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Adaptive and Maladaptive Regulations in Response to Environmental Stress in Adolescent Rodents

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Adaptive and Maladaptive Aspects of Developmental Stress

Part of the book series: Current Topics in Neurotoxicity ((Current Topics Neurotoxicity,volume 3))

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Abstract

Adolescent mammals exhibit a plethora of age-specific behaviours that mark a discontinuity with earlier stages of life and prepare the individual to the challenges of adulthood. Stress sensitivity during adolescence is remarkably different from earlier and later maturational stages. Specifically, although adolescent and adult mammals mount a similar endocrine response to external stressors, such response is excessively prolonged in adolescents. This unique response profile may relate to an asynchronous developmental profile of the several components of the hypothalamic–pituitary–adrenocortical axis. Experiential factors encountered throughout this period are thus likely to persistently adjust long-term regulations to the adult environment. Such age-specific developmental plasticity entails both risks and opportunities. Whilst being sensitive to external stimulation favours the integration of external cues into the mature function, the latter may result pathologic if inappropriately stimulated. For example, precocious experience with drugs of abuse or exposure to adverse environments may favour the onset of conduct disorders (e.g. addiction, emotional disturbances). In this chapter we describe the inextricable link between adolescent plasticity and long-term individual regulations both in terms of predisposition to pathology and in terms of adaptive plasticity to the adult environment.

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References

  • Adriani W, Laviola G (2000) A unique hormonal and behavioral hyporesponsivity to both forced novelty and d-amphetamine in periadolescent mice. Neuropharmacology 39:334–346

    Article  PubMed  CAS  Google Scholar 

  • Adriani W, Laviola G (2004) Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav Pharmacol 15:341–352

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Adriani W, Deroche-Gamonet V, Le Moal M, Laviola G, Piazza PV (2006) Preexposure during or following adolescence differently affects nicotine-rewarding properties in adult rats. Psychopharmacology (Berl) 184:382–390

    Article  CAS  Google Scholar 

  • Andersen SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27:3–18

    Article  PubMed  Google Scholar 

  • Andersen SL, Teicher MH (2008) Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci 31:183–191

    Article  PubMed  CAS  Google Scholar 

  • Bingham B, McFadden K, Zhang X, Bhatnagar S, Beck S, Valentino R (2011) Early adolescence as a critical window during which social stress distinctly alters behavior and brain norepinephrine activity. Neuropsychopharmacology 36:896–909

    Article  PubMed  CAS  Google Scholar 

  • Brenhouse HC, Sonntag KC, Andersen SL (2008) Transient D1 dopamine receptor expression on prefrontal cortex projection neurons: relationship to enhanced motivational salience of drug cues in adolescence. J Neurosci 28:2375–2382

    Article  PubMed  CAS  Google Scholar 

  • Cirulli F, Terranova ML, Laviola G (1996) Affiliation in periadolescent rats: behavioral and corticosterone response to social reunion with familiar or unfamiliar partners. Pharmacol Biochem Behav 54:99–105

    Article  PubMed  CAS  Google Scholar 

  • Ellis BJ, Del Giudice M, Dishion TJ, Figueredo AJ, Gray P etal (2012) The evolutionary basis of risky adolescent behavior: implications for science, policy, and practice. Dev Psychol 48:598–623

    Article  PubMed  Google Scholar 

  • Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447:178–182

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H etal (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2:861–863

    Article  PubMed  CAS  Google Scholar 

  • Hebb DO (1947) The effects of early experience on problem solving at maturity. Am Psychol 2:306–307

    Google Scholar 

  • Heim C, Nemeroff CB (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49:1023–1039

    Article  PubMed  CAS  Google Scholar 

  • Hollon SD, Munoz RF, Barlow DH, Beardslee WR, Bell CC etal (2002) Psychosocial intervention development for the prevention and treatment of depression: promoting innovation and increasing access. Biol Psychiatry 52:610–630

    Article  PubMed  Google Scholar 

  • Laviola G, Adriani W (1998) Evaluation of unconditioned novelty-seeking and d-amphetamine-conditioned motivation in mice. Pharmacol Biochem Behav 59:1011–1020

    Article  PubMed  CAS  Google Scholar 

  • Laviola G, Terranova ML (1998) The developmental psychobiology of behavioural plasticity in mice: the role of social experiences in the family unit. Neurosci Biobehav Rev 23:197–213

    Article  PubMed  CAS  Google Scholar 

  • Laviola G, Wood RD, Kuhn C, Francis R, Spear LP (1995) Cocaine sensitization in periadolescent and adult rats. J Pharmacol Exp Ther 275:345–357

    PubMed  CAS  Google Scholar 

  • Laviola G, Adriani W, Morley-Fletcher S, Terranova ML (2002) Peculiar response of adolescent mice to acute and chronic stress and to amphetamine: evidence of sex differences. Behav Brain Res 130:117–125

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Laviola G, Rea M, Morley-Fletcher S, Di Carlo S, Bacosi A etal (2004) Beneficial effects of enriched environment on adolescent rats from stressed pregnancies. Eur J Neurosci 20:1655–1664

    Article  PubMed  Google Scholar 

  • 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(2):159–168

    Article  PubMed  Google Scholar 

  • Lenroot RK, Giedd JN (2008) The changing impact of genes and environment on brain development during childhood and adolescence: initial findings from a neuroimaging study of pediatric twins. Dev Psychopathol 20:1161–1175

    Article  PubMed  Google Scholar 

  • Lenroot RK, Schmitt JE, Ordaz SJ, Wallace GL, Neale MC etal (2009) Differences in genetic and environmental influences on the human cerebral cortex associated with development during childhood and adolescence. Hum Brain Mapp 30:163–174

    Article  PubMed  Google Scholar 

  • Leussis MP, Andersen SL (2008) Is adolescence a sensitive period for depression? Behavioral and neuroanatomical findings from a social stress model. Synapse 62:22–30

    Article  PubMed  CAS  Google Scholar 

  • Leussis MP, Lawson K, Stone K, Andersen SL (2008) The enduring effects of an adolescent social stressor on synaptic density, part II: poststress reversal of synaptic loss in the cortex by adinazolam and MK-801. Synapse 62:185–192

    Article  PubMed  CAS  Google Scholar 

  • Lurzel S, Kaiser S, Sachser N (2011) Social interaction decreases stress responsiveness during adolescence. Psychoneuroendocrinology 36:1370–1377

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Marco EM, Macri S, Laviola G (2011) Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models. Neurotox Res 19:286–307

    Article  PubMed  Google Scholar 

  • McQuaid RJ, Audet MC, Anisman H (2012) Environmental enrichment in male CD-1 mice promotes aggressive behaviors and elevated corticosterone and brain norepinephrine activity in response to a mild stressor. Stress 15:354–360

    PubMed  CAS  Google Scholar 

  • Morley-Fletcher S, Rea M, Maccari S, Laviola G (2003) 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

    Article  PubMed  Google Scholar 

  • Nestler EJ, Carlezon WA Jr (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59:1151–1159

    Article  PubMed  CAS  Google Scholar 

  • Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697–709

    Article  PubMed  CAS  Google Scholar 

  • Oldehinkel AJ, Bouma EM (2011) Sensitivity to the depressogenic effect of stress and HPA-axis reactivity in adolescence: a review of gender differences. Neurosci Biobehav Rev 35:1757–1770

    Article  PubMed  CAS  Google Scholar 

  • Porsolt RD, Bertin A, Jalfre M (1977a) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229:327–336

    PubMed  CAS  Google Scholar 

  • Porsolt RD, Le Pichon M, Jalfre M (1977b) Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730–732

    Article  PubMed  CAS  Google Scholar 

  • Potegal M, Einon D (1989) Aggressive behaviors in adult rats deprived of playfighting experience as juveniles. Dev Psychobiol 22:159–172

    Article  PubMed  CAS  Google Scholar 

  • Pryce CR (2008) Postnatal ontogeny of expression of the corticosteroid receptor genes in mammalian brains: inter-species and intra-species differences. Brain Res Rev 57:596–605

    Article  PubMed  CAS  Google Scholar 

  • Pryce CR, Ruedi-Bettschen D, Dettling AC, Weston A, Russig H etal (2005) Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci Biobehav Rev 29:649–674

    Article  PubMed  Google Scholar 

  • Rajji TK, Ismail Z, Mulsant BH (2009) Age at onset and cognition in schizophrenia: meta-analysis. Br J Psychiatry 195:286–293

    Article  PubMed  CAS  Google Scholar 

  • Romeo RD (2010) Adolescence: a central event in shaping stress reactivity. Dev Psychobiol 52:244–253

    PubMed  Google Scholar 

  • Romeo RD, Richardson HN, Sisk CL (2002) Puberty and the maturation of the male brain and sexual behavior: recasting a behavioral potential. Neurosci Biobehav Rev 26:381–391

    Article  PubMed  Google Scholar 

  • Romeo RD, Lee SJ, Chhua N, McPherson CR, McEwen BS (2004) Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology 79:125–132

    Article  PubMed  CAS  Google Scholar 

  • Romeo RD, Bellani R, Karatsoreos IN, Chhua N, Vernov M etal (2006) Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. Endocrinology 147:1664–1674

    Article  PubMed  CAS  Google Scholar 

  • Rosenzweig MR, Bennett EL, Hebert M, Morimoto H (1978) Social grouping cannot account for cerebral effects of enriched environments. Brain Res 153:563–576

    Article  PubMed  CAS  Google Scholar 

  • Sachser N (1993) The ability to arrange with conspecifics depends on social experiences around puberty. Physiol Behav 53:539–544

    Article  PubMed  CAS  Google Scholar 

  • Sachser N, Lick C (1991) Social experience, behavior, and stress in guinea pigs. Physiol Behav 50:83–90

    Article  PubMed  CAS  Google Scholar 

  • Sachser N, Lick C, Stanzel K (1994) The environment, hormones, and aggressive behaviour: a 5-year-study in guinea pigs. Psychoneuroendocrinology 19:697–707

    Article  PubMed  CAS  Google Scholar 

  • Sachser N, Hennessy MB, Kaiser S (2011) Adaptive modulation of behavioural profiles by social stress during early phases of life and adolescence. Neurosci Biobehav Rev 35:1518–1533

    Article  PubMed  Google Scholar 

  • Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL etal (2001) Voxel-based morphometric analyses of the brain in children and adolescents prenatally exposed to alcohol. Neuroreport 12:515–523

    Article  PubMed  CAS  Google Scholar 

  • Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463

    Article  PubMed  CAS  Google Scholar 

  • Spear LP, Brake SC (1983) Periadolescence: age-dependent behavior and psychopharmacological responsivity in rats. Dev Psychobiol 16:83–109

    Article  PubMed  CAS  Google Scholar 

  • Spear LP, Varlinskaya EI (2005) Adolescence. Alcohol sensitivity, tolerance, and intake. Recent Dev Alcohol 17:143–159

    Article  PubMed  Google Scholar 

  • Terranova ML, Laviola G, Alleva E (1993) Ontogeny of amicable social behavior in the mouse: gender differences and ongoing isolation outcomes. Dev Psychobiol 26:467–481

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Terranova ML, Cirulli F, Laviola G (1999) Behavioral and hormonal effects of partner familiarity in periadolescent rat pairs upon novelty exposure. Psychoneuroendocrinology 24:639–656

    Article  PubMed  CAS  Google Scholar 

  • Thompson PM, Cannon TD, Narr KL, van Erp T, Poutanen VP etal (2001a) Genetic influences on brain structure. Nat Neurosci 4:1253–1258

    Article  PubMed  CAS  Google Scholar 

  • Thompson PM, Vidal C, Giedd JN, Gochman P, Blumenthal J etal (2001b) Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia. Proc Natl Acad Sci U S A 98:11650–11655

    Article  PubMed  CAS  Google Scholar 

  • Tillerson JL, Caudle WM, Reveron ME, Miller GW (2003) Exercise induces behavioral recovery and attenuates neurochemical deficits in rodent models of Parkinson’s disease. Neuroscience 119:899–911

    Article  PubMed  CAS  Google Scholar 

  • Toth M, Mikics E, Tulogdi A, Aliczki M, Haller J (2011) Post-weaning social isolation induces abnormal forms of aggression in conjunction with increased glucocorticoid and autonomic stress responses. Horm Behav 60:28–36

    Article  PubMed  CAS  Google Scholar 

  • van Dellen A, Blakemore C, Deacon R, York D, Hannan AJ (2000) Delaying the onset of Huntington’s in mice. Nature 404:721–722

    Article  PubMed  Google Scholar 

  • van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266–270

    Article  PubMed  Google Scholar 

  • West-Eberhard MJ (2005) Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U S A 102(suppl 1):6543–6549

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the grant “ECS-EMOTION” from the Department of Antidrug Policies c/o Presidency of the Council of Ministers, Italy to GL and SM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

  1. Section of Behavioral Neuroscience, Department of Cell Biology and Neurosciences, Istituto Superiore di Sanità, Viale Regina Elena 299 (Block 19, Floor D, Room 15), Rome, 00161, Italy

    Simone Macrì & Giovanni Laviola

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  1. Simone Macrì
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  2. Giovanni Laviola
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Correspondence to Simone Macrì .

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  1. Istituto Superiore di Sanità, 299 Viale Regina Elena, Rome, 00161, Italy

    Giovanni Laviola

  2. Istituto Superiore di Sanità, 299 Viale Regina Elena, Rome, 00161, Italy

    Simone Macrì

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Macrì, S., Laviola, G. (2013). Adaptive and Maladaptive Regulations in Response to Environmental Stress in Adolescent Rodents. In: Laviola, G., Macrì, S. (eds) Adaptive and Maladaptive Aspects of Developmental Stress. Current Topics in Neurotoxicity, vol 3. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5605-6_12

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