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Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus.

ABSTRACT: Theta oscillations in the limbic system depend on the integrity of the medial septum. The different populations of medial septal neurons (cholinergic and GABAergic) are assumed to affect different aspects of theta oscillations. Using optogenetic stimulation of cholinergic neurons in ChAT-Cre mice, we investigated their effects on hippocampal local field potentials in both anesthetized and behaving mice. Cholinergic stimulation completely blocked sharp wave ripples and strongly suppressed the power of both slow oscillations (0.5-2 Hz in anesthetized, 0.5-4 Hz in behaving animals) and supratheta (6-10 Hz in anesthetized, 10-25 Hz in behaving animals) bands. The same stimulation robustly increased both the power and coherence of theta oscillations (2-6 Hz) in urethane-anesthetized mice. In behaving mice, cholinergic stimulation was less effective in the theta (4-10 Hz) band yet it also increased the ratio of theta/slow oscillation and theta coherence. The effects on gamma oscillations largely mirrored those of theta. These findings show that medial septal cholinergic activation can both enhance theta rhythm and suppress peri-theta frequency bands, allowing theta oscillations to dominate.

SUBMITTER: Vandecasteele M

PROVIDER: S-EPMC4169920 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus.

Vandecasteele Marie M Varga Viktor V Berényi Antal A Papp Edit E Barthó Péter P Venance Laurent L Freund Tamás F TF Buzsáki György G

Proceedings of the National Academy of Sciences of the United States of America 20140902 37

Theta oscillations in the limbic system depend on the integrity of the medial septum. The different populations of medial septal neurons (cholinergic and GABAergic) are assumed to affect different aspects of theta oscillations. Using optogenetic stimulation of cholinergic neurons in ChAT-Cre mice, we investigated their effects on hippocampal local field potentials in both anesthetized and behaving mice. Cholinergic stimulation completely blocked sharp wave ripples and strongly suppressed the pow ...[more]

PMID: 25197052

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Project description: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.

Dataset Information

Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus.

Publications

Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus.

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