Abstract
Neurodevelopmental risk factors have assumed a critical role in prevailing notions concerning the etiopathogenesis of neuropsychiatric disorders. Staging, diagnostic elements at which phase of disease is determined, provides a means of conceptualizing the degree and extent of factors affecting brain development trajectories, but is concurrently specified through the particular interactions of genes and environment unique to each individual case. For present purposes, staging perspectives in neurodevelopmental aspects of the disease processes are considered from conditions giving rise to neurodevelopmental staging in affective states, adolescence, dopamine disease states, and autism spectrum disorders. Three major aspects influencing the eventual course of individual developmental trajectories appear to possess an essential determinant influence upon outcome: (i) the type of agent that interferes with brain development, whether chemical, immune system activating or absent (anoxia/hypoxia), (ii) the phase of brain development at which the agent exerts disruption, whether prenatal, postnatal, or adolescent, and (iii) the age of expression of structural and functional abnormalities. Clinical staging may be assumed at any or each developmental phase. The present perspective offers both a challenge to bring further order to diagnosis, intervention, and prognosis and a statement regarding the extreme complexities and interwoven intricacies of epigenetic factors, biomarkers, and neurobehavioral entities that aggravate currents notions of the neuropsychiatric disorders.
Similar content being viewed by others
References
Aarnoudse-Moens CS, Weisglas-Kuperus N, van Goudoever JB, Oosterlaan J (2009) Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics 124:717–728
Abe H, Hidaka N, Kawagoe C, Odagiri K, Watanabe Y, Ikeda T, Ishizuka Y, Hashiguchi H, Takeda R, Nishimori T, Ishida Y (2007) Prenatal psychological stress causes higher emotionality, depression-like behavior, and elevated activity in the hypothalamic–pituitary–adrenal axis. Neurosci Res 59:145–151
Acosta M, Gallo V, Batshaw MI (2002) Brain development and the ontogeny of developmental disabilities. Adv Pediatr 49:1–57
Adigun AA, Wrench N, Seidler FJ, Slotkin TA (2009) Neonatal dexamethasone treatment leads to alterations in cell signaling cascades controlling hepatic and cardiac function in adulthood. Neurotoxicol Teratol. October 20. PMID:19853034
Adriani W, Laviola G (2003) Elevated levels of impulsivity and reduced place conditioning with d-amphetamine: two behavior features of adolescents in mice. Behav Neurosci 117:695–703
Adriani W, Chiarotti F, Laviola G (1998) Elevated novelty seeking and peculiar d-amphetamine sensitization in periadolescent mice compared with adult mice. Behav Neurosci 112:1152–1166
Adriani W, Giannakopolous D, Bokulic Z, Jernej B, Alleva E, Laviola G (2006) Response to novelty, social and self-control behaviors, in rats exposed to neonatal anoxia: modulatory effects of an enriched environment. Psychopharmacology 184:155–165
Alsuwaidan MT, Kucyi A, Law CW, McIntyre RS (2009) Exercise and bipolar disorder: a review of neurobiological mediators. Neuromol Med 11:328–336
Alttoa A, Kõiv K, Hinsley TA, Brass A, Harro J (2009) Differential gene expression in a rat model of depression based on persistent differences in exploratory activity. Eur Neuropsychopharmacol. October 23. PMID:19854624
Anand KJ, Scalzo FM (2000) Can adverse neonatal experiences alter brain development and subsequent behavior? Biol Neonate 77:69–82
Andersen SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity. Neurosci Biobehav Rev 27:3–18
Andersen SL, Teicher MH (2008) Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci 31:183–191
Andersen SL, Teicher MH (2009) Desperately driven and no brakes: developmental stress exposure and subsequent risk for substance abuse. Neurosci Biobehav Rev 33:516–524
Andrews G, Pine DS, Hobbs MJ, Anderson TM, Sunderland M (2009) Neurodevelopmental disorders: cluster 2 of the proposed meta-structure for DSM-V and ICD-11. Psychol Med 39:2013–2023
Angarita GA, Pittman B, Gueorguieva R, Kalayasiri R, Lynch WJ, Sughondhabirom A, Morgan PT, Malison RT (2010) Regulation of cocaine self-administration in humans: lack of evidence for loading and maintenance phases. Pharmacol Biochem Behav 95:51–55
Anisman H, Zaharia MD, Meaney MJ, Merali Z (1998) Do early-life events permanently alter behavioral and hormonal responses to stressors? Int J Devel Neurosci 16:149–164
Archer T, Adriansson L, Plancak A, Karlsson E (2007) Influence of affective personality on cognition-mediated emotional processing: need for empowerment. Eur J Psychiatry 21:248–262
Archer T, Adolfsson B, Karlsson E (2008) Affective personality as cognitive-emotional presymptom profiles regulatory for self-reported health predispositions. Neurotox Res 14:1–25
Archer T, Beninger RJ, Palomo T, Kostrzewa RM (2010) Epigenetics and biomarkers in the etiopathogenesis of neuropsychiatric disorders. Neurotox Res (in press)
Arnett J (1992) Reckless behavior in adolescence: a developmental perspective. Dev Rev 12:339–373
Avital A, Richter-Levin G (2005) Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat. Int J Neuropsychopharmacol 2:163–173
Avital A, Ram E, Maayan R, Weizman A, Richter-Levin G (2005) Effects of early life stress on behavior and neurosteroid levels in the rat hypothalamus and entorhinal cortex. Brain Res Bull 6:419–424
Bagner DM, Sheinkopf SJ, Miller-Loncar C, LaGasse LL, Lester BM, Liu J, Bauer CR, Shankaran S, Bada H, Das A (2009) The effect of parenting stress on child behavior problems in high-risk children with prenatal drug exposure. Child Psychiatry Hum Dev 40:73–84
Bagot RC, van Hasselt FN, Champagne DL, Meaney MJ, Krugers HJ, Joëls M (2009) Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol Learn Mem 92:292–300
Baker KD, Skuse DH (2005) Adolescents and young adults with 22q11 deletion syndrome: psychopathology in an at-risk group. Br J Psychiatry 186:115–120
Bardo MT, Klebaur JE, Valone JM, Deaton C (2001) Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats. Psychopharmacology 155:278–284
Barron S, White A, Swartzwelder HS, Bell RL, Rodd ZA, Slawecki CJ, Ehlers CL, Levin ED, Rezvani AH, Spear LP (2005) Adolescent vulnerabilities to chronic alcohol or nicotine exposure: findings from rodent models. Alcohol Clin Exp Res 29:1720–1725
Bazak N, Kozlovsky N, Kaplan Z, Matar M, Golan H, Zohar J, Richter-Levin G, Cohen H (2009) Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor. Psychoneuroendocrinology 34:844–858
Berns GS, Moore S, Capra CM (2009) Adolescent engagement in dangerous behaviors is associated with increased white matter maturity of frontal cortex. PloS ONE 26:e6773
Beydoun H, Saftlas AF (2008) Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence. Paediatr Perinat Epidemiol 22:438–466
Bezard E, Dovero S, Belin D, Duconger S, Jackson-Lewis V, Przedborski S, Piazza PV, Gross CE, Jaber M (2003) Enriched environment confers resistance to 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine and cocaine: involvement of dopamine transporter and trophic factors. J Neurosci 23:10999–11007
Birmaher B, Axelson D, Strober M, Gill MK, Valeri S, Chiappetta L, Ryan N, Leonard H, Hunt J, Iyengar S, Keller M (2006) Clinical course of children and adolescents with bipolar spectrum disorders. Arch Gen Psychiatry 63:175–183
Bjork JM, Smith AR, Danube CL, Hommer DW (2007) Developmental differences in posterior mesofrontal cortex recruitment by risky rewards. J Neurosci 27:4839–4849
Blaylock RL, Strunecka A (2009) Immune-glutamatergic dysfunction as a central mechanism of the autism spectrum disorders. Curr Med Chem 16:157–170
Bonari L, Pinto N, Ahn E, Einarson A, Steiner M, Koren G (2004) Perinatal risks of untreated depression during pregnancy. Can J Psychiatry 49:726–735
Bowling SL, Bardo MT (1994) Locomotor and rewarding effects of amphetamine in enriched, social, and isolate reared rats. Pharmacol Biochem Behav 48:459–464
Bozzini S, Gambelli P, Boiocchi C, Schirinzi S, Falcone R, Buzzi P, Storti C, Falcone C (2009) Coronary artery disease and depression: possible role of brain-derived neurotrophic factor and serotonin transporter gene polymorphisms. Int J Mol Med 24:813–818
Bradberry CW (2000) Acute and chronic dopamine dynamics in a nonhuman primate model of recreational cocaine use. J Neurosci 20:7109–7115
Bradberry CW (2010) Cortical and sub-cortical effects in primate models of cocaine use: implications for addiction and the increased risk of psychiatric illness. Neurotox Res (in press)
Bradberry CW, Roth RH (1989) Cocaine increases extracellular dopamine in rat nucleus accumbens and ventral tegmental area as shown by in vivo microdialysis. Neurosci Lett 103:97–102
Bradberry CW, Rubino SR (2006) Dopaminergic responses to self-administered cocaine in rhesus monkeys do not sensitize following high cumulative intake. Eur J Neurosci 23:2773–2778
Bradberry CW, Barrett-Larimore RL, Jatlow P, Rubino SR (2000) Impact of self-administered cocaine and cocaine cues on extracellular dopamine in mesolimbic and sensorimotor striatum in rhesus monkeys. J Neurosci 20:3874–3883
Bradley RG, Binder EB, Epstein MP, Tang Y, Nair HP, Liu W, Gillespie CF, Berg T, Evces M, Newport DJ, Stowe ZN, Heim CM, Nemeroff CB, Schwartz A, Cubells JF, Ressler KJ (2008) Influence of child abuse on adult depression: moderation by the corticotropin-releasing hormone receptor gene. Arch Gen Psychiatry 65:190–200
Branchi I, D’Andrea I, Cirulli F, Lipp HP, Alleva E (2009) Shaping brain development: Mouse communal nesting blunts adult neuroendocrine and behavioral response to social stress and modifies chronic antidepressant treatment outcome. Psychoneuroendocrinology. November 26. PMID:19945226
Brenhouse HC, Napierata L, Kussmaul L, Leussis M, Andersen SL (2009) Juvenile methylphenidate exposure and factors that influence incentive processing. Dev Neurosci 31:95–106
Brent DA, Oquendo M, Birmaher B, Greenhill L, Kolko D, Stanley B, Zelazny J, Brodsky B, Firinciogullari S, Ellis SP, Mann JJ (2002) Familial pathways to early-onset suicide attempt: risk for suicidal behavior in offspring of mood-disordered suicide attempters. Arch Gen Psychiatry 59:801–807
Bromley RL, Mawer G, Clayton-Smith J, Baker GA, Liverpool and Manchester Neurodevelopment Group (2008) Autism spectrum disorders following in utero exposure to antiepileptic drugs. Neurology 71:1923–1924
Brown GR, McBride L, Bauer MS, Williford WO (2005) Impact of childhood abuse on the course of bipolar disorder: a replication study in US veterans. J Affect Disord 89:57–67
Cabungcal JH, Nicolas D, Kraftsik R, Cuenod M, Do KQ, Hornung JP (2006) Glutathione deficit during development induces anomalies in the rat anterior cingulated GABAergic neurons: relevance to schizophrenia. Neurobiol Dis 22:624–637
Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 95:5335–5340
Canlon B, Erichsen S, Nemlander E, Chen M, Hossain A, Celsi G, Ceccatelli S (2003) Alterations in the intrauterine environment by glucocorticoids modifies the developmental programme of the auditory system. Eur J Neurosci 17:2035–2041
Carroll ME, Anker JJ, Perry JL (2009) Modeling risk factors for nicotine and other drug abuse in the preclinical laboratory. Drug Alcohol Depend 104(Suppl 1):S70–S78
Cate Carter TD, Mundo E, Parikh SV, Kennedy JL (2003) Early age at onset as a risk factor for poor outcome of bipolar disorder. J Psychiatr Res 37:297–303
Chambers RA, Taylor JR, Petenza MN (2003) Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 160:1041–1052
Champagne FA, Meaney MJ (2006) Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol Psychiatry 59:1227–1235
Chauvet C, Lardeux V, Goldberg SR, Jaber M, Solinas M (2009) Environmental enrichment reduces cocaine seeking and reinstatement induced by cues and stress but not by cocaine. Neuropsychopharmacology 34:2767–2778
Cirulli F, Berry A, Alleva E (2003) Early disruption of the mother–infant relationship: effects on brain plasticity and implications for psychopathology. Neurosci Biobehav Rev 27:73–82
Cirulli F, Francia N, Berry A, Aloe L, Alleva E, Suomi SJ (2009a) Early life stress as a risk factor for mental health: role of neurotrophins from rodents to non-human primates. Neurosci Biobehav Rev 33:573–585
Cirulli F, Laviola G, Ricceri L (2009b) Risk factors for mental health: translational models from behavioural neuroscience. Neurosci Biobehav Rev 33:493–497
Cohen H, Kaplan Z, Matar MA, Loewenthal U, Zohar J, Richter-Levin G (2007) Long-lasting behavioral effects of juvenile trauma in an animal model of PTSD associated with a failure of the autonomic nervous system to recover. Eur Neuropsychopharmacol 17:464–477
Columba-Cabezas S, Iaffaldano G, Chiarotti F, Alleva E, Cirulli F (2009) Early handling increases susceptibility to experimental autoimmune encephalomyelitis (EAE) in C57BL/6 male mice. J Neuroimmunol 212:10–16
Covington HE, Miczek KA (2001) Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration “binges”. Psychopharmacology 158:388–398
Cremer H, Chazal G, Goridis C, Represa A (1997) NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 5:323–335
Cremer H, Chazal G, Carleton A, Goridis C, Vincent JD, Lledo PM (1998) Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc Natl Acad Sci USA 22:13242–13247
Crews FT, Nixon K (2009) Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol 44:115–127
Crews FT, He J, Hodge C (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86:189–199
Croen LA, Goines P, Braunschweig D, Yolken R, Yoshida CK, Grether JK, Fireman B, Kharrazi M, Hansen RL, Van de Water J (2008) Brain-derived neurotrophic factor and autism: maternal and infant peripheral blood levels in the Early Markers for Autism (EMA) Study. Autism Res 1:130–137
Crone EA (2009) Executive functions in adolescence: inferences from brain and behavior. Dev Sci 12:825–830
Currenti SA (2009) Understanding and determining the etiology of autism. Cell Mol Neurobiol. September 23. PMID:19774457
Dahl RE (2004) Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address. Ann N Y Acad Sci 1021:1–22
Dandy KL, Gatch MB (2009) The effects of chronic cocaine exposure on impulsivity in rats. Behav Pharmacol 20:400–405
Darnaudery M, Maccari S (2008) Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57:571–585
DeCastro M, El-Khoury N, Parton L, Ballabh P, LaGamma EF (2009) Postnatal betamethasone vs dexamethasone in premature infants with bronchopulmonary dysplasia: a pilot study. J Perinatol 29:297–304
DeSoto MC (2009) Ockham’s Razor and autism: the case for developmental neurotoxins contributing to a disease of neurodevelopment. Neurotoxicology 30:331–337
Diaconescu AO, Menon M, Jensen J, Kapur S, McIntosh AR (2010) Dopamine-induced changes in neural network patterns supporting aversive conditioning. Brain Res 1313:143–161
Dichter GS, Belger A (2008) Atypical modulation of cognitive control by arousal in autism. Psychiatry Res 164:185–197
Doremus TL, Brunell SC, Rajendran Pand Spear LP (2005) Factors influencing elevated ethanol consumption in adolescent relative to adult rats. Alcohol Clin Exp Res 29:1796–1808
Doremus TL, Varlinskaya EI, Spear LP (2007) Factor analysis of elevated plus-maze behavior in adolescent and adult rats. Pharmacol Biochem Behav 83:570–577
Doremus-Fitzwater TL, Spear LP (2007) Developmental differences in acute ethanol withdrawal in adolescent and adult rats. Alcohol Clin Exp Res 31:1516–1527
Doremus-Fitzwater TL, Varlinskaya EI, Spear LP (2009a) Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol Behav 97:484–494
Doremus-Fitzwater TL, Varlinskaya EI, Spear LP (2009b) Effects of pretest manipulation on elevated plus-maze behavior in adolescent and adult male and female Sprague-Dawley rats. Pharmacol Biochem Behav 92:413–423
Doremus-Fitzwater TL, Varlinskaya EI, Spear LP (2009c) Motivational systems in adolescence: possible implications for age differences in substance abuse and other risk-taking behaviors. Brain Cogn 72:114–123
Douaud G, Mackay C, Andersson J, James S, Quested D, Ray MK, Connell J, Roberts N, Crow TJ, Matthews PM, Smith S, James A (2009) Schizophrenia delays and alters maturation of the brain in adolescence. Brain 132:2437–2448
Duhaime AC (2009) Imitation, immaturity, and injury. J Neurosurg Pediatr 4:407–413
El Rawas R, Thiriet N, Lardeux V, Jaber M, Solinas M (2009) Environmental enrichment decreases the rewarding but not the activating effects of heroin. Psychopharmacology 203:561–570
Ernst M, Luckenbaugh DA, Moolchan ET, Temple VA, Jenness J, Korelitz KE, London ED, Kimes AS (2010) Decision-making and facial emotion recognition as predictors of substance-use initiation among adolescents. Addict Behav 35:286–289
Ernst M, Romeo RD, Andersen SL (2009) Neurobiology of the development of motivated behaviors in adolescence: a window into a neural systems model. Pharmacol Biochem Behav 93:199–211
Eshel N, Nelson EE, Blair RJ, Pine DS, Ernst M (2007) Neural substrates of choice selection in adults and adolescents: development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia 45:1270–1279
Ewing Corcoran SB, Howell LL (2010) Impact of early life stress on the reinforcing and behavioral-stimulant effects of psychostimulants in rhesus monkeys. Behav Pharmacol. December 15. PMID:20016373
Fairbanks LA (1989) Early experience and cross-generational continuity of mother–infant contact in vervet monkeys. Dev Psychobiol 22:669–681
Feder A, Nestler EJ, Charney DS (2009) Psychobiology and molecular genetics of resilience. Nat Rev Neurosci 10:446–457
Feleder C, Tseng KY, Calhoon GG, O’Donnell P (2010) Neonatal intrahippocampal immune challenge alters dopamine modulation of prefrontal cortical interneurons in adult rats. Biol Psychiatry 67:386–392
Flagel SB, Vázquez DM, Watson SJ Jr, Neal CR Jr (2002) Effects of tapering neonatal dexamethasone on rat growth, neurodevelopment, and stress response. Am J Physiol Regul Integr Comp Physiol 282:R55–R63
Flagel SB, Robinson TE, Clark JJ, Clinton SM, Watson SJ, Seeman P, Phillips PE, Akil H (2010) An animal model of genetic vulnerability to behavioral disinhibition and responsiveness to reward-related cues: implications for addiction. Neuropsychopharmacology 35:388–400
Francis DD, Diorio J, Liu D, Meaney MJ (1999a) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158
Francis DD, Caldji C, Champagne F, Plotsky PM, Meaney MJ (1999b) The role of corticotrophin-releasing factor-norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biol Psychiatry 46:1153–1166
Frangou S (2009) Risk and resilience in bipolar disorder: rationale and design of the Vulnerability to Bipolar Disorders Study (VIBES). Biochem Soc Trans 37(Pt 5):1085–1089
Franko KL, Forhead AJ, Fowden AL (2010) Differential effects of prenatal stress and glucocorticoid administration on postnatal growth and glucose metabolism in rats. J Endocrinol 204:319–329
Gardner KL, Hale MW, Lightman SL, Plotsky PM, Lowry CA (2009a) Adverse early life experience and social stress during adulthood interact to increase serotonin transporter mRNA expression. Brain Res 1305:47–63
Gardner KL, Hale MW, Oldfield S, Lightman SL, Plotsky PM, Lowry CA (2009b) Adverse experience during early life and adulthood interact to elevate tph2 mRNA expression in serotonergic neurons within the dorsal raphe nucleus. Neuroscience 163:991–1001
Gasic GP, Smoller JW, Perlis RH, Sun M, Lee S, Kim BW, Lee MJ, Holt DJ, Blood AJ, Makris N, Kennedy DK, Hoge RD, Calhoun J, Fava M, Gusella JF, Breiter HC (2009) BDNF, relative preference, and reward circuitry responses to emotional communication. Am J Med Genet B 150B:762–781
Geier C, Luna B (2009) The maturation of incentive processing and cognitive control. Pharmacol Biochem Behav 93:212–221
Geier CF, Terwilliger R, Teslovich T, Velanova K, Luna B (2009a) Immaturities in reward processing and its influence on inhibitory control in adolescence. Cereb Cortex. October 29. PMID:19875675
Geier CF, Garver K, Terwilliger R, Luna B (2009b) Development of working memory maintenance. J Neurophysiol 101:84–99
Giachino C, Canalia N, Capone F, Fasolo A, Alleva E, Riva MA, Cirulli F, Peretto P (2007) Maternal deprivation and early handling affect density of calcium binding protein-containing neurons in selected brain regions and emotional behavior in periadolescent rats. Neuroscience 145:568–578
Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2:861–863
Giedd JN, Lalonde FM, Celano MJ, White SL, Wallace GL, Lee NR, Lenroot RK (2009) Anatomical brain magnetic resonance imaging of typically developing children and adolescents. J Am Acad Child Adolesc Psychiatry 48:465–470
Giorgio A, Watkins KE, Douaud G, James AC, James S, De Stefano N, Matthews PM, Smith SM, Johansen-Berg H (2008) Changes in white matter microstructure during adolescence. Neuroimage 39:52–61
Goeders NE (2002) Stress and cocaine addiction. J Pharmacol Exp Ther 301:785–789
Goldstein BI, Bukstein OG (2009) Comorbid substance use disorders among youth with bipolar disorder: opportunities for early identification and prevention. J Clin Psychiatry. December 1. PMID:19961811
Gotz AA, Stefanski V (2007) Psychosocial maternal stress during pregnancy affects serum corticosterone, blood immune parameters and anxiety behavior in male adult rat offspring. Physiol Behav 90:108–115
Güroğlu B, van den Bos W, Crone EA (2009) Neural correlates of social decision making and relationships: a developmental perspective. Ann N Y Acad Sci 1167:197–206
Hardin MG, Mandell D, Mueller SC, Dahl RE, Pine DS, Ernst M (2009) Inhibitory control in anxious and healthy adolescents is modulated by incentive and incidental affective stimuli. J Child Psychol Psychiatry 50:1550–1558
Heim C, Nemeroff CB (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 12:1023–1039
Heim C, Newport DJ, Heit S, Graham YP, Wilcox M, Bonsall R, Miller AH, Nemeroff CB (2000) Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 284:592–597
Heim C, Plotsky PM, Nemeroff CB (2004) Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 4:641–648
Heim C, Newport DJ, Mletzko T, Miller AH, Nemeroff CB (2008a) The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33:693–710
Heim C, Mletzko T, Purselle D, Musselman DL, Nemeroff CB (2008b) The dexamethasone/corticotropin-releasing factor test in men with major depression: role of childhood trauma. Biol Psychiatry 63:398–405
Hellemans KG, Nobrega JN, Olmstead MC (2005) Early environmental experience alters baseline and ethanol-induced cognitive impulsivity: relationship to forebrain 5-HT1A receptor binding. Behav Brain Res 159:207–220
Hellgren K, Aring E, Jacobson L, Ygge J, Martin L (2009) Visuospatial skills, ocular alignment, and magnetic resonance imaging findings in very low birth weight adolescents. J AAPOS 13:273–279
Hellström P, Edsbagge M, Blomsterwall E, Archer T, Tisell M, Tullberg M, Wikkelsø C (2008) Neuropsychological effects of shunt treatment in idiopathic normal pressure hydrocephalus. Neurosurgery 63:527–535
Ho BC, Magnotta V (2010) Hippocampal volume deficits and shape deformities in young biological relatives of schizophrenia probands. Neuroimage 49:3385–3393
Homberg JR, Schiepers OJ, Schoffelmeer AN, Cuppen E, Vanderschuren LJ (2007) Acute and constitutive increases in central serotonin levels reduce social play behaviour in peri-adolescent rats. Psychopharmacology 195:175–182
Homberg JR, Schubert D, Gaspar P (2010) New perspectives on the neurodevelopmental effects of SSRIs. Trends Pharmacol Sci 31:60–65
Horovitz O, Jacobson-Pick S, Tsoory MM, Richter-Levin G (2007) Exposing rats to juvenile stress affects body weight and open field indices both soon after the exposure and in adulthood, but in opposite directions. Neural plasticity—Abstracts of the 15th Annual Meeting of Israel Society for Neurosciences, vol 1. Eilat, Israel, p 49
Hossain A, Hajman K, Charitidi K, Erhardt S, Zimmermann U, Knipper M, Canlon B (2008) Prenatal dexamethasone impairs behavior and the activation of the BDNF exon IV promoter in the paraventricular nucleus in adult offspring. Endocrinology 149:6356–6365
Hosseini M, Alaei HA, Naderi A, Sharifi MR, Zahed R (2009) Treadmill exercise reduces self-administration of morphine in male rats. Pathophysiology 16:3–7
Ibi D, Nagai T, Kitahara Y, Mizoguchi H, Koike H, Shiraki A, Takuma K, Kamei H, Noda Y, Nitta A, Nabeshima T, Yoneda Y, Yamada K (2009) Neonatal polyI:C treatment in mice results in schizophrenia-like behavioral and neurochemical abnormalities in adulthood. Neurosci Res 64:297–305
Jager G, Ramsey NF (2008) Long-term consequences of adolescent cannabis exposure on the development of cognition, brain structure and function: an overview of animal and human research. Curr Drug Abuse Rev 1:114–123
Janse Van Rensburg K, Taylor A, Hodgson T, Benattayallah A (2009) Acute exercise modulates cigarette cravings and brain activation in response to smoking-related images: an fMRI study. Psychopharmacology 203:589–598
Joffe H, Hayes FJ (2008) Menstrual cycle dysfunction associated with neurologic and psychiatric disorders: their treatment in adolescents. Ann N Y Acad Sci 1135:219–229
Johnson SB, Blum RW, Giedd JN (2009) Adolescent maturity and the brain: the promise and pitfalls of neuroscience research in adolescent health policy. J Adolesc Health 45:216–221
Johnston MV, Ishida A, Ishida WN, Matsushita HB, Nishimura A, Tsuji M (2009) Plasticity and injury in the developing brain. Brain Dev 31:1–10
Kalant H (2009) What neurobiology cannot tell us about addiction. Addiction. November 17. PMID:19919596
Kalia M (2008) Brain development: anatomy, connectivity, adaptive plasticity, and toxicity. Metabolism 57(Suppl 2):S2–S5
Katz M, Liu C, Schaer M, Parker KJ, Ottet MC, Epps A, Buckmaster CL, Bammer R, Moseley ME, Schatzberg AF, Eliez S, Lyons DM (2009) Prefrontal plasticity and stress inoculation-induced resilience. Dev Neurosci 31:293–299
Kempton MJ, Haldane M, Jogia J, Grasby PM, Collier D, Frangou S (2009) Dissociable brain structural changes associated with predisposition, resilience, and disease expression in bipolar disorder. J Neurosci 29:10863–10868
Kilic I, Dagdeviren E, Kaya E (2008) Effects of neonatal dexamethasone or methylprednisolone on rat growth and neurodevelopment. Pediatr Int 50:489–494
Kobak R, Zajac K, Levine S (2009) Cortisol and antisocial behavior in early adolescence: the role of gender in an economically disadvantaged sample. Dev Psychopathol 21:579–591
Kramer MS, Lydon J, Séguin L, Goulet L, Kahn SR, McNamara H, Genest J, Dassa C, Chen MF, Sharma S, Meaney MJ, Thomson S, Van Uum S, Koren G, Dahhou M, Lamoureux J, Platt RW (2009) Stress pathways to spontaneous preterm birth: the role of stressors, psychological distress, and stress hormones. Am J Epidemiol 169:1319–1326
Kroener S, Chandler LJ, Phillips PE, Seamans JK (2009) Dopamine modulates persistent synaptic activity and enhances the signal-to-noise ratio in the prefrontal cortex. PloS ONE 4:e6507
Kurian JR, Bychowski ME, Forbes-Lorman RM, Auger CJ, Auger AP (2008) Mecp2 organizes juvenile social behavior in a sex-specific manner. J Neurosci 28:7137–7142
Kyriakopoulos M, Perez-Iglesias R, Woolley JB, Kanaan RA, Vyas NS, Barker GJ, Frangou S, McGuire PK (2009) Effect of age at onset of schizophrenia on white matter abnormalities. Br J Psychiatry 195:346–353
Lach LM, Kohen DE, Garner RE, Brehaut JC, Miller AR, Klassen AF, Rosenbaum PL (2009) The health and psychosocial functioning of caregivers of children with neurodevelopmental disorders. Disabil Rehabil 31(9):741–752
Lau JY, Goldman D, Buzas B, Hodgkinson C, Leibenluft E, Nelson E, Sankin L, Pine DS, Ernst M (2009) BDNF gene polymorphism (Val66Met) predicts amygdala and anterior hippocampus responses to emotional faces in anxious and depressed adolescents. Neuroimage. November 17. PMID:19931400
Laviola G, Adriani W, Terranova MI, Gerra G (1999) Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neurosci Biobehav Rev 23:993–1010
Laviola G, Macri S, Morley-Fletcher S, Adriani W (2003) Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci Biobehav Rev 27:19–31
Laviola G, Hannan AJ, Macri S, Solinas M, Jaber M (2008) Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol Dis 31:159–168
Laviola G, Ognibene E, Romano E, Adriani W, Keller F (2009) Gene–environment interaction during early development in the heterozygous reeler mouse: clues for modeling of major neurobehavioral syndromes. Neurosci Biobehav Rev 33:560–572
Law AJ, Pei Q, Walker M, Gordon-Andrews H, Weickert CS, Feldon J, Pryce CR, Harrison PJ (2009) Early parental deprivation in the marmoset monkey produces long-term changes in hippocampal expression of genes involved in synaptic plasticity and implicated in mood disorder. Neuropsychopharmacology 34:1381–1394
Lazinski MJ, Shea AK, Steiner M (2008) Effects of maternal prenatal stress on offspring development: a commentary. Arch Women’s Ment Health 11:363–375
Lenroot RK, Giedd JN (2010) Sex differences in the adolescent brain. Brain Cogn 72:46–55
Leo D, Adriani W, Cavaliere C, Cirillo G, Marco EM, Romano E, di Porzio U, Papa M, Perrone-Capano C, Laviola G (2009) Methylphenidate to adolescent rats drives enduring changes of accumbal Htr7 expression: implications for impulsive behavior and neuronal morphology. Genes Brain Behav 8:356–368
Levine S (2002) Enduring effects of early experience on adult behavior. In: Pfaff DW, Arnold AP, Fohrbach SE et al (eds) Hormones, brain and behavior. Academic Press, San Diego, pp 535–542
Levitt NS, Lindsay RS, Holmes MC, Seckl JR (1996) Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring of the rat. Neuroendocrinology 64:412–418
Lewitus GM, Schwartz M (2009) Behavioral immunization: immunity to self-antigens contributes to psychological stress resilience. Mol Psychiatry 14:532–536
Liu Q, Wong-Riley MT (2010) Postnatal changes in the expressions of serotonin 1A, 1B, and 2A receptors in ten brain stem nuclei of the rat: implication for a sensitive period. Neuroscience 165:61–78
Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662
Lodge DJ, Behrens MM, Grace AA (2009) A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci 29:2344–2354
López-Bendito G, Sánchez-Alcañiz JA, Pla R, Borrell V, Picó E, Valdeolmillos M, Marín O (2008) Chemokine signaling controls intracortical migration and final distribution of GABAergic interneurons. J Neurosci 28:1613–1624
Lopez-Duran NL, Hajal NJ, Olson SL, Felt BT, Vazquez DM (2009a) Individual differences in cortisol responses to fear and frustration during middle childhood. J Exp Child Psychol 103:285–295
Lopez-Duran NL, Olson SL, Hajal NJ, Felt BT, Vazquez DM (2009b) Hypothalamic pituitary adrenal axis functioning in reactive and proactive aggression in children. J Abnorm Child Psychol 37:169–182
Lotfipour S, Ferguson E, Leonard G, Perron M, Pike B, Richer L, Séguin JR, Toro R, Veillette S, Pausova Z, Paus T (2009) Orbitofrontal cortex and drug use during adolescence: role of prenatal exposure to maternal smoking and BDNF genotype. Arch Gen Psychiatry 66:1244–1252
Lu L, Shepard JD, Hall FS, Shaham Y (2003) Effects of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 27:457–491
Lubman DI, Yücel M, Hall WD (2007) Substance use and the adolescent brain: a toxic combination? J Psychopharmacol 21:792–794
Luciana M (2010) Adolescent brain development: current themes and future directions. Introduction to the special issue. Brain Cogn 72:1–5
Luna B (2009) Developmental changes in cognitive control through adolescence. Adv Child Dev Behav 37:233–278
Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA (2004) Maturation of cognitive processes from late childhood to adulthood. Child Dev 75:1357–1372
Luna B, Geier C, Padmanabhan A (2010) Immaturities in incentive processing and executive function in adolescence. Neurotoxicity Res (in press)
Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O (2003) Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 27:119–127
Macrì S, Pascuali P, Bonsignore LT, Pieretti S, Cirulli F, Chiarotti F, Laviola G (2007) Moderate neonatal stress decreases within-group variation in behavioral, immune and HPA responses in adult mice. PLoS ONE 2:e1015
Macrì S, Granstrem O, Shumilina M, Antunes Gomes dos Santos FJ, Berry A, Saso L, Laviola G (2009) Resilience and vulnerability are dose-dependently related to neonatal stressors in mice. Horm Behav 56:391–398
Magid V, Colder CR, Stroud LR, Nichter M, Nichter M, TERN Members (2009) Negative affect, stress, and smoking in college students: unique associations independent of alcohol and marijuana use. Addict Behav 34:973–975
Maia TV, Cooney RE, Peterson BS (2008) The neural bases of obsessive-compulsive disorder in children and adults. Dev Psychopathol 20:1251–1283
Mala E (2008) Schizophrenia in childhood and adolescence. Neuro Endocrinol Lett 29:831–836
Maldonado-Avilés JG, Curley AA, Hashimoto T, Morrow AL, Ramsey AJ, O’Donnell P, Volk DW, Lewis DA (2009) Altered markers of tonic inhibition in the dorsolateral prefrontal cortex of subjects with schizophrenia. Am J Psychiatry 166:450–459
Marco EM, Macri S, Laviola G (2010) Critical age windows for neurodevelopmental psychiatric diseases: evidence from animal models. Neurotox Res (in press)
Marinelli M, Piazza PV (2002) Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur J Neurosci 16:387–394
Marsh R, Zhu H, Schultz RT, Quackenbush G, Royal J, Skudlarski P, Peterson BS (2006) A developmental fMRI study of self-regulatory control. Hum Brain Mapp 27:848–863
Marsh R, Maia TV, Peterson BS (2009) Functional disturbances within frontostriatal circuits across multiple childhood psychopathologies. Am J Psychiatry 166:664–674
Maslova LN, Bulygina VV, Markel AL (2002) Chronic stress during prepubertal development: immediate and long-lasting effects on arterial blood pressure and anxiety-related behavior. Psychoneuroendocrinology 5:549–561
Matsui F, Morimoto M, Yoshimoto K, Nakatomi Y, Syoji H, Nishimura A, Isoda K, Tanda K, Hosoi H (2009) Effects of stress of postnatal development on corticosterone, serotonin and behavioral changes. Brain Dev. October 7. PMID:19818569
McCormick CM (2009) An animal model of social instability stress in adolescence and risk for drugs of abuse. Physiol Behav. January 23. PMID:20006986
McCormick CM, Mathews IZ (2009) Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory. Prog Neuropsychopharmacol Biol Psychiatry. September 25. PMID:19782715
McCormick CM, Mathews IZ, Thomas C, Waters P (2010) Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain Cogn 72:73–85
McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904
Meyer U, Feldon J (2009) Neural basis of psychosis-related behaviour in the infection model of schizophrenia. Behav Brain Res 204:322–334
Mill J, Petronis A (2008) Pre- and Peri-natal environmental risks for attention-deficit hyperactivity disorder (ADHD): the potential role of epigenetic processes in mediating susceptibility. J Child Psychol Psychiatry Allied Discipl 49:1020–1030
Miller MW, Spear LP (2007) The alcoholism generator. Alcohol Clin Exp Res 30:1466–1469
Morgan C, Fisher H (2007) Environment and schizophrenia: environmental factors in schizophrenia: childhood trauma—a critical review. Schizophr Bull 33:3–10
Morley-Fletcher S, Rea M, Maccari S, Laviola G (2003) Environmental enrichment during adolescence reverses the effects of prenatal stress on play behavior and HPA axis reactivity in rats. Eur J Neurosci 18:3367–3374
Nasrallah NA, Yang TW, Bernstein IL (2009) Long-term risk preference and suboptimal decision making following adolescent alcohol use. Proc Natl Acad Sci USA 106:17600–17604
Navailles S, Hof PR, Schmauss C (2008) Antidepressant drug-induced stimulation of mouse hippocampal neurogenesis is age-dependent and altered by early life stress. J Comp Neurol 509:372–381
Neal CR Jr, VanderBeek BL, Vázquez DM, Watson SJ Jr (2003) Dexamethasone exposure during the neonatal period alters ORL1 mRNA expression in the hypothalamic paraventricular nucleus and hippocampus of the adult rat. Brain Res Dev Brain Res 146:15–24
Neal CR Jr, Weidemann G, Kabbaj M, Vázquez DM (2004) Effect of neonatal dexamethasone exposure on growth and neurological development in the adult rat. Am J Physiol Regul Integr Comp Physiol 287:R375–R385
Nemeroff CB (2004) Neurobiological consequences of childhood trauma. J Clin Psychiatry 65(Suppl 1):18–28
New AS, Fan J, Murrough JW, Liu X, Liebman RE, Guise KG, Tang CY, Charney DS (2009) A functional magnetic resonance imaging study of deliberate emotion regulation in resilience and posttraumatic stress disorder. Biol Psychiatry 66:656–664
Newport DJ, Stowe ZN, Nemeroff CB (2002) Parental depression: animal models of an adverse life event. Am J Psychiatry 159:1265–1283
Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev 7:697–709
O’Brien K, Sekimoto H, Boney C, Malee M (2008) Effect of fetal dexamethasone exposure on the development of adult insulin sensitivity in a rat model. J Matern Fetal Neonatal Med 21:623–628
O’Donnell P (2010) Adolescent maturation of cortical dopamine. In: Palomo T, Beninger RJ, Kostrzewa RM, Archer T (eds) Staging neuropsychiatric disorders: implications for etiopathogenesis and treatment. Fundación Cerebro y Mente, Madrid
O’Donnell K, O’Connor TG, Glover V (2009) Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta. Dev Neurosci 31:285–292
O’Hearn K, Asato M, Ordaz S, Luna B (2008) Neurodevelopment and executive function in autism. Dev Psychopathol 20:1103–1132
Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM (2008) Prenatal exposure to maternal depression, neonatal methylation of glucocorticoid receptor gene NR3C1 and infant cortisol stress responses. Epigenetics 3:97–107
Oberlander TF, Gingrich JA, Ansorge MS (2009) Sustained neurobehavioral effects of exposure to SSRI antidepressants during development: molecular to clinical evidence. Clin Pharmacol Ther 86:672–677
Owesson-White CA, Ariansen J, Stuber GD, Cleaveland NA, Cheer JF, Wightman RM, Carelli RM (2009) Neural encoding of cocaine-seeking behavior is coincident with phasic dopamine release in the accumbens core and shell. Eur J Neurosci 30:1117–1127
Pace TW, Mletzko TC, Alagbe O, Musselman DL, Nemeroff CB, Miller AH, Heim CM (2006) Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am J Psychiatry 163:1630–1633
Painter RC, Roseboom TJ, Bleker OP (2005) Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol 20:345–352
Papadeas ST, Halloran C, McCown TJ, Breese GR, Blake BL (2008) Changes in apical dendritic structure correlate with sustained ERK1/2 phosphorylation in medial prefrontal cortex of a rat model of dopamine D1 receptor agonist sensitization. J Comp Neurol 511:271–285
Pardo CA, Eberhart CG (2007) The neurobiology of autism. Brain Pathol 17:434–447
Pascual M, Blanco AM, Cauli O, Minarro J, Guerri C (2007) Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. Eur J Neurosci 25:541–550
Pattij T, Vanderschuren LJ (2008) The neuropharmacology of impulsive behaviour. Trends Pharmacol Sci 29:192–199
Paus T, Kashavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev 9:947–957
Pautassi RM, Myers M, Spear LP, Molina JC, Spear NE (2008) Adolescent but not adult rats exhibit ethanol-mediated appetitive second-order conditioning. Alcohol Clin Exp Res 32:2016–2027
Penn PR, Rose FD, Johnson DA (2009) Virtual enriched environments in paediatric neuropsychological rehabilitation following traumatic brain injury: feasibility, benefits and challenges. Dev Neurorehabil 12:32–43
Pereira LO, Strapasson AC, Nabinger PM, Achaval M, Netto CA (2008) Early enriched housing results in partial recovery of memory deficits in female, but not in male, rats after neonatal hypoxia-ischemia. Brain Res 1218:257–266
Pérez-Edgar K, Bar-Haim Y, McDermott JM, Gorodetsky E, Hodgkinson CA, Goldman D, Ernst M, Pine DS, Fox NA (2009) Variations in the serotonin-transporter gene are associated with attention bias patterns to positive and negative emotion faces. Biol Psychol. August 31. PMID:19723555
Pfeifer JH, Masten CL, Borofsky LA, Dapretto M, Fuligni AJ, Lieberman MD (2009) Neural correlates of direct and reflected self-appraisals in adolescents and adults: when social perspective-taking informs self-perception. Child Dev 80:1016–1038
Plotsky PM, Meaney MJ (1993) Early, postnatal experience alters hypothalamic corticotrophin-releasing factor CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 18:195–200
Post RM (2010) Mechanisms of illness progression in the recurrent affective disorders. Neurotox Res (in press)
Post RM, Leverich GS (2006) The role of psychosocial stress in the onset and progression of bipolar disorder and its comorbidities: the need for earlier and alternative modes of therapeutic intervention. Dev Psychopathol 18:1181–1211
Puri BK (2010) Progressive structural brain changes in schizophrenia. Expert Rev Neurother 10:33–42
Rende R, Birmaher B, Axelson D, Strober M, Gill MK, Valeri S, Chiappetta L, Ryan N, Leonard H, Hunt J, Iyengar S, Keller M (2007) Childhood-onset bipolar disorder: evidence for increased familial loading of psychiatric illness. J Am Acad Child Adolesc Psychiatry 46:197–204
Resnick MD, Bearman PS, Blum RW, Bauman KE, Harris KM, Jones J, Tabor J, Beuhring T, Sieving RE, Shew M, Ireland M, Bearinger LH, Udry JR (1997) Protecting adolescents from harm. Findings from the National Longitudinal Study on adolescent health. JAMA 278:823–832
Richardson HN, Zorrilla EP, Mandyam CD, Rivier CL (2006) Exposure to repetitive versus varied stress during prenatal development generates two distinct anxiogenic and neuroendocrine profiles in adulthood. Endocrinology 147:2506–2517
Ristuccia RC, Spear LP (2004) Adolescent ethanol sensitivity: hypothermia and acute tolerance. Ann N Y Acad Sci 1021:445–447
Rofey DL, Kolko RP, Iosif AM, Silk JS, Bost JE, Feng W, Szigethy EM, Noll RB, Ryan ND, Dahl RE (2009) A longitudinal study of childhood depression and anxiety in relation to weight gain. Child Psychiatry Hum Dev 40:517–526
Rüedi-Bettschen D, Feldon J, Pryce CR (2004) The impaired coping induced by early deprivation is reversed by chronic fluoxetine treatment in adult Fischer rats. Behav Pharmacol 5–6:413–421
Sanchez MM, Ladd CO, Plotsky PM (2001) Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 3:419–449
Sandi C (2004) Stress, cognitive impairment and cell adhesion molecules. Nat Rev Neurosci 12:917–930
Santana N, Mengod G, Artigas F (2009) Quantitative analysis of the expression of dopamine D1 and D2 receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb Cortex 19:849–860
Sawaguchi T, Goldman-Rakic PS (1991) D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science 251:947–950
Sawaguchi T, Goldman-Rakic PS (1994) The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. J Neurophysiol 71:515–528
Schapiro S, Geller E, Eiduson S (1962) Neonatal adrenal cortical response to stress and vasopressin. Proc Soc Exp Biol Med 109:937–941
Schulz KM, Zehr JL, Salas-Ramirez KY, Sisk CL (2009) Testosterone programs adult social behavior before and during, but not after, adolescence. Endocrinology 150:3690–3698
Sebastian C, Viding E, Williams KD, Blakemore SJ (2010) Social brain development and the affective consequences of ostracism in adolescence. Brain Cogn 72:134–145
Shafritz KM, Dichter GS, Baranek GT, Belger A (2008) The neural circuitry mediating shifts in behavioral response and cognitive set in autism. Biol Psychiatry 63:974–980
Sharf R, Guarnieri DJ, Taylor JR, Dileone RJ (2009) Orexin mediates morphine place preference, but not morphine-induced hyperactivity or sensitization. Brain Res. December 21
Shinwell ES, Eventov-Friedman S (2009) Impact of perinatal corticosteroids on neuromotor development and outcome: review of the literature and new meta-analysis. Semin Fetal Neonatal Med 14:164–170
Sidiropoulou K, Lu FM, Fowler MA, Xiao R, Phillips C, Ozkan ED, Zhu MX, White FJ, Cooper DC (2009) Dopamine modulates an mGluR5-mediated depolarization underlying prefrontal persistent activity. Nat Neurosci 12:190–199
Singh B, Henneberger C, Betances D, Arevalo MA, Rodrigurz-Tebar A, Meier JC, Grantyn R (2006) Altered balance of glutamatergic/GABAergic synaptic input and associated changes in dendrite morphology after BDNF expression in BDNF-deficient hippocampal neurons. J Neurosci 26:7189–7200
Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology 158:343–359
Smith M, Spence MA, Flodman P (2009) Nuclear and mitochondrial genome defects in autisms. Ann N Y Acad Sci 1151:102–132
Solinas M, Chauvet C, Thiriet N, El Rawas R, Jaber M (2008) Reversal of cocaine addiction by environmental enrichment. PNAS 105:17145–17150
Solinas M, Thiriet N, El Rawas R, Lardeux V, Jaber M (2009) Environmental enrichment during early stages of life reduces the behavioral, neurochemical, and molecular effects of cocaine. Neuropsychopharmacology 34:1102–1111
Sowell ER, Thompson PM, Tessner KD, Toga AW (2001) Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. J Neurosci 232:232–235
Spear LP (2000) The adolescent brain and age-related manifestations. Neurosci Biobehav Rev 4:417–463
Spear LP (2004) Adolescent brain development and animal models. Ann N Y Acad Sci 1021:23–26
Spear LP (2007) Assessment of adolescent neurotoxicity: rationale and methodological considerations. Neurotoxicol Teratol 29:1–9
Spear LP (2009) Heightened stress responsivity and emotional reactivity during pubertal maturation: implications for psychopathology. Dev Psychopathol 21:87–97
Spear LP, Varlinskaya EI (2005a) Low dose effects in psychopharmacology: ontogenetic considerations. Nonlinearity Biol Toxicol Med 3:97–111
Spear LP, Varlinskaya EI (2005b) Adolescence. Alcohol sensitivity, tolerance, and intake. Recent Dev Alcohol 17:143–159
Squeglia LM, Jacobus J, Tapert SF (2009) The influence of substance use on adolescent brain development. Clin EEG Neurosci 40:31–38
Steinberg L (2004) Risk taking in adolescence: what changes, and why? Ann N Y Acad Sci 1021:51–58
Steinberg L (2005) Cognitive and affective development in adolescence. Trends Cogn Sci 9:69–74
Steinberg L (2008) A social neuroscience perspective on adolescent risk-taking. Dev Rev 28:78–106
Steinberg L (2009) A behavioral scientist looks at the science of adolescent brain development. Brain Cogn. December 4
Stevens MC, Skudlarski P, Pearlson GD, Calhoun VD (2009) Age-related cognitive gains are mediated by the effects of white matter development on brain network integration. Neuroimage 48:738–746
Sturman D, Moghaddam B (2010) Neurodevelopment and learning in adolescence: relevance to staging in psychiatric disorders. Neurotoxicity Res (in press)
Sullivan R, Wilson DA, Feldon J, Yee BK, Meyer U, Richter-Levin G, Avi A, Michael T, Gruss M, Bock J, Helmeke C, Braun K (2006) The International Society for Developmental Psychobiology annual meeting symposium: impact of early life experiences on brain and behavioral development. Dev Psychobiol 48:583–602
Tau GZ, Peterson BS (2010) Normal development of brain circuits. Neuropsychopharmacology 35:147–168
Thiel KJ, Sanabria F, Pentkowski NS, Neisewander JL (2009) Anti-craving effects of environmental enrichment. Int J Neuropsychopharmacol 12:1151–1156
Thomas MB, Hu M, Lee TM, Bhatnagar S, Becker JB (2009) Sex-specific susceptibility to cocaine in rats with a history of prenatal stress. Physiol Behav 97:270–277
Toth E, Avital A, Leshem M, Richter-Levin G, Braun K (2008a) Neonatal and juvenile stress induces changes in adult social behavior without affecting cognitive function. Behav Brain Res 190:135–139
Toth E, Gersner R, Wilf-Yarkoni A, Raizel H, Dar DE, Richter-Levin G, Levit O, Zangen A (2008b) Age-dependent effects of chronic stress on brain plasticity and depressive behavior. J Neurochem 107:522–532
Trezza V, Vanderschuren LJ (2008) Cannabinoid and opioid modulation of social play behavior in adolescent rats: differential behavioral mechanisms. Eur Neuropsychopharmacol 18:519–530
Trezza V, Vanderschuren LJ (2009) Divergent effects of anandamide transporter inhibitors with different target selectivity on social play behavior in adolescent rats. J Pharmacol Exp Ther 328:343–350
Trezza V, Damsteegt R, Vanderschuren LJ (2009) Conditioned place preference induced by social play behavior: parametrics, extinction, reinstatement and disruption by methylphenidate. Eur Neuropsychopharmacol 19:659–669
Tseng KY, O’Donnell P (2004) Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms. J Neurosci 24:5131–5139
Tseng KY, O’Donnell P (2005) Post-pubertal emergence of prefrontal cortical up states induced by D1-NMDA co-activation. Cereb Cortex 15:49–57
Tseng KY, O’Donnell P (2007a) D2 dopamine receptors recruit a GABA component for their attenuation of excitatory synaptic transmission in the adult rat prefrontal cortex. Synapse 61:843–850
Tseng KY, O’Donnell P (2007b) Dopamine modulation of prefrontal cortical interneurons changes during adolescence. Cereb Cortex 17:1235–1240
Tseng KY, Lewis BL, Hashimoto T, Sesack SR, Kloc M, Lewis DA, O’Donnell P (2008) A neonatal ventral hippocampal lesion causes functional deficits in adult prefrontal cortical interneurons. J Neurosci 28:12691–12699
Tseng KY, Chambers RA, Lipska BK (2009a) The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia. Behav Brain Res 204:295–305
Tseng KY, Feleder C, Calhoon GG, O’Donnell P (2009b) Neonatal intra-hippocampal immune challenge alters dopamine modulation of prefrontal cortical interneurons in adult rats. Biol Psychiatry (in press)
Tsoory MM, Richter-Levin G (2006) Learning under stress in the adult rat is differentially affected by ‘juvenile’ or ‘adolescent’ stress. Int J Neuropsychopharmacol 6:713–728
Tsoory MM, Cohen H, Richter-Levin G (2007) Juvenile stress induces a predisposition to anxiety or depressive-like symptoms following stress in adulthood. Eur Neuropsychopharmacol 17:245–256
Tsoory MM, Guterman A, Richter-Levin G (2008) Exposure to stressors during juvenility disrupts development-related alterations in the PSA-NCAM to NCAM expression ratio: relevance for mood and anxiety disorders. Neuropsychopharmacology 33:378–393
Tsoory MM, Guterman A, Richter-Levin G (2010) “Juvenile stress” alters maturation-related changes in expression of the neural cell adhesion molecule L1 in the limbic system: relevance for stress-related psychopathologies. J Neurosci Res 88:369–380
van Lier PA, Vitaro F, Barker ED, Koot HM, Tremblay RE (2009) Developmental links between trajectories of physical violence, vandalism, theft, and alcohol-drug use from childhood to adolescence. J Abnorm Child Psychol 37:481–492
Vanderschuren LJ, Trezza V, Griffioen-Roose S, Schiepers OJ, Van Leeuwen N, De Vries TJ, Schoffelmeer AN (2008) Methylphenidate disrupts social play behavior in adolescent rats. Neuropsychopharmacology 33:2946–2956
Varlinskaya EI, Spear LP (2006a) Ontogeny of acute tolerance to ethanol-induced social inhibition in Sprague-Dawley rats. Alcohol Clin Exp Res 30:1833–1844
Varlinskaya EI, Spear LP (2006b) Differences in the social consequences of ethanol emerge during the course of adolescence in rats: social facilitation, social inhibition, and anxiolysis. Dev Psychobiol 48:146–161
Varlinskaya EI, Spear LP (2007) Chronic tolerance to the social consequences of ethanol in adolescent and adult Sprague-Dawley rats. Neurotoxicol Teratol 29:23–30
Varlinskaya EI, Spear LP (2008) Social interactions in adolescent and adult Sprague-Dawley rats: impact of social deprivation and test context familiarity. Behav Brain Res 188:398–405
Varlinskaya EI, Spear LP (2009) Ethanol-induced social facilitation in adolescent rats: role of endogenous activity at mu opioid receptors. Alcohol Clin Exp Res 33:991–1000
Vazquez DM (1998) Stress and the developing limbic-hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology 7:663–700
Velanova K, Wheeler ME, Luna B (2009) The maturation of task set-related activation supports late developmental improvements in inhibitory control. J Neurosci 29:12558–12567
Venerosi A, Valanzano A, Cirulli F, Alleva E, Calamandrei G (2004) Acute global anoxia during C-section birth affects dopamine-mediated behavioural responses and reactivity to stress. Behav Brain Res 154:155–164
Voets NL, Hough MG, Douaud G, Matthews PM, James A, Winmill L, Webster P, Smith S (2008) Evidence for abnormalities of cortical development in adolescent-onset schizophrenia. Neuroimage 43:665–675
Wahlstrom D, Collins P, White T, Luciana M (2010) Developmental changes in dopamine neurotransmission in adolescence: behavioral implications and issues in assessment. Brain Cogn 72:146–159
Wanchoo SJ, Lee MJ, Swann AC, Dafny N (2009) Bilateral six-hydroxydopamine administration to PFC prevents the expression of behavioral sensitization to methylphenidate. Brain Res. November 22
Wang L, Huettel S, De Bellis MD (2008) Neural substrates for processing task-irrelevant sad images in adolescents. Dev Sci 11:23–32
Weaver IC (2009) Shaping adult phenotypes through early life environments. Birth Defects Res 87:314–326
Weaver IC, Meaney MJ, Szyf M (2006) Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci USA 103:3480–3485
White AM (2009) Understanding adolescent brain development and its implications for the clinician. Adolesc Med State Art Rev 20:73–90
White T, Schmidt M, Karatekin C (2009) White matter ‘potholes’ in early-onset schizophrenia: a new approach to evaluate white matter microstructure using diffusion tensor imaging. Psychiatry Res 174:110–115
Wilmouth CE, Spear LP (2009) Hedonic sensitivity in adolescent and adult rats: taste reactivity and voluntary sucrose consumption. Pharmacol Biochem Behav 92:566–573
Xiao MF, Xu JC, Tereshchenko Y, Novak D, Schachner M, Kleene R (2009) Neural cell adhesion molecule modulates dopaminergic signaling and behavior by regulating dopamine D2 receptor internalization. J Neurosci 29:14752–14763
Xu Z, Hou B, Gao Y, He F, Zhang C (2007) Effects of enriched environment on morphine-induced reward in mice. Exp Neurol 204:714–719
Zafeiriou DI, Ververi A, Vargiami E (2009) The serotonergic system: its role in pathogenesis and early developmental treatment of autism. Curr Neuropharmacol 7:150–157
Zaias J, Queeney TJ, Kelley JB, Zakharova ES, Izenwasser S (2008) Social and physical environmental enrichment differentially affect growth and activity of preadolescent and adolescent male rats. J Am Assoc Lab Anim Sci 47:30–44
Zakharova E, Miller J, Unterwald E, Wade D, Izenwasser S (2009) Social and physical environment alter cocaine conditioned place preference and dopaminergic markers in adolescent male rats. Neuroscience 163:890–897
Zhao W, Becker JB (2009) Sensitization enhances acquisition of cocaine self-administration in female rats: Estradiol further enhances cocaine intake after acquisition. Horm Behav. September 19. PMID:19769970
Zimmerberg B, Blaskey LG (1998) Prenatal stress effects are partially ameliorated by prenatal administration of the neurosteriod allopregnanolone. Pharmacol Biochem Behav 59:819–827
Zuena AR, Mairesse J, Casolini P, Cinque C, Alema GS, Morley-Fletcher S, Chiodi V, Spagnoli LG, Gradini R, Catalani A, Nicoletti F, Maccari S (2008) Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PloS ONE 3:e2170
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Archer, T., Kostrzewa, R.M., Beninger, R.J. et al. Staging Perspectives in Neurodevelopmental Aspects of Neuropsychiatry: Agents, Phases and Ages at Expression. Neurotox Res 18, 287–305 (2010). https://doi.org/10.1007/s12640-010-9162-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12640-010-9162-6