Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models.

Rice, D; Barone, S

doi:10.1289/ehp.00108s3511

Cited by 2,944Neurogenesis and neuroplasticity mechanismsAnesthesia and Neurotoxicity ResearchPharmacological Effects and Toxicity Studies

Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models.

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Rice, D, Barone, S·2000·Environmental Health Perspectives

DOI 10.1289/ehp.00108s3511PMC PMC1637807

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Abstract

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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The number of neurons increases rapidly and peaks between week 13 and 16 of gestation in humans, specifically in the dorsal telencephalon.
“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]
The Proliferation discussion (pp. 514–515) describes rapid neocortical cell proliferation and region-specific timelines of neurogenesis. It does not state that neuron numbers peak at human gestational weeks 13–16, or locate such a peak specifically in the dorsal telencephalon; its explicit peak-proliferation range is GD 13–18 in rats. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Rodent exposures in early infancy (i.e., the neonatal period) mimic human 3rd trimester exposures for several organs, including the lung and brain.
“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]
The early postnatal window is critical to central nervous system development and equivalent to human third trimester brain development.
“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]
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.
“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
These neurodevelopmental processes physiologically occur during the first and second trimester of pregnancy.
“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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Brain development in rodents and humans: identifying benchmarks of maturation and vulnerability to injury across species
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Early-life programming of later-life brain and behavior: a critical role for the immune system
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Neonatal Exposure to Sevoflurane Induces Abnormal Social Behaviors and Deficits in Fear Conditioning in Mice
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Neonatal Exposure to Perfluorooctane Sulfonate (PFOS) and Perfluorooctanoic Acid (PFOA) Causes Neurobehavioural Defects in Adult Mice
Johansson, N., Fredriksson, A., & Eriksson, P. (2008) · NeuroToxicology · doi:10.1016/j.neuro.2007.10.008 · Cited by 463 · see citing works
What causes autism? Exploring the environmental contribution
Landrigan, P. J. (2010) · Current Opinion in Pediatrics · doi:10.1097/mop.0b013e328336eb9a · Cited by 429 · see citing works
Endocrine disruptors and childhood social impairment
Miodovnik, A., Engel, S. M., Zhu, C., Ye, X., Soorya, L. V., Silva, M. J., Calafat, A. M., & Wolff, M. S. (2011) · NeuroToxicology · doi:10.1016/j.neuro.2010.12.009 · Cited by 423 · see citing works
Potential developmental neurotoxicity of pesticides used in Europe
Bjørling-Poulsen, M., Andersen, H. R., & Grandjean, P. (2008) · Environmental Health · doi:10.1186/1476-069x-7-50 · Cited by 407 · see citing works
Development of prefrontal cortex
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Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter
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“, the neonatal period) mimic human 3rd trimester exposures for several organs, including the lung [50] and brain [51].”
Background
Chronic Δ9-Tetrahydrocannabinol During Adolescence Provokes Sex-Dependent Changes in the Emotional Profile in Adult Rats: Behavioral and Biochemical Correlates
Rubino, T., Vigano', D., Realini, N., Guidali, C., Braida, D., Capurro, V., Castiglioni, C., Cherubino, F., Romualdi, P., Candeletti, S., et al. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301664 · Cited by 345 · see citing works
Human pluripotent stem cell-derived neural constructs for predicting neural toxicity
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Perinatal iron deficiency and neurocognitive development
Radlowski, E. C., & Johnson, R. W. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00585 · Cited by 315 · see citing works
Prefrontal Cortex Development in Health and Disease: Lessons from Rodents and Humans
Chini, M., & Hanganu-Opatz, I. L. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2020.10.017 · Cited by 253 · see citing works
Environmental factors associated with a spectrum of neurodevelopmental deficits
Mendola, P., Selevan, S. G., Gutter, S., & Rice, D. (2002) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.10033 · Cited by 279 · see citing works
Self-citation
Sensitive periods in human social development: New insights from research on oxytocin, synchrony, and high-risk parenting
Feldman, R. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000048 · Cited by 271 · 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
Evidence of Toxicity, Oxidative Stress, and Neuronal Insult in Autism
Kern, J. K., & Jones, A. M. (2006) · Journal of Toxicology and Environmental Health, Part B · doi:10.1080/10937400600882079 · Cited by 265 · see citing works
Maternal serum vitamin D levels during pregnancy and offspring neurocognitive development
Whitehouse, A. J. O., Holt, B. J., Serralha, M., Holt, P. G., Kusel, M. M. H., & Hart, P. H. (2012) · Pediatrics · doi:10.1542/peds.2011-2644 · Cited by 259 · see citing works
Developmental neurotoxicity of inhaled ambient ultrafine particle air pollution: Parallels with neuropathological and behavioral features of autism and other neurodevelopmental disorders
Allen, J. L., Oberdorster, G., Morris-Schaffer, K., Wong, C., Klocke, C., Sobolewski, M., Conrad, K., Mayer-Proschel, M., & Cory-Slechta, D. A. (2017) · NeuroToxicology · doi:10.1016/j.neuro.2015.12.014 · Cited by 241 · see citing works
Cognition and brain structure following early childhood surgery with anesthesia
Backeljauw, B., Holland, S. K., Altaye, M., & Loepke, A. W. (2015) · PEDIATRICS · doi:10.1542/peds.2014-3526 · Cited by 239 · see citing works
The Role of Iron in Learning and Memory
Fretham, S. J. B., Carlson, E. S., & Georgieff, M. K. (2011) · Advances in Nutrition · doi:10.3945/an.110.000190 · Cited by 235 · see citing works
Paracetamol use during pregnancy — a call for precautionary action
Bauer, A. Z., Swan, S. H., Kriebel, D., Liew, Z., Taylor, H. S., Bornehag, C.-G., Andrade, A. M., Olsen, J., Jensen, R. H., Mitchell, R. T., et al. (2021) · Nature Reviews Endocrinology · doi:10.1038/s41574-021-00553-7 · Cited by 228 · see citing works
Developmental Neurotoxicity of Perfluorinated Chemicals Modeled <i>in Vitro</i>
Slotkin, T. A., MacKillop, E. A., Melnick, R. L., Thayer, K. A., & Seidler, F. J. (2008) · Environmental Health Perspectives · doi:10.1289/ehp.11253 · Cited by 225 · see citing works
The Effects of the World Trade Center Event on Birth Outcomes among Term Deliveries at Three Lower Manhattan Hospitals
Lederman, S. A., Rauh, V., Weiss, L., Stein, J. L., Hoepner, L. A., Becker, M., & Perera, F. P. (2004) · Environmental Health Perspectives · doi:10.1289/ehp.7348 · Cited by 220 · see citing works
Maternal tobacco smoking, nicotine replacement and neurobehavioural development
Pauly, J. R., & Slotkin, T. A. (2008) · Acta Paediatrica · doi:10.1111/j.1651-2227.2008.00852.x · Cited by 214 · see citing works
Perinatal iron deficiency alters apical dendritic growth in hippocampal CA1 pyramidal neurons
Jorgenson, L. A., Wobken, J. D., & Georgieff, M. K. (2003) · Developmental Neuroscience · doi:10.1159/000075667 · Cited by 209 · see citing works
Polychlorinated Biphenyl and Organochlorine Pesticide Concentrations in Maternal Mid-Pregnancy Serum Samples: Association with Autism Spectrum Disorder and Intellectual Disability
Lyall, K., Croen, L. A., Sjödin, A., Yoshida, C. K., Zerbo, O., Kharrazi, M., & Windham, G. C. (2017) · Environmental Health Perspectives · doi:10.1289/ehp277 · Cited by 203 · see citing works
Early-life adversity and brain development: Is the microbiome a missing piece of the puzzle?
O’Mahony, S. M., Clarke, G., Dinan, T. G., & Cryan, J. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.068 · Cited by 203 · see citing works
Role of Prenatal Hypoxia in Brain Development, Cognitive Functions, and Neurodegeneration
Nalivaeva, N. N., Turner, A. J., & Zhuravin, I. A. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00825 · Cited by 181 · see citing works
Early life nutrition and neural plasticity
Georgieff, M. K., Brunette, K. E., & Tran, P. V. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000061 · Cited by 177 · see citing works
Project TENDR: Targeting Environmental Neuro-Developmental Risks The TENDR Consensus Statement
Bennett, D., Bellinger, D. C., Birnbaum, L. S., DABT, A.T.S, Bradman, A., Chen, A., Cory-Slechta, D. A., Engel, S. M., Fallin, M. D., et al. (2016) · Environmental Health Perspectives · doi:10.1289/ehp358 · Cited by 169 · see citing works
Lower maternal folate status in early pregnancy is associated with childhood hyperactivity and peer problems in offspring
Schlotz, W., Jones, A., Phillips, D. I. W., Gale, C. R., Robinson, S. M., & Godfrey, K. M. (2010) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2009.02182.x · Cited by 165 · see citing works
Fetal iron deficiency disrupts the maturation of synaptic function and efficacy in area CA1 of the developing rat hippocampus
Jorgenson, L. A., Sun, M., O'Connor, M., & Georgieff, M. K. (2005) · Hippocampus · doi:10.1002/hipo.20128 · Cited by 162 · see citing works
Childhood autism spectrum disorders and exposure to nitrogen dioxide, and particulate matter air pollution: A review and meta-analysis
Flores-Pajot, M.-C., Ofner, M., Do, M. T., Lavigne, E., & Villeneuve, P. J. (2016) · Environmental Research · doi:10.1016/j.envres.2016.07.030 · Cited by 157 · 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
Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models
Marco, E. M., Macrì, S., & Laviola, G. (2011) · Neurotoxicity Research · doi:10.1007/s12640-010-9205-z · Cited by 144 · see citing works
Circulating 25-hydroxyvitamin D3 in pregnancy and infant neuropsychological development
Morales, E., Guxens, M., Llop, S., Rodríguez-Bernal, C. L., Tardón, A., Riaño, I., Ibarluzea, J., Lertxundi, N., Espada, M., Rodriguez, A., et al. (2012) · Pediatrics · doi:10.1542/peds.2011-3289 · Cited by 140 · see citing works
Fetal and Infant Outcomes in the Offspring of Parents With Perinatal Mental Disorders: Earliest Influences
Aktar, E., Qu, J., Lawrence, P. J., Tollenaar, M. S., Elzinga, B. M., & Bögels, S. M. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00391 · Cited by 140 · see citing works
Association between Early Life Exposure to Air Pollution and Working Memory and Attention
Rivas, I., Basagaña, X., Cirach, M., López-Vicente, M., Suades-González, E., Garcia-Esteban, R., Álvarez-Pedrerol, M., Dadvand, P., & Sunyer, J. (2019) · Environmental Health Perspectives · doi:10.1289/ehp3169 · Cited by 140 · see citing works
Maternal Autoantibodies in Autism
Braunschweig, D., & Van de Water, J. (2012) · Archives of Neurology · doi:10.1001/archneurol.2011.2506 · Cited by 122 · see citing works
Teeth as a biomarker of past chemical exposure
Arora, M., & Austin, C. (2013) · Current Opinion in Pediatrics · doi:10.1097/mop.0b013e32835e9084 · Cited by 114 · see citing works
Putative adverse outcome pathways relevant to neurotoxicity
Bal-Price, A., Crofton, K. M., Sachana, M., Shafer, T. J., Behl, M., Forsby, A., Hargreaves, A., Landesmann, B., Lein, P. J., Louisse, J., et al. (2015) · Critical Reviews in Toxicology · doi:10.3109/10408444.2014.981331 · Cited by 114 · see citing works
The emergence of gonadal hormone influences on dopaminergic function during puberty
Kuhn, C., Johnson, M., Thomae, A., Luo, B., Simon, S. A., Zhou, G., & Walker, Q. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.10.015 · Cited by 113 · see citing works
The role of cerebellar circuitry alterations in the pathophysiology of autism spectrum disorders
Mosconi, M. W., Wang, Z., Schmitt, L. M., Tsai, P., & Sweeney, J. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00296 · Cited by 112 · see citing works
Hubs in the human fetal brain network
van den Heuvel, M. I., Turk, E., Manning, J. H., Hect, J., Hernandez-Andrade, E., Hassan, S. S., Romero, R., van den Heuvel, M. P., & Thomason, M. E. (2018) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2018.02.001 · Cited by 108 · see citing works
“Insight into hub emergence before birth may be of great importance, since the fetal period is a critical time in brain development (Rice and Barone, 2000; Keunen et al., 2017) in which seemingly small disturbances, insults or exposures can produce lifelong changes in neurological and mental…”
Maternal vitamin D levels and the autism phenotype among offspring
Whitehouse, A. J. O., Holt, B. J., Serralha, M., Holt, P. G., Hart, P. H., & Kusel, M. M. H. (2013) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-012-1676-8 · Cited by 100 · see citing works
Genome-wide expression studies in Autism spectrum disorder, Rett syndrome, and Down syndrome
Lintas, C., Sacco, R., & Persico, A. M. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.11.010 · Cited by 96 · see citing works
Physical activity and brain development
Gomes da Silva, S., & Arida, R. M. (2015) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.2015.1077115 · Cited by 89 · see citing works
Bisphenol A Impairs Synaptic Plasticity by Both Pre‐ and Postsynaptic Mechanisms
Hu, F., Li, T., Gong, H., Chen, Z., Jin, Y., Xu, G., & Wang, M. (2017) · Advanced Science · doi:10.1002/advs.201600493 · Cited by 87 · see citing works
Long-term consequences of parental death in childhood: Psychological and physiological manifestations.
Luecken, L. J. (2008) · Handbook of bereavement research and practice: Advances in theory and intervention. · doi:10.1037/14498-019 · Cited by 89 · see citing works
Neuropathological Consequences of Gestational Exposure to Concentrated Ambient Fine and Ultrafine Particles in the Mouse
Klocke, C., Allen, J. L., Sobolewski, M., Mayer-Pröschel, M., Blum, J. L., Lauterstein, D., Zelikoff, J. T., & Cory-Slechta, D. A. (2017) · Toxicological Sciences · doi:10.1093/toxsci/kfx010 · Cited by 87 · see citing works
Testing for developmental neurotoxicity using a battery of in vitro assays for key cellular events in neurodevelopment
Harrill, J. A., Freudenrich, T., Wallace, K., Ball, K., Shafer, T. J., & Mundy, W. R. (2018) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2018.04.001 · Cited by 86 · see citing works
Got worms? Perinatal exposure to helminths prevents persistent immune sensitization and cognitive dysfunction induced by early-life infection
Williamson, L. L., McKenney, E. A., Holzknecht, Z. E., Belliveau, C., Rawls, J. F., Poulton, S., Parker, W., & Bilbo, S. D. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.07.006 · Cited by 84 · see citing works
Adolescent voluntary exercise attenuated hippocampal innate immunity responses and depressive-like behaviors following maternal separation stress in male rats
Sadeghi, M., Peeri, M., & Hosseini, M.-J. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.05.017 · Cited by 83 · see citing works
Neurocognitive consequences of cigarette smoking in young adults–a comparison with pre-drug performance
Fried, P. A., Watkinson, B., & Gray, R. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.06.003 · Cited by 81 · see citing works
Elevated 5-hydroxymethylcytosine in the Engrailed-2 (EN-2) promoter is associated with increased gene expression and decreased MeCP2 binding in autism cerebellum
James, S. J., Shpyleva, S., Melnyk, S., Pavliv, O., & Pogribny, I. P. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.87 · Cited by 79 · see citing works
Magnitude and timing of major white matter tract maturation from infancy through adolescence with NODDI
Lynch, K. M., Cabeen, R. P., Toga, A. W., & Clark, K. A. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116672 · Cited by 79 · see citing works
When mothering goes awry: challenges and opportunities for utilizing evidence across rodent, nonhuman primate and human studies to better define the biological consequences of negative early caregiving
Drury, S. S., Sánchez, M. M., & Gonzalez, A. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.10.007 · Cited by 72 · see citing works
Effects of Adolescent THC Exposure on the Prefrontal GABAergic System: Implications for Schizophrenia-Related Psychopathology
Renard, J., Rushlow, W. J., & Laviolette, S. R. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00281 · Cited by 62 · see citing works
Linking genetics to epigenetics: The role of folate and folate‐related pathways in neurodevelopmental disorders
Lintas, C. (2019) · Clinical Genetics · doi:10.1111/cge.13421 · Cited by 62 · see citing works
Perfluorododecanoic Acid Exposure Induced Developmental Neurotoxicity in Zebrafish Embryos
Guo, X., Zhang, S., Lu, S., Zheng, B., Xie, P., Chen, J., Li, G., Liu, C., Wu, Q., Cheng, H., et al. (2018) · Environmental Pollution · doi:10.1016/j.envpol.2018.06.013 · Cited by 58 · see citing works
Developmental Lead Exposure Alters Synaptogenesis through Inhibiting Canonical Wnt Pathway In Vivo and In Vitro
Hu, F., Xu, L., Liu, Z.-H., Ge, M.-M., Ruan, D.-Y., & Wang, H.-L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101894 · Cited by 54 · see citing works
Innate immunity and cellular senescence: The good and the bad in the developmental and aged brain
Santoro, A., Spinelli, C. C., Martucciello, S., Nori, S. L., Capunzo, M., Puca, A. A., & Ciaglia, E. (2018) · Journal of Leukocyte Biology · doi:10.1002/jlb.3mr0118-003r · Cited by 50 · see citing works
The effect of lead exposure on brain iron homeostasis and the expression of DMT1/FP1 in the brain in developing and aged rats
Zhu, G., Fan, G., Feng, C., Li, Y., Chen, Y., Zhou, F., Du, G., Jiao, H., Liu, Z., Xiao, X., et al. (2013) · Toxicology Letters · doi:10.1016/j.toxlet.2012.11.024 · Cited by 48 · see citing works
Scientific Validation of Human Neurosphere Assays for Developmental Neurotoxicity Evaluation
Koch, K., Bartmann, K., Hartmann, J., Kapr, J., Klose, J., Kuchovská, E., Pahl, M., Schlüppmann, K., Zühr, E., & Fritsche, E. (2022) · Frontiers in Toxicology · doi:10.3389/ftox.2022.816370 · Cited by 48 · see citing works
Divergent structural brain abnormalities between different genetic subtypes of children with Prader–Willi syndrome
Lukoshe, A., White, T., Schmidt, M. N., van der Lugt, A., & Hokken-Koelega, A. C. (2013) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-5-31 · Cited by 49 · see citing works
A Mixture of Persistent Organic Pollutants and Perfluorooctanesulfonic Acid Induces Similar Behavioural Responses, but Different Gene Expression Profiles in Zebrafish Larvae
Khezri, A., Fraser, T., Nourizadeh-Lillabadi, R., Kamstra, J., Berg, V., Zimmer, K., & Ropstad, E. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18020291 · Cited by 47 · see citing works
Between Dysbiosis, Maternal Immune Activation and Autism: Is There a Common Pathway?
Suprunowicz, M., Tomaszek, N., Urbaniak, A., Zackiewicz, K., Modzelewski, S., & Waszkiewicz, N. (2024) · Nutrients · doi:10.3390/nu16040549 · Cited by 44 · see citing works
Microbiome-Gut-Mucosal-Immune-Brain Axis and Autism Spectrum Disorder (ASD): A Novel Proposal of the Role of Gut Microbiome in ASD Aetiology
De Sales-Millán, A., Aguirre-Garrido, J. F., González-Cervantes, R. M., & Velázquez-Aragón, J. A. (2023) · doi:10.20944/preprints202305.1223.v1 · Cited by 44 · see citing works
Neural and phenotypic representation under the free-energy principle
Ramstead, M. J. D., Hesp, C., Tschantz, A., Smith, R., Constant, A., & Friston, K. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.11.024 · Cited by 43 · see citing works
Effects of Environmental Pollutants on Calcium Release and Uptake by Rat Cortical Microsomes
Dusza, H. M., Cenijn, P. H., Kamstra, J. H., Westerink, R. H. S., Leonards, P. E. G., & Hamers, T. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.07.015 · Cited by 38 · see citing works
Methylphenidate Decreases ATP Levels and Impairs Glutamate Uptake and Na+,K+-ATPase Activity in Juvenile Rat Hippocampus
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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
DOI: 10.1289/ehp.00108s3511
PMC: PMC1637807
OpenAlex: W2120095635
Cited by: 2,944
References: 407
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
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor, 6420 d)
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

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Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models.

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