Shared rhythmic subcortical GABAergic input to the entorhinal cortex and presubiculum

Abstract

Rhythmic theta frequency (~5-12 Hz) oscillations coordinate neuronal synchrony and higher frequency oscillations across the cortex. Spatial navigation and context-dependent episodic memories are represented in several interconnected regions including the hippocampal and entorhinal cortices, but the cellular mechanisms for their dynamic coupling remain to be defined. Using monosynaptically-restricted retrograde viral tracing in mice, we identified a subcortical GABAergic input from the medial septum that terminated in the entorhinal cortex, with collaterals innervating the dorsal presubiculum. Extracellularly recording and labeling GABAergic entorhinal-projecting neurons in awake behaving mice show that these subcortical neurons, named orchid cells, fire in long rhythmic bursts during immobility and locomotion. Orchid cells discharge near the peak of hippocampal and entorhinal theta oscillations, couple to entorhinal gamma oscillations, and target subpopulations of extra-hippocampal GABAergic interneurons. Thus, orchid cells are a specialized source of rhythmic subcortical GABAergic modulation of 'upstream' and 'downstream' cortico-cortical circuits involved in mnemonic functions.

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. Tim James Viney

    Department of Pharmacology, University of Oxford, Oxford, United Kingdom
    For correspondence
    tim.viney@pharm.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6444-1188
  2. Minas Salib

    Department of Pharmacology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9938-7978
  3. Abhilasha Joshi

    Department of Pharmacology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Gunes Unal

    Department of Pharmacology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3013-0271
  5. Naomi Berry

    Department of Pharmacology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Peter Somogyi

    Department of Pharmacology, University of Oxford, Oxford, United Kingdom
    For correspondence
    peter.somogyi@pharm.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.

Funding

Medical Research Council (MC_UU_12024/4)

  • Tim James Viney
  • Minas Salib
  • Abhilasha Joshi
  • Gunes Unal
  • Naomi Berry
  • Peter Somogyi

Wellcome (108726/Z/15/Z)

  • Tim James Viney
  • Minas Salib
  • Abhilasha Joshi
  • Gunes Unal
  • Naomi Berry
  • Peter Somogyi

Felix Doctoral Scholarship

  • Abhilasha Joshi

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

Reviewing Editor

  1. Laura Colgin, The University of Texas at Austin, Center for Learning and Memory, United States

Ethics

Animal experimentation: All procedures involving experimental animals were approved by the Department of Pharmacology Animal Welfare and Ethical Review Body under approved personal and project licenses (project licence number: 30/3240) in accordance with the Animals (Scientific Procedures) Act, 1986 (UK) and associated regulations. All surgery was performed under isoflurane anesthesia with a peri-operative dose of buprenorphine, and every effort was made to minimize suffering.

Version history

  1. Received: December 15, 2017
  2. Accepted: April 4, 2018
  3. Accepted Manuscript published: April 5, 2018 (version 1)
  4. Version of Record published: April 19, 2018 (version 2)

Copyright

© 2018, Viney 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. Tim James Viney
  2. Minas Salib
  3. Abhilasha Joshi
  4. Gunes Unal
  5. Naomi Berry
  6. Peter Somogyi
(2018)
Shared rhythmic subcortical GABAergic input to the entorhinal cortex and presubiculum
eLife 7:e34395.
https://doi.org/10.7554/eLife.34395

Share this article

https://doi.org/10.7554/eLife.34395

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