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

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 (ChR2) in principal neurons in each of the three regions allowed for 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 and 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 powerful 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 GABA_A receptors or AMPA/kainate receptors, and insensitive to blockade of NMDA receptors. These results indicate that a fast excitatory-inhibitory feedback loop underlies the generation of gamma oscillations in all three regions.

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