Effects of theta phase precessing optogenetic intervention on hippocampal neuronal reactivation and spatial maps

Yuki Aoki; Taiki Yokoi; Shota Morikawa; Nahoko Kuga; Yuji Ikegaya; Takuya Sasaki

doi:10.1016/j.isci.2023.107233

Effects of theta phase precessing optogenetic intervention on hippocampal neuronal reactivation and spatial maps

iScience. 2023 Jun 28;26(7):107233. doi: 10.1016/j.isci.2023.107233. eCollection 2023 Jul 21.

Authors

Yuki Aoki¹, Taiki Yokoi², Shota Morikawa^{1

3}, Nahoko Kuga², Yuji Ikegaya^{1

3

4}, Takuya Sasaki^{1

2}

Affiliations

¹ Graduate School of Pharmaceutical Sciences, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
² Department of Pharmacology, Graduate School of Pharmaceutical Sciences, Tohoku University, 6-3 Aramaki-Aoba, Aoba-Ku, Sendai 980-8578, Japan.
³ Institute for AI and Beyond, The University of Tokyo, Tokyo 113-0033, Japan.
⁴ Center for Information and Neural Networks, 1-4 Yamadaoka, Suita City, Osaka 565-0871, Japan.

Abstract

As animals explore environments, hippocampal place cells sequentially fire at progressively earlier phases of theta oscillations in hippocampal local field potentials. In this study, we evaluated the network-level significance of theta phase-entrained neuronal activity in organizing place cell spike patterns. A closed-loop system was developed in which optogenetic stimulation with a temporal pattern replicating theta phase precession is delivered to hippocampal CA1 neurons when rats traversed a particular region on a linear track. Place cells that had place fields during phase precessing stimulation, but not random phase stimulation, showed stronger reactivation during hippocampal sharp-wave ripples in a subsequent rest period. After the rest period, place cells with place fields that emerged during phase precessing stimulation showed more stable place fields. These results imply that neuronal reactivation and stability of spatial maps are mediated by theta phase precession in the hippocampus.

Keywords: Neuroscience; Sensory neuroscience.