Extracellular Calcium Controls the Expression of Two Different Forms of Ripple-Like Hippocampal Oscillations

  1. Aivar Mateo, Paloma 1
  2. Valero, Manuel 1
  3. Bellistri, Elisa 1
  4. Menéndez de la Prida, Liset 1
  1. 1 Consejo Superior de Investigaciones Científicas
    info

    Consejo Superior de Investigaciones Científicas

    Madrid, España

    ROR https://ror.org/02gfc7t72

Journal:
The Journal of Neuroscience

ISSN: 0270-6474,  1529-2401

Year of publication: 2014

Volume: 34

Issue: 8

Pages: 2989-3004

Type: Article

DOI: 10.1523/JNEUROSCI.2826-13.2014 GOOGLE SCHOLAR lock_openOpen access editor

More publications in: The Journal of Neuroscience

Abstract

Hippocampal high-frequency oscillations (HFOs) are prominent in physiological and pathological conditions. During physiological ripples (100–200 Hz), few pyramidal cells fire together coordinated by rhythmic inhibitory potentials. In the epileptic hippocampus, fast ripples (>200 Hz) reflect population spikes (PSs) from clusters of bursting cells, but HFOs in the ripple and the fast ripple range are vastly intermixed. What is the meaning of this frequency range? What determines the expression of different HFOs? Here, we used different concentrations of Ca2+ in a physiological range (1–3 mm) to record local field potentials and single cells in hippocampal slices from normal rats. Surprisingly, we found that this sole manipulation results in the emergence of two forms of HFOs reminiscent of ripples and fast ripples recorded in vivo from normal and epileptic rats, respectively. We scrutinized the cellular correlates and mechanisms underlying the emergence of these two forms of HFOs by combining multisite, single-cell and paired-cell recordings in slices prepared from a rat reporter line that facilitates identification of GABAergic cells. We found a major effect of extracellular Ca2+ in modulating intrinsic excitability and disynaptic inhibition, two critical factors shaping network dynamics. Moreover, locally modulating the extracellular Ca2+ concentration in an in vivo environment had a similar effect on disynaptic inhibition, pyramidal cell excitability, and ripple dynamics. Therefore, the HFO frequency band reflects a range of firing dynamics of hippocampal networks.

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Funding information

This work was supported by Spanish Ministry of Science and Innovation Grant BFU2009-07989 and ERANET-Neuron Project EPINET Grant EUI2009-04093. We thank Ivan Cohen for sharing his interface chamber design with us, Richard Miles for his generous support, comments, and discussion, and François Laurent for the MATLAB routine for the Hotelling's t test. VGAT–Venus transgenic rats were generated by Drs. Y. Yanagawa, M. Hirabayashi, and Y. Kawaguchi at the National Institute for Physiological Sciences (Okazaki, Japan) using pCS2–Venus provided by Dr. A. Miyawaki. VGAT line progenitors were provided by the National Bioresource Project Rat (Kyoto, Japan). We thank Ane Altuna, Javier Berganzo, Luis J. Fernandez, Rosa Villa, and other colleagues from IKERLAN and National Center of Microelectronics–Spanish National Research Council for contributing to develop integrated fluidic probes. We also thank Elena Cid for helping with histological localization. Correspondence should be addressed to Liset Menendez de la Prida, Cajal Institute, Spanish National Research Council, Avenida Doctor Arce, 37, Madrid E-28012, Spain. lmprida@cajal.csic.es

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