Sex dimorphic behaviors as markers of neuroendocrine disruption by environmental chemicals: the case of chlorpyrifos
Abstract
The complexity of the neuroendocrine level of investigation requires the assessment of behavioral patterns that extend beyond the reproductive functions, which are age- and sex-specific in rodents, described by defined clusters of behavioral items regulated by genetic, hormonal, and epigenetic factors. The study of social behavior in laboratory rodents reveals sex-dimorphic effects of environmental chemicals that may be undetected either by a traditional neurotoxicological approach or referring to the classical definition of endocrine disrupting chemicals. Here we review data on the neurobehavioral effects of developmental exposure to the non-persistent organophosphorus insecticide chlorpyrifos, whose neurotoxic activity at low doses is currently a matter of concern for children's health. In mice exposed to chlorpyrifos in utero and/or in early development social/emotional responses are differently affected in the two sexes in parallel with sex-dependent interference on hypothalamic neuroendocrine pathways regulating social behaviors (vasopressin, oxytocin, and steroid regulated systems). Through the analysis of complex sex-dimorphic behavioral patterns we show that neurotoxic and endocrine disrupting activities of CPF overlap. This widely diffused organophosphorus pesticide might thus be considered as a neuroendocrine disruptor possibly representing a risk factor for sex-biased neurodevelopmental disorders in children.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Exposure to atrazine, PCBs, and chlorpyrifos is associated with perturbations of normal social interactions.
“Exposure to other EDCs such as atrazine (mice: Belloni et al., 2011), PCBs (rats: Jolous-Jamshidi et al., 2010), and chlorpyrifos (mice: Venerosi et al., 2012) are associated with perturbations of normal social interactions.”
From The effects of prenatal PCBs on adult social behavior in rats (2015) · cites this paper as Venerosi et al., 2012
Developmental exposure to CPF in mice and rats results in long-lasting, sometimes sex-specific, effects on emotional functions, activity, learning, serotonergic and dopaminergic transmission, neuronal differentiation, and synaptogenesis.
“Work in mice and rats has repeatedly shown that developmental exposure results in long-lasting (and sometimes sex specific) effects on emotional functions, activity, learning, serotonergic and dopaminergic transmission, neuronal differentiation, and synaptogenesis (108).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [108]
Cites
Brain oxytocin: A key regulator of emotional and social behaviours in both females and males
Neumann, I. D. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01726.x · Cited by 743 · see citing works
Rauh, V., Arunajadai, S., Horton, M., Perera, F., Hoepner, L., Barr, D. B., & Whyatt, R. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1003160 · Cited by 524 · cited 2× · see citing works
“In a recent US study (Rauh et al., 2011) cognitive and motor development of a inner-city children cohort was analyzed as a function of CPF levels in umbilical cord plasma, and demonstrated a delayed development in children with the higher CPF exposure.”
BackgroundWhat 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
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
Palanza, P. L., Howdeshell, K. L., Parmigiani, S., & vom Saal, F. S. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.02110s3415 · Cited by 268 · see citing works
Veenema, A. H., Bredewold, R., & Neumann, I. D. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.02.008 · Cited by 263 · see citing works
Long-term effects on hypothalamic neuropeptides after developmental exposure to chlorpyrifos in mice
Tait, S., Ricceri, L., Venerosi, A., Maranghi, F., Mantovani, A., & Calamandrei, G. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.11696 · Cited by 64 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
EDC-2: the endocrine society's second scientific statement on endocrine-disrupting chemicals
Gore, A. C., Chappell, V. A., Fenton, S. E., Flaws, J. A., Nadal, A., Prins, G. S., Toppari, J., & Zoeller, R. T. (2015) · Endocrine Reviews · doi:10.1210/er.2015-1010 · Cited by 2,407 · see citing works
Transgenerational effects of prenatal bisphenol A on social recognition
Wolstenholme, J. T., Goldsby, J. A., & Rissman, E. F. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.09.007 · Cited by 157 · see citing works
The effects of prenatal PCBs on adult social behavior in rats
Reilly, M. P., Weeks, C. D., Topper, V. Y., Thompson, L. M., Crews, D., & Gore, A. C. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.06.002 · Cited by 65 · see citing works
“Exposure to other EDCs such as atrazine (mice: Belloni et al., 2011), PCBs (rats: Jolous-Jamshidi et al., 2010), and chlorpyrifos (mice: Venerosi et al., 2012) are associated with perturbations of normal social interactions.”
Chang, C.-H., Yu, C.-J., Du, J.-C., Chiou, H.-C., Chen, H.-C., Yang, W., Chung, M.-Y., Chen, Y.-S., Hwang, B., Mao, I.-F., et al. (2018) · Environmental Research · doi:10.1016/j.envres.2017.10.011 · Cited by 54 · see citing works
Endocrine Disruption of Vasopressin Systems and Related Behaviors
Patisaul, H. B. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00134 · Cited by 54 · see citing works
“Work in mice and rats has repeatedly shown that developmental exposure results in long-lasting (and sometimes sex specific) effects on emotional functions, activity, learning, serotonergic and dopaminergic transmission, neuronal differentiation, and synaptogenesis (108).”
Background
- Authors
- Venerosi, A., Ricceri, L., Tait, S., & Calamandrei, G.
- Affiliations
- Istituto Superiore di Sanità (IT)
- Corresponding author
- Ricceri, L.
- Venue
- NeuroToxicology
- Publisher
- Elsevier BV
- Published
- 2012-12
- Volume
- 33
- Issue
- 6
- Pages
- 1420-1426
- ISSN
- 0161-813X (ISSN-L)
- OpenAlex
- W2052702994
- Cited by
- 66
- References
- 7
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 3 · 2023: 2 · 2022: 4 · 2021: 2 · 2020: 4 · 2019: 6 · 2018: 6 · 2017: 7 · 2016: 5 · 2015: 10 · 2014: 5 · 2013: 5
- FWCI
- 0.68
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroToxicology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- ISS-NIH 530F/52
- ISS-11/US/11
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Pesticide Exposure and Toxicity
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- chlorpyrifos, neuroendocrine disruption, endocrine disruptors, organophosphate insecticides, developmental neurotoxicity, social behavior, vasopressin, oxytocin, prenatal exposure, rodent models
- MeSH terms
- Age Factors, Animals, Behavior, Animal, Brain, Dose-Response Relationship, Drug, Chlorpyrifos, Emotions, Environmental Pollutants, Female, Humans, Male, Pregnancy, Prenatal Exposure Delayed Effects, Sex Characteristics, Sex Factors, Social Behavior, Risk Assessment, Neurotoxicity Syndromes, Mice, Endocrine Disruptors
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
