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Interplay between population firing stability and single neuron dynamics in hippocampal networks

  1. Edden Slomowitz
  2. Boaz Styr
  3. Irena Vertkin
  4. Hila Milshtein-Parush
  5. Israel Nelken
  6. Michael Slutsky
  7. Inna Slutsky  Is a corresponding author
  1. Tel Aviv University, Israel
  2. Hebrew University, Israel
  3. Mantis Vision, Israel
Research Article
  • Cited 33
  • Views 3,648
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Cite this article as: eLife 2015;4:e04378 doi: 10.7554/eLife.04378

Abstract

Neuronal circuits' ability to maintain the delicate balance between stability and flexibility in changing environments is critical for normal neuronal functioning. However, to what extent individual neurons and neuronal populations maintain internal firing properties remains largely unknown. Here, we show that distributions of spontaneous population firing rates and synchrony are subject to accurate homeostatic control following increase of synaptic inhibition in cultured hippocampal networks. Reduction in firing rate triggered synaptic and intrinsic adaptive responses operating as global homeostatic mechanisms to maintain firing macro-stability, without achieving local homeostasis at the single-neuron level. Adaptive mechanisms, while stabilizing population firing properties, reduced short-term facilitation essential for synaptic discrimination of input patterns. Thus, invariant ongoing population dynamics emerge from intrinsically unstable activity patterns of individual neurons and synapses. The observed differences in the precision of homeostatic control at different spatial scales challenge cell-autonomous theory of network homeostasis and suggest existence of network-wide regulation rules.

Article and author information

Author details

  1. Edden Slomowitz

    Department of Physiology and Pharmacology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
    Competing interests
    The authors declare that no competing interests exist.
  2. Boaz Styr

    Department of Physiology and Pharmacology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Irena Vertkin

    Department of Physiology and Pharmacology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
    Competing interests
    The authors declare that no competing interests exist.
  4. Hila Milshtein-Parush

    Department of Physiology and Pharmacology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Israel Nelken

    Department of Neurobiology, The Alexander Silberman Institute of Life Sciences, Hebrew University, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Michael Slutsky

    Mantis Vision, Kfar Saba, Israel
    Competing interests
    The authors declare that no competing interests exist.
  7. Inna Slutsky

    Department of Physiology and Pharmacology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
    For correspondence
    islutsky@post.tau.ac.il
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All animal experiments were approved by the Tel Aviv University Committee on Animal Care (permit number M-11-005).

Reviewing Editor

  1. Sacha B Nelson, Brandeis University, United States

Publication history

  1. Received: August 14, 2014
  2. Accepted: December 31, 2014
  3. Accepted Manuscript published: January 3, 2015 (version 1)
  4. Version of Record published: January 30, 2015 (version 2)

Copyright

© 2015, Slomowitz 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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