Dendritic osmosensors modulate activity-induced calcium influx in oxytocinergic magnocellular neurons of the mouse PVN

  1. Wanhui Sheng  Is a corresponding author
  2. Scott W Harden  Is a corresponding author
  3. Yalun Tan  Is a corresponding author
  4. Eric G Krause  Is a corresponding author
  5. Charles J Frazier  Is a corresponding author
  1. University of Florida, United States

Abstract

Hypothalamic oxytocinergic magnocellular neurons have a fascinating ability to release peptide from both their axon terminals and from their dendrites. Existing data indicates that the relationship between somatic activity and dendritic release is not constant, but the mechanisms through which this relationship can be modulated are not completely understood. Here we use a combination of electrical and optical recording techniques to quantify activity-induced calcium influx in proximal vs. distal dendrites of oxytocinergic magnocellular neurons located in the paraventricular nucleus of the hypothalamus (OT-MCNs). Results reveal that the dendrites of OT-MCNs are weak conductors of somatic voltage changes, however activity-induced dendritic calcium influx can be robustly regulated by both osmosensitive and non-osmosensitive ion channels located along the dendritic membrane. Overall, this study reveals that dendritic conductivity is a dynamic and endogenously regulated feature of OT-MCNs that is likely to have substantial functional impact on central oxytocin release.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.

Article and author information

Author details

  1. Wanhui Sheng

    Department of Pharmacodynamics, University of Florida, Gainesville, United States
    For correspondence
    shengwanhui@ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Scott W Harden

    Department of Pharmacodynamics, University of Florida, Gainesville, United States
    For correspondence
    swharden@ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0757-1979
  3. Yalun Tan

    Department of Pharmacodynamics, University of Florida, Gainesville, United States
    For correspondence
    yaluntan@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
  4. Eric G Krause

    Department of Pharmacodynamics, University of Florida, Gainesville, United States
    For correspondence
    EKrause@cop.ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
  5. Charles J Frazier

    Department of Pharmacodynamics, University of Florida, Gainesville, United States
    For correspondence
    cjfraz@ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3550-4789

Funding

National Institute of Mental Health (R01MH104641)

  • Charles J Frazier

National Heart, Lung, and Blood Institute (R01HL122494)

  • Eric G Krause

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Ryohei Yasuda, Max Planck Florida Institute for Neuroscience, United States

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All animal procedures were reviewed and approved by the Institutional Animal Care and Use Committee (IACUC) at the University of Florida (under protocol # 201701866).

Version history

  1. Received: September 25, 2020
  2. Preprint posted: January 26, 2021 (view preprint)
  3. Accepted: July 11, 2021
  4. Accepted Manuscript published: July 12, 2021 (version 1)
  5. Version of Record published: September 22, 2021 (version 2)

Copyright

© 2021, Sheng et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,824
    Page views
  • 213
    Downloads
  • 3
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Wanhui Sheng
  2. Scott W Harden
  3. Yalun Tan
  4. Eric G Krause
  5. Charles J Frazier
(2021)
Dendritic osmosensors modulate activity-induced calcium influx in oxytocinergic magnocellular neurons of the mouse PVN
eLife 10:e63486.
https://doi.org/10.7554/eLife.63486

Share this article

https://doi.org/10.7554/eLife.63486

Further reading

    1. Neuroscience
    Katharina Eichler, Stefanie Hampel ... Andrew M Seeds
    Research Advance

    Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.