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Hippocampal oscillatory dynamics in freely behaving rats during exploration of social and non-social stimuli

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Abstract

Hippocampal CA2 supports social memory and encodes information about social experiences. Our previous study showed that CA2 place cells responded specifically to social stimuli (Nat Commun, (Alexander et al. 2016)). In addition, a prior study showed that activation of CA2 induces slow gamma rhythms (~ 25–55 Hz) in the hippocampus (Elife, (Alexander 2018)). Together, these results raise the question of whether slow gamma rhythms coordinate CA2 activity during social information processing. We hypothesized that slow gamma would be associated with transmission of social memories from CA2 to CA1, perhaps to integrate information across regions or promote social memory retrieval. We recorded local field potentials from hippocampal subfields CA1, CA2, and CA3 of 4 rats performing a social exploration task. We analyzed the activity of theta, slow gamma, and fast gamma rhythms, as well as sharp wave-ripples (SWRs), within each subfield. We assessed interactions between subfields during social exploration sessions and during presumed social memory retrieval in post-social exploration sessions. We found that CA2 slow gamma rhythms increased during social interactions but not during non-social exploration. CA2–CA1 theta-show gamma coupling was enhanced during social exploration. Furthermore, CA1 slow gamma rhythms and SWRs were associated with presumed social memory retrieval. In conclusion, these results suggest that CA2–CA1 interactions via slow gamma rhythms occur during social memory encoding, and CA1 slow gamma is associated with retrieval of social experience.

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The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China grants 81870847 and 31800889 (to C.Z.), the Natural Science Foundation of Tianjin Municipality No. 19JCYBJC25200 and 20JCZDJC00540 (to C.Z.), DOD CDMRP award W81XWH1810314 (to L.L.C.), the National Natural Science Foundation of China grants 81871517 (to J.Y.) and 82001420 (to X.X.), and the General Financial Grant from the China Postdoctoral Science Foundation 2020M670645 (to X.X.).

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NZ, YZ, CZ and LLC designed the experiment; NZ, CZ, XX, YW and JY carried out the electrophysiological recordings, behavioral testing, and histology; YZ, NZ, CZ, and JY designed analyses; NZ, YZ, and CZ wrote analysis programs and analyzed the data; CZ, NZ and LLC wrote the paper; CZ supervised the project. All authors discussed results.

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Correspondence to Chenguang Zheng.

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Zhu, N., Zhang, Y., Xiao, X. et al. Hippocampal oscillatory dynamics in freely behaving rats during exploration of social and non-social stimuli. Cogn Neurodyn 17, 411–429 (2023). https://doi.org/10.1007/s11571-022-09829-8

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  • DOI: https://doi.org/10.1007/s11571-022-09829-8

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