Abstract
A disruption in normal brain development has been hypothesized to contribute to the aetiology of major psychiatric disorders. According to the ‘double-hit’ hypothesis, mutant genes-based deviations, associated with specific environmental insults during brain development, may result in neurobehavioural disturbances. The existence of age windows of vulnerability to environmental conditions during brain maturation will be discussed, using as examples a series of studies we have performed during the last years. Major deviations from normative neurobehavioural trajectories have been reported in animal models following exposure to severe stress (either episodes of maternal separation, deprivation or corticosterone supplementation) early in infancy. Rodent models of difficult and/or stressful pregnancies, including obstetric complications (e.g. prenatal restrain stress or neonatal hypoxia) and gestational exposure to infection (e.g prenatal immune challenge), have been associated with profound long-lasting deficits in the offspring’s emotional and social behaviour, and with immune and endocrine changes. More recently, adolescence, characterized by elevated rates of brain plasticity, has emerged as an additional period during which sensitivity to environmental influence (either adverse or stimulatory) is maximal. We have reported that both pharmacological (methylphenidate) and environmental (physical or social enrichment) interventions can be used to counteract the detrimental effects of earlier-origin developmental insults. Present findings indicate that these age periods (i.e. prenatal stage, early infancy and adolescence) do represent critical windows open to plastic changes and might be susceptible to both adverse and supportive shaping environmental forces. Taken together, age-related neuroplasticity might be considered not only as a risk factor for psychopathology but also as a potent mechanism for compensation. A better understanding of these critical periods of brain development is a concern for public health and may provide new insights into prevention strategies and into novel therapeutic approaches in neuropsychiatry.
Similar content being viewed by others
Notes
Please note that daily water intake per kg of body weight is approximately four-fold higher in mice than in rats. Therefore, whereas 200 mg/l constitute a low dose of corticosterone supplementation in rats, 100 mg/l constitute a high corticosterone dose in mice.
References
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 hypothalamo-pituitary-adrenal axis. Neurosci Res 59:145–151
Abi-Dargham A (2007) Alterations of serotonin transmission in schizophrenia. Int Rev Neurobiol 78:133–164
Acosta M, Gallo V, Batshaw ML (2002) Brain development and the ontogeny of developmental disabilities. Adv Pediatr 49:1–57
Adriani W, Laviola G (2004) Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav Pharmacol 15:341–352
Adriani W, Spijker S, Deroche-Gamonet V, Laviola G, Le Moal M, Smit AB, Piazza PV (2003) Evidence for enhanced neurobehavioral vulnerability to nicotine during periadolescence in rats. J Neurosci 23:4712–4716
Adriani W, Giannakopoulou D, Bokulic Z, Jernej B, Alleva E, Laviola G (2006a) Response to novelty, social and self-control behaviors, in rats exposed to neonatal anoxia: modulatory effects of an enriched environment. Psychopharmacology (Berl) 184:155–165
Adriani W, Leo D, Greco D, Rea M, di Porzio U, Laviola G, Perrone-Capano C (2006b) Methylphenidate administration to adolescent rats determines plastic changes on reward-related behavior and striatal gene expression. Neuropsychopharmacology 31:1946–1956
Adriani W, Canese R, Podo F, Laviola G (2007) 1H MRS-detectable metabolic brain changes and reduced impulsive behavior in adult rats exposed to methylphenidate during adolescence. Neurotoxicol Teratol 29:116–125
Agid O, Shapira B, Zislin J, Ritsner M, Hanin B, Murad H, Troudart T, Bloch M, Heresco-Levy U, Lerer B (1999) Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Mol Psychiatr 4:163–172
Akil H (2005) Stressed and depressed. Nat Med 11:116–118
Alleva E (1993) Assessment of aggressive behavior in rodents. Methods Neurosci 14:111–137
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 R 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 1–11
Angelini DJ, Verklan MT (2009) Complications during the intrapartum and newborn period. J Perinatal Neonatal Nurs 23:1–2
Bellinger DL, Lubahn C, Lorton D (2008) Maternal and early life stress effects on immune function: relevance to immunotoxicology. J Immunotoxicol 5:419–444
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 Perinatal Epidemiol 22:438–466
Bezard E, Gross CE, Fournier MC, Dovero S, Bloch B, Jaber M (1999) Absence of MPTP-induced neuronal death in mice lacking the dopamine transporter. Exp Neurol 155:268–273
Biederman J (2005) Attention-deficit/hyperactivity disorder: a selective overview. Biol Psychiatr 57:1215–1220
Biscaia M, Marin S, Fernandez B, Marco EM, Rubio M, Guaza C, Ambrosio E, Viveros MP (2003) Chronic treatment with CP 55, 940 during the peri-adolescent period differentially affects the behavioural responses of male and female rats in adulthood. Psychopharmacology (Berl) 170:301–308
Blakemore SJ (2008) The social brain in adolescence. Nat Rev Neurosci 9:267–277
Boksa P (2008) Maternal infection during pregnancy and schizophrenia. J Psychiatry Neurosci 33:183–185
Bolanos CA, Barrot M, Berton O, Wallace-Black D, Nestler EJ (2003) Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood. Biol Psychiatr 54:1317–1329
Borrell J, Vela JM, Arevalo-Martin A, Molina-Holgado E, Guaza C (2002) Prenatal immune challenge disrupts sensorimotor gating in adult rats. Implications for the etiopathogenesis of schizophrenia. Neuropsychopharmacology 26:204–215
Bowlby J (1969) Attachment and loss, Attachment. Basic Books, New York
Bowlby J (1988) Developmental psychiatry comes of age. Am J Psychiatr 145:1–10
Boyce WT, Ellis BJ (2005) Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol 17:271–301
Braga RJ, Petrides G, Figueira I (2004) Anxiety disorders in schizophrenia. Compr Psychiatr 45:460–468
Brandon CL, Marinelli M, Baker LK, White FJ (2001) Enhanced reactivity and vulnerability to cocaine following methylphenidate treatment in adolescent rats. Neuropsychopharmacology 25:651–661
Brown AS (2006) Prenatal infection as a risk factor for schizophrenia. Schizophr Bull 32:200–202
Brown AS, Susser ES (2002) In utero infection and adult schizophrenia. Ment Retard Dev Disabil Res Rev 8:51–57
Brown SA, Tapert SF (2004) Adolescence and the trajectory of alcohol use: basic to clinical studies. Ann NY Acad Sci 1021:234–244
Butz M, Worgotter F, van Ooyen A (2009) Activity-dependent structural plasticity. Brain Res Rev 60:287–305
Buwalda B, Nyakas C, Vosselman HJ, Luiten PG (1995) Effects of early postnatal anoxia on adult learning and emotion in rats. Behav Brain Res 67:85–90
Cannon M, Jones PB, Murray RM (2002) Obstetric complications and schizophrenia: historical and meta-analytic review. Am J Psychiatr 159:1080–1092
Caputa M, Rogalska J, Wentowska K, Nowakowska A (2005) Perinatal asphyxia, hyperthermia and hyperferremia as factors inducing behavioural disturbances in adulthood: a rat model. Behav Brain Res 163:246–256
Carlezon WA Jr, Mague SD, Andersen SL (2003) Enduring behavioral effects of early exposure to methylphenidate in rats. Biol Psychiatr 54:1330–1337
Casey BJ, Jones RM, Hare TA (2008) The adolescent brain. Ann NY Acad Sci 1124:111–126
Casolini P, Zuena AR, Cinque C, Matteucci P, Alema GS, Adriani W, Carpinelli G, Santoro F, Alleva E, Bosco P, Nicoletti F, Laviola G, Catalani A (2005) Sub-neurotoxic neonatal anoxia induces subtle behavioural changes and specific abnormalities in brain group-I metabotropic glutamate receptors in rats. J Neurochem 95:137–145
Catalani A, Marinelli M, Scaccianoce S, Nicolai R, Muscolo LA, Porcu A, Koranyi L, Piazza PV, Angelucci L (1993) Progeny of mothers drinking corticosterone during lactation has lower stress-induced corticosterone secretion and better cognitive performance. Brain Res 624:209–215
Catalani A, Casolini P, Scaccianoce S, Patacchioli FR, Spinozzi P, Angelucci L (2000) Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny. Neuroscience 100:319–325
Chen Y, Hillefors-Berglund M, Herrera-Marschitz M, Bjelke B, Gross J, Andersson K, von Euler G (1997) Perinatal asphyxia induces long-term changes in dopamine D1, D2, and D3 receptor binding in the rat brain. Exp Neurol 146:74–80
Cirulli F, Francia N, Berry A, Aloe L, Alleva E, Suomi SJ (2009) 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
Coe CL, Kramer M, Kirschbaum C, Netter P, Fuchs E (2002) Prenatal stress diminishes the cytokine response of leukocytes to endotoxin stimulation in juvenile rhesus monkeys. J Clin Endocrinol Metab 87:675–681
D’Amato FR, Cabib S, Puglisi-Allegra S, Patacchioli FR, Cigliana G, Maccari S, Angelucci L (1992) Effects of acute and repeated exposure to stress on the hypothalamo-pituitary-adrenocortical activity in mice during postnatal development. Horm Behav 26:474–485
Dabkowska M, Rybakowski J (1994) Stress, depression and schizophrenia in view of psychoimmunology. Psychiatr Pol 28:23–32
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
de Haan M, Wyatt JS, Roth S, Vargha-Khadem F, Gadian D, Mishkin M (2006) Brain and cognitive-behavioural development after asphyxia at term birth. Dev Sci 9:350–358
de Irala J, Ruiz-Canela M, Martinez-Gonzalez MA (2005) Causal relationship between cannabis use and psychotic symptoms or depression. Should we wait and see? A public health perspective. Med Sci Monit 11:RA355–RA358
de Kloet ER (2003) Hormones, brain and stress. Endocr Regul 37:51–68
de Kloet ER, Derijk RH, Meijer OC (2007) Therapy insight: is there an imbalanced response of mineralocorticoid and glucocorticoid receptors in depression? Nat Clin Pract Endocrinol Metab 3:168–179
Dean B, Sundram S, Bradbury R, Scarr E, Copolov D (2001) Studies on [3H]CP-55940 binding in the human central nervous system: regional specific changes in density of cannabinoid-1 receptors associated with schizophrenia and cannabis use. Neuroscience 103:9–15
Decker MJ, Hue GE, Caudle WM, Miller GW, Keating GL, Rye DB (2003) Episodic neonatal hypoxia evokes executive dysfunction and regionally specific alterations in markers of dopamine signaling. Neuroscience 117:417–425
Di Forti M, Morrison PD, Butt A, Murray RM (2007) Cannabis use and psychiatric and cognitive disorders: the chicken or the egg? Curr Opin Psychiatr 20:228–234
Dluzen DE, Anderson LI, McDermott JL, Kucera J, Walro JM (2002) Striatal dopamine output is compromised within +/− BDNF mice. Synapse 43:112–117
Doremus-Fitzwater TL, Varlinskaya EI Spear LP (2009) Motivational systems in adolescence: Possible implications for age differences in substance abuse and other risk-taking behaviors. Brain Cogn 72:114–123
Dwyer JB, McQuown SC, Leslie FM (2009) The dynamic effects of nicotine on the developing brain. Pharmacol Therapeut 122:125–139
Elenkov IJ, Chrousos GP (2002) Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann N Y Acad Sci 966:290–303
El-Khodor BF, Boksa P (1997) Long-term reciprocal changes in dopamine levels in prefrontal cortex versus nucleus accumbens in rats born by Caesarean section compared to vaginal birth. Exp Neurol 145:118–129
El-Khodor BF, Boksa P (1998) Birth insult increases amphetamine-induced behavioral responses in the adult rat. Neuroscience 87:893–904
El-Khodor B, Boksa P (2001) Caesarean section birth produces long term changes in dopamine D1 receptors and in stress-induced regulation of D3 and D4 receptors in the rat brain. Neuropsychopharmacology 25:423–439
Ellenbroek BA, Cools AR (1995) Maternal separation reduces latent inhibition in the conditioned taste aversion paradigm. Neurosci Res Commun 17:27–33
Ellenbroek BA, Cools AR (2002) Early maternal deprivation and prepulse inhibition: the role of the postdeprivation environment. Pharmacol Biochem Behav 73:177–184
Ellenbroek BA, van den Kroonenberg PT, Cools AR (1998) The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr Res 30:251–260
Ellenbroek BA, de Bruin NM, van Den Kroonenburg PT, van Luijtelaar EL, Cools AR (2004) The effects of early maternal deprivation on auditory information processing in adult Wistar rats. Biol Psychiatr 55:701–707
Ellenbroek BA, Derks N, Park HJ (2005) Early maternal deprivation retards neurodevelopment in Wistar rats. Stress 8:247–257
Ellgren M, Spano SM, Hurd YL (2007) Adolescent cannabis exposure alters opiate intake and opioid limbic neuronal populations in adult rats. Neuropsychopharmacology 32:607–615
Ellickson PL, Tucker JS, Klein DJ (2001) High-risk behaviors associated with early smoking: results from a 5-year follow-up. J Adolesc Health 28:465–473
Ellis BJ, Essex MJ, Boyce WT (2005) Biological sensitivity to context: II. Empirical explorations of an evolutionary-developmental theory. Dev Psychopathol 17:303–328
Escorihuela RM, Fernandez-Teruel A, Zapata A, Nunez JF, Tobena A (1993) Flumazenil prevents the anxiolytic effects of diazepam, alprazolam and adinazolam on the early acquisition of two-way active avoidance. Pharmacol Res 28:53–58
Evenden JL, Ryan CN (1999) The pharmacology of impulsive behaviour in rats VI: the effects of ethanol and selective serotonergic drugs on response choice with varying delays of reinforcement. Psychopharmacology (Berl) 146:413–421
Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481–1489
Faeh D, Viswanathan B, Chiolero A, Warren W, Bovet P (2006) Clustering of smoking, alcohol drinking and cannabis use in adolescents in a rapidly developing country. BMC Public Health 6:169
Fan X, Goff DC, Henderson DC (2007) Inflammation and schizophrenia. Expert Rev Neurother 7:789–796
Fatemi SH, Folsom TD (2009) The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr Bull 35:528–548
Fenton WS (2001) Comorbid conditions in schizophrenia. Curr Opin Psychiatr 14:17–23
Fernandez-Teruel A, Escorihuela RM, Castellano B, Gonzalez B, Tobena A (1997) Neonatal handling and environmental enrichment effects on emotionality, novelty/reward seeking, and age-related cognitive and hippocampal impairments: focus on the Roman rat lines. Behav Genet 27:513–526
Fernandez-Teruel A, Driscoll P, Gil L, Aguilar R, Tobena A, Escorihuela RM (2002a) Enduring effects of environmental enrichment on novelty seeking, saccharin and ethanol intake in two rat lines (RHA/Verh and RLA/Verh) differing in incentive-seeking behavior. Pharmacol Biochem Behav 73:225–231
Fernandez-Teruel A, Gimenez-Llort L, Escorihuela RM, Gil L, Aguilar R, Steimer T, Tobena A (2002b) Early-life handling stimulation and environmental enrichment: are some of their effects mediated by similar neural mechanisms? Pharmacol Biochem Behav 73:233–245
Fone KC, Porkess MV (2008) Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav R 32:1087–1102
Fortier ME, Joober R, Luheshi GN, Boksa P (2004) Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring. J Psychiatr Res 38:335–345
Fox C, Merali Z, Harrison C (2006) Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 175:1–8
Francis DD, Meaney MJ (1999) Maternal care and the development of stress responses. Curr Opin Neurobiol 9:128–134
Francis DD, Diorio J, Plotsky PM, Meaney MJ (2002) Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 22:7840–7843
Freud S (1918) From the history of an infantile neurosis. Hogarth Press, London
Fritzsche M (2001) Are cannabinoid receptor knockout mice animal models for schizophrenia? Med Hypotheses 56:638–643
Giedd JN (2008) The teen brain: insights from neuroimaging. J Adolesc Health 42:335–343
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 Psychiatr 48:465–470
Goggi J, Pullar IA, Carney SL, Bradford HF (2002) Modulation of neurotransmitter release induced by brain-derived neurotrophic factor in rat brain striatal slices in vitro. Brain Res 941:34–42
Gottesman II, Hanson DR (2005) Human development: biological and genetic processes. Annu Rev Psychol 56:263–286
Gotz AA, Stefanski V (2007) Psychosocial maternal stress during pregnancy affects serum corticosterone, blood immune parameters and anxiety behaviour in adult male rat offspring. Physiol Behav 90:108–115
Greaves-Lord K, Huizink AC, Oldehinkel AJ, Ormel J, Verhulst FC, Ferdinand RF (2009) Baseline cortisol measures and developmental pathways of anxiety in early adolescence. Acta psychiatrica Scandinavica 120:178–186
Grech A, Van Os J, Jones PB, Lewis SW, Murray RM (2005) Cannabis use and outcome of recent onset psychosis. Eur Psychiatr 20:349–353
Green AI, Canuso CM, Brenner MJ, Wojcik JD (2003) Detection and management of comorbidity in patients with schizophrenia. Psychiatr Clin North Am 26:115–139
Grojean S, Schroeder H, Pourie G, Charriaut-Marlangue C, Koziel V, Desor D, Vert P, Daval JL (2003) Histopathological alterations and functional brain deficits after transient hypoxia in the newborn rat pup: a long term follow-up. Neurobiol Dis 14:265–278
Guillin O, Abi-Dargham A, Laruelle M (2007) Neurobiology of dopamine in schizophrenia. Int Rev Neurobiol 78:1–39
Hall W, Degenhardt L (2008) Cannabis use and the risk of developing a psychotic disorder. World Psychiatr 7:68–71
Harlow HF, Harlow MK (1965) The affectional systems. In: Schrier AM, Harlow HF, Stollnitz, F (eds) Behavior of nonhuman primates. Academic Press, New York and London, pp 287–334
Harlow HF, Rowland GL, Griffin GA (1964) The effect of total social deprivation on the development of monkey behavior. Psychiatr Res Rep Am Psychiatr Assoc 19:116–135
Heim C, Nemeroff CB (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatr 49:1023–1039
Heim C, Newport DJ, Mletzko T, Miller AH, Nemeroff CB (2008) The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33:693–710
Iuvone L, Geloso MC, Dell’Anna E (1996) Changes in open field behavior, spatial memory, and hippocampal parvalbumin immunoreactivity following enrichment in rats exposed to neonatal anoxia. Exp Neurol 139:25–33
Johansen EB, Aase H, Meyer A, Sagvolden T (2002) Attention-deficit/hyperactivity disorder (ADHD) behaviour explained by dysfunctioning reinforcement and extinction processes. Behav Brain Res 130:37–45
Johnson MH (2005) Sensitive periods in functional brain development: problems and prospects. Dev Psychobiol 46:287–292
Kandel DB, Yamaguchi K, Chen K (1992) Stages of progression in drug involvement from adolescence to adulthood: further evidence for the gateway theory. J Stud Alcohol 53:447–457
Kelley AE, Schochet T, Landry CF (2004) Risk taking and novelty seeking in adolescence: introduction to part I. Ann NY Acad Sci 1021:27–32
Kendler KS, Sheth K, Gardner CO, Prescott CA (2002) Childhood parental loss and risk for first-onset of major depression and alcohol dependence: the time-decay of risk and sex differences. Psychol Med 32:1187–1194
Koenig JI, Elmer GI, Shepard PD, Lee PR, Mayo C, Joy B, Hercher E, Brady DL (2005) Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behav Brain Res 156:251–261
Kofman O (2002) The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci Biobehav Rev 26:457–470
Kolevzon A, Gross R, Reichenberg A (2007) Prenatal and perinatal risk factors for autism: a review and integration of findings. Arch Pediatr Adolesc Med 161:326–333
Kostrzewa RM, Reader TA, Descarries L (1998) Serotonin neural adaptations to ontogenetic loss of dopamine neurons in rat brain. J Neurochem 70:889–898
La Greca AM, Prinstein MJ, Fetter MD (2001) Adolescent peer crowd affiliation: linkages with health-risk behaviors and close friendships. J Pediatr Psychol 26:131–143
Lai S, Lai H, Page JB, McCoy CB (2000) The association between cigarette smoking and drug abuse in the United States. J Addict Dis 19:11–24
Laviola G, Adriani W, Terranova ML, Gerra G (1999) Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neurosci Biobehav Rev 23:993–1010
Laviola G, Macrì 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, Adriani W, Rea M, Aloe L, Alleva E (2004a) Social withdrawal, neophobia, and stereotyped behavior in developing rats exposed to neonatal asphyxia. Psychopharmacology (Berl) 175:196–205
Laviola G, Rea M, Morley-Fletcher S, Di Carlo S, Bacosi A, De Simone R, Bertini M, Pacifici R (2004b) Beneficial effects of enriched environment on adolescent rats from stressed pregnancies. Eur J Neurosci 20:1655–1664
Laviola G, Hannan AJ, Macrì 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 modelling 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 Womens Ment Health 11:363–375
Lee JH, Kim HJ, Kim JG, Ryu V, Kim BT, Kang DW, Jahng JW (2007a) Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci Res 58:32–39
Lee PR, Brady DL, Shapiro RA, Dorsa DM, Koenig JI (2007b) Prenatal stress generates deficits in rat social behavior: reversal by oxytocin. Brain Res 1156:152–167
Lehmann J, Pryce CR, Jongen-Relo AL, Stohr T, Pothuizen HH, Feldon J (2002) Comparison of maternal separation and early handling in terms of their neurobehavioral effects in aged rats. Neurobiol Aging 23:457–466
Lemaire V, Koehl M, Le Moal M, Abrous DN (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032–11037
Lemaire V, Lamarque S, Le Moal M, Piazza PV, Abrous DN (2006) Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol Psychiatr 59:786–792
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 (1957) Infantile experience and resistance to physiological stress. Science 126:405
Levine S (2000) Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. Eur J Pharmacol 405:149–160
Levine S (2005) Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 30:939–946
Levine S, Alpert M, Lewis GW (1957) Infantile experience and the maturation of the pituitary adrenal axis. Science 126:1347
Levine S, Huchton DM, Wiener SG, Rosenfeld P (1991) Time course of the effect of maternal deprivation on the hypothalamic-pituitary-adrenal axis in the infant rat. Dev Psychobiol 24:547–558
Leweke FM, Koethe D (2008) Cannabis and psychiatric disorders: it is not only addiction. Addict Biol 13:264–275
Leweke FM, Giuffrida A, Wurster U, Emrich HM, Piomelli D (1999) Elevated endogenous cannabinoids in schizophrenia. Neuroreport 10:1665–1669
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
Llorente E, Brito ML, Machado P, Gonzalez MC (2002) Effect of prenatal stress on the hormonal response to acute and chronic stress and on immune parameters in the offspring. J Physiol Biochem 58:143–149
Llorente R, Arranz L, Marco EM, Moreno E, Puerto M, Guaza C, De la FM, Viveros MP (2007) Early maternal deprivation and neonatal single administration with a cannabinoid agonist induce long-term sex-dependent psychoimmunoendocrine effects in adolescent rats. Psychoneuroendocrinology 32:636–650
Llorente R, Llorente-Berzal A, Petrosino S, Marco EM, Guaza C, Prada C, Lopez-Gallardo M, Di Marzo V, Viveros MP (2008) Gender-dependent cellular and biochemical effects of maternal deprivation on the hippocampus of neonatal rats: a possible role for the endocannabinoid system. Dev Neurobiol 68:1334–1347
Lockwood CA, Menter CG, Moggi-Cecchi J, Keyser AW (2007) Extended male growth in a fossil hominin species. Science 318:1443–1446
Lorenz K (1937/1957) The conception of instinctive behavior. In: Schiller CH (ed) Instinctive behavior. International Universities Press, New York, pp 129–175
Lowry CA, Hale MW, Evans AK, Heerkens J, Staub DR, Gasser PJ, Shekhar A (2008) Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 1148:86–94
Maccari S, Morley-Fletcher S (2007) Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32 Suppl 1:S10–S15
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
Mackowiak M, Chocyk A, Markowicz-Kula K, Wedzony K (2004) Neurogenesis in the adult brain. Pol J Pharmacol 56:673–687
Macrì S, Chiarotti F, Wurbel H (2008) Maternal separation and maternal care act independently on the development of HPA responses in male rats. Behav Brain Res 191:227–234
Macrì S, Laviola G (2004) Single episode of maternal deprivation and adult depressive profile in mice: interaction with cannabinoid exposure during adolescence. Behav Brain Res 154:231–238
Macrì S, Wurbel H (2006) Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm Behav 50:667–680
Macrì S, Mason GJ, Wurbel H (2004) Dissociation in the effects of neonatal maternal separations on maternal care and the offspring’s HPA and fear responses in rats. Eur J Neurosci 20:1017–1024
Macrì S, Pasquali P, Bonsignore LT, Pieretti S, Cirulli F, Chiarotti F, Laviola G (2007a) Moderate neonatal stress decreases within-group variation in behavioral, immune and HPA responses in adult mice. PLoS One 2:e1015
Macrì S, Spinelli S, Adriani W, Dee Higley J, Laviola G (2007b) Early adversity and alcohol availability persistently modify serotonin and hypothalamic-pituitary-adrenal-axis metabolism and related behavior: what experimental research on rodents and primates can tell us. Neurosci Biobehav Rev 31:172–180
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
Maneru C, Junque C, Botet F, Tallada M, Guardia J (2001) Neuropsychological long-term sequelae of perinatal asphyxia. Brain Inj 15:1029–1039
Marchetti B, Morale MC, Testa N, Tirolo C, Caniglia S, Amor S, Dijkstra CD, Barden N (2001) Stress, the immune system and vulnerability to degenerative disorders of the central nervous system in transgenic mice expressing glucocorticoid receptor antisense RNA. Brain Res Brain Res Rev 37:259–272
Marco EM, Granstrem O, Moreno E, Llorente R, Adriani W, Laviola G, Viveros MP (2007) Subchronic nicotine exposure in adolescence induces long-term effects on hippocampal and striatal cannabinoid-CB1 and mu-opioid receptors in rats. Eur J Pharmacol 557:37–43
Marco EM, Adriani W, Llorente R, Laviola G, Viveros MP (2009) Detrimental psychophysiological effects of early maternal deprivation in adolescent and adult rodents: altered responses to cannabinoid exposure. Neurosci Biobehav Rev 33:498–507
Matthews K, Robbins TW (2003) Early experience as a determinant of adult behavioural responses to reward: the effects of repeated maternal separation in the rat. Neurosci Biobehav Rev 27:45–55
McBride WJ, Bell RL, Rodd ZA, Strother WN, Murphy JM (2005) Adolescent alcohol drinking and its long-range consequences. Studies with animal models. Recent Dev Alcohol 17:123–142
Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–1192
Meaney MJ, Diorio J, Francis D, Weaver S, Yau J, Chapman K, Seckl JR (2000) Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: the effects of thyroid hormones and serotonin. J Neurosci 20:3926–3935
Meijer A (1985) Child psychiatric sequelae of maternal war stress. Acta Psychiatr Scand 72:505–511
Merlot E, Couret D, Otten W (2008) Prenatal stress, fetal imprinting and immunity. Brain Behav Immun 22:42–51
Meyer U, Feldon J, Fatemi SH (2009) In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci Biobehav Rev 33:1061–1079
Michel GF, Tyler AN (2005) Critical period: a history of the transition from questions of when, to what, to how. Dev Psychobiol 46:156–162
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 49:1020–1030
Mittal VA, Ellman LM, Cannon TD (2008) Gene-environment interaction and covariation in schizophrenia: the role of obstetric complications. Schizophr Bull 34:1083–1094
Moffett MC, Vicentic A, Kozel M, Plotsky P, Francis DD, Kuhar MJ (2007) Maternal separation alters drug intake patterns in adulthood in rats. Biochem Pharmacol 73:321–330
Montoya AG, Sorrentino R, Lukas SE, Price BH (2002) Long-term neuropsychiatric consequences of “ecstasy” (MDMA): a review. Harv Rev Psychiatr 10:212–220
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, Darnaudery M, Koehl M, Casolini P, Van Reeth O, Maccari S (2003a) Prenatal stress in rats predicts immobility behavior in the forced swim test. Effects of a chronic treatment with tianeptine. Brain Res 989:246–251
Morley-Fletcher S, Rea M, Maccari S, Laviola G (2003b) Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 18:3367–3374
Moy SS, Nadler JJ (2008) Advances in behavioral genetics: mouse models of autism. Mol Psychiatr 13:4–26
Muller N, Riedel M, Gruber R, Ackenheil M, Schwarz MJ (2000) The immune system and schizophrenia. An integrative view. Ann NY Acad Sci 917:456–467
Nemeroff CB, Owens MJ (2009) The role of serotonin in the pathophysiology of depression: as important as ever. Clin Chem 55:1578–1579
Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697–709
Nocjar C, Roth BL, Pehek EA (2002) Localization of 5-HT(2A) receptors on dopamine cells in subnuclei of the midbrain A10 cell group. Neuroscience 111:163–176
Nowakowski RS, Hayes NL (1999) CNS development: an overview. Dev Psychopathol 11:395–417
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’Shea M, Singh ME, McGregor IS, Mallet PE (2004) Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J Psychopharmacol 18:502–508
O’Tuathaigh CM, Babovic D, O’Meara G, Clifford JJ, Croke DT, Waddington JL (2007) Susceptibility genes for schizophrenia: characterisation of mutant mouse models at the level of phenotypic behaviour. Neurosci Biobehav Rev 31:60–78
Painter MJ (1995) Animal models of perinatal asphyxia: contributions, contradictions, clinical relevance. Semin Pediatr Neurol 2:37–56
Patterson PH (2007) Neuroscience. Maternal effects on schizophrenia risk. Science 318:576–577
Patterson PH (2009) Immune involvement in schizophrenia and autism: etiology, pathology and animal models. Behav Brain Res 204:313–321
Penner JD, Brown AS (2007) Prenatal infectious and nutritional factors and risk of adult schizophrenia. Expert Rev Neurother 7:797–805
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
Pereira LO, Nabinger PM, Strapasson AC, Nardin P, Goncalves CA, Siqueira IR, Netto CA (2009) Long-term effects of environmental stimulation following hypoxia-ischemia on the oxidative state and BDNF levels in rat hippocampus and frontal cortex. Brain Res 1247:188–195
Phillips LJ, McGorry PD, Garner B, Thompson KN, Pantelis C, Wood SJ, Berger G (2006) Stress, the hippocampus and the hypothalamic-pituitary-adrenal axis: implications for the development of psychotic disorders. Aust NZ J Psychiatr 40:725–741
Pickering C, Gustafsson L, Cebere A, Nylander I, Liljequist S (2006) Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res 1099:101–108
Piper BJ (2007) A developmental comparison of the neurobehavioral effects of ecstasy (MDMA). Neurotoxicol Teratol 29:288–300
Plotsky PM, Meaney MJ (1993) Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 18:195–200
Primus RJ, Kellogg CK (1989) Pubertal-related changes influence the development of environment-related social interaction in the male rat. Dev Psychobiol 22:633–643
Pryce CR, Feldon J (2003) Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev 27:57–71
Raju TN (1992) Some animal models for the study of perinatal asphyxia. Biol Neonate 62:202–214
Rasmuson S, Olsson T, Henriksson BG, Kelly PA, Holmes MC, Seckl JR, Mohammed AH (1998) Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus. Brain Res Mol Brain Res 53:285–290
Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108 (Suppl 3):511–533
Rice F, Jones I, Thapar A (2007) The impact of gestational stress and prenatal growth on emotional problems in offspring: a review. Acta Psychiatr Scand 115:171–183
Rice F, Harold GT, Boivin J, van den Bree M, Hay DF, Thapar A (2009) The links between prenatal stress and offspring development and psychopathology: disentangling environmental and inherited influences. Psychol Med 1–11
Roceri M, Hendriks W, Racagni G, Ellenbroek BA, Riva MA (2002) Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatr 7:609–616
Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65
Rosenzweig MR, Bennett EL, Hebert M, Morimoto H (1978) Social grouping cannot account for cerebral effects of enriched environments. Brain Res 153:563–576
Rozeboom AM, Akil H, Seasholtz AF (2007) Mineralocorticoid receptor overexpression in forebrain decreases anxiety-like behavior and alters the stress response in mice. Proc Natl Acad Sci USA 104:4688–4693
Rubino T, Parolaro D (2008) Long lasting consequences of cannabis exposure in adolescence. Mol Cell Endocrinol 286:S108–S113
Ruedi-Bettschen D, Pedersen EM, Feldon J, Pryce CR (2005) Early deprivation under specific conditions leads to reduced interest in reward in adulthood in Wistar rats. Behav Brain Res 156:297–310
Rufini O, Valanzano A, Calamandrei G (2001) Animal models of hypoxic-ischemic encephalopathy. Ann Ist Super Sanita 37:561–566
Sarkar NN (2008) The impact of intimate partner violence on women’s reproductive health and pregnancy outcome. J Obstet Gynaecol 28:266–271
Sawamura N, Sawa A (2006) Disrupted-in-schizophrenia-1 (DISC1): a key susceptibility factor for major mental illnesses. Ann NY Acad Sci 1086:126–133
Scheepens A, Wassink G, Blanco CE (2003) The effect of a global birth asphyxia on the ontogeny of BDNF and NGF protein expression in the juvenile brain. Brain Res Dev Brain Res 140:215–221
Schepis TS, Adinoff B, Rao U (2008) Neurobiological processes in adolescent addictive disorders. Am J Addict 17:6–23
Schiepers OJ, Wichers MC, Maes M (2005) Cytokines and major depression. Prog Neuropsychopharmacol Biol Psychiatr 29:201–217
Schmidt M, Enthoven L, van Woezik JH, Levine S, de Kloet ER, Oitzl MS (2004) The dynamics of the hypothalamic-pituitary-adrenal axis during maternal deprivation. J Neuroendocrinol 16:52–57
Schneider M (2008) Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict Biol 13:253–263
Schneider M, Koch M (2003) Chronic pubertal, but not adult chronic cannabinoid treatment impairs sensorimotor gating, recognition memory, and the performance in a progressive ratio task in adult rats. Neuropsychopharmacology 28:1760–1769
Schneirla TC, Rosenblatt JS (1963) “Critical Periods” in the Development of Behavior. Science 139:1110–1115
Schwarz MJ, Chiang S, Muller N, Ackenheil M (2001) T-helper-1 and T-helper-2 responses in psychiatric disorders. Brain Behav Immun 15:340–370
Scott JP (1962) Critical periods in behavioral development. Science 138:949–958
Scott J, McNeill Y, Cavanagh J, Cannon M, Murray R (2006) Exposure to obstetric complications and subsequent development of bipolar disorder: systematic review. Br J Psychiatr 189:3–11
Shea A, Walsh C, Macmillan H, Steiner M (2005) Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females. Psychoneuroendocrinology 30:162–178
Shi L, Fatemi SH, Sidwell RW, Patterson PH (2003) Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 23:297–302
Siqueira LM, Brook JS (2003) Tobacco use as a predictor of illicit drug use and drug-related problems in Colombian youth. J Adolesc Health 32:50–57
Skosnik PD, Spatz-Glenn L, Park S (2001) Cannabis use is associated with schizotypy and attentional disinhibition. Schizophr Res 48:83–92
Slotkin TA (2002) Nicotine and the adolescent brain: insights from an animal model. Neurotoxicol Teratol 24:369–384
Slotkin TA, MacKillop EA, Rudder CL, Ryde IT, Tate CA, Seidler FJ (2007) Permanent, sex-selective effects of prenatal or adolescent nicotine exposure, separately or sequentially, in rat brain regions: indices of cholinergic and serotonergic synaptic function, cell signaling, and neural cell number and size at 6 months of age. Neuropsychopharmacology 32:1082–1097
Smotherman WP, Bell RW (1980) Maternal mediation of early experience. In: Smotherman WP, Bell RL (eds) Maternal influences and early behavior. Spectrum, New York, pp 201–210
Sondeijker FE, Ferdinand RF, Oldehinkel AJ, Tiemeier H, Ormel J, Verhulst FC (2008) HPA-axis activity as a predictor of future disruptive behaviors in young adolescents. Psychophysiology 45:398–404
Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463
Stein DJ (2008) Depression, anhedonia, and psychomotor symptoms: the role of dopaminergic neurocircuitry. CNS Spectr 13:561–565
Stern JM, Johnson SK (1990) Ventral somatosensory determinants of nursing behavior in Norway rats. I. Effects of variations in the quality and quantity of pup stimuli. Physiol Behav 47:993–1011
Strous RD, Shoenfeld Y (2006) Schizophrenia, autoimmunity and immune system dysregulation: a comprehensive model updated and revisited. J Autoimmun 27:71–80
Suárez J, Llorente R, Romero-Zerbo SY, Mateos B, Bermudez-Silva FJ, de Fonseca FR, Viveros MP (2009) Early maternal deprivation induces gender-dependent changes on the expression of hippocampal CB(1) and CB(2) cannabinoid receptors of neonatal rats. Hippocampus 19:623–632
Suchecki D, Tufik S (1997) Long-term effects of maternal deprivation on the corticosterone response to stress in rats. Am J Physiol 273:R1332–R1338
Susman EJ (2006) Psychobiology of persistent antisocial behavior: stress, early vulnerabilities and the attenuation hypothesis. Neurosci Biobehav Rev 30:376–389
Talge NM, Neal C, Glover V (2007) Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatr 48:245–261
Teicher MH, Tomoda A, Andersen SL (2006) Neurobiological consequences of early stress and childhood maltreatment: are results from human and animal studies comparable? Ann NY Acad Sci 1071:313–323
Terranova ML, Laviola G, de Acetis L, Alleva E (1998) A description of the ontogeny of mouse agonistic behavior. J Comp Psychol 112:3–12
Tohmi M, Tsuda N, Watanabe Y, Kakita A, Nawa H (2004) Perinatal inflammatory cytokine challenge results in distinct neurobehavioral alterations in rats: implication in psychiatric disorders of developmental origin. Neurosci Res 50:67–75
Tuchscherer M, Kanitz E, Otten W, Tuchscherer A (2002) Effects of prenatal stress on cellular and humoral immune responses in neonatal pigs. Vet Immunol Immunopathol 86:195–203
Ujike H, Morita Y (2004) New perspectives in the studies on endocannabinoid and cannabis: cannabinoid receptors and schizophrenia. J Pharmacol Sci 96:376–381
Van den Hove DL, Steinbusch HW, Scheepens A, Van de Berg WD, Kooiman LA, Boosten BJ, Prickaerts J, Blanco CE (2006) Prenatal stress and neonatal rat brain development. Neuroscience 137:145–155
van Handel M, Swaab H, de Vries LS, Jongmans MJ (2007) Long-term cognitive and behavioral consequences of neonatal encephalopathy following perinatal asphyxia: a review. Eur J Pediatr 166:645–654
van Oers HJ, de Kloet ER, Levine S (1997) Persistent, but paradoxical, effects on HPA regulation of infants maternally deprived at different ages. Stress 1:249–262
van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191–198
Vanderschuren LJ, Niesink RJ, Van Ree JM (1997) The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 21:309–326
Vidal J, Bie J, Granneman RA, Wallinga AE, Koolhaas JM, Buwalda B (2007) Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity. Physiol behav 92:824–830
Wakuda T, Matsuzaki H, Suzuki K, Iwata Y, Shinmura C, Suda S, Iwata K, Yamamoto S, Sugihara G, Tsuchiya KJ, Ueki T, Nakamura K, Nakahara D, Takei N, Mori N (2008) Perinatal asphyxia reduces dentate granule cells and exacerbates methamphetamine-induced hyperlocomotion in adulthood. PLoS One 3:e3648
Ward IL, Stehm KE (1991) Prenatal stress feminizes juvenile play patterns in male rats. Physiol Behav 50:601–605
Watanabe Y, Hashimoto S, Kakita A, Takahashi H, Ko J, Mizuno M, Someya T, Patterson PH, Nawa H (2004) Neonatal impact of leukemia inhibitory factor on neurobehavioral development in rats. Neurosci Res 48:345–353
Weaver IC, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854
Weininger O (1954) Physiological damage under emotional stress as a function of early experience. Science 119:285–286
Weininger O, Mc CW, Arima RK (1954) Gentling and weight gain in the albino rat. Can J Psychol 8:147–151
Weinstock M (2002) Can the behaviour abnormalities induced by gestational stress in rats be prevented or reversed? Stress 5:167–176
Weinstock M (2007) Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 32:1730–1740
Weinstock M (2008) The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32:1073–1086
Wetzels JJ, Kremers SP, Vitoria PD, de Vries H (2003) The alcohol-tobacco relationship: a prospective study among adolescents in six European countries. Addiction 98:1755–1763
Yolken RH, Karlsson H, Yee F, Johnston-Wilson NL, Torrey EF (2000) Endogenous retroviruses and schizophrenia. Brain Res Brain Res Rev 31:193–199
Zimmerberg B, Shartrand AM (1992) Temperature-dependent effects of maternal separation on growth, activity, and amphetamine sensitivity in the rat. Dev Psychobiol 25:213–226
Zuckerman L, Rehavi M, Nachman R, Weiner I (2003) Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 28:1778–1789
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
Acknowledgements
Supported by the collaborative program NIH–ISS 0F14 and by FP6-Program ERARE-EuroRETT Network (to GL). EM Marco has been supported by a post-doctoral fellowship from the Spanish ‘Ministerio de Ciencia e Innovación (MCINN)’, and is now at the Departamento de Fisiología (Fisiología Animal II) (planta 13, despacho 16) Facultad de CC. Biológicas Universidad Complutense de Madrid, Madrid (Spain). S Macrì has been supported by a NARSAD young investigator award. G.L. and S.M. acknowledge the support by the project ‘ECS-EMOTION’ from the Department of Antidrug Policies c/o Presidency of the Council of Ministers, Italy. We would also like to acknowledge our expert colleagues that contributed to the original research data presented: W. Adriani, S. Morley-Fletcher, M. Rea and L. Aloe.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marco, E.M., Macrì, S. & Laviola, G. Critical Age Windows for Neurodevelopmental Psychiatric Disorders: Evidence from Animal Models. Neurotox Res 19, 286–307 (2011). https://doi.org/10.1007/s12640-010-9205-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12640-010-9205-z