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Comparison of three gamma oscillations in the mouse entorhinal–hippocampal system

Butler, JL; Hay, YA; Paulsen, O; (2018) Comparison of three gamma oscillations in the mouse entorhinal–hippocampal system. European Journal of Neuroscience , 48 (8) pp. 2795-2806. 10.1111/ejn.13831. Green open access

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Abstract

The entorhinal–hippocampal system is an important circuit in the brain, essential for certain cognitive tasks such as memory and navigation. Different gamma oscillations occur in this circuit, with the medial entorhinal cortex (mEC), CA3 and CA1 all generating gamma oscillations with different properties. These three gamma oscillations converge within CA1, where much work has gone into trying to isolate them from each other. Here, we compared the gamma generators in the mEC, CA3 and CA1 using optogenetically induced theta–gamma oscillations. Expressing channelrhodopsin‐2 in principal neurons in each of the three regions allowed for the induction of gamma oscillations via sinusoidal blue light stimulation at theta frequency. Recording the oscillations in CA1 in vivo, we found that CA3 stimulation induced slower gamma oscillations than CA1 stimulation, matching in vivo reports of spontaneous CA3 and CA1 gamma oscillations. In brain slices ex vivo, optogenetic stimulation of CA3 induced slower gamma oscillations than stimulation of either mEC or CA1, whose gamma oscillations were of similar frequency. All three gamma oscillations had a current sink–source pair between the perisomatic and dendritic layers of the same region. Taking advantage of this model to analyse gamma frequency mechanisms in slice, we showed using pharmacology that all three gamma oscillations were dependent on the same types of synaptic receptor, being abolished by blockade of either type A γ‐aminobutyric acid receptors or α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionic acid/kainate receptors, and insensitive to blockade of N‐methyl‐d‐aspartate receptors. These results indicate that a fast excitatory–inhibitory feedback loop underlies the generation of gamma oscillations in all three regions.

Type: Article
Title: Comparison of three gamma oscillations in the mouse entorhinal–hippocampal system
Open access status: An open access version is available from UCL Discovery
DOI: 10.1111/ejn.13831
Publisher version: https://doi.org/10.1111/ejn.13831
Language: English
Additional information: © 2018 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/).
Keywords: neural circuit, neural network, optogenetics, theta
UCL classification: UCL > Provost and Vice Provost Offices
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > Clinical and Movement Neurosciences
URI: http://discovery.ucl.ac.uk/id/eprint/10054168
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