Details

Autor(en) / Beteiligte

• Seenivasan, Pavithraa
• Basak, Reshma
• Narayanan, Rishikesh

Titel

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

Ist Teil von

• The Journal of physiology, 2024-05, Vol.602 (10), p.2315-2341

Ort / Verlag

England: Wiley Subscription Services, Inc

Erscheinungsjahr

2024

Link zum Volltext

Quelle

MEDLINE

Beschreibungen/Notizen

• Brain rhythms have been postulated to play central roles in animal cognition. A prominently reported dichotomy of hippocampal rhythms links theta‐frequency oscillations (4–12 Hz) and ripples (120–250 Hz) exclusively to preparatory and consummatory behaviours, respectively. However, because of the differential power expression of these two signals across hippocampal strata, such exclusivity requires validation through analyses of simultaneous multi‐strata recordings. We 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. We then defined theta epochs based on theta oscillations detected from the stratum lacunosum‐moleculare (SLM) or the stratum radiatum (SR). We found ∼20% of ripple events (in SP) to co‐occur with theta epochs identified from SR/SLM channels, defined here as theta ripples. Strikingly, when theta epochs were instead identified from the SP channel, such co‐occurrences were significantly reduced because of a progressive reduction in theta power along the SLM‐SR‐SP axis. Behaviourally, we found most theta ripples to occur during immobile periods, with comparable theta power during exploratory and immobile theta epochs. Furthermore, the progressive reduction in theta power along the SLM‐SR‐SP axis was common to exploratory and immobile periods. Finally, we found a strong theta‐phase preference of theta ripples within the fourth quadrant [3π/2 – 2π] of the associated theta oscillation. 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. Key points The brain manifests oscillations in recorded electrical potentials, with different frequencies of oscillation associated with distinct behavioural states. A prominently reported dichotomy assigns theta‐frequency oscillations (4–12 Hz) and ripples (120–250 Hz) recorded in the hippocampus to be exclusively associated with preparatory and consummatory behaviours, respectively. Our multi‐strata recordings from the rodent hippocampus coupled with cross‐strata analyses provide direct quantitative evidence for the occurrence of ripple events nested within theta oscillations. These results highlight the need for an analysis pipeline that explicitly accounts for the specific strata where individual oscillatory power is high, in analysing simultaneously recorded data from multiple strata. Our observations open avenues for investigations involving cross‐strata interactions between theta oscillations and ripples across different behavioural states. figure legend There are several lines of evidence from the rodent hippocampus that theta frequency oscillations (4–12 Hz) are rich in distal strata, while ripples (120–250 Hz) are prominent in strata that are within and around the pyramidal cell layer. Our goal here was to explore possible co‐occurrence of these distinct bands of signals with differential distribution across strata. We simultaneously recorded extracellular signals from multiple strata in the hippocampus of foraging rats using multi‐site silicon polytrodes. We identified theta epochs from extracellular signals recorded from distal strata and detected ripples from signals recorded through electrode sites closer to the pyramidal cell layer. We found ∼20% of ripple events to be nested within a stream of theta oscillations. We referred to such ripples that co‐occurred with theta oscillations as theta‐ripples. We found that theta ripples occurred preferentially during the fourth quadrant of the associated theta oscillation.