Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models

Marco, Eva M.; Macrì, Simone; Laviola, Giovanni

doi:10.1007/s12640-010-9205-z

Cited by 144Maternal Mental Health During Pregnancy and PostpartumStress Responses and CortisolNeurogenesis and neuroplasticity mechanisms

Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models

Marco, Eva M., Macrì, Simone, Laviola, Giovanni·2011·Neurotoxicity Research

DOI 10.1007/s12640-010-9205-z

Open this paper in CoChat — free account

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.

Integrity signals

Registry

Crossref · 10.1007/s12640-010-9205-z

Cites

260 of 260 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Adolescence is a critical period for social interaction and the emergence of psychiatric diseases.
“Indeed, adolescence is a critical period for not only social interaction (Larsen and Luna, 2018; ) but also the emergence of psychiatric diseases (Orben et al., 2020; Marco et al., 2011), and social isolation during adolescence can exacerbate mental health problems (Larsen and Luna, 2018; Almeida et al., 2021; ; Graf et al., 2021; Andersen, 2021).”
From Oxytocin neurons mediate the effect of social isolation via the VTA circuits (2022) · cites this paper as Marco et al., 2011

1 retracted

Retracted: Maternal and early life stress effects on immune function: relevance to immunotoxicology
Bellinger, D. L., Lubahn, C. L., & Lorton, D. (2008) · Journal of Immunotoxicology · doi:10.1080/15476910802483415 · Cited by 64 · see citing works
Retracted
Untitled work
(1969) · Cited by 18,340 · see citing works
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
Neural systems of reinforcement for drug addiction: from actions to habits to compulsion
Everitt, B. J., & Robbins, T. W. (2005) · Nature Neuroscience · doi:10.1038/nn1579 · Cited by 3,785 · see citing works
<i>The Adolescent Brain</i>
Casey, B. J., Jones, R. M., & Hare, T. A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1440.010 · Cited by 3,345 · see citing works
Maternal Care, Hippocampal Glucocorticoid Receptors, and Hypothalamic-Pituitary-Adrenal Responses to Stress
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170 · see citing works
Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models.
Rice, D., & Barone, S. (2000) · Environmental Health Perspectives · doi:10.1289/ehp.00108s3511 · Cited by 2,944 · see citing works
The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies
Heim, C., & Nemeroff, C. B. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01157-x · Cited by 2,791 · see citing works
Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
Neural consequences of enviromental enrichment
van Praag, H., Kempermann, G., & Gage, F. H. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044558 · Cited by 2,468 · see citing works
Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity
BOYCE, W. T., & ELLIS, B. J. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050145 · Cited by 2,078 · see citing works
The social brain in adolescence
Blakemore, S.-J. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2353 · Cited by 1,896 · see citing works
Enriched environments, experience-dependent plasticity and disorders of the nervous system
Nithianantharajah, J., & Hannan, A. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1970 · Cited by 1,771 · see citing works
The link between childhood trauma and depression: insights from HPA axis studies in humans
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.03.008 · Cited by 1,704 · see citing works
Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
Trajectories of brain development: point of vulnerability or window of opportunity?
Andersen, S. L. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00005-8 · Cited by 1,503 · see citing works
Antenatal maternal stress and long‐term effects on child neurodevelopment: how and why?
Talge, N. M., Neal, C., Glover, V., & the Early Stress, T. R. A. P. S. N. F. A. N. E. O. C. A. A. M. H. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01714.x · Cited by 1,349 · see citing works
Attention-Deficit/Hyperactivity Disorder: A Selective Overview
Biederman, J. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.10.020 · Cited by 1,343 · see citing works
Cytokines and major depression
Schiepers, O. J. G., Wichers, M. C., & Maes, M. (2005) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2004.11.003 · Cited by 1,235 · see citing works
Obstetric Complications and Schizophrenia: Historical and Meta-Analytic Review
Cannon, M. D., Jones, P. B., & Murray, R. M. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.7.1080 · Cited by 1,138 · see citing works
The long-term behavioural consequences of prenatal stress
Weinstock, M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.002 · Cited by 1,045 · see citing works
Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus
Lemaire, V., Koehl, M., Le Moal, M., & Abrous, D. N. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.20.11032 · Cited by 1,044 · see citing works
Stages of progression in drug involvement from adolescence to adulthood: further evidence for the gateway theory.
Kandel, D. B., Yamaguchi, K., & Chen, K. (1992) · Journal of Studies on Alcohol · doi:10.15288/jsa.1992.53.447 · Cited by 1,039 · see citing works
Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring
Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00297.2003 · Cited by 1,025 · see citing works
Stress, sensitive periods and maturational events in adolescent depression
Andersen, S. L., & Teicher, M. H. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.01.004 · Cited by 1,005 · see citing works
Stress Hormones, Proinflammatory and Antiinflammatory Cytokines, and Autoimmunity
ELENKOV, I. J., & CHROUSOS, G. P. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04229.x · Cited by 983 · see citing works
Developmental psychiatry comes of age
(1988) · American Journal of Psychiatry · doi:10.1176/ajp.145.1.1 · Cited by 978 · see citing works
Psychobiology of plasticity: Effects of training and experience on brain and behavior
Rosenzweig, M. R., & Bennett, E. L. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00216-2 · Cited by 972 · see citing works
Behavioural and neurochemical effects of post-weaning social isolation in rodents—Relevance to developmental neuropsychiatric disorders
Fone, K. C. F., & Porkess, M. V. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.003 · Cited by 864 · see citing works
The Neurodevelopmental Hypothesis of Schizophrenia, Revisited
Fatemi, S. H., & Folsom, T. D. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn187 · Cited by 860 · see citing works
Biological Sensitivity to Context
Ellis, B. J., & Boyce, W. (2008) · Current Directions in Psychological Science · doi:10.1111/j.1467-8721.2008.00571.x · Cited by 797 · see citing works
The teen brain: insights from neuroimaging
Giedd, J. N. (2008) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2008.01.007 · Cited by 775 · see citing works
Immune involvement in schizophrenia and autism: Etiology, pathology and animal models
Patterson, P. H. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.016 · Cited by 766 · see citing works
Maternal care and the development of stress responses
Francis, D. D., & Meaney, M. J. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80016-6 · Cited by 677 · see citing works
Environmental Enrichment Reverses the Effects of Maternal Separation on Stress Reactivity
Francis, D. D., Diorio, J., Plotsky, P. M., & Meaney, M. J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-18-07840.2002 · Cited by 663 · see citing works
Infantile Experience and Resistance to Physiological Stress
Levine, S. (1957) · Science · doi:10.1126/science.126.3270.405 · Cited by 659 · see citing works
Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence
Laviola, G., Macrı̀, S., Morley-Fletcher, S., & Adriani, W. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00006-x · Cited by 621 · see citing works
Self-citation
Developmental determinants of sensitivity and resistance to stress
Levine, S. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.03.013 · Cited by 574 · see citing works
Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia
Agid, O., Shapira, B., Zislin, J., Ritsner, M., Hanin, B., Murad, H., Troudart, T., Bloch, M., Heresco‐Levy, U., & Lerer, B. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000473 · Cited by 568 · see citing works
Environment and Schizophrenia: Environmental Factors in Schizophrenia: Childhood Trauma--A Critical Review
Morgan, C., & Fisher, H. (2006) · Schizophrenia Bulletin · doi:10.1093/schbul/sbl053 · Cited by 568 · see citing works
The Affectional Systems
Harlow, H. F., & Harlow, M. K. (1965) · Elsevier eBooks · doi:10.1016/b978-1-4832-2821-1.50008-2 · Cited by 564 · see citing works
The dynamic effects of nicotine on the developing brain
Dwyer, J. B., McQuown, S. C., & Leslie, F. M. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.003 · Cited by 559 · see citing works
The neurobiology of social play behavior in rats
Vanderschuren, L. J. M. J., Niesink, R. J. M., & Van Pee, J. M. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00020-6 · Cited by 559 · see citing works
Prenatal Infection as a Risk Factor for Schizophrenia
Brown, A. S. (2006) · Schizophrenia Bulletin · doi:10.1093/schbul/sbj052 · Cited by 540 · see citing works
Prenatal stress and long-term consequences: implications of glucocorticoid hormones
Maccari, S., Darnaudéry, M., Morley‐Fletcher, S., Zuena, A. R., Cinque, C., & Reeth, O. V. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00014-9 · Cited by 529 · see citing works
Prenatal and Perinatal Risk Factors for Autism
Kolevzon, A. L., Gross, R., & Reichenberg, A. (2007) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.161.4.326 · Cited by 514 · see citing works
Prenatal Stress and Neurodevelopment of the Child: Focus on the HPA Axis and Role of the Placenta
O’Donnell, K. J., O’Connor, T. G., & Glover, V. A. S. (2009) · Developmental Neuroscience · doi:10.1159/000216539 · Cited by 509 · see citing works
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
Zuckerman, L., Rehavi, M., Nachman, R., & Weiner, I. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300248 · Cited by 501 · see citing works
Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus
Roceri, M., Hendriks, W. J. A. J., Racagni, G., Ellenbroek, B. A., & Riva, M. A. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001036 · Cited by 465 · see citing works
Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms
Pryce, C. R., & Feldon, J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00009-5 · Cited by 460 · see citing works
Elevated endogenous cannabinoids in schizophrenia
Leweke, F. M., Giuffrida, A., Wurster, U., Emrich, H. M., & Piomelli, D. (1999) · Neuroreport · doi:10.1097/00001756-199906030-00008 · Cited by 431 · see citing works
Chronic Pubertal, but not Adult Chronic Cannabinoid Treatment Impairs Sensorimotor Gating, Recognition Memory, and the Performance in a Progressive Ratio Task in Adult Rats
Schneider, M., & Koch, M. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300225 · Cited by 425 · see citing works
Critical Periods in Behavioral Development
Scott, J. P. (1962) · Science · doi:10.1126/science.138.3544.949 · Cited by 416 · see citing works
Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence
Beydoun, H. A., & Saftlas, A. F. (2008) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2008.00951.x · Cited by 413 · see citing works
Epigenetic programming of the stress response in male and female rats by prenatal restraint stress
Darnaudéry, M., & Maccari, S. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.11.004 · Cited by 412 · see citing works
Motivational systems in adolescence: Possible implications for age differences in substance abuse and other risk-taking behaviors
Doremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.08.008 · Cited by 397 · see citing works
The impact of intimate partner violence on women's reproductive health and pregnancy outcome
Sarkar, N. N. (2008) · Journal of Obstetrics and Gynaecology · doi:10.1080/01443610802042415 · Cited by 392 · see citing works
Neurobiological Consequences of Early Stress and Childhood Maltreatment: Are Results from Human and Animal Studies Comparable?
Teicher, M. H., Tomoda, A., & Andersen, S. L. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1364.024 · Cited by 389 · see citing works
Social grouping cannot account for cerebral effects of enriched environments
Rosenzweig, M. R., Bennett, E. L., Hébert, M., & Morimoto, H. (1978) · Brain Research · doi:10.1016/0006-8993(78)90340-2 · Cited by 383 · see citing works
Biological sensitivity to context: II. Empirical explorations of an evolutionary–developmental theory
ELLIS, B. J., ESSEX, M. J., & BOYCE, W. T. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050157 · Cited by 383 · see citing works
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
Dean, B., Sundram, S., Bradbury, R., Scarr, E., & Copolov, D. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00552-2 · Cited by 381 · see citing works
Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females
Shea, A., Walsh, C., MacMillan, H., & Steiner, M. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2004.07.001 · Cited by 378 · see citing works
The links between prenatal stress and offspring development and psychopathology: disentangling environmental and inherited influences
Rice, F. J., Harold, G. T., Boivin, J., van den Bree, M. B. M., Hay, D. F., & Thapar, A. (2009) · Psychological Medicine · doi:10.1017/s0033291709005911 · Cited by 377 · see citing works
Long-term cognitive and behavioral consequences of neonatal encephalopathy following perinatal asphyxia: a review
van Handel, M., Swaab, H., de Vries, L. S., & Jongmans, M. J. (2007) · European Journal of Pediatrics · doi:10.1007/s00431-007-0437-8 · Cited by 376 · see citing works
Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats.
Morley‐Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03070.x · Cited by 373 · see citing works
In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders
Meyer, U., Feldon, J., & Fatemi, S. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.001 · Cited by 367 · see citing works
Neurobiology of Dopamine in Schizophrenia
Guillin, O., Abi‐Dargham, A., & Laruelle, M. (2007) · International Review of Neurobiology · doi:10.1016/s0074-7742(06)78001-1 · Cited by 365 · see citing works
Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour
Weinstock, M. (2007) · Neurochemical Research · doi:10.1007/s11064-007-9339-4 · Cited by 349 · see citing works
Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models
Laviola, G., Adriani, W., Terranova, M. L., & Gerra, G. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00032-9 · Cited by 345 · see citing works
Psychobiology of persistent antisocial behavior: Stress, early vulnerabilities and the attenuation hypothesis
Susman, E. J. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.08.002 · Cited by 340 · see citing works
Prenatal Restraint Stress Generates Two Distinct Behavioral and Neurochemical Profiles in Male and Female Rats
Zuena, A. R., Mairesse, J., Casolini, P., Cinque, C., Alemà, G., Morley‐Fletcher, S., Chiodi, V., Spagnoli, L. G., Gradini, R., Catalani, A., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002170 · Cited by 339 · see citing works
The role of prenatal stress in the etiology of developmental behavioural disorders
Kofman, O. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00015-5 · Cited by 331 · see citing works
Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure
Schneider, M. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00110.x · Cited by 330 · see citing works
Desperately driven and no brakes: Developmental stress exposure and subsequent risk for substance abuse
Andersen, S. L., & Teicher, M. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.09.009 · Cited by 326 · see citing works
Risk Taking and Novelty Seeking in Adolescence: Introduction to Part I
KELLEY, A. E., SCHOCHET, T., & LANDRY, C. F. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.003 · Cited by 325 · see citing works
Activity-dependent structural plasticity
Butz, M., Wörgötter, F., & Arjen Van Ooyen, B. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.12.023 · Cited by 321 · see citing works
Prenatal Immune Challenge Disrupts Sensorimotor Gating in Adult Rats Implications for the Etiopathogenesis of Schizophrenia
Borrell, J. I. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00360-8 · Cited by 307 · see citing works
Time course of the effect of maternal deprivation on the hypothalamic‐pituitary‐adrenal axis in the infant rat
Levine, S. D., Huchton, D. M., Wiener, S. G., & Rosenfeld, P. (1991) · Developmental Psychobiology · doi:10.1002/dev.420240803 · Cited by 304 · see citing works
Effects of prenatal restraint stress on the hypothalamus–pituitary–adrenal axis and related behavioural and neurobiological alterations
Maccari, S., & Morley-Fletcher, S. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.06.005 · Cited by 302 · see citing works
Ventral somatosensory determinants of nursing behavior in Norway rats. I. Effects of variations in the quality and quantity of pup stimuli
Stern, J. M., & Johnson, S. K. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90026-z · Cited by 301 · see citing works
Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders
Laviola, G., Hannan, A. J., Macrì, S., Solinas, M., & Jaber, M. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.05.001 · Cited by 300 · see citing works
Self-citation
Anatomical Brain Magnetic Resonance Imaging of Typically Developing Children and Adolescents
Gerber, A. J., Peterson, B. S., Giedd, J. N., Lalonde, F. M., Celano, M. J., White, S., Wallace, G. L., Lee, N., & Lenroot, R. (2009) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e31819f2715 · Cited by 298 · see citing works
Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia
Koenig, J. I., Elmer, G. I., Shepard, P. D., Lee, P. R., Mayo, C. L., Joy, B., Hercher, E., & Brady, D. L. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.05.030 · Cited by 297 · see citing works
Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats
O’Shea, M., Singh, M. E., McGregor, I. S., & Mallet, P. E. (2004) · Journal of Psychopharmacology · doi:10.1177/0269881104047277 · Cited by 292 · see citing works
Adolescent Cannabis Exposure Alters Opiate Intake and Opioid Limbic Neuronal Populations in Adult Rats
Ellgren, M., Spano, S., & Hurd, Y. L. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301127 · Cited by 287 · see citing works
Nicotine and the adolescent brain: insights from an animal model
Slotkin, T. (2002) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(02)00199-x · Cited by 284 · see citing works
Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress
Fox, C., Merali, Z., & Harrison, C. R. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.016 · Cited by 283 · see citing works
High-risk behaviors associated with early smoking: results from a 5-year follow-up
Ellickson, P. L., Tucker, J. S., & Klein, D. J. (2001) · Journal of Adolescent Health · doi:10.1016/s1054-139x(00)00202-0 · Cited by 282 · see citing works
Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin
Lee, P. R., Brady, D. L., Shapiro, R. A., Dorsa, D. M., & Koenig, J. I. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.042 · Cited by 270 · see citing works
Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood
Bolaños, C. A., Barrot, M., Berton, O., Wallace-Black, D., & Nestler, E. J. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00570-5 · Cited by 267 · see citing works
Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model
Adriani, W., & Laviola, G. (2004) · Behavioural Pharmacology · doi:10.1097/00008877-200409000-00005 · Cited by 267 · see citing works
Postnatal Handling Increases the Expression of cAMP-Inducible Transcription Factors in the Rat Hippocampus: The Effects of Thyroid Hormones and Serotonin
Meaney, M. J., Diorio, J., Francis, D., Weaver, S., Yau, J., Chapman, K., & Seckl, J. R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-10-03926.2000 · Cited by 266 · see citing works
The effects of an early stressful life event on sensorimotor gating in adult rats
Ellenbroek, B. A., van den Kroonenberg, P. T. J. M., & Cools, A. R. (1998) · Schizophrenia Research · doi:10.1016/s0920-9964(97)00149-7 · Cited by 265 · see citing works
Serotonergic Systems, Anxiety, and Affective Disorder
Lowry, C. A., Hale, M. W., Evans, A. K., Heerkens, J., Staub, D. R., Gasser, P. J., & Shekhar, A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1410.004 · Cited by 265 · see citing works
From the history of an infantile neurosis
Riggs, D. W. (2018) · Routledge eBooks · doi:10.4324/9780429478307-3 · Cited by 264 · see citing works
In utero infection and adult schizophrenia
Brown, A. S., & Susser, E. (2002) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.10004 · Cited by 261 · see citing works
Enhanced reactivity and vulnerability to cocaine following methylphenidate treatment in adolescent rats
Brandon, C. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00281-0 · Cited by 259 · see citing works
Prenatal stress, fetal imprinting and immunity
Merlot, É., Couret, D., & Otten, W. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.05.007 · Cited by 257 · see citing works
Influence of psychological variables on the activity of the hypothalamic–pituitary–adrenal axis
Levine, S. D. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00548-3 · Cited by 257 · see citing works
Evidence for enhanced neurobehavioral vulnerability to nicotine during periadolescence in rats
Adriani, W., Spijker, S., Deroche-Gamonet, V., Laviola, G., Le Moal, M., Smit, A. B., & Piazza, P. V. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-11-04712.2003 · Cited by 257 · see citing works
Hormones, brain and stress.
de Kloet, E. R. (2003) · PubMed · Cited by 255 · see citing works
Developmental plasticity of HPA and fear responses in rats: A critical review of the maternal mediation hypothesis
Macrı̀, S., & Würbel, H. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.015 · Cited by 253 · see citing works
Self-citation
Enduring behavioral effects of early exposure to methylphenidate in rats
Carlezon, W. A., Mague, S. D., & Andersen, S. L. (2003) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.08.020 · Cited by 248 · see citing works
Adolescent Peer Crowd Affiliation: Linkages With Health-Risk Behaviors and Close Friendships
Greca, A. M. L. (2001) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/26.3.131 · Cited by 243 · see citing works
Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats
Macrı̀, S., Mason, G. J., & Würbel, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03541.x · Cited by 237 · see citing works
Self-citation
Adolescence and the Trajectory of Alcohol Use: Basic to Clinical Studies
Brown, S. A., & Tapert, S. F. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.028 · Cited by 235 · see citing works
Early experience as a determinant of adult behavioural responses to reward: the effects of repeated maternal separation in the rat
Matthews, K., & Robbins, T. W. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00008-3 · Cited by 231 · see citing works
Stress, the Hippocampus and the Hypothalamic-Pituitary-Adrenal Axis: Implications for the Development of Psychotic Disorders
Phillips, L., McGorry, P. D., Garner, B., Thompson, K. N., Pantelis, C., Wood, S. J., & Berger, G. E. (2006) · Australian & New Zealand Journal of Psychiatry · doi:10.1080/j.1440-1614.2006.01877.x · Cited by 230 · see citing works
Cannabis use and outcome of recent onset psychosis
Grech, A., van Os, J., Jones, P. B., Lewis, S. W., & Murray, R. M. (2005) · European Psychiatry · doi:10.1016/j.eurpsy.2004.09.013 · Cited by 230 · see citing works
Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation
Lee, J.-H., Kim, H. J., Kim, J. G., Ryu, V., Kim, B.-T., Kang, D. W., & Jahng, J. W. (2007) · Neuroscience Research · doi:10.1016/j.neures.2007.01.008 · Cited by 228 · see citing works
Pre- and peri-natal environmental risks for attention-deficit hyperactivity disorder (ADHD): the potential role of epigenetic processes in mediating susceptibility.
Mill, J., & Petronis, A. (2008) · Journal of Child Psychology and Psychiatry and Allied Disciplines · doi:10.1111/j.1469-7610.2008.01909.x · Cited by 228 · see citing works
Absence of MPTP-Induced Neuronal Death in Mice Lacking the Dopamine Transporter
Bézard, E., Gross, C. E., Fournier, M.-C., Doveró, S., Bloch, B., & Jaber, M. (1999) · Experimental Neurology · doi:10.1006/exnr.1998.6995 · Cited by 227 · see citing works
Maternal Influences and Early Behavior
(1980) · Springer eBooks · doi:10.1007/978-94-011-6287-6 · Cited by 227 · see citing works
Early life stress as a risk factor for mental health: Role of neurotrophins from rodents to non-human primates
Cirulli, F., Francia, N., Berry, A., Aloe, L., Alleva, E., & Suomi, S. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.09.001 · Cited by 225 · see citing works
Schizophrenia, autoimmunity and immune system dysregulation: A comprehensive model updated and revisited
Strous, R. D., & Shoenfeld, Y. (2006) · Journal of Autoimmunity · doi:10.1016/j.jaut.2006.07.006 · Cited by 225 · see citing works
T-helper-1 and T-helper-2 Responses in Psychiatric Disorders
Schwarz, M., Chiang, S. S. W., Müller, N., & Ackenheil, M. (2001) · Brain Behavior and Immunity · doi:10.1006/brbi.2001.0647 · Cited by 220 · see citing works
Cannabis and psychiatric disorders: it is not only addiction
Leweke, F. M., & Koethe, D. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00106.x · Cited by 213 · see citing works
The association between cigarette smoking and drug abuse in the United States
Lai, S., Lai, H., Page, J. B., & McCoy, C. B. (2000) · Journal of Addictive Diseases · doi:10.1300/j069v19n04_02 · Cited by 212 · see citing works
Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis
Lemaire, V., Lamarque, S., Le Moal, M., Piazza, P.-V., & Abrous, D. N. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.11.009 · Cited by 211 · see citing works
The pharmacology of impulsive behaviour in rats VI: the effects of ethanol and selective serotonergic drugs on response choice with varying delays of reinforcement
Evenden, J. L., & Ryan, C. N. (1999) · Psychopharmacology · doi:10.1007/pl00005486 · Cited by 207 · see citing works
Neonatal Handling and Environmental Enrichment Effects on Emotionality, Novelty/Reward Seeking, and Age-Related Cognitive and Hippocampal Impairments: Focus on the Roman Rat Lines
Fernández‐Teruel, A., Escorihuela, R. M., Castellano, B., González, B., & Tobeña, A. (1997) · Behavior Genetics · doi:10.1023/a:1021400830503 · Cited by 207 · see citing works
Mineralocorticoid receptor overexpression in forebrain decreases anxiety-like behavior and alters the stress response in mice
Rozeboom, A. M., Akil, H., & Seasholtz, A. F. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606067104 · Cited by 206 · see citing works
Gene-Environment Interaction and Covariation in Schizophrenia: The Role of Obstetric Complications
Mittal, V. A., Ellman, L. M., & Cannon, T. D. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn080 · Cited by 203 · see citing works
Maternal separation alters drug intake patterns in adulthood in rats
Moffett, M. C., Vicentic, A., Kozel, M. A., Plotsky, P. M., Francis, D. D., & Kuhar, M. J. (2006) · Biochemical Pharmacology · doi:10.1016/j.bcp.2006.08.003 · Cited by 199 · see citing works
Advances in behavioral genetics: mouse models of autism
Moy, S. S., & Nadler, J. J. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4002082 · Cited by 197 · see citing works
Attention-deficit/hyperactivity disorder (ADHD) behaviour explained by dysfunctioning reinforcement and extinction processes
Johansen, E. B., Aase, H., Meyer, A., & Sagvolden, T. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00434-x · Cited by 195 · see citing works
Therapy Insight: is there an imbalanced response of mineralocorticoid and glucocorticoid receptors in depression?
de Kloet, E. R., DeRijk, R. H., & Meijer, O. C. (2007) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0403 · Cited by 193 · see citing works
Prenatal stress and neonatal rat brain development
van den Hove, D., Steinbusch, H. W. M., Scheepens, A., van de Berg, W. D. J., Kooiman, L. A. M., Boosten, B. J. G., Prickaerts, J., & Blanco, C. E. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.060 · Cited by 192 · see citing works
The Immune System and Schizophrenia: An Integrative View
Müller, N., Riedel, M. J., Gruber, R., Ackenheil, M., & Schwarz, M. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb05410.x · Cited by 189 · see citing works
Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring.
Fortier, M., Joober, R., Luheshi, G., & Boksa, P. (2004) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2003.10.001 · Cited by 186 · see citing works
Prenatal stress in rats predicts immobility behavior in the forced swim test
Morley‐Fletcher, S., Darnaudéry, M., Koehl, M., Casolini, P., Reeth, O. V., & Maccari, S. (2003) · Brain Research · doi:10.1016/s0006-8993(03)03293-1 · Cited by 184 · see citing works
Endogenous retroviruses and schizophrenia
Yolken, R. H. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00037-5 · Cited by 182 · see citing works
Brain and cognitive‐behavioural development after asphyxia at term birth
de Haan, M. D. H., Wyatt, J. S., Roth, S. C., Vargha‐Khadem, F., Gadian, D. G., & Mishkin, M. (2006) · Developmental Science · doi:10.1111/j.1467-7687.2006.00499.x · Cited by 180 · see citing works
Cannabis use and the risk of developing a psychotic disorder
Hall, W., & Degenhardt, L. J. (2008) · World Psychiatry · doi:10.1002/j.2051-5545.2008.tb00158.x · Cited by 178 · see citing works
Human Development: Biological and Genetic Processes
Gottesman, I. I., & Hanson, D. R. (2004) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070208 · Cited by 176 · see citing works
Childhood parental loss and risk for first-onset of major depression and alcohol dependence: the time-decay of risk and sex differences
Kendler, K. S., Sheth, K. N., GARDNER, C. O., & Prescott, C. A. (2002) · Psychological Medicine · doi:10.1017/s0033291702006219 · Cited by 176 · see citing works
Maternal Effects on Schizophrenia Risk
Patterson, P. H. (2007) · Science · doi:10.1126/science.1150196 · Cited by 175 · see citing works
Early-life handling stimulation and environmental enrichment
Fernández-Teruel, A., Giménez-Llort, L., Escorihuela, R. M., Gil, L., Aguilar, R., Steimer, T., & Tobeña, A. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00787-6 · Cited by 171 · see citing works
Localization of 5-HT2A receptors on dopamine cells in subnuclei of the midbrain A10 cell group
Nocjar, C., Roth, B. L., & Pehek, E. A. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00593-0 · Cited by 169 · see citing works
Child psychiatric sequelae of maternal war stress
Meijer, A. (1985) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.1985.tb02647.x · Cited by 168 · see citing works
Effects of prenatal stress on cellular and humoral immune responses in neonatal pigs
Tuchscherer, M., Kanitz, E., Otten, W., & Tuchscherer, A. (2002) · Veterinary Immunology and Immunopathology · doi:10.1016/s0165-2427(02)00035-1 · Cited by 165 · see citing works
The impact of gestational stress and prenatal growth on emotional problems in offspring: a review
Rice, F. J., Jones, I. R., & Thapar, A. (2006) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.2006.00895.x · Cited by 164 · see citing works
Cannabis use is associated with schizotypy and attentional disinhibition
Skosnik, P. D., Spatz-Glenn, L., & Park, S. (2001) · Schizophrenia Research · doi:10.1016/s0920-9964(00)00132-8 · Cited by 160 · see citing works
Detection and management of comorbidity in patients with schizophrenia
Green, A. I., Canuso, C. M., Brenner, M. J., & Wojcik, J. (2003) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(02)00014-x · Cited by 159 · see citing works
Prenatal psychological stress causes higher emotionality, depression-like behavior, and elevated activity in the hypothalamo-pituitary-adrenal axis
Abe, H., Hidaka, N., Kawagoe, C., Odagiri, K., Watanabe, Y., Ikeda, T., Ishizuka, Y., Hashiguchi, H., Takeda, R., Nishimori, T., et al. (2007) · Neuroscience Research · doi:10.1016/j.neures.2007.06.1465 · Cited by 157 · see citing works
Beneficial effects of enriched environment on adolescent rats from stressed pregnancies.
Laviola, G., Rea, M., Morley‐Fletcher, S., Di Carlo, S., Bacosi, A., De Simone, R., Bertini, M., & Pacifici, R. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03597.x · Cited by 155 · see citing works
Sensitive periods in functional brain development: Problems and prospects
Johnson, M. H. (2005) · Developmental Psychobiology · doi:10.1002/dev.20057 · Cited by 154 · see citing works
Long lasting consequences of cannabis exposure in adolescence
Rubino, T., & Parolaro, D. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.02.003 · Cited by 152 · see citing works
Susceptibility genes for schizophrenia: Characterisation of mutant mouse models at the level of phenotypic behaviour
O’Tuathaigh, C. M. P., Babovic, D., O’Meara, G. F., Clifford, J. J., Croke, D. T., & Waddington, J. L. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.04.002 · Cited by 151 · see citing works
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
Slotkin, T. A., MacKillop, E. A., Rudder, C. L., Ryde, I. T., Tate, C. A., & Seidler, F. J. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301231 · Cited by 149 · see citing works
Pubertal-related changes influence the development of environment-related social interaction in the male rat
Primus, R. J., & Kellogg, C. K. (1989) · Developmental Psychobiology · doi:10.1002/dev.420220608 · Cited by 146 · see citing works
Early maternal deprivation induces gender‐dependent changes on the expression of hippocampal CB1 and CB2 cannabinoid receptors of neonatal rats
Suárez, J., Llorente, R., Romero‐Zerbo, S., Mateos, B., Bermúdez‐Silva, F. J., de Fonseca, F. R., & Viveros, M. (2008) · Hippocampus · doi:10.1002/hipo.20537 · Cited by 142 · see citing works
Clustering of smoking, alcohol drinking and cannabis use in adolescents in a rapidly developing country
Faeh, D., Viswanathan, B., Chioléro, A., Warren, W. C., & Bovet, P. (2006) · BMC Public Health · doi:10.1186/1471-2458-6-169 · Cited by 141 · see citing works
Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny
Catalani, A., Casolini, P., Scaccianoce, S., Patacchioli, F. R., Spinozzi, P., & Angelucci, L. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00277-3 · Cited by 140 · see citing works
Chronic treatment with CP 55,940 during the peri-adolescent period differentially affects the behavioural responses of male and female rats in adulthood
Fernández, J. M. B., Marín, S., Fernández, B., Marco, E. M., Rubio, M., Guaza, C., Ambrosio, E., & Viveros, M. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1550-7 · Cited by 137 · see citing works
Self-citation
Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus
Rasmuson, S., Olsson, T., Henriksson, B. G., Kelly, P. A. T., Holmes, M. C., Seckl, J. R., & Mohammed, A. H. S. (1998) · Molecular Brain Research · doi:10.1016/s0169-328x(97)00317-3 · Cited by 134 · see citing works
Critical period: A history of the transition from questions of when, to what, to how
Michel, G. F., & Tyler, A. N. (2005) · Developmental Psychobiology · doi:10.1002/dev.20058 · Cited by 134 · see citing works
Progeny of mothers drinking corticosterone during lactation has lower stress-induced corticosterone secretion and better cognitive performance
Catalani, A., Marinelli, M., Scaccianoce, S., Nicolai, R., Muscolo, L. A. A., Porcu, A., Kora´nyi, L., Piazza, P. V., & Angelucci, L. (1993) · Brain Research · doi:10.1016/0006-8993(93)90079-3 · Cited by 133 · see citing works
Methylphenidate Administration to Adolescent Rats Determines Plastic Changes on Reward-Related Behavior and Striatal Gene Expression
Adriani, W., Leo, D., Greco, D., Rea, M., di Porzio, U., Laviola, G., & Perrone‐Capano, C. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300962 · Cited by 130 · see citing works
Extended Male Growth in a Fossil Hominin Species
Lockwood, C. A., Menter, C. G., Moggi‐Cecchi, J., & Keyser, A. W. (2007) · Science · doi:10.1126/science.1149211 · Cited by 130 · see citing works
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
Fernández‐Teruel, A., Driscoll, P., Gil, L., Aguilar, R., Tobeña, A., & Escorihuela, R. M. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00784-0 · Cited by 126 · see citing works
Prenatal stress feminizes juvenile play patterns in male rats
Ward, I. L., & Stehm, K. E. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90552-y · Cited by 125 · see citing works
Early maternal deprivation and prepulse inhibition
Ellenbroek, B. A., & Cools, A. R. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00794-3 · Cited by 124 · see citing works
Episodic neonatal hypoxia evokes executive dysfunction and regionally specific alterations in markers of dopamine signaling
Decker, M. J., Hue, G., Caudle, W. M., Miller, G. W., Keating, G. L., & Rye, D. B. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00805-9 · Cited by 122 · see citing works
Effects of maternal prenatal stress on offspring development: a commentary
Lazinski, M. J., Shea, A. K., & Steiner, M. S. (2008) · Archives of Women s Mental Health · doi:10.1007/s00737-008-0035-4 · Cited by 120 · see citing works
Cannabis use and psychiatric and cogitive disorders: the chicken or the egg?
di Forti, M., Morrison, P., Butt, A., & Murray, R. (2007) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e3280fa838e · Cited by 120 · see citing works
Physiological Damage under Emotional Stress as a Function of Early Experience
Weininger, O. (1954) · Science · doi:10.1126/science.119.3087.285 · Cited by 117 · see citing works
Inflammation and schizophrenia
Fan, X., GOFF, D. C., & Henderson, D. C. (2007) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.7.7.789 · Cited by 117 · see citing works
Modulation of neurotransmitter release induced by brain-derived neurotrophic factor in rat brain striatal slices in vitro
Goggi, J., Pullar, I. A., Carney, S. L., & Bradford, H. F. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02505-2 · Cited by 116 · see citing works
Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex
Pickering, C., Gustafsson, L., Cebere, A., Nylander, I., & Liljequist, S. (2006) · Brain Research · doi:10.1016/j.brainres.2006.04.136 · Cited by 115 · see citing works
Infantile Experience and the Maturation of the Pituitary Adrenal Axis
Levine, S., Alpert, M., & Lewis, G. W. (1957) · Science · doi:10.1126/science.126.3287.1347 · Cited by 114 · see citing works
Anxiety disorders in schizophrenia
Braga, R. J., Petrides, G., & Figueira, I. L. D. V. (2004) · Comprehensive Psychiatry · doi:10.1016/j.comppsych.2004.07.009 · Cited by 112 · see citing works
The Dynamics of the Hypothalamic‐Pituitary‐Adrenal Axis During Maternal Deprivation
Schmidt, M. V., Enthoven, L., Woezik, J. H. G. V., Levine, S. D., de Kloet, E. R., & Oitzl, M. S. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01123.x · Cited by 111 · see citing works
Depression, Anhedonia, and Psychomotor Symptoms:The Role of Dopaminergic Neurocircuitry
Stein, D. J. (2008) · CNS Spectrums · doi:10.1017/s1092852900016837 · Cited by 110 · see citing works
Maternal separation and maternal care act independently on the development of HPA responses in male rats
Macrı̀, S., Chiarotti, F., & Würbel, H. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.03.031 · Cited by 109 · see citing works
Self-citation
Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity
Vidal, J., de Bie, J., Granneman, R. A., Wallinga, A. E., Koolhaas, J. M., & Buwalda, B. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.06.004 · Cited by 108 · see citing works
Temperature‐dependent effects of maternal separation on growth, activity, and amphetamine sensitivity in the rat
Zimmerberg, B., & Shartrand, A. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250306 · Cited by 108 · see citing works
Prenatal Stress Diminishes the Cytokine Response of Leukocytes to Endotoxin Stimulation in Juvenile Rhesus Monkeys
Coe, C. L., Kramer, M., Kirschbaum, C., Netter, P., & Fuchs, E. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.2.8233 · Cited by 108 · see citing works
A description of the ontogeny of mouse agonistic behavior.
Terranova, M. L., Giovanni Laviola, A., Acetis, L. D., & Alleva, E. (1998) · Journal of comparative psychology · doi:10.1037/0735-7036.112.1.3 · Cited by 107 · see citing works
Early maternal deprivation retards neurodevelopment in Wistar rats
Ellenbroek, B. A., Derks, N. M., & Park, H. (2005) · Stress · doi:10.1080/10253890500404634 · Cited by 105 · see citing works
Long-Term Reciprocal Changes in Dopamine Levels in Prefrontal Cortex versus Nucleus Accumbens in Rats Born by Caesarean Section Compared to Vaginal Birth
El‐Khodor, B. F., & Boksa, P. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6437 · Cited by 104 · see citing works
Changes in Open Field Behavior, Spatial Memory, and Hippocampal Parvalbumin Immunoreactivity Following Enrichment in Rats Exposed to Neonatal Anoxia
Iuvone, L., Geloso, M. C., & Dell’Anna, E. (1996) · Experimental Neurology · doi:10.1006/exnr.1996.0077 · Cited by 104 · see citing works
Comparison of maternal separation and early handling in terms of their neurobehavioral effects in aged rats
Lehmann, J. (2002) · Neurobiology of Aging · doi:10.1016/s0197-4580(01)00320-7 · Cited by 103 · see citing works
Long-Term Neuropsychiatric Consequences of "Ecstasy" (MDMA): A Review
Montoya, A. G., Sorrentino, R. M., Lukas, S. E., & Price, B. H. (2002) · Harvard Review of Psychiatry · doi:10.1080/hrp.10.4.212.220 · Cited by 102 · see citing works
Maternal Mediation of Early Experience
Smotherman, W. P., & Bell, R. W. (1980) · Springer eBooks · doi:10.1007/978-94-011-6287-6_8 · Cited by 100 · see citing works
Alterations of Serotonin Transmission in Schizophrenia
Abi‐Dargham, A. (2007) · International review of neurobiology · doi:10.1016/s0074-7742(06)78005-9 · Cited by 98 · see citing works
Early deprivation under specific conditions leads to reduced interest in reward in adulthood in Wistar rats
Rüedi-Bettschen, D., Pedersen, E.-M., Feldon, J., & Pryce, C. R. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.06.001 · Cited by 97 · see citing works
New Perspectives in the Studies on Endocannabinoid and Cannabis: Cannabinoid Receptors and Schizophrenia
Ujike, H., & Morita, Y. (2004) · Journal of Pharmacological Sciences · doi:10.1254/jphs.fmj04003x4 · Cited by 95 · see citing works
Detrimental psychophysiological effects of early maternal deprivation in adolescent and adult rodents: Altered responses to cannabinoid exposure
Marco, E. M., Adriani, W., Llorente, R., Giovanni Laviola, A., & Viveros, M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.008 · Cited by 95 · see citing works
Self-citation
Neurobiological Processes in Adolescent Addictive Disorders
Schepis, T. S., Adinoff, B. H., & Rao, U. (2008) · American Journal on Addictions · doi:10.1080/10550490701756146 · Cited by 95 · see citing works
Neurodevelopmental disorders: Cluster 2 of the proposed meta-structure for DSM-V and ICD-11: Paper 3 of 7 of the thematic section: ‘A proposal for a meta-structure for DSM-V and ICD-11’
Andrews, G., Pine, D. S., Hobbs, M. J., Anderson, T. M., & Sunderland, M. (2009) · Psychological Medicine · doi:10.1017/s0033291709990274 · Cited by 94 · see citing works
Some Animal Models for the Study of Perinatal Asphyxia
Raju, T. N. K. (2009) · Biology of the Neonate · doi:10.1159/000243873 · Cited by 93 · see citing works
The alcohol–tobacco relationship: a prospective study among adolescents in six European countries
Wetzels, J., Kremers, S., Vitória, P., & de Vries, H. (2003) · Addiction · doi:10.1111/j.1360-0443.2003.00553.x · Cited by 90 · see citing works
Early maternal deprivation and neonatal single administration with a cannabinoid agonist induce long-term sex-dependent psychoimmunoendocrine effects in adolescent rats
Llorente, R., Arranz, L., Marco, E. M., Moreno, E., Puerto, M., Guaza, C., la Fuente, M. D., & Viveros, M. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.04.002 · Cited by 90 · see citing works
Self-citation
From the Editors
Angelini, D. J. (2009) · The Journal of Perinatal & Neonatal Nursing · doi:10.1097/jpn.0b013e3181969c39 · Cited by 90 · see citing works
Psychosocial maternal stress during pregnancy affects serum corticosterone, blood immune parameters and anxiety behaviour in adult male rat offspring
Götz, A. A., & Stefanski, V. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.09.014 · Cited by 87 · see citing works
Serotonin Neural Adaptations to Ontogenetic Loss of Dopamine Neurons in Rat Brain
Kostrzewa, R. M., Reader, T. A., & Descarries, L. (1998) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1998.70030889.x · Cited by 87 · see citing works
Gender‐dependent cellular and biochemical effects of maternal deprivation on the hippocampus of neonatal rats: A possible role for the endocannabinoid system
Llorente, R., Llorente‐Berzal, A., Petrosino, S., Marco, E. M., Guaza, C., Prada, C., López‐Gallardo, M., Marzo, V. D., & Viveros, M. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20666 · Cited by 85 · see citing works
Self-citation
Early enriched housing results in partial recovery of memory deficits in female, but not in male, rats after neonatal hypoxia–ischemia
Pereira, L. O., Strapasson, A. C. P., Nabinger, P. M., Achaval, M., & Netto, C. A. (2008) · Brain Research · doi:10.1016/j.brainres.2008.04.010 · Cited by 84 · see citing works

Flagged first, then by citations

Sorted by citations

Developmental trajectories during adolescence in males and females: A cross-species understanding of underlying brain changes
Brenhouse, H. C., & Andersen, S. L. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.04.013 · Cited by 340 · see citing works
Psychological stress in early life as a predisposing factor for the development of chronic pain: clinical and preclinical evidence and neurobiological mechanisms
Burke, N. N., Finn, D. P., McGuire, B. E., & Roche, M. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.23802 · Cited by 268 · see citing works
Environmental toxicology: Sensitive periods of development and neurodevelopmental disorders
Heyer, D. B., & Meredith, R. M. (2016) · NeuroToxicology · doi:10.1016/j.neuro.2016.10.017 · Cited by 237 · see citing works
Defeat stress in rodents: from behavior to molecules
Hammels, C., Pishva, E., De Vry, J., van den Hove, D. L. A., Prickaerts, J., van Winkel, R., Selten, J.-P., Lesch, K.-P., Daskalakis, N. P., Steinbusch, H. W. M., et al. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.10.006 · Cited by 230 · see citing works
Prenatal maternal stress predicts autism traits in 6½ year-old children: Project Ice Storm
Walder, D. J., Laplante, D. P., Sousa-Pires, A., Veru, F., Brunet, A., & King, S. (2014) · Psychiatry Research · doi:10.1016/j.psychres.2014.04.034 · Cited by 183 · see citing works
Cardiovascular Risk Factors From Childhood and Midlife Cognitive Performance
Rovio, S., Pahkala, K., Nevalainen, J., Juonala, M., Salo, P., Kähönen, M. A. P., Hutri‐Kähönen, N., Lehtimäki, T. J., Jokinen, E. V., Laitinen, T. P., et al. (2017) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2017.02.060 · Cited by 145 · see citing works
Environmental factors in Tourette syndrome
Hoekstra, P. J., Dietrich, A., Edwards, M. J., Elamin, I., & Martino, D. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.10.010 · Cited by 143 · see citing works
Adolescent drug exposure: A review of evidence for the development of persistent changes in brain function
Salmanzadeh, H., Ahmadi‐Soleimani, S. M., Pachenari, N., Azadi, M., Halliwell, R. F., Rubino, T., & Azizi, H. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.01.007 · Cited by 146 · see citing works
Altered Development of Synapse Structure and Function in Striatum Caused by Parkinson's Disease-Linked LRRK2-G2019S Mutation
Matikainen‐Ankney, B. A., Kezunovic, N., Mesias, R., Tian, Y., Williams, F. M. K., Huntley, G. W., & Benson, D. L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3314-15.2016 · Cited by 131 · see citing works
Early life stress disrupts social behavior and prefrontal cortex parvalbumin interneurons at an earlier time-point in females than in males
Holland, F. H., Ganguly, P., Potter, D. N., Chartoff, E. H., & Brenhouse, H. C. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.02.023 · Cited by 125 · see citing works
The lasting impact of early‐life adversity on individuals and their descendants: potential mechanisms and hope for intervention
Cowan, C. S. M., Callaghan, B. L., Kan, J. M., & Richardson, R. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12263 · Cited by 127 · see citing works
Environmental Mechanisms of Neurodevelopmental Toxicity
Rock, K. D., & Patisaul, H. B. (2018) · Current Environmental Health Reports · doi:10.1007/s40572-018-0185-0 · Cited by 124 · see citing works
The maternal deprivation animal model revisited.
Marco, E. M., Llorente, R., López-Gallardo, M., Mela, V., Llorente-Berzal, Á., Prada, C., & Viveros, M.-P. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.015 · Cited by 132 · see citing works
Self-citation
Loss of Environmental Enrichment Increases Vulnerability to Cocaine Addiction
Nader, J., Chauvet, C., Rawas, R. E., Favot, L., Jaber, M., Thiriet, N., & Solinas, M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.2 · Cited by 116 · see citing works
Tracing the development of psychosis and its prevention: what can be learned from animal models
Piontkewitz, Y., Arad, M., & Weiner, I. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.019 · Cited by 108 · see citing works
Opinion: Sex, gender and the diagnosis of autism—A biosocial view of the male preponderance
Goldman, S. (2013) · Research in Autism Spectrum Disorders · doi:10.1016/j.rasd.2013.02.006 · Cited by 108 · see citing works
Long Term Sex-Dependent Psychoneuroendocrine Effects of Maternal Deprivation and Juvenile Unpredictable Stress in Rats
Llorente, R., Miguel-Blanco, C., Aisa, B., Lachize, S., Borcel, É., Meijer, O. C., Ramírez, M. J., de Kloet, E. R., & Viveros, M. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02109.x · Cited by 101 · see citing works
Exposure to variable prenatal stress in rats: Effects on anxiety-related behaviors, innate and contextual fear, and fear extinction
Wilson, C., Vazdarjanova, A. I., & Terry, A. V. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.003 · Cited by 96 · see citing works
Consequences of early life stress on the expression of endocannabinoid-related genes in the rat brain
Marco, E. M., Echeverry‐Alzate, V., López‐Moreno, J. A., Giné, E., Peñasco, S., & Viveros, M. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000068 · Cited by 95 · see citing works
Self-citation
Social dysfunction after pediatric traumatic brain injury: A translational perspective
Ryan, N. P., Catroppa, C., Godfrey, C., Noble‐Haeusslein, L. J., Shultz, S. R., O'Brien, T. J., Anderson, V. A., & Semple, B. D. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.02.020 · Cited by 95 · see citing works
Ontogeny of contextual fear memory formation, specificity, and persistence in micePreprint
Akers, K. G., Arruda-Carvalho, M., Josselyn, S. A., & Frankland, P. W. (2012) · Learning & Memory · doi:10.1101/lm.027581.112 · Cited by 88 · see citing works
Cannabinoids for People with ASD: A Systematic Review of Published and Ongoing Studies
Fusar‐Poli, L., Cavone, V., Tinacci, S., Concas, I., Petralia, A., Signorelli, M. S., Díaz‐Caneja, C. M., & Aguglia, E. (2020) · Brain Sciences · doi:10.3390/brainsci10090572 · Cited by 84 · see citing works
Cognitive biases predict symptoms of depression, anxiety and wellbeing above and beyond neuroticism in adolescence
Smith, E. M., Reynolds, S., Orchard, F., Whalley, H. C., & Chan, S. W. (2018) · Journal of Affective Disorders · doi:10.1016/j.jad.2018.08.051 · Cited by 83 · see citing works
Oxytocin neurons mediate the effect of social isolation via the VTA circuits
Musardo, S., Contestabile, A., Knoop, M., Baud, O., & Bellone, C. (2022) · eLife · doi:10.7554/elife.73421 · Cited by 77 · see citing works
White matter connectivity and aerobic fitness in male adolescents
Herting, M. M., Colby, J. B., Sowell, E. R., & Nagel, B. J. (2013) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2013.11.003 · Cited by 75 · see citing works
Environmental neuroscience linking exposome to brain structure and function underlying cognition and behavior
Liu, F., Xu, J., Guo, L., Qin, W., Liang, M., Schumann, G., & Yu, C. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01669-6 · Cited by 72 · see citing works
The chlorine contents and chain lengths influence the neurobehavioral effects of commercial chlorinated paraffins on zebrafish larvae
Yang, X., Zhang, B., Gao, Y., Chen, Y., Yin, D., & Xu, T. (2019) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2019.05.047 · Cited by 68 · see citing works
Targeting brains, producing responsibilities: The use of neuroscience within British social policy
Broer, T., & Pickersgill, M. D. (2015) · Social Science & Medicine · doi:10.1016/j.socscimed.2015.03.022 · Cited by 66 · see citing works
Long-lasting effects of prenatal stress on HPA axis and inflammation: A systematic review and multilevel meta-analysis in rodent studies
Creutzberg, K. C., Sanson, A., Viola, T. W., Marchisella, F., Begni, V., Grassi‐Oliveira, R., & Riva, M. A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.04.032 · Cited by 65 · see citing works
The endocannabinoid system in the regulation of emotions throughout lifespan: a discussion on therapeutic perspectives
Marco, E. M., & Laviola, G. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111408459 · Cited by 65 · see citing works
Self-citation
Cumulative multiple early life hits- a potent threat leading to neurological disorders
Sarkar, T., Patro, N., & Patro, I. K. (2019) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2019.02.005 · Cited by 62 · see citing works
Neurobehavioral and metabolic long-term consequences of neonatal maternal deprivation stress and adolescent olanzapine treatment in male and female rats
Llorente‐Berzal, A., Mela, V., Borcel, É., Valero, M., López‐Gallardo, M., Viveros, M., & Marco, E. M. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.07.031 · Cited by 55 · see citing works
Self-citation
How might stress contribute to increased risk for schizophrenia in children with chromosome 22q11.2 deletion syndrome?
Beaton, E. A., & Simon, T. J. (2010) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-010-9069-9 · Cited by 55 · see citing works
Hyperactivity, increased nicotine consumption and impaired performance in the five-choice serial reaction time task in adolescent rats prenatally exposed to nicotine
Schneider, T., Bizarro, L., Asherson, P., & Stolerman, I. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2728-7 · Cited by 59 · see citing works
Differences in Brain Activity during a Verbal Associative Memory Encoding Task in High- and Low-fit Adolescents
Herting, M. M., & Nagel, B. J. (2012) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00344 · Cited by 54 · see citing works
What’s wrong with my experiment?: The impact of hidden variables on neuropsychopharmacology research
Butler-Struben, H. M., Kentner, A. C., & Trainor, B. C. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01309-1 · Cited by 47 · see citing works
Early life adversities or high fat diet intake reduce cognitive function and alter BDNF signaling in adult rats: Interplay of these factors changes these effects
Arcego, D. M., Krolow, R., Lampert, C., Toniazzo, A. P., Berlitz, C. G. B., Lazzaretti, C., Schmitz, F., Rodrigues, A. F., Wyse, Â. T. D. S., & Dalmaz, C. (2016) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2016.03.001 · Cited by 47 · see citing works
Early maternal deprivation immunologically primes hippocampal synapses by redistributing interleukin-1 receptor type I in a sex dependent manner
Viviani, B., Boraso, M., Valero, M., Gardoni, F., Marco, E. M., Llorente, R., Corsini, E., Galli, C. L., Luca, M. D., Marinovich, M., et al. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.09.008 · Cited by 47 · see citing works
Self-citation
Neuroplasticity and non-invasive brain stimulation in the developing brain
Bandeira, I. D., Lins-Silva, D. H., Barouh, J. L., Faria-Guimarães, D., Dorea-Bandeira, I., Souza, L. S., Alves, G. S., Brunoni, A. R., Nitsche, M. A., Fregni, F., et al. (2021) · Progress in brain research · doi:10.1016/bs.pbr.2021.04.003 · Cited by 45 · see citing works
Investigating mechanisms underlying neurodevelopmental phenotypes of autistic and intellectual disability disorders: a perspective
Kroon, T., Sierksma, M. C., & Meredith, R. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00075 · Cited by 56 · see citing works
Aerobic Fitness Linked to Cortical Brain Development in Adolescent Males: Preliminary Findings Suggest a Possible Role of BDNF Genotype
Herting, M. M., Keenan, M. F., & Nagel, B. J. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00327 · Cited by 42 · see citing works
Hippocampal cell fate regulation by chronic cocaine during periods of adolescent vulnerability: Consequences of cocaine exposure during adolescence on behavioral despair in adulthood
García‐Cabrerizo, R., Keller, B., & García-Fuster, M. J. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.07.040 · Cited by 41 · see citing works
Variable prenatal stress results in impairments of sustained attention and inhibitory response control in a 5-choice serial reaction time task in rats
Wilson, C. A., Schade, R., & Terry, A. V. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.05.040 · Cited by 40 · see citing works
Neonatal tryptophan depletion and corticosterone supplementation modify emotional responses in adult male mice
Zoratto, F., Fiore, M., Ali, S. F., Giovanni Laviola, A., & Macrı̀, S. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.04.015 · Cited by 39 · see citing works
Self-citation
Early life stress and development of the endocannabinoid system: A bidirectional process in programming future coping
Ferber, S. G., Trezza, V., & Weller, A. (2019) · Developmental Psychobiology · doi:10.1002/dev.21944 · Cited by 33 · see citing works
Using animal models for the studies of schizophrenia and depression: The value of translational models for treatment and prevention
Uliana, D. L., Zhu, X., Gomes, F. V., & Grace, A. A. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.935320 · Cited by 32 · see citing works
Physical exercise prevents short and long-term deficits on aversive and recognition memory and attenuates brain oxidative damage induced by maternal deprivation
das Neves, B.-H. S., Menezes, J., Souza, M. A., & Mello‐Carpes, P. B. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.09.019 · Cited by 33 · see citing works
Variable maternal stress in rats alters locomotor activity, social behavior, and recognition memory in the adult offspring
Wilson, C., & Terry, A. V. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2012.12.015 · Cited by 32 · see citing works
Exercise and fluoxetine treatment during adolescence protect against early life stress-induced behavioral abnormalities in adult rats
Zolfaghari, F. S., Pirri, F., Gauvin, E., Peeri, M., & Amiri, S. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2021.173190 · Cited by 31 · see citing works
Adolescent cocaine exposure enhances goal-tracking behavior and impairs hippocampal cell genesis selectively in adult bred low-responder rats
García-Fuster, M. J., Parsegian, A., Watson, S. J., Akil, H., & Flagel, S. B. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4566-0 · Cited by 31 · see citing works
Regional and traffic-related air pollutants are associated with higher consumption of fast food and trans fat among adolescents
Chen, Z., Herting, M. M., Chatzi, L., Belcher, B. R., Alderete, T. L., McConnell, R., & Gilliland, F. D. (2018) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy232 · Cited by 30 · see citing works
Exposure to sublethal concentrations of a pesticide or predator cues induces changes in brain architecture in larval amphibians
Woodley, S. K., Mattes, B. M., Yates, E. K., & Relyea, R. A. (2015) · Oecologia · doi:10.1007/s00442-015-3386-3 · Cited by 29 · see citing works
Glucocorticoids alter neuronal differentiation of human neuroepithelial-like cells by inducing long-lasting changes in the reactive oxygen species balance
Raciti, M., Ong, J., Weis, L., Edoff, K., Battagli, C., Falk, A., & Ceccatelli, S. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.03.022 · Cited by 27 · see citing works
Animal models recapitulating the multifactorial origin of Tourette syndrome.
Macrì, S., Onori, M., Roessner, V., & Laviola, G. (2013) · International review of neurobiology · doi:10.1016/b978-0-12-411546-0.00008-1 · Cited by 22 · see citing works
Self-citation
Early Social Enrichment Improves Social Motivation and Skills in a Monogenic Mouse Model of Autism, theOprm1−/−Mouse
Garbugino, L., Centofante, E., & D'Amato, F. R. (2016) · Neural Plasticity · doi:10.1155/2016/5346161 · Cited by 28 · see citing works
Effects of In utero environment and maternal behavior on neuroendocrine and behavioral alterations in a mouse model of prenatal trauma
Golub, Y., Canneva, F., Funke, R., Frey, S., Distler, J. H. W., von Hörsten, S., Freitag, C. M., Kratz, O., Moll, G. H., & Solati, J. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22387 · Cited by 27 · see citing works
Associations between brain imaging and polygenic scores of mental health and educational attainment in children aged 9–11
Fernández‐Cabello, S., Alnæs, D., van der Meer, D., Dahl, A., Holm, M. C., Kjelkenes, R., Maximov, I. I., Norbom, L. B., Pedersen, M. L., Voldsbekk, I., et al. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119611 · Cited by 26 · see citing works
Anxiety- and depressive-like behaviors in olfactory deficient Cnga2 knockout mice
Chen, Y., Liu, X., Jia, X., Zong, W., Ma, Y., Xu, F., & Wang, J. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.08.042 · Cited by 26 · see citing works
Adolescent cocaine exposure enhanced negative affect following drug re-exposure in adult rats: Attenuation of c-Fos activation
García‐Cabrerizo, R., & García-Fuster, M. J. (2018) · Journal of Psychopharmacology · doi:10.1177/0269881118812353 · Cited by 26 · see citing works
Theoretical and practical considerations behind the use of laboratory animals for the study of Tourette syndrome.
Macrì, S., Proietti-Onori, M., & Laviola, G. (2013) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.014 · Cited by 27 · see citing works
Self-citation
Enduring effects of post-weaning rearing condition on depressive- and anxiety-like behaviors and motor activity in male rats
Mosaferi, B., Babri, S., Ebrahimi, H., & Mohaddes, G. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.02.015 · Cited by 25 · see citing works
Olfactory experience modulates immature neuron development in postnatal and adult guinea pig piriform cortex
He, X., Zhang, X.-M., Wu, J., Fu, J. X., Mou, L.-P., Lu, D., Cai, Y., Luo, X.-G., Pan, A., & Yan, X.-X. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.11.056 · Cited by 25 · see citing works
Disrupted Circadian Rhythm as a Common Player in Developmental Models of Neuropsychiatric Disorders
Marco, E. M., Velarde, E., Llorente, R., & Laviola, G. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_419 · Cited by 25 · see citing works
Self-citation
Pro-social preference in an automated operant two-choice reward task under different housing conditions: Exploratory studies on pro-social decision making
Kentrop, J., Kalamari, A., Danesi, C. H., Kentrop, J. J., van IJzendoorn, M. H., Bakermans‐Kranenburg, M. J., Joëls, M., & van der Veen, R. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100827 · Cited by 25 · see citing works
Role of IL-6 In The Etiology Of Hyperexcitable Neuropsychiatric Conditions: Experimental Evidence And Therapeutic Implications
Atzori, M., García‐Oscos, F., & Méndez, J. A. T. (2012) · Future Medicinal Chemistry · doi:10.4155/fmc.12.156 · Cited by 25 · see citing works
Insecticide-induced changes in amphibian brains: How sublethal concentrations of chlorpyrifos directly affect neurodevelopment
McClelland, S. J., Bendis, R. J., Relyea, R. A., & Woodley, S. K. (2018) · Environmental Toxicology and Chemistry · doi:10.1002/etc.4240 · Cited by 24 · see citing works
Long term effects of stress on hippocampal function: Emphasis on early life stress paradigms and potential involvement of neuropeptide Y
Alviña, K., Farshbaf, M. J., & Mondal, A. K. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24614 · Cited by 23 · see citing works
Perinatal Positive and Negative Influences on the Early Neurobehavioral Reflex and Motor Development
Horváth, G., Reglődi, D., Farkas, J. I., Vadasz, G., Mammel, B., Kvárik, T., Bodzai, G., Kiss-Illes, B., Farkas, D., Matkovits, A., et al. (2014) · Advances in neurobiology · doi:10.1007/978-1-4939-1372-5_8 · Cited by 23 · see citing works
Choline chloride modulates learning, memory, and synaptic plasticity impairments in maternally separated adolescent male rats
Shahraki, S., Esmaeilpour, K., Shabani, M., Sepehri, G., Rajizadeh, M. A., Maneshian, M., Joushi, S., & Sheibani, V. (2021) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10155 · Cited by 22 · see citing works
Independent and Combined Associations of Urinary Arsenic Exposure and Serum Sex Steroid Hormones Among 6-19 - Year Old Children and Adolescents in NHANES 2013 - 2016
Zhang, Y., Xing, H., Hu, Z., Xu, W., Tang, Y., Zhang, J., Niu, Q., & Hu, Y. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.160883 · Cited by 21 · see citing works
Chronic social stress during adolescence: Interplay of paroxetine treatment and ageing
Scharf, S. H., Sterlemann, V., Liebl, C., Müller, M. B., & Schmidt, M. V. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.035 · Cited by 22 · see citing works
The Use of Compounds Derived from Cannabis sativa in the Treatment of Epilepsy, Painful Conditions, and Neuropsychiatric and Neurodegenerative Disorders
Stasiłowicz-Krzemień, A., Nogalska, W., Maszewska, Z., Maleszka, M., Dobroń, M., Szary, A., Kępa, A., Żarowski, M., Hojan, K., Łukowicz, M., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115749 · Cited by 26 · see citing works
Long-term effects of stimulants on neurocognitive performance of Taiwanese children with attention-deficit/hyperactivity disorder
Tsai, C., Huang, Y., Wu, C.-L., Hwang, F., Young, K.-B., Tsai, M.-H., & Chu, S. (2013) · BMC Psychiatry · doi:10.1186/1471-244x-13-330 · Cited by 21 · see citing works
Effects of Environmental Enrichment in Maternally Separated Rats: Age and Sex-Specific Outcomes
Doreste-Méndez, R., Ríos-Ruiz, E. J., Rivera-López, L. L., Gutierrez, A., & Torres-Reverón, A. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00198 · Cited by 21 · see citing works
Prenatal Stress and Peripubertal Stimulation of the Endocannabinoid System Differentially Regulate Emotional Responses and Brain Metabolism in Mice
Macrì, S., Ceci, C., Canese, R., & Laviola, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041821 · Cited by 20 · see citing works
Self-citation
Adolescent GBR12909 exposure induces oxidative stress, disrupts parvalbumin-positive interneurons, and leads to hyperactivity and impulsivity in adult mice
Khan, A., de Jong, L. A. W., Kamenski, M. E., Higa, K. K., Lucero, J. D., Young, J. W., Behrens, M. M., & Powell, S. B. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.11.022 · Cited by 18 · see citing works
Cellular and molecular mechanisms of neurodevelopmental disorders
Ghiani, C. A., & Faúndez, V. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.24041 · Cited by 19 · see citing works
Complex Housing, but Not Maternal Deprivation Affects Motivation to Liberate a Trapped Cage-Mate in an Operant Rat Task
Kalamari, A., Kentrop, J., Danesi, C. H., Graat, E. A. M., van IJzendoorn, M. H., Bakermans‐Kranenburg, M. J., Joëls, M., & van der Veen, R. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.698501 · Cited by 18 · see citing works
Stress and Adrenergic Function: HIF1α, a Potential Regulatory Switch
Wong, D. L., Tai, T. C., Wong‐Faull, D. C., Claycomb, R., Siddall, B. J., Bell, R. A., & Květňanský, R. (2010) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-010-9567-z · Cited by 18 · see citing works
Occupational exposure to inhaled nanoparticles: Are young workers being left in the dust?
Graczyk, H., & Riediker, M. (2019) · Journal of Occupational Health · doi:10.1002/1348-9585.12056 · Cited by 17 · see citing works
Becoming Stressed: Does the Age Matter? Reviewing the Neurobiological and Socio-Affective Effects of Stress throughout the Lifespan
Mañas-Ojeda, A., Ros‐Bernal, F., Olucha-Bordonau, F. E., & Castillo-Gómez, E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165819 · Cited by 16 · see citing works
Brain network modularity predicts changes in cortical thickness in children involved in a physical activity intervention
Chaddock‐Heyman, L., Weng, T. B., Loui, P., Kienzler, C., Weisshappel, R., Drollette, E. S., Raine, L. B., Westfall, D. R., Kao, S., Pindus, D. M., et al. (2021) · Psychophysiology · doi:10.1111/psyp.13890 · Cited by 18 · see citing works
Clinical and neuroimaging correlates of cardiorespiratory fitness in adolescents with bipolar disorder
Popel, N., Kennedy, K. G., Fıksenbaum, L., Mitchell, R. H. B., MacIntosh, B. J., & Goldstein, B. I. (2020) · Bipolar Disorders · doi:10.1111/bdi.12993 · Cited by 16 · see citing works
Examining litter specific variability in mice and its impact on neurodevelopmental studies
Valiquette, V., Guma, E., Cupo, L., Gallino, D., Anastassiadis, C., Snook, E., Devenyi, G. A., & Chakravarty, M. M. (2023) · NeuroImage · doi:10.1016/j.neuroimage.2023.119888 · Cited by 18 · see citing works
Staging Perspectives in Neurodevelopmental Aspects of Neuropsychiatry: Agents, Phases and Ages at Expression
Archer, T., Kostrzewa, R. M., Beninger, R. J., & Palomo, T. (2010) · Neurotoxicity Research · doi:10.1007/s12640-010-9162-6 · Cited by 16 · see citing works
A novel neurobehavioral framework of the effects of positive early postnatal experience on incentive and consummatory reward sensitivity
Fu, Y., & Depue, R. A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.026 · Cited by 16 · see citing works
Prenatal corticosterone and adolescent URB597 administration modulate emotionality and CB1 receptor expression in mice
Ceci, C., Mela, V., Macrı̀, S., Marco, E. M., Viveros, M., & Laviola, G. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3367-3 · Cited by 15 · see citing works
Self-citation
Region‐specific regulation of the serotonin 2 A receptor expression in development and ageing in post mortem human brain
Marinova, Z., Monoranu, C., Fetz, S., Walitza, S., & Grünblatt, E. (2014) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12167 · Cited by 14 · see citing works
The effect of early burn injury on sensitivity to future painful stimuli in dairy heifers
Adcock, S., & Tucker, C. B. (2020) · PLoS ONE · doi:10.1371/journal.pone.0233711 · Cited by 13 · see citing works
Sensitive development windows of prenatal air pollution and cognitive functioning in preschool age Mexican children
Hsu, H. L., Lane, J. M., Schnaas, L., Coull, B. A., Osorio-Valencia, E., Chiu, Y.-H. M., Wilson, A., Just, A. C., Kloog, I., Bellinger, D. C., et al. (2024) · Environmental Epidemiology · doi:10.1097/ee9.0000000000000291 · Cited by 10 · see citing works
Corticotropin-releasing factor infusion in the bed nucleus of the stria terminalis of lactating mice alters maternal care and induces behavioural phenotypes in offspring
Creutzberg, K. C., Kestering-Ferreira, É., Viola, T. W., Wearick‐Silva, L. E., Orso, R., Heberle, B. A., Albrechet‐Souza, L., de Almeida, R. M. M., & Grassi‐Oliveira, R. (2020) · Scientific Reports · doi:10.1038/s41598-020-77118-7 · Cited by 10 · see citing works
Automatic Intra-/Extra-Dimensional Attentional Set-Shifting Task in Adolescent Mice
Ciampoli, M., Scheggia, D., & Papaleo, F. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.704684 · Cited by 10 · see citing works
Delayed yet persistent effects of daily risperidone on activity in developing rats
Stevens, R. M., Gannon, M. A., Griffith, M. S., & Bardgett, M. E. (2016) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000230 · Cited by 10 · see citing works
Animal Models of Developmental Psychopathology
Howell, B., Neigh, G. N., & Sánchez, M. M. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy205 · Cited by 10 · see citing works
Neuronal mechanisms regulating locomotion in adult Drosophila
Gowda, S. B. M., Banu, A., Hussain, S., & Mohammad, F. (2024) · Journal of Neuroscience Research · doi:10.1002/jnr.25332 · Cited by 9 · see citing works
Early life stress and development: preclinical science
Guzman, D., Howell, B., & Sánchez, M. M. (2016) · doi:10.1002/9781118356142.ch3 · Cited by 9 · see citing works
Emotional Vulnerability in Adolescents (EVA) Longitudinal Study: Identifying individual differences in symptoms of adolescent depression and anxiety and their biopsychosocial mechanisms based on demographic and mental health characteristics
Tariq, A., Gray, E., Gregory, A. M., & Chan, S. W. Y. (2024) · Wellcome Open Research · doi:10.12688/wellcomeopenres.22685.1 · Cited by 10 · see citing works
Animal models of developmental dyslexia: Where we are and what we are missing
Lampis, V., Ventura, R., Segni, M. D., Marino, C., D'Amato, F. R., & Mascheretti, S. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.10.022 · Cited by 9 · see citing works
Delayed postnatal brain development and ontogenesis of behavior and cognition in a mouse model of intellectual disability
Gonzalez, L., Sebrié, C., Laroche, S., Vaillend, C., & Poirier, R. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106163 · Cited by 8 · see citing works
Genetically predisposed and resilient animal models of depression reveal divergent responses to early-life adversity
Whitney, A., Lindeque, J. Z., Kruger, R., & Steyn, S. F. (2023) · Acta Neuropsychiatrica · doi:10.1017/neu.2023.37 · Cited by 8 · see citing works

The Long-Term Impact of Early Adversities on Psychiatric Disorders: Focus on Neuronal Plasticity
Luoni, A., Richetto, J., Racagni, G., & Molteni, R. (2015) · Current Pharmaceutical Design · doi:10.2174/1381612821666150105142824 · Cited by 52 · see citing works
Developmental timing and critical windows for the treatment of psychiatric disorders
Marín, O. (2016) · Nature Medicine · doi:10.1038/nm.4225 · Cited by 374 · see citing works
Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models
SÁNCHEZ, M. M., LADD, C. O., & PLOTSKY, P. M. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003029 · Cited by 1,003 · see citing works
Prenatal stress impacts foetal neurodevelopment: Temporal windows of gestational vulnerability
Collins, J. M., Keane, J. M., Deady, C., Khashan, A. S., McCarthy, F. P., O’Keeffe, G. W., Clarke, G. A., Cryan, J. F., Caputi, V., & O’Mahony, S. M. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105793 · Cited by 50 · see citing works
Stress during development: Impact on neuroplasticity and relevance to psychopathology
Fumagalli, F., Molteni, R., Racagni, G., & Riva, M. A. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.01.002 · Cited by 218 · see citing works

Authors: Marco, E. M., Macrì, S., & Laviola, G.
Affiliations: Istituto Superiore di Sanità (IT)
ORCID: Marco, Eva M.
Venue: Neurotoxicity Research
Publisher: Springer Science and Business Media LLC
Published: 2010-07-07
Volume: 19
Issue: 2
Pages: 286-307
ISSN: 1029-8428 (ISSN-L)
1476-3524
DOI: 10.1007/s12640-010-9205-z
OpenAlex: W2111063637
Cited by: 144
References: 260
Citations by year: 2026: 3 · 2025: 7 · 2024: 8 · 2023: 6 · 2022: 10 · 2021: 14 · 2020: 13 · 2019: 8 · 2018: 6 · 2017: 5 · 2016: 15 · 2015: 9 · 2014: 7 · 2013: 10 · 2012: 13
FWCI: 1.52
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Neurotoxicity Research (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: double-hit hypothesis, prenatal stress, maternal separation, corticosterone, prenatal hypoxia, prenatal immune challenge, pregnancy complications, methylphenidate, social enrichment, neuroplasticity
MeSH terms: Age Factors, Animals, Mental Disorders, Critical Period, Psychological, Disease Models, Animal, Female, Humans, Pregnancy, Prenatal Exposure Delayed Effects, Risk Factors, Stress, Psychological, Evidence-Based Medicine

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks