Adolescent cortical development: A critical period of vulnerability for addiction

Cortical growth and remodeling continues from birth through youth and adolescence to stable adult levels changing slowly into senescence. There are critical periods of cortical development when specific experiences drive major synaptic rearrangements and learning that only occur during the critical period. For example, visual cortex is characterized by a critical period of plasticity involved in establishing visual acuity. Adolescence is defined by characteristic behaviors that include high levels of risk taking, exploration, novelty and sensation seeking, social interaction and play behaviors. In addition, adolescence is the final period of development of the adult during which talents, reasoning and complex adult behaviors mature. This maturation of behaviors corresponds with periods of marked changes in neurogenesis, cortical synaptic remodeling, neurotransmitter receptors and transporters, as well as major changes in hormones. Frontal cortical development is later in adolescence and likely contributes to refinement of reasoning, goal and priority setting, impulse control and evaluating long and short term rewards. Adolescent humans have high levels of binge drinking and experimentation with other drugs. This review presents findings supporting adolescence as a critical period of cortical development important for establishing life long adult characteristics that are disrupted by alcohol and drug use.

[1]  R. Depue,et al.  Conceptualizing a serotonin trait. A behavioral dimension of constraint. , 1986, Annals of the New York Academy of Sciences.

[2]  S. Takashima,et al.  Development of GABAergic neurons and their transporter in human temporal cortex. , 2001, Pediatric neurology.

[3]  Martin H. Teicher,et al.  Delayed Effects of Early Stress on Hippocampal Development , 2004, Neuropsychopharmacology.

[4]  F. Crews,et al.  Neurogenesis in adolescent brain is potently inhibited by ethanol , 2006, Neuroscience.

[5]  I. Bernstein,et al.  Patterns of affiliation among immature rhesus monkeys (Macaca mulatta) , 1987, American journal of primatology.

[6]  S. Eggan,et al.  Postnatal Development of Prefrontal Inhibitory Circuits and the Pathophysiology of Cognitive Dysfunction in Schizophrenia , 2004, Annals of the New York Academy of Sciences.

[7]  Patrick M. O'Malley,et al.  Monitoring the Future National Results on Adolescent Drug Use: Overview of Key Findings, 2004. , 2003 .

[8]  F. Tarazi,et al.  Postnatal development of dopamine D4-like receptors in rat forebrain regions: comparison with D2-like receptors. , 1998, Brain research. Developmental brain research.

[9]  L. Steinberg,et al.  Handbook of adolescent psychology , 2009 .

[10]  A. Toga,et al.  Localizing Age-Related Changes in Brain Structure between Childhood and Adolescence Using Statistical Parametric Mapping , 1999, NeuroImage.

[11]  Fulton Crews,et al.  CREB and NF-κB Transcription Factors Regulate Sensitivity to Excitotoxic and Oxidative Stress Induced Neuronal Cell Death , 2006, Cellular and Molecular Neurobiology.

[12]  L. Steinberg Pubertal maturation and parent-adolescent distance: An evolutionary perspective. , 1989 .

[13]  Eric J. Nestler,et al.  Chronic Antidepressant Treatment Increases Neurogenesis in Adult Rat Hippocampus , 2000, The Journal of Neuroscience.

[14]  Jonathan D. Cohen,et al.  A Developmental Functional MRI Study of Prefrontal Activation during Performance of a Go-No-Go Task , 1997, Journal of Cognitive Neuroscience.

[15]  F. Crews,et al.  Cognitive deficits and CNS damage after a 4-day binge ethanol exposure in rats , 2002, Pharmacology Biochemistry and Behavior.

[16]  H. Uylings,et al.  Development of the dopaminergic innervation in the prefrontal cortex of the rat , 1988, The Journal of comparative neurology.

[17]  M P Stryker,et al.  Experience-Dependent Plasticity of Binocular Responses in the Primary Visual Cortex of the Mouse , 1996, The Journal of Neuroscience.

[18]  D. Morilak,et al.  Ontogeny of 5-hydroxytryptamine2 receptor immunoreactivity in the developing rat brain , 1993, Neuroscience.

[19]  A. J. Wintink,et al.  Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats , 2005, Behavioural Brain Research.

[20]  D. Delis,et al.  Improved memory functioning and frontal lobe maturation between childhood and adolescence: A structural MRI study , 2001, Journal of the International Neuropsychological Society.

[21]  Douglas C. Noll,et al.  A pediatric functional MRI study of prefrontal activation during performance of a Go-No-Go task , 1996, NeuroImage.

[22]  D. Baumrind,et al.  A developmental perspective on adolescent risk taking in contemporary America. , 1987, New directions for child development.

[23]  Margo Wilson,et al.  Competitiveness, risk taking, and violence: the young male syndrome , 1985, Ethology and Sociobiology.

[24]  M. Domjan,et al.  Learning mechanisms in food selection , 1977 .

[25]  T. Guilarte Chapter 15 – The N-Methyl-D- Aspartate Receptor: Physiology and Neurotoxicology in the Developing Brain , 1998 .

[26]  A. Biglan,et al.  Social and behavioral factors associated with high-risk sexual behavior among adolescents , 1990, Journal of Behavioral Medicine.

[27]  J. Swann,et al.  Developmental neuroplasticity: roles in early life seizures and chronic epilepsy. , 1999, Advances in neurology.

[28]  C. van Hartesveldt,et al.  Locomotion elicited by MK801 in developing and adult rats: temporal, environmental, and gender effects. , 1999, European journal of pharmacology.

[29]  R. Duman,et al.  Neuronal plasticity and survival in mood disorders , 2000, Biological Psychiatry.

[30]  F. Crews,et al.  Neurogenesis decreases during brain maturation from adolescence to adulthood , 2007, Pharmacology Biochemistry and Behavior.

[31]  A. S. Ramoa,et al.  Early alcohol exposure impairs ocular dominance plasticity throughout the critical period. , 2005, Brain research. Developmental brain research.

[32]  F. Gage,et al.  Mammalian neural stem cells. , 2000, Science.

[33]  J. Lacaille,et al.  Late maturation of GABAB synaptic transmission in area CA1 of the rat hippocampus , 1999, Neuropharmacology.

[34]  C. Vargas,et al.  Expression of 5-HT7 receptor mRNA in rat brain during postnatal development , 1997, Neuroscience Letters.

[35]  J. Merrick,et al.  Adolescent injury risk behavior , 2004, International journal of adolescent medicine and health.

[36]  B. Jacobs,et al.  Adult brain neurogenesis and psychiatry: a novel theory of depression , 2000, Molecular Psychiatry.

[37]  T. Baram,et al.  Enhanced CREB phosphorylation in immature dentate gyrus granule cells precedes neurotrophin expression and indicates a specific role of CREB in granule cell differentiation , 2001, The European journal of neuroscience.

[38]  Gerd Kempermann,et al.  Why New Neurons? Possible Functions for Adult Hippocampal Neurogenesis , 2002, The Journal of Neuroscience.

[39]  Ronald S Duman,et al.  Cell Proliferation in Adult Hippocampus is Decreased by Inescapable Stress: Reversal by Fluoxetine Treatment , 2003, Neuropsychopharmacology.

[40]  Anat Biegon,et al.  Fetal human brain exhibits a prenatal peak in the density of serotonin 5-HT1A receptors , 1991, Neuroscience Letters.

[41]  M. Csíkszentmihályi,et al.  The ecology of adolescent activity and experience , 1977, Journal of youth and adolescence.

[42]  M. Le Moal,et al.  Mesocorticolimbic dopaminergic network: functional and regulatory roles. , 1991, Physiological reviews.

[43]  A. Kelley,et al.  Risk Taking and Novelty Seeking in Adolescence: Introduction to Part I , 2004, Annals of the New York Academy of Sciences.

[44]  H. Cameron,et al.  Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus , 1994, Neuroscience.

[45]  G. Awatramani,et al.  Adolescent development alters stressor-induced Fos immunoreactivity in rat brain , 1998, Neuroscience.

[46]  J. Palacios,et al.  Early localization of mRNA coding for 5-HT1A receptors in human brain during development. , 1998, Brain research. Molecular brain research.

[47]  T. Duka,et al.  Acute alcohol effects on cognitive function in social drinkers: their relationship to drinking habits , 2002, Psychopharmacology.

[48]  S. Blakemore,et al.  Development of the adolescent brain: implications for executive function and social cognition. , 2006 .

[49]  U. Rudolph,et al.  GABA(A)-receptor subtypes: a new pharmacology. , 2001, Current opinion in pharmacology.

[50]  C. van Hartesveldt,et al.  The locomotor effects of MK801 in the nucleus accumbens of developing and adult rats. , 1999, European journal of pharmacology.

[51]  B Devlin,et al.  Association study of brain‐derived neurotrophic factor in adults with a history of childhood onset mood disorder , 2004, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[52]  E. Nestler,et al.  The many faces of CREB , 2005, Trends in Neurosciences.

[53]  Alcino J. Silva,et al.  CREB and memory. , 1998, Annual review of neuroscience.

[54]  Smith Kl,et al.  Developmental neuroplasticity : Roles in early life seizures and chronic epilepsy , 1999 .

[55]  S. Christian,et al.  Linkage disequilibrium of the brain-derived neurotrophic factor Val66Met polymorphism in children with a prepubertal and early adolescent bipolar disorder phenotype. , 2004, The American journal of psychiatry.

[56]  J. Giedd Structural Magnetic Resonance Imaging of the Adolescent Brain , 2004, Annals of the New York Academy of Sciences.

[57]  D. Winder,et al.  LTP in the mouse nucleus accumbens is developmentally regulated , 2002, Synapse.

[58]  T. Krahe,et al.  Early alcohol exposure induces persistent alteration of cortical columnar organization and reduced orientation selectivity in the visual cortex. , 2005, Journal of neurophysiology.

[59]  JaneR . Taylor,et al.  Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. , 2003, The American journal of psychiatry.

[60]  Kellogg Ck Early developmental modulation of GABAA receptor function. Influence on adaptive responses. , 1998 .

[61]  M. McCarthy,et al.  Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster. , 2006, Journal of neurobiology.

[62]  Matcheri S Keshavan,et al.  Prefrontal cortex, thalamus, and cerebellar volumes in adolescents and young adults with adolescent-onset alcohol use disorders and comorbid mental disorders. , 2005, Alcoholism, clinical and experimental research.

[63]  P. Huttenlocher Synapse elimination and plasticity in developing human cerebral cortex. , 1984, American journal of mental deficiency.

[64]  J. Parnavelas,et al.  The Development of the Synaptic Organization of the Serotonergic System Differs in Brain Areas with Different Functions , 1998, Experimental Neurology.

[65]  Mark J. Thomas,et al.  Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine , 2001, Nature Neuroscience.

[66]  O. Witte,et al.  Changes in neocortical and hippocampal GABAA receptor subunit distribution during brain maturation and aging , 2006, Brain Research.

[67]  C. Büchel,et al.  Temporal and Spatial Dynamics of Brain Structure Changes during Extensive Learning , 2006, The Journal of Neuroscience.

[68]  R. Depue,et al.  A Behavioral Dimension of Constraint , 1986 .

[69]  B. Grant,et al.  Age of onset of drug use and its association with DSM-IV drug abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. , 1998, Journal of substance abuse.

[70]  R. Douglas,et al.  Developmental plasticity of mouse visual acuity , 2003, The European journal of neuroscience.

[71]  F. Crews,et al.  Consequences of multiple withdrawals from alcohol. , 2004, Alcoholism, clinical and experimental research.

[72]  T. Hedner,et al.  Developmental variations in CSF monoamine metabolites during childhood. , 1986, Biology of the neonate.

[73]  C. Kellogg,et al.  Norepinephrine utilization in the hypothalamus of the male rat during adolescent development. , 1992, Developmental neuroscience.

[74]  Paul J. Harrison,et al.  Detection and quantitation of 5-HT1A and 5-HT2A receptor mRNAs in human hippocampus using a reverse transcriptase-polymerase chain reaction (RT-PCR) technique and their correlation with binding site densities and age , 1994, Neuroscience Letters.

[75]  R. Fagen Exercise, Play, and Physical Training in Animals , 1976 .

[76]  Kenneth J Sher,et al.  Adolescence: booze, brains, and behavior. , 2005, Alcoholism, clinical and experimental research.

[77]  T. Duka,et al.  Mixed emotions: alcoholics’ impairments in the recognition of specific emotional facial expressions , 2003, Neuropsychologia.

[78]  J. Parnavelas,et al.  The serotonin innervation of the basal forebrain shows a transient phase during development. , 1997, Brain research. Developmental brain research.

[79]  S. Roper,et al.  Brain‐derived neurotrophic factor enhances fast excitatory synaptic transmission in human epileptic dentate gyrus , 2001, Annals of neurology.

[80]  M. Cynader,et al.  Autoradiographic localization of serotonin receptor subtypes in cat visual cortex: transient regional, laminar, and columnar distributions during postnatal development , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[81]  E. Bennett,et al.  Psychobiology of plasticity: effects of training and experience on brain and behavior , 1996, Behavioural Brain Research.

[82]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[83]  J. Blendy,et al.  Antidepressant action: to the nucleus and beyond. , 2005, Trends in pharmacological sciences.

[84]  F. Crews,et al.  Binge ethanol exposure decreases neurogenesis in adult rat hippocampus , 2002, Journal of neurochemistry.

[85]  Martin H. Teicher,et al.  Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats , 2000, Synapse.

[86]  H Wechsler,et al.  Correlates of college student binge drinking. , 1995, American journal of public health.

[87]  C. Irwin Adolescent social behavior and health , 1987 .

[88]  Alan C. Evans,et al.  Intellectual ability and cortical development in children and adolescents , 2006, Nature.

[89]  T. Hensch Critical period plasticity in local cortical circuits , 2005, Nature Reviews Neuroscience.

[90]  D. Coulter,et al.  gamma-Aminobutyric acid(A) receptor subunit expression predicts functional changes in hippocampal dentate granule cells during postnatal development. , 2001, Journal of neurochemistry.

[91]  E. Alleva,et al.  Response to novelty, social and self-control behaviors, in rats exposed to neonatal anoxia: modulatory effects of an enriched environment , 2005, Psychopharmacology.

[92]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[93]  M. Silveri,et al.  Decreased sensitivity to the hypnotic effects of ethanol early in ontogeny. , 1998, Alcoholism, clinical and experimental research.

[94]  L. Butcher,et al.  Postnatal development of cholinergic neurons in the rat: I. Forebrain , 1991, Brain Research Bulletin.

[95]  M. Ticku,et al.  Effect of chronic administration of ethanol on GABAA receptor assemblies derived from α2-, α3-, β2- and γ2-subunits in the rat cerebral cortex , 2005, Brain Research.

[96]  P. Rakić,et al.  Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. , 1989, Brain research. Developmental brain research.

[97]  D. Coulter,et al.  γ‐Aminobutyric acidA receptor subunit expression predicts functional changes in hippocampal dentate granule cells during postnatal development , 2001 .

[98]  F. Tarazi,et al.  Comparative postnatal development of dopamine D1, D2 and D4 receptors in rat forebrain , 2000, International Journal of Developmental Neuroscience.

[99]  R. Archer,et al.  The relationship of MMPI and Sensation Seeking Scales to adolescent drug use. , 1989, Journal of personality assessment.

[100]  C Byrne Adolescence to adulthood--a journey or a struggle. , 1999, The Queensland nurse.

[101]  Y. Munakata,et al.  Developmental cognitive neuroscience: progress and potential , 2004, Trends in Cognitive Sciences.

[102]  F. Crews,et al.  Alcohol-induced neurodegeneration: when, where and why? , 2004, Alcoholism, clinical and experimental research.

[103]  H. Uylings,et al.  The development of the rat prefrontal cortex. Its size and development of connections with thalamus, spinal cord and other cortical areas. , 1990, Progress in brain research.

[104]  R. Hen,et al.  Requirement of Hippocampal Neurogenesis for the Behavioral Effects of Antidepressants , 2003, Science.

[105]  D. Redburn Development of GABAergic neurons in the mammalian retina. , 1992, Progress in brain research.

[106]  A. Toga,et al.  Mapping brain maturation , 2006, Trends in Neurosciences.

[107]  D. Coppola,et al.  Neonatal Alcohol Exposure Induces Long-Lasting Impairment of Visual Cortical Plasticity in Ferrets , 2003, The Journal of Neuroscience.

[108]  T. Guilarte,et al.  Lead exposure alters cyclic-AMP response element binding protein phosphorylation and binding activity in the developing rat brain. , 2003, Brain research. Developmental brain research.

[109]  F. Crews,et al.  Glutamate and Alcohol-Induced Neurotoxicity , 2002 .

[110]  Bogdan Draganski,et al.  Neuroplasticity: Changes in grey matter induced by training , 2004, Nature.

[111]  G. L. Pleger,et al.  Altered stressor-induced changes in GABAA receptor function in the cerebral cortex of adult rats exposed in utero to diazepam , 1993, Pharmacology Biochemistry and Behavior.

[112]  Louis W. Chang,et al.  Handbook of Developmental Neurotoxicology , 1998 .

[113]  Philip Smith,et al.  Does play matter? Functional and evolutionary aspects of animal and human play , 1982, Behavioral and Brain Sciences.

[114]  Adolescence to Adulthood. , 1980 .

[115]  I. Kostović,et al.  Structural and histochemical reorganization of the human prefrontal cortex during perinatal and postnatal life. , 1990, Progress in brain research.

[116]  M. Reiff,et al.  Maturation of brain function associated with response inhibition. , 2003 .

[117]  Anat Biegon,et al.  Autoradiographic analysis of serotonin 5-HT1A receptor binding in the human brain postmortem: effects of age and alcohol , 1991, Brain Research.

[118]  T. Foster,et al.  Insensitivity of the Hippocampus to Environmental Stimulation during Postnatal Development , 1997, The Journal of Neuroscience.

[119]  J. S. Johnson,et al.  Critical period effects in second language learning: The influence of maturational state on the acquisition of English as a second language , 1989, Cognitive Psychology.

[120]  L. Spear The adolescent brain and age-related behavioral manifestations , 2000, Neuroscience & Biobehavioral Reviews.

[121]  J. Lauder Ontogeny of the Serotonergic System in the Rat: Serotonin as a Developmental Signal a , 1990, Annals of the New York Academy of Sciences.

[122]  F. Bloom,et al.  Ontogeny of monoamine neurons in the locus coeruleus, raphe nuclei and substantia nigra of the rat. I. Cell differentiation , 1974, The Journal of comparative neurology.

[123]  Patrick M. O'Malley,et al.  Monitoring the Future: National Survey Results on Drug Use, 1975-2003. Volume I: Secondary School Students 2003. NIH Publication No. 04-5507. , 2004 .

[124]  E. Walker,et al.  Developmental changes in cortisol secretion in normal and at-risk youth , 2001, Development and Psychopathology.

[125]  G. Laviola,et al.  Behavioral and Neurochemical Vulnerability During Adolescence in Mice: Studies with Nicotine , 2004, Neuropsychopharmacology.

[126]  Mark A. Ungless,et al.  Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons , 2001, Nature.

[127]  A. Basbaum,et al.  Autoradiographic evidence of serotonin1 binding sites on primary afferent fibres in the dorsal horn of the rat spinal cord , 1987, Neuroscience Letters.

[128]  T. Wills,et al.  Novelty seeking, risk taking, and related constructs as predictors of adolescent substance use: an application of Cloninger's theory. , 1994, Journal of substance abuse.

[129]  Elizabeth Gould,et al.  Serotonin and Hippocampal Neurogenesis , 1999, Neuropsychopharmacology.

[130]  T. J. Berndt,et al.  Developmental Changes in Conformity to Peers and Parents , 1979 .

[131]  D. Rosenberg,et al.  Changes in the dopaminergic innervation of monkey prefrontal cortex during late postnatal development: A tyrosine hydroxylase immunohistochemical study , 1994, Biological Psychiatry.

[132]  N. Dahmen,et al.  Confirmation of association of the GABRA2 gene with alcohol dependence by subtype-specific analysis , 2006, Psychiatric genetics.

[133]  Suzanne E. Welcome,et al.  Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children , 2022 .

[134]  J. Panksepp The ontogeny of play in rats. , 1981, Developmental psychobiology.

[135]  E. Gould,et al.  Neurogenesis in the adult is involved in the formation of trace memories , 2001, Nature.

[136]  Eric R. Kandel,et al.  Cell Adhesion Molecules, CREB, and the Formation of New Synaptic Connections , 1996, Neuron.

[137]  T. Insel,et al.  The ontogeny of excitatory amino acid receptors in rat forebrain—I.N-methyl-d-aspartate and quisqualate receptors , 1990, Neuroscience.

[138]  Martin H. Teicher,et al.  Evidence for dopamine receptor pruning between adolescence and adulthood in striatum but not nucleus accumbens. , 1995, Brain research. Developmental brain research.

[139]  F. Tarazi,et al.  Postnatal development of dopamine and serotonin transporters in rat caudate-putamen and nucleus accumbens septi , 1998, Neuroscience Letters.

[140]  J. Arnett Reckless behavior in adolescence: A developmental perspective , 1992 .

[141]  C. Kellogg,et al.  Control of endogenous norepinephrine release in the hypothalamus of male rats changes over adolescent development. , 1997, Brain research. Developmental brain research.

[142]  P. Mcgonigle,et al.  Ontogeny of dopamine D3 receptors in the nucleus accumbens of the rat , 1997, Neuroscience Letters.

[143]  E Gould,et al.  Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone‐dependent mechanism , 2001, The Journal of comparative neurology.