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Perinatal exposure to nicotine disrupts circadian locomotor and learning efficiency rhythms in juvenile mice

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Abstract

The increased rates of nicotine exposure by electronic nicotine delivery systems (vaping), ingestion, or patches during pregnancy as an alternative to the smoking of tobacco arise concerns about the neurodevelopmental, cognitive, and behavioral long-term consequences in the juvenile offspring. Nowadays, the use of electronic cigarettes as supposed a safer smoking alternative has been increased mainly in young females at reproductive age, due to the “safety” misconception. However, previous studies suggest that exposure to nicotine during pregnancy and prenatal development may lead to detrimental effects in the postnatal lifespan. Nicotine, as an alkaloid, alters the reward system acting as acetylcholine (ACh) agonist on nicotinic cholinergic receptors (nAChRs). In early brain development, the cholinergic system is also involved in neurite outgrowth, cell survival, proliferation, differentiation, neurogenesis, and many other critical processes being considered as a developmental signal marker. The nicotine noxious effect at those early stages may impact the system programming and plasticity in the long-term postnatal life. In this study, we analyze the circadian locomotor activity and learning efficiency rhythms in the juvenile male offspring of mice exposed to nicotine through pregnancy and lactation. Attenuated rhythm amplitude and relative power of the circadian component were found in the nicotine exposed offspring (pN). The acrophase (the best performance during a 24-h cycle) of learning efficiency was delayed and the long-term memory consolidation task failed after 8 days of learning experience. The aforementioned results suggest nicotine exposure in uterus modifies the circadian modulation related to the memory consolidation and locomotor systems as well as its environmental temporal synchronization.

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Acknowledgements

This research was partially supported by PD-LBAE-FC UNAM 2015-2018 and PCBM-2016. Martin A. Fuentes-Cano is a doctoral student from Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM) and received fellowship 364988 from CONACYT. We thank Liliana Rivera Espinosa, Technician INP-SS, and Roberto Enrique Llanos Romero, Technician Lab Fitoquímica, FC-UNAM for assistance with nicotine/cotinine quantification in blood samples and solution, Martín Fuentes Cruz, engineer IIMAS-UNAM for developing DACIR (Data Acquisition CIrcadian Rhythms system) and Dr. Rosa María Vigueras Villaseñor, researcher, INP-SS for comments that greatly improved the manuscript. We also thank Dr. Manuel Miranda from UMDI-FC, UNAM and Dr. Luz Navarro Angulo, FM, UNAM who provided insight and expertise that greatly assisted the research, although they may not agree with all of the interpretations/conclusions of this paper. We are also immensely grateful to Jesús González Ruano, Nayeli Ortega Villegas and Roberto Mendoza Barraza, undergraduate students for assistance in the animals’ care and recording supervision. Finally, we thank Ms. Maria Cox for her English language revision.

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Correspondence to Pilar Durán.

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Fuentes-Cano, M.A., Bustamante-Valdez, D.J. & Durán, P. Perinatal exposure to nicotine disrupts circadian locomotor and learning efficiency rhythms in juvenile mice. Brain Struct Funct 225, 2287–2297 (2020). https://doi.org/10.1007/s00429-020-02126-2

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  • DOI: https://doi.org/10.1007/s00429-020-02126-2

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