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Published October 22, 2014 | Accepted Version
Journal Article Open

Theta Phase Segregation of Input-Specific Gamma Patterns in Entorhinal-Hippocampal Networks

Abstract

Precisely how rhythms support neuronal communication remains obscure. We investigated interregional coordination of gamma oscillations using high-density electrophysiological recordings in the rat hippocampus and entorhinal cortex. We found that 30–80 Hz gamma dominated CA1 local field potentials (LFPs) on the descending phase of CA1 theta waves during navigation, with 60–120 Hz gamma at the theta peak. These signals corresponded to CA3 and entorhinal input, respectively. Above 50 Hz, interregional phase-synchronization of principal cell spikes occurred mostly for LFPs in the axonal target domain. CA1 pyramidal cells were phase-locked mainly to fast gamma (>100 Hz) LFP patterns restricted to CA1, which were strongest at the theta trough. While theta phase coordination of spiking across entorhinal-hippocampal regions depended on memory demands, LFP gamma patterns below 100 Hz in the hippocampus were consistently layer specific and largely reflected afferent activity. Gamma synchronization as a mechanism for interregional communication thus rapidly loses efficacy at higher frequencies.

Additional Information

© 2014 Elsevier Inc. Accepted: August 22, 2014; Available online 25 September 2014. Published: September 25, 2014. Supplemental Information includes Supplemental Experimental Procedures, seven figures, and one table and can be found with this article online at http://dx.doi.org/10.1016/j.neuron.2014.08.051. This work was supported by the National Institute of Health Grants NS34994 and MH54671 (G.B.) and NS074015 (C.K.), National Science Foundation Grant SBE 0542013, the Human Frontier Science Program (C.K., G.B.), the James S. McDonnell Foundation (G.B.), G. Harold and Leila Y. Mathers Charitable Foundation (C.K.), the European Molecular Biology Organization and Fundancio´ n ''La Caixa'' (A.F.-R.), EU-FP7-ERC-2013-Starting grant (No. 337075; A.B.), the ''Momentum'' program of the Hungarian Academy of Sciences (A.B.), and the Swiss National Science Foundation (C.A.A.). Results consistent with the present findings have been reported earlier (Sirota et al., 2009, Soc. Neurosci., abstract). We thank Anton Sirota for many useful discussions and advice, Azahara Oliva for assistance with LFP analysis, Pilar Garce´ s for providing code for cross-frequency analysis, Kamran Diba for providing simultaneous CA1 and CA3 recordings, John Long and Andres Grosmark for providing the recording with EMG electrodes, and Jagdish Patel for comments on the manuscript.

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August 20, 2023
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