Developmental Nicotine Exposure Disrupts Dendritic Arborization Patterns of Hypoglossal Motoneurons in the Neonatal Rat

Overview

Journal Dev Neurobiol

Specialties Biology
Neurology

Date 2016 Jan 29

PMID 26818139

Citations 10

Authors

Gregory L Powell

Joshua Gaddy

Fei Xu

Ralph F Fregosi

Richard B Levine

Affiliations

Soon will be listed here.

Abstract

Maternal smoking or use of other products containing nicotine during pregnancy can have significant adverse consequences for respiratory function in neonates. We have shown, in previous studies, that developmental nicotine exposure (DNE) in a model system compromises the normal function of respiratory circuits within the brainstem. The effects of DNE include alterations in the excitability and synaptic interactions of the hypoglossal motoneurons, which innervate muscles of the tongue. This study was undertaken to test the hypothesis that these functional consequences of DNE are accompanied by changes in the dendritic morphology of hypoglossal motoneurons. Hypoglossal motoneurons in brain stem slices were filled with neurobiotin during whole-cell patch clamp recordings and subjected to histological processing to reveal dendrites. Morphometric analysis, including the Sholl method, revealed significant effects of DNE on dendritic branching patterns. In particular, whereas within the first five postnatal days there was significant growth of the higher-order dendritic branches of motoneurons from control animals, the growth was compromised in motoneurons from neonates that were subjected to DNE. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1125-1137, 2016.

Citing Articles

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Beyeler S, Hodges M, Huxtable A Respir Physiol Neurobiol. 2020; 274:103357.

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Developmental Nicotine Exposure Alters Synaptic Input to Hypoglossal Motoneurons and Is Associated with Altered Function of Upper Airway Muscles.

Wollman L, Clarke J, DeLucia C, Levine R, Fregosi R eNeuro. 2019; 6(6).

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References

Carrascal L, Nieto-Gonzalez J, Cameron W, Torres B, Nunez-Abades P . Changes during the postnatal development in physiological and anatomical characteristics of rat motoneurons studied in vitro. Brain Res Brain Res Rev. 2005; 49(2):377-87. DOI: 10.1016/j.brainresrev.2005.02.003. View

Pilarski J, Wakefield H, Fuglevand A, Levine R, Fregosi R . Developmental nicotine exposure alters neurotransmission and excitability in hypoglossal motoneurons. J Neurophysiol. 2010; 105(1):423-33. PMC: 3023378. DOI: 10.1152/jn.00876.2010. View

Huang Y, Brown A, Costy-Bennett S, Luo Z, Fregosi R . Influence of prenatal nicotine exposure on postnatal development of breathing pattern. Respir Physiol Neurobiol. 2004; 143(1):1-8. DOI: 10.1016/j.resp.2004.07.002. View

Berger A . Development of synaptic transmission to respiratory motoneurons. Respir Physiol Neurobiol. 2011; 179(1):34-42. PMC: 3157583. DOI: 10.1016/j.resp.2011.03.002. View

Mychasiuk R, Muhammad A, Gibb R, Kolb B . Long-term alterations to dendritic morphology and spine density associated with prenatal exposure to nicotine. Brain Res. 2013; 1499:53-60. DOI: 10.1016/j.brainres.2012.12.021. View

Wong Y, Lee C, Xie W, Cui B, Poo M . Activity-dependent BDNF release via endocytic pathways is regulated by synaptotagmin-6 and complexin. Proc Natl Acad Sci U S A. 2015; 112(32):E4475-84. PMC: 4538679. DOI: 10.1073/pnas.1511830112. View

Lavezzi A, Corna M, Mingrone R, Matturri L . Study of the human hypoglossal nucleus: normal development and morpho-functional alterations in sudden unexplained late fetal and infant death. Brain Dev. 2009; 32(4):275-84. DOI: 10.1016/j.braindev.2009.05.006. View

Kuczewski N, Porcher C, Lessmann V, Medina I, Gaiarsa J . Activity-dependent dendritic release of BDNF and biological consequences. Mol Neurobiol. 2009; 39(1):37-49. PMC: 5352827. DOI: 10.1007/s12035-009-8050-7. View

Hua J, Smith S . Neural activity and the dynamics of central nervous system development. Nat Neurosci. 2004; 7(4):327-32. DOI: 10.1038/nn1218. View

10.

Gentry C, Lukas R . Regulation of nicotinic acetylcholine receptor numbers and function by chronic nicotine exposure. Curr Drug Targets CNS Neurol Disord. 2003; 1(4):359-85. DOI: 10.2174/1568007023339184. View

11.

Alm B, Milerad J, Wennergren G, Skjaerven R, Oyen N, Norvenius G . A case-control study of smoking and sudden infant death syndrome in the Scandinavian countries, 1992 to 1995. The Nordic Epidemiological SIDS Study. Arch Dis Child. 1998; 78(4):329-34. PMC: 1717534. DOI: 10.1136/adc.78.4.329. View

12.

Rosenberg S, Spitzer N . Calcium signaling in neuronal development. Cold Spring Harb Perspect Biol. 2011; 3(10):a004259. PMC: 3179332. DOI: 10.1101/cshperspect.a004259. View

13.

Adams J . Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem. 1981; 29(6):775. DOI: 10.1177/29.6.7252134. View

14.

Roy T, Seidler F, Slotkin T . Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J Pharmacol Exp Ther. 2001; 300(1):124-33. DOI: 10.1124/jpet.300.1.124. View

15.

ONeill K, Akum B, Dhawan S, Kwon M, Langhammer C, Firestein B . Assessing effects on dendritic arborization using novel Sholl analyses. Front Cell Neurosci. 2015; 9:285. PMC: 4519774. DOI: 10.3389/fncel.2015.00285. View

16.

Cline H, Haas K . The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis. J Physiol. 2008; 586(6):1509-17. PMC: 2375708. DOI: 10.1113/jphysiol.2007.150029. View

17.

Mitchell E, Milerad J . Smoking and the sudden infant death syndrome. Rev Environ Health. 2006; 21(2):81-103. DOI: 10.1515/reveh.2006.21.2.81. View

18.

England L, Bunnell R, Pechacek T, Tong V, McAfee T . Nicotine and the Developing Human: A Neglected Element in the Electronic Cigarette Debate. Am J Prev Med. 2015; 49(2):286-93. PMC: 4594223. DOI: 10.1016/j.amepre.2015.01.015. View

19.

Pilarski J, Wakefield H, Fuglevand A, Levine R, Fregosi R . Increased nicotinic receptor desensitization in hypoglossal motor neurons following chronic developmental nicotine exposure. J Neurophysiol. 2011; 107(1):257-64. PMC: 3349681. DOI: 10.1152/jn.00623.2011. View

20.

Nunez-Abades P, Cameron W . Morphology of developing rat genioglossal motoneurons studied in vitro: relative changes in diameter and surface area of somata and dendrites. J Comp Neurol. 1995; 353(1):129-42. DOI: 10.1002/cne.903530112. View