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bioRxiv · 10.1101/2022.11.15.516579

Cross-strata co-occurrence of ripples with theta-frequency oscillations in the hippocampus of foraging rats

Abstract

Background and motivationBrain rhythms have been postulated to play central roles in animal cognition. A prominently reported dichotomy of hippocampal rhythms, driven primarily by historic single-strata recordings, assigns theta-frequency oscillations (4-12 Hz) and ripples (120-250 Hz) to be exclusively associated with preparatory and consummatory behaviors, respectively. However, due to the differential power expression of these two signals across hippocampal strata, reports of such exclusivity require validation through simultaneous multi-strata recordings and cross-strata analysis of these oscillatory patterns. MethodologyWe assessed co-occurrence of theta-frequency oscillations with ripples in multi-channel recordings of extracellular potentials across hippocampal strata from foraging rats. We detected all ripple events from an identified stratum pyramidale (SP) channel based on rigorous thresholds relating to the spectro-temporal and spatial characteristics of ripples. We then defined theta epochs based on theta oscillations detected from each of the different channels spanning the SP to the stratum lacunosum-moleculare (SLM) through the stratum radiatum (SR). We calculated the proportion of ripples embedded within theta epochs. ResultsWe found [~]20% (across rats) of ripple events (in SP) to co-occur with theta epochs identified from SR/SLM channels, defined here as theta ripples. All characteristics of theta ripples were comparable with ripples that occurred in the absence of theta oscillations. Furthermore, the power of theta oscillations in the immediate vicinity of theta ripples was similar to theta power across identified theta epochs, together validating the identification process of theta ripples. Strikingly, when theta epochs were instead identified from the SP channel, such co-occurrences were significantly lower in number. The reduction in the number of theta ripples was consequent to progressive reduction in theta power along the SLM-SR-SP axis. We assessed the behavioral state of rats during ripple events and found most theta ripples to occur during immobile periods. We confirmed that across sessions and rats, the theta power observed during exploratory theta epochs was comparable with theta power during immobile theta epochs. In addition, the progressive reduction in theta power along the SLM-SR-SP axis was common to both exploratory and immobile periods. Finally, we found a strong theta-phase preference of theta ripples within the third quadrant [3{pi}/2-2{pi}] of the associated theta oscillation. ImplicationsOur analyses provide direct quantitative evidence for the occurrence of ripple events nested within theta oscillations in the rodent hippocampus. These analyses emphasize that the prevalent dichotomy about the manifestation of theta-frequency oscillations and ripples needs to be reevaluated, after explicitly accounting for the differential stratum-dependent expression of these two oscillatory patterns. The prevalence of theta ripples expands the potential roles of ripple-frequency oscillations to span the continuum of encoding, retrieval, and consolidation, achieved through interactions with theta oscillations.

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BibTeXRIS

Seenivasan, P., Basak, R., Narayanan, R.. 2022-11-15. Cross-strata co-occurrence of ripples with theta-frequency oscillations in the hippocampus of foraging rats. https://doi.org/10.1101/2022.11.15.516579

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