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Critical Age Windows for Neurodevelopmental Psychiatric Disorders: Evidence from Animal Models
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.
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“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
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Items 201–260 of 260
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
Neuropsychological long-term sequelae of perinatal asphyxia
Mañeru, C., Junqué, C., Botet, F., Tallada, M., & Guàrdia‐Olmos, J. (2001) · Brain Injury · doi:10.1080/02699050110074178 · Cited by 84
Maternal infection during pregnancy and schizophrenia
Boksa, P. (2008) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0818 · Cited by 83
Macrı̀, S., & Laviola, G. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.02.009 · Cited by 81
Self-citationStein, D. J., Ives-Deliperi, V. L., & Thomas, K. G. F. (2008) · CNS Spectrums · doi:10.1017/s1092852900013869 · Cited by 80
Tohmi, M., Tsuda, N., Watanabe, Y., Kakita, A., & Nawa, H. (2004) · Neuroscience Research · doi:10.1016/j.neures.2004.05.010 · Cited by 78
Laviola, G., Ognibene, E., Romano, E., Adriani, W., & Keller, F. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.09.006 · Cited by 76
Long-term effects of maternal deprivation on the corticosterone response to stress in rats
Suchecki, D., & Tufik, S. (1997) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1997.273.4.r1332 · Cited by 75
Tobacco use as a predictor of illicit drug use and drug-related problems in Colombian youth
SIQUEIRA, L., & Brook, J. S. (2002) · Journal of Adolescent Health · doi:10.1016/s1054-139x(02)00534-7 · Cited by 74
Nowakowski, R. S., & Hayes, N. L. (1999) · Development and Psychopathology · doi:10.1017/s0954579499002126 · Cited by 74
Law, A. J., Pei, Q., Walker, M. A., Gordon-Andrews, H., Weickert, C. S., Feldon, J., Pryce, C. R., & Harrison, P. J. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.106 · Cited by 74
van Oers, H. V., de Kloet, E. D., & Levine, S. (1997) · Stress · doi:10.3109/10253899709013745 · Cited by 73
The effects of early maternal deprivation on auditory information processing in adult wistar rats
Ellenbroek, B. A., de Bruin, N. M. W. J., Kroonenburg, P. T. J. M. V. D., van Luijtelaar, E. L. J. M., & Cools, A. R. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.10.024 · Cited by 73
Giovanni Laviola, A., Adriani, W., Rea, M., Aloe, L., & Alleva, E. (2004) · Psychopharmacology · doi:10.1007/s00213-004-1800-3 · Cited by 72
Spindler, G. D. (1992) · Anthropology News · doi:10.1111/an.1992.33.7.3.2 · Cited by 70
Effects of early postnatal anoxia on adult learning and emotion in rats
Buwalda, B., Nyakas, C. J., Vosselman, H. J., & Luiten, P. G. M. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(94)00108-r · Cited by 70
Birth insult increases amphetamine-induced behavioral responses in the adult rat
El‐Khodor, B. F., & Boksa, P. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00194-8 · Cited by 69
D'Amato, F. R. (1992) · Hormones and Behavior · doi:10.1016/0018-506x(92)90015-n · Cited by 68
Resilience and vulnerability are dose-dependently related to neonatal stressors in mice
Macrı̀, S., Granstrem, O., Shumilina, M. V., Santos, F. J., Berry, A., Saso, L., & Laviola, G. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.07.006 · Cited by 68
Self-citationMarco, E. M., Granstrem, O., Moreno, E., Llorente, R., Adriani, W., Giovanni Laviola, A., & Viveros, M. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.11.013 · Cited by 67
Self-citationLeo, D., Adriani, W., Cavaliere, C., Cirillo, G., Marco, E. M., Romano, E., di Porzio, U., Papa, M., Perrone‐Capano, C., & Giovanni Laviola, A. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00486.x · Cited by 66
Self-citationTHE EFFECT OF TOTAL SOCIAL DEPRIVATION ON THE DEVELOPMENT OF MONKEY BEHAVIOR.
Harlow, H. F., Gl, R., & Ga, G. (1964) · PubMed · Cited by 66
The Role of Serotonin in the Pathophysiology of Depression: As Important As Ever
Nemeroff, C. B., & Owens, M. J. (2009) · Clinical Chemistry · doi:10.1373/clinchem.2009.123752 · Cited by 64
Marchetti, B., Morale, M. C., Testa, N., Tirolo, C., Caniglia, S., Amor, S., Dijkstra, C. D., & Barden, N. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00130-8 · Cited by 62
Striatal dopamine output is compromised within +/− BDNF mice
Dluzen, D. E., Anderson, L. I., McDermott, J. L., Kučera, J., & Walro, J. M. (2001) · Synapse · doi:10.1002/syn.10027 · Cited by 62
Macrì, S., Pasquali, P., Bonsignore, L. T., Pieretti, S., Cirulli, F., Chiarotti, F., & Laviola, G. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001015 · Cited by 60
Self-citationPrenatal infectious and nutritional factors and risk of adult schizophrenia
Penner, J. D., & Brown, A. S. (2007) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.7.7.797 · Cited by 58
Pereira, L. O., Nabinger, P. M., Strapasson, A. C. P., Nardin, P., Gonçalves, C. A., Siqueira, I. R., & Netto, C. A. (2008) · Brain Research · doi:10.1016/j.brainres.2008.10.017 · Cited by 58
Adriani, W., Canese, R., Podo, F., & Laviola, G. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.11.010 · Cited by 56
Llorente, E., Brito, M. L., Machado, P., & González, M. C. (2002) · Journal of Physiology and Biochemistry · doi:10.1007/bf03179851 · Cited by 56
Akil, H. (2005) · Nature Medicine · doi:10.1038/nm0205-116 · Cited by 54
A developmental comparison of the neurobehavioral effects of ecstasy (MDMA)
Piper, B. J. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.10.002 · Cited by 54
Maternal Separation Reduces Latent Inhibition in the Conditioned Taste-Aversion Paradigm
Ellenbroek, B. A., & Cools, A. R. (1995) · Radboud Repository (Radboud University) · Cited by 50
El-Khodor, B., & Boksa, P. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00228-7 · Cited by 49
Adolescent Alcohol Drinking and Its Long-Range Consequences
McBride, W. J., Bell, R. L., Rodd, Z. A., Strother, W. N., & Murphy, J. M. (2005) · Kluwer Academic Publishers-Plenum Publishers eBooks · doi:10.1007/0-306-48626-1_6 · Cited by 48
Disrupted‐in‐Schizophrenia‐1 (DISC1)
Sawamura, N., & Sawa, A. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1377.018 · Cited by 48
Comorbid conditions in schizophrenia
Fenton, W. S. (2001) · Current Opinion in Psychiatry · doi:10.1097/00001504-200101000-00004 · Cited by 46
Assessment of Aggressive Behavior in Rodents
Alleva, E. (1993) · Methods in neurosciences · doi:10.1016/b978-0-12-185277-1.50012-5 · Cited by 44
Chen, Y., Hillefors, M., Herrera‐Marschitz, M., Bjelke, B., Gross, J., Andersson, K., & von Euler, G. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6497 · Cited by 44
Neonatal impact of leukemia inhibitory factor on neurobehavioral development in rats
Watanabe, Y., Hashimoto, S., Kakita, A., Takahashi, H., Ko, J., Mizuno, M., Someya, T., Patterson, P. H., & Nawa, H. (2004) · Neuroscience Research · doi:10.1016/j.neures.2003.12.001 · Cited by 43
HPA‐axis activity as a predictor of future disruptive behaviors in young adolescents
Sondeijker, F., Ferdinand, R. F., Oldehinkel, A. J., Tiemeier, H. W., Ormel, J., & Verhulst, F. C. (2008) · Psychophysiology · doi:10.1111/j.1469-8986.2008.00639.x · Cited by 43
Grojean, S., Schroeder, H., Pourié, G., Charriaut‐Marlangue, C., Koziel, V., Desor, D., Vert, P., & Daval, J. (2003) · Neurobiology of Disease · doi:10.1016/s0969-9961(03)00082-2 · Cited by 42
Caputa, M., Rogalska, J., Wentowska, K., & Nowakowska, A. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.05.015 · Cited by 38
Can the Behaviour Abnormalities Induced by Gestational Stress in Rats be Prevented or Reversed?
Weinstock, M. (2002) · Stress · doi:10.1080/1025389021000010503 · Cited by 37
Are cannabinoid receptor knockout mice animal models for schizophrenia?
Fritzsche, M. (2001) · Medical Hypotheses · doi:10.1054/mehy.2000.1261 · Cited by 37
Animal models of perinatal asphyxia: Contributions, contradictions, clinical relevance
Painter, M. J. (1995) · Seminars in Pediatric Neurology · doi:10.1016/s1071-9091(05)80004-x · Cited by 36
Escorihuela, R. M., Fernández‐Teruel, A., Zapata, A. G., Núñez, J. F., & Tobeña, A. (1993) · Pharmacological Research · doi:10.1006/phrs.1993.1109 · Cited by 36
Scheepens, A., Wassink, G., & Blanco, C. E. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00608-9 · Cited by 35
Gentling and weight gain in the albino rat.
Weininger, O., McClelland, W. J., & Arima, R. K. (1954) · Canadian Journal of Psychology/Revue Canadienne de Psychologie · doi:10.1037/h0083606 · Cited by 35
Adriani, W., Giannakopoulou, D., Bokulić, Z., Jernej, B., Alleva, E., & Giovanni Laviola, A. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0223-0 · Cited by 35
Macrı̀, S., Spinelli, S., Adriani, W., Higley, J. D., & Laviola, G. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.06.026 · Cited by 34
Self-citationCasolini, P., Zuena, A. R., Cinque, C., Matteucci, P., Alemà, G., Adriani, W., Carpinelli, G., Santoro, F., Alleva, E., Bosco, P., et al. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03349.x · Cited by 33
"Critical Periods" in the Development of Behavior
Schneirla, T. C., & Rosenblatt, J. S. (1963) · Science · doi:10.1126/science.139.3559.1110 · Cited by 32
Wakuda, T., Matsuzaki, H., Suzuki, K., Iwata, Y., Shinmura, C., Suda, S., Iwata, K., Yamamoto, S., Sugihara, G., Tsuchiya, K. J., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003648 · Cited by 31
de Irala, J., Ruiz‐Canela, M., & Martínez‐González, M. Á. (2005) · PubMed · Cited by 28
Baseline cortisol measures and developmental pathways of anxiety in early adolescence
Greaves‐Lord, K., Huizink, A. C., Oldehinkel, A. J., Ormel, J., Verhulst, F. C., & Ferdinand, R. F. (2009) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.2009.01402.x · Cited by 21
Neurogenesis in the adult brain.
Maćkowiak, M., Chocyk, A., Markowicz-Kula, K., & Wędzony, K. (2004) · PubMed · Cited by 18
Brain development and the ontogeny of developmental disabilities.
Acosta, M. T., Gallo, V., & Batshaw, M. L. (2002) · PubMed · Cited by 17
Stress, depression and schizophrenia in view of psychoimmunology.
Dąbkowska, M., & RYBAKOWSKI, J. K. (1992) · PubMed · Cited by 5
[Animal models of hypoxic-ischemic encephalopathy].
Rufini, O., Valanzano, A., & Calamandrei, G. (2001) · PubMed · Cited by 1
Flagged first, then by citations
Research works printed but not linked: 1
- Lorenz K (1937/1957) The conception of instinctive behavior. In: Schiller CH (ed) Instinctive behavior. International Universities Press, New York, pp 129–175
Cited by
Sorted by citations
Brenhouse, H. C., & Andersen, S. L. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.04.013 · Cited by 363
Burke, N. N., Finn, D. P., McGuire, B. E., & Roche, M. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.23802 · Cited by 268
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 247
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
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 193
Metadata
- Authors
- Marco, E. M., Macrì, S., & Laviola, G.
- Affiliations
- Istituto Superiore di Sanità (IT)
- ORCID
- Marco, Eva M.
- Venue
- Neurotoxicity Research
- Published
- 2010-07-07
- Volume
- 19
- Issue
- 2
- Pages
- 286-307
- ISSN
- 1029-8428 (ISSN-L)
- 1476-3524
- 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
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