Skip to main content
bioRxiv
  • Home
  • About
  • Submit
  • ALERTS / RSS
Advanced Search
New Results

Coordinated postnatal maturation of striatal cholinergic interneurons and dopamine release dynamics in mice

Avery McGuirt, Ori Lieberman, Michael Post, Irena Pigulevskiy, View ORCID ProfileDavid Sulzer
doi: https://doi.org/10.1101/2020.04.02.022152
Avery McGuirt
1Departments of Psychiatry and Neurology, New York State Psychiatric Institute, Columbia University College of Physicians and Surgeons, New York, NY, 10032, United States, , , , ,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: afm2150@cumc.columbia.edu ojl2106@cumc.columbia.edu mrp2201@cumc.columbia.edu ip2382@cumc.columbia.edu ds43@cumc.columbia.edu
Ori Lieberman
1Departments of Psychiatry and Neurology, New York State Psychiatric Institute, Columbia University College of Physicians and Surgeons, New York, NY, 10032, United States, , , , ,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: ojl2106@columbia.edu ds43@columbia.edu afm2150@cumc.columbia.edu ojl2106@cumc.columbia.edu mrp2201@cumc.columbia.edu ip2382@cumc.columbia.edu ds43@cumc.columbia.edu
Michael Post
1Departments of Psychiatry and Neurology, New York State Psychiatric Institute, Columbia University College of Physicians and Surgeons, New York, NY, 10032, United States, , , , ,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: afm2150@cumc.columbia.edu ojl2106@cumc.columbia.edu mrp2201@cumc.columbia.edu ip2382@cumc.columbia.edu ds43@cumc.columbia.edu
Irena Pigulevskiy
1Departments of Psychiatry and Neurology, New York State Psychiatric Institute, Columbia University College of Physicians and Surgeons, New York, NY, 10032, United States, , , , ,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: afm2150@cumc.columbia.edu ojl2106@cumc.columbia.edu mrp2201@cumc.columbia.edu ip2382@cumc.columbia.edu ds43@cumc.columbia.edu
David Sulzer
1Departments of Psychiatry and Neurology, New York State Psychiatric Institute, Columbia University College of Physicians and Surgeons, New York, NY, 10032, United States, , , , ,
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for David Sulzer
  • For correspondence: ojl2106@columbia.edu ds43@columbia.edu afm2150@cumc.columbia.edu ojl2106@cumc.columbia.edu mrp2201@cumc.columbia.edu ip2382@cumc.columbia.edu ds43@cumc.columbia.edu
  • Abstract
  • Full Text
  • Info/History
  • Metrics
  • Preview PDF
Loading

Abstract

Dynamic changes in motor abilities and motivated behaviors occur during the juvenile and adolescent periods. The striatum is a subcortical nucleus critical for action selection, motor learning and reward processing. Its tonically active cholinergic interneuron (ChI) is an integral regulator of the synaptic activity of other striatal neurons, as well as afferent axonal projections of midbrain dopamine neurons. Thalamic and dopaminergic inputs initiate pauses in ChI firing following salient sensory cues that are extended for several hundred milliseconds by intrinsic regenerative currents. Here, we characterize the electrophysiological and morphological features of ChIs during mouse postnatal development. We demonstrate that ChI spontaneous activity increases with age while the duration of the pause in firing induced by depolarizing inputs decreases during postnatal development. Maturation of ChI activity is driven by two distinct physiological changes: decreased amplitude of the afterhypolarization between P14 and P18 and and increased Ih conductance between the late postnatal period and adulthood. Finally, we uncover postnatal changes in dopamine release properties that are mediated by cholinergic signalling. At P10, striatal dopamine release is diminished compared to the adult, but our data show efficient summation of dopamine relase evoked by multiple grouped stimuli that subsides by P28. Blockade of nictonic acetylcholine receptors enhances release summation in mice older than P28 but has little effect at P10. These data demonstrate a physiological maturation of ChI activity and indicate a reciprocal interaction between the postnatal maturation of striatal ChI and dopamine neurotransmission.

Significance Statement Motor skills and motivated behavior regimes develop rapidly during the postnatal period. The functional development of the striatal cholinergic interneuron (ChI), which contributes to these behaviors in adulthood, remains unexplored. In this study, we tracked the ontogeny of spontaneous ChI activity and cellular morphology, as well as the developmental trajectory of ion conductances characteristic to this population. We further report a developmental link between ChI activity and dopamine release, revealing a change in the frequency-dependence of dopamine release during the early postnatal period that is mediated by cholinergic signaling. This study provides evidence that striatal microcircuits are dynamic during the postnatal period and that they undergo coordinated maturation.

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 4.0 International license.
Back to top
PreviousNext
Posted April 03, 2020.
Download PDF
Email

Thank you for your interest in spreading the word about bioRxiv.

NOTE: Your email address is requested solely to identify you as the sender of this article.

Enter multiple addresses on separate lines or separate them with commas.
Coordinated postnatal maturation of striatal cholinergic interneurons and dopamine release dynamics in mice
(Your Name) has forwarded a page to you from bioRxiv
(Your Name) thought you would like to see this page from the bioRxiv website.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Coordinated postnatal maturation of striatal cholinergic interneurons and dopamine release dynamics in mice
Avery McGuirt, Ori Lieberman, Michael Post, Irena Pigulevskiy, David Sulzer
bioRxiv 2020.04.02.022152; doi: https://doi.org/10.1101/2020.04.02.022152
Reddit logo Twitter logo Facebook logo LinkedIn logo Mendeley logo
Citation Tools
Coordinated postnatal maturation of striatal cholinergic interneurons and dopamine release dynamics in mice
Avery McGuirt, Ori Lieberman, Michael Post, Irena Pigulevskiy, David Sulzer
bioRxiv 2020.04.02.022152; doi: https://doi.org/10.1101/2020.04.02.022152

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Subject Area

  • Neuroscience
Subject Areas
All Articles
  • Animal Behavior and Cognition (4857)
  • Biochemistry (10802)
  • Bioengineering (8046)
  • Bioinformatics (27314)
  • Biophysics (13987)
  • Cancer Biology (11130)
  • Cell Biology (16062)
  • Clinical Trials (138)
  • Developmental Biology (8788)
  • Ecology (13298)
  • Epidemiology (2067)
  • Evolutionary Biology (17364)
  • Genetics (11689)
  • Genomics (15926)
  • Immunology (11034)
  • Microbiology (26114)
  • Molecular Biology (10655)
  • Neuroscience (56596)
  • Paleontology (418)
  • Pathology (1733)
  • Pharmacology and Toxicology (3005)
  • Physiology (4551)
  • Plant Biology (9644)
  • Scientific Communication and Education (1615)
  • Synthetic Biology (2690)
  • Systems Biology (6979)
  • Zoology (1510)