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Prenatal Methadone Exposure Disrupts Behavioral Development and Alters Motor Neuron Intrinsic Properties and Local Circuitry

View ORCID ProfileGregory G. Grecco, Briana Mork, View ORCID ProfileJui Yen Huang, Corinne E. Metzger, View ORCID ProfileDavid L. Haggerty, View ORCID ProfileKaitlin C. Reeves, Yong Gao, Hunter Hoffman, Simon N. Katner, Andrea R. Masters, View ORCID ProfileCameron W. Morris, Erin A. Newell, Eric A. Engleman, View ORCID ProfileAnthony J. Baucum II, Jieun Kim, View ORCID ProfileBryan K. Yamamoto, Matthew R. Allen, View ORCID ProfileYu-Chien Wu, View ORCID ProfileHui-Chen Lu, View ORCID ProfilePatrick L. Sheets, View ORCID ProfileBrady K. Atwood
doi: https://doi.org/10.1101/2020.09.25.314013
Gregory G. Grecco
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
2Indiana University School of Medicine, Medical Scientist Training Program, Indianapolis, IN 46202
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Briana Mork
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
3Program in Medical Neuroscience, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, 46220
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Jui Yen Huang
4Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, 47405
5The Linda and Jack Gill Center for Biomolecular Sciences, Department of Psychological and Brain Science, Program in Neuroscience, Indiana University, Bloomington, IN 47405
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Corinne E. Metzger
6Department of Anatomy, Cell Biology & Physiology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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David L. Haggerty
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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Kaitlin C. Reeves
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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Yong Gao
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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Hunter Hoffman
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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Simon N. Katner
7Deparment of Psychiatry, Indiana University School of Medicine, Indianapolis, IN, 46202
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Andrea R. Masters
8Clinical Pharmacology Analytical Core-Indiana University Simon Cancer Center, Indiana University School of Medicine, Indianapolis, Indiana
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Cameron W. Morris
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
9Department of Biology, Indiana University-Purdue University, Indianapolis, Indiana, USA
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Erin A. Newell
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Eric A. Engleman
7Deparment of Psychiatry, Indiana University School of Medicine, Indianapolis, IN, 46202
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Anthony J. Baucum II
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
9Department of Biology, Indiana University-Purdue University, Indianapolis, Indiana, USA
10Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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Jieun Kim
10Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
11Department of Radiology and Imaging Sciences, Indiana University School of Medicine, Indianapolis, IN, 46202
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Bryan K. Yamamoto
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
10Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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Matthew R. Allen
6Department of Anatomy, Cell Biology & Physiology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
12Indiana Center for Musculoskeletal Health, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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Yu-Chien Wu
10Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
11Department of Radiology and Imaging Sciences, Indiana University School of Medicine, Indianapolis, IN, 46202
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Hui-Chen Lu
4Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, 47405
5The Linda and Jack Gill Center for Biomolecular Sciences, Department of Psychological and Brain Science, Program in Neuroscience, Indiana University, Bloomington, IN 47405
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Patrick L. Sheets
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
10Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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Brady K. Atwood
1Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
10Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, 46202, USA
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  • For correspondence: bkatwood@iu.edu
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ABSTRACT

Despite the rising prevalence of methadone treatment in pregnant women with opioid use disorder, the effects of methadone on neurobehavioral development remain unclear. We developed a translational mouse model of prenatal methadone exposure (PME) that resembles the typical pattern of opioid use by pregnant women who first use oxycodone then switch to methadone maintenance pharmacotherapy, and subsequently become pregnant while maintained on methadone. We investigated the effects of PME on physical development, sensorimotor behavior, and motor neuron properties using a multidisciplinary approach of physical, biochemical, and behavioral assessments along with brain slice electrophysiology and in vivo magnetic resonance imaging. PME produced substantial impairments in offspring physical growth, activity in an open field, and sensorimotor milestone acquisition which were associated with alterations in motor neuron functioning and connectivity. The present study adds to the limited work examining PME by providing a comprehensive, translationally relevant characterization of how PME disrupts offspring development.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This revision contains updates to clarify some introductory information on the model, further additions of limitations to the work, and additional details of methods.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 02, 2020.
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Prenatal Methadone Exposure Disrupts Behavioral Development and Alters Motor Neuron Intrinsic Properties and Local Circuitry
Gregory G. Grecco, Briana Mork, Jui Yen Huang, Corinne E. Metzger, David L. Haggerty, Kaitlin C. Reeves, Yong Gao, Hunter Hoffman, Simon N. Katner, Andrea R. Masters, Cameron W. Morris, Erin A. Newell, Eric A. Engleman, Anthony J. Baucum II, Jieun Kim, Bryan K. Yamamoto, Matthew R. Allen, Yu-Chien Wu, Hui-Chen Lu, Patrick L. Sheets, Brady K. Atwood
bioRxiv 2020.09.25.314013; doi: https://doi.org/10.1101/2020.09.25.314013
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Prenatal Methadone Exposure Disrupts Behavioral Development and Alters Motor Neuron Intrinsic Properties and Local Circuitry
Gregory G. Grecco, Briana Mork, Jui Yen Huang, Corinne E. Metzger, David L. Haggerty, Kaitlin C. Reeves, Yong Gao, Hunter Hoffman, Simon N. Katner, Andrea R. Masters, Cameron W. Morris, Erin A. Newell, Eric A. Engleman, Anthony J. Baucum II, Jieun Kim, Bryan K. Yamamoto, Matthew R. Allen, Yu-Chien Wu, Hui-Chen Lu, Patrick L. Sheets, Brady K. Atwood
bioRxiv 2020.09.25.314013; doi: https://doi.org/10.1101/2020.09.25.314013

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