Neural basis for regulation of vasopressin secretion by anticipated disturbances in osmolality

  1. Angela Kim
  2. Joseph C Madara
  3. Chen Wu
  4. Mark L Andermann
  5. Bradford B Lowell  Is a corresponding author
  1. Beth Israel Deaconess Medical Center, United States

Abstract

Water balance, tracked by extracellular osmolality, is regulated by feedback and feedforward mechanisms. Feedback regulation is reactive, occurring as deviations in osmolality are detected. Feedforward or presystemic regulation is proactive, occurring when disturbances in osmolality are anticipated. Vasopressin (AVP) is a key hormone regulating water balance and is released during hyperosmolality to limit renal water excretion. AVP neurons are under feedback and feedforward regulation. Not only do they respond to disturbances in blood osmolality, but they are also rapidly suppressed and stimulated, respectively, by drinking and eating, which will ultimately decrease and increase osmolality. Here, we demonstrate that AVP neuron activity is regulated by multiple anatomically- and functionally-distinct neural circuits. Notably, presystemic regulation during drinking and eating are mediated by non-overlapping circuits that involve the lamina terminalis and hypothalamic arcuate nucleus, respectively. These findings reveal neural mechanisms that support differential regulation of AVP release by diverse behavioral and physiological stimuli.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Angela Kim

    Medicine, Beth Israel Deaconess Medical Center, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9475-0798
  2. Joseph C Madara

    Department of Medicine, Division of Endocrinology, Beth Israel Deaconess Medical Center, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Chen Wu

    Medicine, Beth Israel Deaconess Medical Center, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Mark L Andermann

    Department of Endocrinology, Beth Israel Deaconess Medical Center, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9882-933X
  5. Bradford B Lowell

    Department of Medicine, Division of Endocrinology, Beth Israel Deaconess Medical Center, Boston, United States
    For correspondence
    blowell@bidmc.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0436-3760

Funding

National Institute of Diabetes and Digestive and Kidney Diseases (F31 DK109575)

  • Angela Kim

Pew Charitable Trusts (Pew Scholar Award)

  • Mark L Andermann

National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK075632)

  • Bradford B Lowell

National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK096010)

  • Bradford B Lowell

National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK089044)

  • Bradford B Lowell

National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK111401)

  • Bradford B Lowell

National Institute of Diabetes and Digestive and Kidney Diseases (P30 DK046200)

  • Bradford B Lowell

National Institute of Diabetes and Digestive and Kidney Diseases (DP2 DK105570)

  • Mark L Andermann

National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK109930)

  • Mark L Andermann

McKnight Foundation (McKnight Scholar Award)

  • Mark L Andermann

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

Ethics

Animal experimentation: All animal care and experimental procedures were approved in advance by the National Institute of Health and Beth Israel Deaconess Medical Center Institutional Animal Care and Use Committee.

Reviewing Editor

  1. Richard D Palmiter, Howard Hughes Medical Institute, University of Washington, United States

Publication history

  1. Received: January 16, 2021
  2. Preprint posted: January 27, 2021 (view preprint)
  3. Accepted: September 28, 2021
  4. Accepted Manuscript published: September 29, 2021 (version 1)
  5. Version of Record published: November 18, 2021 (version 2)

Copyright

© 2021, Kim 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.

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  1. Angela Kim
  2. Joseph C Madara
  3. Chen Wu
  4. Mark L Andermann
  5. Bradford B Lowell
(2021)
Neural basis for regulation of vasopressin secretion by anticipated disturbances in osmolality
eLife 10:e66609.
https://doi.org/10.7554/eLife.66609