized effects of pubertal onset (increase in gonadal hormone release) on adolescent plasticity, illustrated by two distinct lines. The solid line represents Hypothesis 1, stating that plasticity for higher cognitive functions increases after pubertal onset. The dashed line represents Hypothesis 2, stating that plasticity for higher cognitive functions decreases after pubertal onset. The box lists potential mechanisms (i.e., neurotransmitters and cell types) that are thought to be involved in the opening or closing of sensitive periods. B. Expected age differences in benefits from cognitive training under each hypothesis, separately for pre-pubertal children (triangle and purple), post-pubertal adolescents (square and green), and adults (circle and blue). GABA: γ- aminobutyric acid; BDNF: Brain Derived Neurotrophic Factor.

References

    1. Adkins-Regan E. Do hormonal control systems produce evolutionary inertia? Philos. Trans. R. Soc. B. 2007;363(1497)
    1. Aksglaede L., Olsen L.W., Sørensen T.I.A., Juul A. Forty years trends in timing of pubertal growth spurt in 157,000 Danish school children. PLoS One. 2008;3(7)
    1. Alarcón G., Cservenka A., Fair D.A., Nagel B.J. Sex differences in the neural substrates of spatial working memory during adolescence are not mediated by endogenous testosterone. Brain Res. 2014;1593:40–54.
    1. Arango-González B., Cellerino A., Kohler K. Exogenous Brain-Derived Neurotrophic Factor (BDNF) reverts phenotypic changes in the retinas of transgenic mice lacking the bdnf gene. Invest. Ophthalmol. Vis. Sci. 2009;50(3):1416–1422.
    1. Asato M.R., Terwilliger R., Woo J., Luna B. White matter development in adolescence: a DTI study. Cereb. Cortex. 2010;20(9):2122–2131.
    1. Bedny M., Paus T., Doesburg S.M., Giedd J., Rowshanak H., Kolb B., Purdon P.L., Rakic P., Sisk C.L. Understanding effects of experience on neurocognitive development through the lens of early adolescence. In: Benasich A.A., Ribary U., editors. Manifestations and Mechanisms of Dynamic Brain Coordination Over Development (Strüngmann Forum Reports, Vol. 25) MIT Press; Cambridge, MA: 2018. pp. 179–183.
    1. Best J.R., Miller P.H. A developmental perspective on executive function. Child Dev. 2010;81(6):1641–1660.
    1. Biro F.M., Pinney S.M., Huang B., Baker E.R., Chandler D.W., Dorn L.D. Hormone changes in peripubertal girls. J. Clin. Endocrinol. Metab. 2014;99(10):3829–3835.
    1. Blakemore S.-J., Mills K.L. Is adolescence a sensitive period for sociocultural processing? Annu. Rev. Psychol. 2014;65:187–207.
    1. Braams B.R., van Duijvenvoorde A.C.K., Peper J.S., Crone E.A. Longitudinal changes in adolescent risk-taking: a comprehensive study of neural responses to rewards, pubertal development, and risk-taking behavior. J. Neurosci. 2015;35(18):7226–7238.
    1. Bramen J.E., Hranilovich J.A., Dahl R.E., Chen J., Rosso C., Forbes E.E. Sex matters during adolescence: testosterone-related cortical thickness maturation differs between boys and girls. PLoS One. 2012;7(3)
    1. Brass M., von Cramon D.Y. Decomposing components of task preparation with functional magnetic resonance imaging. J. Cogn. Neurosci. 2004;16(4):609–620.
    1. Brehmer Y., Li S.C., Müller V., Von Oertzen T., Lindenberger U. Memory plasticity across the life span: uncovering children’s latent potential. Dev. Psychol. 2007;43(2):465–478.
    1. Brehmer Y., Li S.C., Straube B., Stoll G., von Oertzen T., Müller V., Lindenberger U. Comparing Memory Skill Maintenance Across the Life Span: Preservation in Adults, Increase in Children. Psychology & Aging. 2008;23(2):227–238.
    1. Brehmer Y., Shing Y.L., Heekeren H.R., Lindenberger U., Bäckman L. Training-induced changes in subsequent-memory effects: No major differences among children, younger adults, and older adults. NeuroImage. 2016;131:214–225.
    1. Brouwer R.M., Koenis M.M.G., Schnack H.G., van Baal, van Soelen, Boomsma D.I., Hulshoff Pol H.E. Longitudinal Development of Hormone Levels and Grey Matter. Density in 9 and 12-Year-Old Twins. Behavior Genetics. 2015;45(3):313–323.
    1. Brydges C.R., Fox A.M., Reid C.L., Anderson M. The differentiation of executive functions in middle and late childhood: a longitudinal latent-variable analysis. Intelligence. 2014;47:34–43.
    1. Bunge S.A., Dudukovic N.M., Thomason M.E., Chandan J.V., Gabrieli J.D.E. Immature frontal lobe contributions to cognitive control in children: evidence from fMRI. Neuron. 2002;33:301–311.
    1. Buttelmann F., Karbach J. Development and plasticity of cognitive flexibility in early and middle childhood. Front. Psychol. 2017;8:1040.
    1. Caras M.L., Sanes D.H. Neural variability limits adolescent skill learning. J. Neurosci. 2019;39(15):2878–2902.
    1. Cardoos S.L., Ballonoff A., Johnson M., Bos W., Van Den Hinshaw S.P., Dahl R.E. Social status strategy in early adolescent girls: testosterone and value-based decision making. Psychoneuroendocrinology. 2017;81:14–21.
    1. Cepeda N.J., Kramer A.F., Gonzalez de Sather J.C. Changes in executive control across the life span: examination of task-switching performance. Dev. Psychol. 2001;37(5):715–730.
    1. Chaku N., Hoyt L.T. Developmental trajectories of executive functioning and puberty in boys and girls. J. Youth Adolesc. 2019;48(7):1365–1378.
    1. Church J.A., Bunge S.A., Petersen S.E., Schlaggar B.L. Preparatory engagement of cognitive control networks increases late in childhood. Cereb. Cortex. 2017;27(3):2139–2153.
    1. Cooke B.M., Woolley C.S. Effects of prepubertal gonadectomy on a male-typical behavior and excitatory synaptic transmission in the amygdala. Dev. Neurobiol. 2009;69(2–3):141–152.
    1. Crone E.A., Dahl R.E. Understanding adolescence as a period of social-affective engagement and goal flexibility. Nat. Rev. Neurosci. 2012;13(9):636–650.
    1. Crone E.A., Ridderinkhof K.R., Worm M., Somsen R.J.M., Van Der Molen M.W. Switching between spatial stimulus-response mappings: a developmental study of cognitive flexibility. Dev. Sci. 2004;7(4):443–455.
    1. Crone E.A., Donohue S.E., Honomichl R., Wendelken C., Bunge S.A. Brain regions mediating flexible rule use during development. J. Neurosci. 2006;26(43):11239–11247.
    1. Dahl R.E., Allen N.B., Wilbrecht L., Suleiman A.B. Importance of investing in adolescence from a developmental science perspective. Nature. 2018;554(7693):441–450.
    1. Dai J., Scherf K.S. Puberty and functional brain development in humans: convergence in findings? Dev. Cogn. Neurosci. 2019;39(August):100690.
    1. Darki F., Klingberg T. The role of fronto-parietal and fronto-striatal networks in the development of working memory: a longitudinal study. Cereb. Cortex. 2015;25(6):1587–1595.
    1. Dews P.B., Wiesel T.N. Consequences of monocular deprivation on visual behavior in kittens. J. Physiol. 1970;206(2):437–455.
    1. Donato F., Rompani S.B., Caroni P. Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature. 2013;504(7479):272–276.
    1. Dorn L.D., Dahl R.E., Woodward H.R., Biro F. Defining the boundaries of early adolescence: a user’s guide to assessing pubertal status and pubertal timing in re- search with adolescents. Appl. Dev. Sci. 2006;10:30–56.
    1. Dorrn A.L., Yuan K., Barker A.J., Schreiner C.E., Froemke R.C. Developmental sensory experience balances cortical excitation and inhibition. Nature. 2010;465(7300):932–936.
    1. Dumontheil I. Development of abstract thinking during childhood and adolescence: the role of rostrolateral prefrontal cortex. Dev. Cogn. Neurosci. 2014;10:57–76.
    1. Eisenegger C., Naef M., Snozzi R., Heinrichs M., Fehr E. Prejudice and truth about the effect of testosterone on human bargaining behaviour. Nature. 2010;463(7279):356–359.
    1. Fagiolini M., Hensch T.K. Inhibitory threshold for critical-period activation in primary visual cortex. Nature. 2000;404(6774):183–186.
    1. Fandakova Y., Bunge S.A., Wendelken C., Desautels P., Hunter L., Lee J.K., Ghetti S. The importance of knowing when you don’t remember: Neural signaling of retrieval failure predicts memory improvement over time. Cerebral Cortex. 2018;28(1):90–102.
    1. Fandakova Y., Selmeczy D., Leckey S., Grimm K.J., Wendelken C., Bunge S.A., Ghetti S. Changes in ventromedial prefrontal and insular cortex support the development of metamemory from childhood into adolescence. Proc. Natl. Acad. Sci. U. S. A. 2017;114(29):7582–7587.
    1. Finn A.S., Sheridan M.A., Hudson Kam C.L., Hinshaw S., D’Esposito M. Longitudinal evidence for functional specialization of the neural circuit supporting working memory in the human brain. J. Neurosci. 2010;30(33):11062–11067.
    1. Fuhrmann D., Knoll L.J., Blakemore S.J. Adolescence as a sensitive period of brain development. Trends Cogn. Sci. 2015;19(10):558–566.
    1. Galván A. Neural plasticity of development and learning. Hum. Brain Mapp. 2010;31(6):879–890.
    1. Ghetti S., Bunge S.A. Neural changes underlying the development of episodic memory during middle childhood. Dev. Cogn. Neurosci. 2012;2(4):381–395.
    1. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999;2(10):861–863.
    1. Glorioso C., Sabatini M., Unger T., Hashimoto T., Monteggia L.M., Lewis D.A., Mirnics K. Specificity and timing of neocortical transcriptome changes in response to BDNF gene ablation during embryogenesis or adulthood. Mol. Psychiatry. 2006;11(7):633–648.
    1. Goddings A.L., Mills K.L., Clasen L.S., Giedd J.N., Viner R.M., Blakemore S.J. The influence of puberty on subcortical brain development. NeuroImage. 2014;88:242–251.
    1. Harley C.W., Malsbury C.W., Squires A., Brown R.A.M. Testosterone decrease CA1 plasticity in vivo in gonadectomized male rats. Hippocampus. 2000;10(6):693–697.
    1. Hebbard P.C., King R.R., Malsbury C.W., Harley C.W. Two organizational effects of pubertal testosterone in male rats: transient social memory and a shift away from long-term potentiation following a tetanus in hippocampal CA1. Exp. Neurol. 2003;182(2):470–475.
    1. Hensch T.K. Critical period regulation. Annu. Rev. Neurosci. 2004;27(1):549–579.
    1. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 2005;6(11):877–888.
    1. Herting M.M., Sowell E.R. Puberty and structural brain development in humans. Front. Neuroendocrinol. 2017;44:122–137.
    1. Herting M.M., Gautam P., Spielberg J.M., Kan E., Dahl R.E., Sowell E.R. The role of testosterone and estradiol in brain volume changes across adolescence: a longitudinal structural MRI study. Hum. Brain Mapp. 2014;35(11):5633–5645.
    1. Hill R.A., Wu Y.W.C., Kwek P., Van den Buuse M. Modulatory effects of sex steroid hormones on brain-derived neurotrophic factor-tyrosine kinase B expression during adolescent development in C57Bl/6 mice. J. Neuroendocrinol. 2012;24(5):774–788.
    1. Hoops D., Flores C. Making dopamine connections in adolescence. Trends Neurosci. 2017;40(12):709–719.
    1. Hubel D.H., Wiesel T.N. Receptive Fields of Cells in Striate Cortex of Very Young, Visually Inexperienced Kittens. J. Neurophysiol. 1963;26:994–1002.
    1. Huizinga M., Dolan C.V., van der Molen M.W. Age-related change in executive function: developmental trends and a latent variable analysis. Neuropsychologia. 2006;44(11):2017–2036.
    1. Huizinga M., van der Molen M.W. Age-Group Differences in Set-Switching and Set-Maintenance on the Wisconsin Card Sorting Task. Dev. Neuropsychol. 2007;31(2):193–215.
    1. Jolles D.D., Crone E.A. Training the developing brain: a neurocognitive perspective. Front. Hum. Neurosci. 2012;6:76.
    1. Jolles D.D., Van Buchem M.A., Rombouts S.A.R.B., Crone E.A. Practice effects in the developing brain: a pilot study. Dev. Cogn. Neurosci. 2012:S180–S191.
    1. Jolles D.D., Van Buchem M.A., Crone E.A., Rombouts S.A.R.B. Functional brain connectivity at rest changes after working memory training. Hum. Brain Mapp. 2013;34(2):396–406.
    1. Juraska J.M., Willing J. Pubertal onset as a critical transition for neural development and cognition. Brain Res. 2017;1654:87–94.
    1. Kadosh K.C., Linden D.E.J., Lau J.Y.F. Plasticity during childhood and adolescence: innovative approaches to investigating neurocognitive development. Dev. Sci. 2013;16(4):574–583.
    1. Karbach J., Kray J. How useful is executive control training? Age differences in near and far transfer of task-switching training. Dev. Sci. 2009;12(6):978–990.
    1. Karbach J., Unger K. Executive control training from middle childhood to adolescence. Front. Psychol. 2014;5:390.
    1. Karbach J., Könen T., Spengler M. Who benefits the most? Individual differences in the transfer of executive control training across the lifespan. J. Cogn. Enhanc. 2017;1(4):394–405.
    1. Keresztes A., Bender A.R., Bodammer N.C., Lindenberger U., Shing Y.L., Werkle-Bergner M. Hippocampal maturity promotes memory distinctiveness in childhood and adolescence. Proc. Natl. Acad. Sci. U. S. A. 2017;114(34):9212–9217.
    1. Kievit R.A., Brandmaier A.M., Ziegler G., van Harmelen A.L., de Mooij S.M.M., Moutoussis M. Developmental cognitive neuroscience using latent change score models: a tutorial and applications. Dev. Cogn. Neurosci. 2018;33:99–117.
    1. Knoll L.J., Fuhrmann D., Sakhardande A.L., Stamp F., Speekenbrink M., Blakemore S.-J. A window of opportunity for cognitive training in adolescence. Psychol. Sci. 2016;27(12):1620–1631.
    1. Kolb B., Gibb R. Brain plasticity and behaviour in the developing brain. J. Can. Acad. Child Adolesc. Psychiatry. 2011;20(4):265–276.
    1. Koolschijn P.C.M.P., Peper J.S., Crone E.A. The influence of sex steroids on structural brain maturation in adolescence. PLoS One. 2014;9(1)
    1. Kuhn C., Johnson M., Thomae A., Luo B., Simon S.A., Zhou G., Walker Q.D. The emergence of gonadal hormone influences on dopaminergic function during puberty. Horm. Behav. 2010;58(1):122–137.
    1. Kühn S., Lindenberger U. Research on human plasticity in adulthood: a lifespan agenda. In: Schaie K.W., Willis S.L., editors. Handbook of the Psychology of Aging. 8th ed. Academic Press; Amsterdam: 2016. pp. 105–123.
    1. Larsen B., Luna B. Adolescence as a neurobiological critical period for the development of higher-order cognition. Neurosci. Biobehav. Rev. 2018;94(March):179–195.
    1. Laube C., Lorenz R., van den Bos W. Pubertal testosterone correlates with adolescent impatience and dorsal striatal activity. Dev. Cogn. Neurosci. 2020;42:100749.
    1. Laube C., van den Bos W. Hormones and affect in adolescent decision making. In: Kim S., Reeve J., Bong M., editors. Recent Developments in Neuroscience Research on Human Motivation (Advances in Motivation and Achievement, Volume 19) Emerald Group Publishing Limited; UK: 2016. pp. 259–281.
    1. Lebel C., Beaulieu C. Longitudinal development of human brain wiring continues from childhood into adulthood. J. Neurosci. 2011;31(30):10937–10947.
    1. LeDoux J. The emotional brain, fear, and the amygdala. Cell. Mol. Neurobiol. 2003;23(4–5):727–738.
    1. Lee P.A. Normal ages of pubertal events among American males and females. J. Adolesc. Health Care. 1980;1(1):26–29.
    1. Lee J.K., Fandakova Y., Johnson E.G., Cohen N.J., Bunge S.A., Ghetti S. Changes in anterior and posterior hippocampus differentially predict item-space, item-time, and item-item memory improvement. Developmental Cognitive Neuroscience. 2019;41:100741.
    1. Leranth C., Petnehazy O., MacLusky N.J. Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. J. Neurosci. 2003;23(5):1588–1592.
    1. Liu Y., Rutlin M., Huang S., Barrick C.A., Wang F., Jones K.R. Sexually dimorphic BDNF signaling directs sensory innervation of the mammary gland. Science. 2012;338(6112):1357–1360.
    1. Lövdén M., Bäckman L., Lindenberger U., Schaefer S., Schmiedek F. A theoretical framework for the study of adult cognitive plasticity. Psychol. Bull. 2010;136(4):659–676.
    1. Lövdén M., Wenger E., Mårtensson J., Lindenberger U., Bäckman L. Structural brain plasticity in adult learning and development. Neuroscience and Biobehavioral Reviews. 2013;37(9):2296–2310.
    1. Luna B., Garver K.E., Urban T.A., Lazar N.A., Sweeney J.A. Maturation of cognitive processes from late childhood to adulthood. Child Dev. 2004;75(5):1357–1372.
    1. Luna B., Marek S., Larsen B., Tervo-Clemmens B., Chahal R. An integrative model of the maturation of cognitive control. Annu. Rev. Neurosci. 2015;38(1):151–170.
    1. Lundborg G. Brain Plasticity and hand function. J. Hand Surg. 1998;25(3):242–252.
    1. MacLusky N.J., Luine V.N., Hajszan T., Leranth C. The 17α and 17β isomers of estradiol both induce rapid spine synapse formation in the Ca1 hippocampal subfield of ovariectomized female rats. Endocrinology. 2005;146(1):287–293.
    1. Marceau K., Dorn L.D., Susman E.J. Stress and puberty-related hormone reactivity, negative emotionality, and parent-adolescent relationships. Psychoneuroendocrinology. 2012;37:1286–1298.
    1. Marques J.P., Kober T., Krueger G., van der Zwaag W., Van de Moortele P.F., Gruetter R. MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field. NeuroImage. 2010;49(2):1271–1281.
    1. Marshall W.A., Tanner J.M. Variations in the pattern of pubertal changes in boys. Arch. Dis. Child. 1970;45(13):13–23.
    1. Mayberry R.I., Lock E. Age constraints on first versus second language acquisition: evidence for linguistic plasticity and epigenesis. Brain Lang. 2003;87(3):369–384.
    1. McClure S.M., Laibson D.I., Loewenstein G.F., Cohen J.D. Separate neural systems value immediate and delayed monetary rewards. Science. 2004;306(5695):503–507.
    1. McLaughlin K.A., King K. Developmental trajectories of anxiety and depression in early adolescence. J. Abnorm. Child Psychol. 2014;43(2):311–323.
    1. Mendle J., Ferrero J. Detrimental psychological outcomes associated with pubertal timing in adolescent boys. Dev. Rev. 2012;32(1):49–66.
    1. Mendle J., Turkheimer E., Emery R.E. Detrimental psychological outcomes associated with early pubertal timing in adolescent girls. Dev. Rev. 2007;27(2):151–171.
    1. Mendle J., Harden K.P., Brooks-Gunn J., Graber J.A. Development’s tortoise and hare: pubertal timing, pubertal tempo, and depressive symptoms in boys and girls. Dev. Psychol. 2010;46(5):1341–1353.
    1. Mensah F.K., Bayer J.K., Wake M., Carlin J.B., Allen N.B., Patton G.C. Early puberty and childhood social and behavioral adjustment. J. Adolesc. Health. 2013;53(1):118–124.
    1. Meyer G., Ferres-Torres R., Mas M. The effects of puberty and castration on hippocampal dendritic spines of mice. A Golgi study. Brain Res. 1978;155(1):108–112.
    1. Miyake A., Friedman N.P. The nature and organization of individual differences in executive functions: four general conclusions. Curr. Dir. Psychol. Sci. 2012;21(1):8–14.
    1. Mogg K., Bradley B.P. Anxiety and threat-related attention: cognitive-motivational framework and treatment. Trends Cogn. Sci. 2018;22(3):225–240.
    1. Morales B., Choi S.-Y., Kirkwood A. Dark rearing alters the development of GABAergic transmission in visual cortex. J. Neurosci. 2002;22(18):8084–8090.
    1. Murty V.P., Calabro F., Luna B. The role of experience in adolescent cognitive development: integration of executive, memory, and mesolimbic systems. Neurosci. Biobehav. Rev. 2016;70:46–58.
    1. Nakazawa K., McHugh T.J., Wilson M.A., Tonegawa S. NMDA receptors, place cells and hippocampal spatial memory. Nat. Rev. Neurosci. 2004;5:361–372.
    1. Naneix F., Marchand A.R., Di Scala G., Pape J.R., Coutureau E. Parallel maturation of goal-directed behavior and dopaminergic systems during adolescence. J. Neurosci. 2012;32(46):16223–16232.
    1. Nguyen T.-V., McCracken J., Ducharme S., Botteron K.N., Mahabir M., Johnson W. Testosterone-related cortical maturation across childhood and adolescence. Cereb. Cortex. 2013;23(6):1424–1432.
    1. Nguyen T.-V., Hudziak J.J., Albaugh M.D., Botteron K.N., Hudziak J.J., Ducharme S. A testosterone-related structural brain phenotype predicts aggressive behavior from childhood to adulthood. Psychoneuroendocrinology. 2015;63:109–118.
    1. Nguyen T.-V., Lew J., Albaugh M.D., Botteron K.N., Hudziak J.J., Fonov V.S. Sex-specific associations of testosterone with prefrontal-hippocampal development and executive function. Psychoneuroendocrinology. 2017;76:206–217.
    1. Patton G.C., Viner R. Pubertal transitions in health. Lancet. 2007;369(9567):1130–1139.
    1. Peper J.S., Dahl R.E. The teenage brain: Surging hormones–brain-behavior interactions during puberty. Curr. Dir. Psychol. Sci. 2013;22(2):134–139.
    1. Peters S., Braams B.R., Raijmakers M.E.J., Koolschijn P.C.M.P., Crone E.A. The neural coding of feedback learning across child and adolescent development. J. Cogn. Neurosci. 2013;26(6):1–10.
    1. Piekarski D.J., Boivin J.R., Wilbrecht L. Ovarian hormones organize the maturation of inhibitory neurotransmission in the frontal cortex at puberty onset in female mice. Curr. Biol. 2017;27(12):1735–1745. e3.
    1. Piekarski D.J., Johnson C.M., Boivin J.R., Thomas A.W., Lin W.C., Delevich K. Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? Brain Res. 2017;1654:123–144.
    1. Prayer D., Roberts T., Barkovich A.J., Prayer L., Kucharczyk J., Moseley M., Arieff A. Diffusion-weighted MRI of myelination in the rat brain following treatment with gonadal hormones. Neuroradiology. 1997;39(5):320–325.
    1. Purves-Tyson T.D., Allen K., Fung S., Rothmond D., Noble P.L., Handelsman D.J., Shannon Weickert C. Adolescent testosterone influences BDNF and TrkB mRNA and neurotrophin-interneuron marker relationships in mammalian frontal cortex. Schizophr. Res. 2015;168(3):661–670.
    1. Reardon L., Leen-Feldner E., Hayward C. A critical review of the empirical literature on the relation between anxiety and puberty. Clin. Psychol. Rev. 2009;29(1):1–23.
    1. Reimers S., Maylor E.A. Task switching across the life span: effects of age on general and specific switch costs. Dev. Psychol. 2005;41(4):661–671.
    1. Reynolds L.M., Pokinko M., Torres-Berrío A., Cuesta S., Lambert L.C., Del Cid Pellitero E. DCC receptors drive prefrontal cortex maturation by determining dopamine axon targeting in adolescence. Biol. Psychiatry. 2018;83(2):181–192.
    1. Reynolds L.M., Yetnikoff L., Pokinko M., Wodzinski M., Epelbaum J.G., Lambert L.C. Early adolescence is a critical period for the maturation of inhibitory behavior. Cereb. Cortex. 2019;29(9):3676–3686.
    1. Roney J.R. Theoretical frameworks for human behavioral endocrinology. Horm. Behav. 2016;84:97–110.
    1. Rubia K., Smith A.B., Woolley J., Nosarti C., Heyman I., Taylor E., Brammer M. Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Hum. Brain Mapp. 2006;27(12):973–993.
    1. Rubin D.C., Schulkind M.D. Distribution of important and wordcued autobiographical memories. Psychol. Aging. 1997;12(3):524–535.
    1. Sander M.C., Lindenberger U., Werkle-Bergner M. Lifespan age differences in working memory: A two-component framework. Neuroscience & Biobehavioral Reviews. 2012;36:2007–2033.
    1. Sapolsky R.M. Testicular function, social rank and personality among wild baboons. Psychoneuroendocrinology. 1991;16(4):281–293.
    1. Satterthwaite T.D., Wolf D.H., Erus G., Ruparel K., Elliott M.A., Gennatas E.D. Functional maturation of the executive system during adolescence. J. Neurosci. 2013;33(41):16249–16261.
    1. Schmiedek F., Lövdén M., Lindenberger U. Hundred days of cognitive training enhance broad cognitive abilities in adulthood: findings from the COGITO study. Front. Aging Neurosci. 2010;2:27.
    1. Schneider W., Pressley M. Lawrence Erlbaum Associates; Mahwah, NJ: 1997. Memory development between two and twenty.
    1. Schultz W., Apicella P., Scarnati E., Ljungberg T. Neuronal activity in monkey ventral striatum related to the expectation of reward. J. Neurosci. 1992;12(12):4595–4610.
    1. Selemon L.D. A role for synaptic plasticity in the adolescent development of executive function. Transl. Psychiatry. 2013;3(3):e238–e239.
    1. Selmeczy D., Fandakova Y., Grimm K.J., Bunge S.A., Ghetti S. Longitudinal trajectories of hippocampal and prefrontal contributions to episodic retrieval: effects of age and puberty. Dev. Cogn. Neurosci. 2019;36:100599.
    1. Sharma A., Dorman M.F., Kral A. The influence of a sensitive period on central auditory development in children with unilateral and bilateral cochlear implants. Hear. Res. 2005;203(1–2):134–143.
    1. Shen H., Gong Q.H., Aoki C., Yuan M., Ruderman Y., Dattilo M. Reversal of neurosteroid effects at α4β2δ GABAA receptors triggers anxiety at puberty. Nat. Neurosci. 2007;10(4):469–477.
    1. Shen H., Sabaliauskas N., Sherpa A., Fenton A.A.A., Stelzer A., Aoki C., Smith S.S. A critical role for α4βδ GABAA receptors in shaping learning deficits at puberty in mice. Science. 2010;327(5972):1515–1518.
    1. Shing Y.L., Werkle-Bergner M., Li S.C., Lindenberger U. Associative and strategic components of episodic memory: a life-span dissociation. J. Exp. Psychol. Gen. 2008;137(3):495–513.
    1. Shirtcliff E.A., Dahl R.E., Pollak S.D. Pubertal development: correspondence between hormonal and physical development. Child Dev. 2009;80(2):327–337.
    1. Sluzenski J., Newcombe N.S., Kovacs S.L. Binding, relational memory, and recall of naturalistic events: a developmental perspective. J. Exp. Psychol. Learn. Mem. Cogn. 2006;32(1):89–100.
    1. Sowell E.R., Peterson B.S., Thompson P.M., Welcome S.E., Henkenius A.L., Toga A.W. Mapping cortical change across the human life span. Nat. Neurosci. 2003;6(3):309–315.
    1. Spielberg J.M., Olino T.M., Forbes E.E., Dahl R.E. Exciting fear in adolescence: Does pubertal development alter threat processing? Dev. Cogn. Neurosci. 2014;8:86–95.
    1. Spielberg J.M., Forbes E.E., Ladouceur C.D., Worthman C.M., Olino T.M., Ryan N.D., Dahl R.E. Pubertal testosterone influences threat-related amygdala – orbitofrontal cortex coupling. Soc. Cogn. Affect. Neurosci. 2015;10(3):408–415.
    1. Steinberg L. A social neuroscience perspective on adolescent risk-taking. Dev. Rev. 2008;28(1):78–106.
    1. Steinberg L. A behavioral scientist looks at the science of adolescent brain development. Brain and Cognition. 2010;72(1):160–164.
    1. Stroemer R.P., Kent T.A., Hulsebosch C.E. Enhanced neocortical neural sprouting, synaptogenesis, and behavioral recovery with D-amphetamine therapy after neocortical infarction in rats. Stroke. 1998:2381–2395.
    1. Toyoizumi T., Miyamoto H., Yazaki-Sugiyama Y., Atapour N., Hensch T.K., Miller K.D. A theory of the transition to critical period plasticity: inhibition selectively suppresses spontaneous activity. Neuron. 2013;80(1):51–63.
    1. Ullman H., Almeida R., Klingberg T. Structural maturation and brain activity predict future working memory capacity during childhood development. J. Neurosci. 2014;34(5):1592–1598.
    1. Vendetti M.S., Bunge S.A. Evolutionary and developmental changes in the lateral frontoparietal network: a little goes a long way for higher-level cognition. Neuron. 2014;84(5):906–917.
    1. Vijayakumar N., Op de Macks Z., Shirtcliff E.A., Pfeifer J.H. Puberty and the human brain: insights into adolescent development. Neurosci. Biobehav. Rev. 2018;92:417–436.
    1. Villuendas G., Sánchez-Franco F., Palacios N., Fernández M., Cacicedo L. Involvement of VIP on BDNF-induced somatostatin gene expression in cultured fetal rat cerebral cortical cells. Mol. Brain Res. 2001;94(1–2):59–66.
    1. Walvoord E.C. The timing of puberty: is it changing? Does it matter? J. Adolesc. Health. 2010;47(5):433–439.
    1. Weiskopf N., Suckling J., Williams G., Correia M., M. M, Inkster B., Tait R. Quantitative multi-parameter mapping of R1, PD*, MT, and R2* at 3T: a multi-center validation. Front. Neurosci. 2013;7:95.
    1. Wendelken C., O’Hare E.D., Whitaker K.J., Ferrer E., Bunge S.A. Increased functional selectivity over development in rostrolateral prefrontal cortex. J. Neurosci. 2011;31(47):17260–17268.
    1. Wendelken C., Ferrer E., Ghetti S., Bailey S.K., Cutting L., Bunge S.A. Frontoparietal structural connectivity in childhood predicts development of functional connectivity and reasoning ability: a large-scale longitudinal investigation. J. Neurosci. 2017;37(35):8549–8558.
    1. Werker J.F., Hensch T.K. Critical periods in speech perception: new directions. Annu. Rev. Psychol. 2015;66:173–196.
    1. Wierenga L.M., Bos M.G.N., Schreuders E., vd Kamp F., Peper J.S., Tamnes C.K., Crone E.A. Unraveling age, puberty and testosterone effects on subcortical brain development across adolescence. Psychoneuroendocrinology. 2018;91:105–114.
    1. Wiesel T.N., Hubel D.H. Extent of recovery from the effects of visual deprivation in kittens. J. Neurophysiol. 2017;28(6):1060–1072.
    1. Wise R. Dopamine, learning and motivation. Nat. Rev. Neurosci. 2004;5:483–494.
    1. Wu Y.W.C., Du X., Van den Buuse M., Hill R.A. Sex differences in the adolescent developmental trajectory of parvalbumin interneurons in the hippocampus: a role for estradiol. Psychoneuroendocrinology. 2014;45:167–178.
    1. Yates M.A., Juraska J.M. Pubertal ovarian hormone exposure reduces the number of myelinated axons in the splenium of the rat corpus callosum. Exp. Neurol. 2008;209(1):284–287.
    1. Zelazo P.D., Carlson S.M., Kesek A. The development of executive function in childhood. In: Nelson C.A., Luciana M., editors. Developmental cognitive neuroscience. MIT Press; 2008. pp. 553–574.

Source: PubMed

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