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Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models.
Open accessAbstract
Vulnerable periods during the development of the nervous system are sensitive to environmental insults because they are dependent on the temporal and regional emergence of critical developmental processes (i.e., proliferation, migration, differentiation, synaptogenesis, myelination, and apoptosis). Evidence from numerous sources demonstrates that neural development extends from the embryonic period through adolescence. In general, the sequence of events is comparable among species, although the time scales are considerably different. Developmental exposure of animals or humans to numerous agents (e.g., X-ray irradiation, methylazoxymethanol, ethanol, lead, methyl mercury, or chlorpyrifos) demonstrates that interference with one or more of these developmental processes can lead to developmental neurotoxicity. Different behavioral domains (e.g., sensory, motor, and various cognitive functions) are subserved by different brain areas. Although there are important differences between the rodent and human brain, analogous structures can be identified. Moreover, the ontogeny of specific behaviors can be used to draw inferences regarding the maturation of specific brain structures or neural circuits in rodents and primates, including humans. Furthermore, various clinical disorders in humans (e.g., schizophrenia, dyslexia, epilepsy, and autism) may also be the result of interference with normal ontogeny of developmental processes in the nervous system. Of critical concern is the possibility that developmental exposure to neurotoxicants may result in an acceleration of age-related decline in function. This concern is compounded by the fact that developmental neurotoxicity that results in small effects can have a profound societal impact when amortized across the entire population and across the life span of humans.
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“By the time the apical radial glial progenitors within the prefrontal subdomains start dividing asymmetrically, the number of neurons will increase rapidly and peaks between week 13 and 16 of gestation in human (E10-E15 rodents/E43-E50 primates), specifically in the dorsal telencephalon [44–47].”
From Development of prefrontal cortex (2022) · cites this paper as [47]
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“This is based on developmental endpoints, since rodent exposures in early infancy (i.e., the neonatal period) mimic human 3rd trimester exposures for several organs, including the lung [50] and brain [51].”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [51]
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“This window of exposure is critical to central nervous system development and equivalent to human 3rd trimester brain development [51].”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [51]
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“Developmental neurotoxicity (DNT) testing is particularly critical, as chemical-induced disruptions in neurogenesis, synaptogenesis, migration, or network formation during vulnerable developmental windows can cause lifelong neurological deficits (Rice and Barone, 2000; Grandjean and Landrigan, 2014).”
From Challenges and solutions in transitioning to animal-free standards: a comprehensive analysis of components in human cell-based developmental neurotoxicity assays (2026) · cites this paper as Rice and Barone, 2000
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“These neurodevelopmental processes physiologically occurs during the first and second trimester of pregnancy [231].”
From Consensus Paper: Pathological Role of the Cerebellum in Autism (2012) · cites this paper as [231]
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“This field is especially promising for cerebellar neuropathology, in light of the prolonged developmental time window exposing cerebellar circuits to damage by environmental agents in genetically susceptible individuals not only prenatally, but also postnatally [231].”
From Consensus Paper: Pathological Role of the Cerebellum in Autism (2012) · cites this paper as [231]
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Semple, B. D., Blomgren, K., Gimlin, K., Ferriero, D. M., & Noble-Haeusslein, L. J. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.04.001 · Cited by 2,132
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Metadata
- Authors
- Rice, D., & Barone, S.
- Affiliations
- Environmental Protection Agency (US)
- Venue
- Environmental Health Perspectives
- Publisher
- American Chemical Society (ACS)
- Published
- 2000-06-01
- Volume
- 108
- Issue
- suppl 3
- Pages
- 511-533
- ISSN
- 0091-6765 (ISSN-L)
- 1552-9924
- PMC
- PMC1637807
- OpenAlex
- W2120095635
- Cited by
- 2,944
- References
- 455
- Citations by year
- 2026: 46 · 2025: 94 · 2024: 148 · 2023: 180 · 2022: 173 · 2021: 181 · 2020: 177 · 2019: 163 · 2018: 168 · 2017: 141 · 2016: 150 · 2015: 183 · 2014: 141 · 2013: 124 · 2012: 124
- FWCI
- 1.77
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Environmental Health Perspectives (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- U.S. Environmental Protection Agency
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Anesthesia and Neurotoxicity Research
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Pharmacological Effects and Toxicity Studies
- Keywords
- critical period, developmental neurotoxicity, brain development, neuronal proliferation, neuronal migration, neuronal differentiation, synaptogenesis, myelination, apoptosis, early life exposure, X-ray irradiation, methylazoxymethanol, ethanol, lead, methylmercury, chlorpyrifos, behavioral development, brain maturation, schizophrenia, dyslexia, epilepsy, autism spectrum disorder, age-related cognitive decline
- MeSH terms
- Adult, Aged, Aging, Animals, Cell Differentiation, Cell Movement, Child, Child, Preschool, Female, Embryonic and Fetal Development, Humans, Infant, Infant, Newborn, Middle Aged, Nervous System, Neuronal Plasticity, Neurotoxins, Pregnancy, Primates, Time Factors, Xenobiotics, Apoptosis, Mice, Rats
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.
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