Developmental Exposure to Polychlorinated Biphenyls Interferes with Experience-Dependent Dendritic Plasticity and Ryanodine Receptor Expression in Weanling Rats
Open accessAbstract
Background: Neurodevelopmental disorders are associated with altered patterns of neuronal connectivity. A critical determinant of neuronal connectivity is the dendritic morphology of individual neurons, which is shaped by experience. The identification of environmental exposures that interfere with dendritic growth and plasticity may, therefore, provide insight into environmental risk factors for neurodevelopmental disorders. Objective: We tested the hypothesis that polychlorinated biphenyls (PCBs) alter dendritic growth and/or plasticity by promoting the activity of ryanodine receptors (RyRs). Methods and Results: The Morris water maze was used to induce experience-dependent neural plasticity in weanling rats exposed to either vehicle or Aroclor 1254 (A1254) in the maternal diet throughout gestation and lactation. Developmental A1254 exposure promoted dendritic growth in cerebellar Purkinje cells and neocortical pyramidal neurons among untrained animals but attenuated or reversed experience-dependent dendritic growth among maze-trained littermates. These structural changes coincided with subtle deficits in spatial learning and memory, increased [3H]-ryanodine binding sites and RyR expression in the cerebellum of untrained animals, and inhibition of training-induced RyR upregulation. A congener with potent RyR activity, PCB95, but not a congener with negligible RyR activity, PCB66, promoted dendritic growth in primary cortical neuron cultures and this effect was blocked by pharmacologic antagonism of RyR activity. Conclusions: Developmental exposure to PCBs interferes with normal patterns of dendritic growth and plasticity, and these effects may be linked to changes in RyR expression and function. These findings identify PCBs as candidate environmental risk factors for neurodevelopmental disorders, especially in children with heritable deficits in calcium signaling.
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Developmental exposure to PCB 95 or Aroclor 1254 (a commercial mixture of PCBs enriched for NDL PCBs) impairs cognitive behavior in weanling rats at doses that enhance neuronal connectivity in vivo.
“Consistent with this hypothesis, developmental exposure to PCB 95 or Aroclor 1254, a commercial mixture of PCBs enriched for NDL PCBs, impairs cognitive behavior in weanling rats at doses that enhance neuronal connectivity in vivo (Schantz et al., 1997;Kenet et al., 2007;Yang et al., 2009).”
From The Environmental Neurotoxicant PCB 95 Promotes Synaptogenesis via Ryanodine Receptor-Dependent miR132 Upregulation (2014) · cites this paper as Yang et al., 2009
The Results sections on spatial learning and dendritic plasticity report that developmental Aroclor 1254 exposure at 1 mg/kg/day impaired learning and memory in weanling rats while increasing dendritic length in untrained animals. The paper does not report cognitive impairment after developmental PCB 95 exposure: its PCB 95 dendritic-growth experiment used cultured neurons, not rats. No page numbers are available in the indexed passages. (LLM, conf=0.88)
Experimental — accuracy not yet measuredA nonmonotonic dose-response relationship has also been reported for NDL PCB effects on dendritic arborization of cultured rat hippocampal neurons and learning and memory deficits in rats exposed throughout gestation and lactation to NDL PCBs in the maternal diet.
“Interestingly, a nonmonotonic dose–response relationship has also been reported for NDL PCB effects on dendritic arborization of cultured rat hippocampal neurons [ 107 ] and learning and memory deficits in rats exposed throughout gestation and lactation to NDL PCBs in the maternal diet [ 117 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [117]
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References 92 · Cited by 166
Research works printed but not linked: 1
- Pessah IN Wong PW Robertson L Hansen L 2001 Etiology of PCB Neurotoxicity: from molecules to cellular dysfunction Progress In Polychlorinated Biphenyl Toxicology New York, NY Academic Press 179 184
- Authors
- Yang, D., Kim, K. H., Phimister, A., Bachstetter, A. D., Ward, T. R., Stackman, R. W., Mervis, R. F., Wisniewski, A. B., Klein, S. L., Kodavanti, P. R. S., Anderson, K. A., Wayman, G., Pessah, I. N., & Lein, P. J.
- Affiliations
- Oregon Health & Science University (US)
- University of California, Davis (US)
- University of South Florida (US)
- Environmental Protection Agency (US)
- Florida Atlantic University (US)
- University of Oklahoma Health Sciences Center (US)
- Johns Hopkins University (US)
- Oregon State University (US)
- Washington State University (US)
- Corresponding author
- Lein, Pamela J.
- ORCID
- Venue
- Environmental Health Perspectives
- Publisher
- American Chemical Society (ACS)
- Published
- 2008-09-12
- Volume
- 117
- Issue
- 3
- Pages
- 426-435
- ISSN
- 0091-6765 (ISSN-L)
- 1552-9924
- PMC
- PMC2661913
- OpenAlex
- W2031021430
- Cited by
- 166
- References
- 92
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 4 · 2023: 10 · 2022: 12 · 2021: 13 · 2020: 12 · 2019: 6 · 2018: 13 · 2017: 10 · 2016: 9 · 2015: 6 · 2014: 10 · 2013: 11 · 2012: 7
- FWCI
- 6.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- public-domain
- creativecommons.org/licenses/by/4.0/ (vor, 3395 d)
- Locations
- Environmental Health Perspectives (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of General Medical Sciences (GM 041292, R01GM041292)
- National Institute of Neurological Disorders and Stroke (NS 046649, R01NS046649)
- National Institute of Environmental Health Sciences (1 P01-ES11269, P01ES011269, R01ES014901)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD40936, R03HD040936)
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- polychlorinated biphenyls, developmental neurotoxicity, dendritic plasticity, ryanodine receptor, Aroclor 1254, Purkinje cells, pyramidal neurons, spatial learning and memory, cerebellum, calcium signaling, environmental risk factors, neurodevelopmental disorders, weanling rats
- MeSH terms
- Animals, Animals, Newborn, Body Weight, Dendrites, Female, Litter Size, Memory, Microtubule-Associated Proteins, Neuronal Plasticity, Pregnancy, Prenatal Exposure Delayed Effects, Sex Ratio, Rats, Sprague-Dawley, Gene Expression Regulation, Developmental, Maze Learning, Ryanodine Receptor Calcium Release Channel, Chlorodiphenyl (54% Chlorine), Green Fluorescent Proteins, Rats
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