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Cooling of Medial Septum Reveals Theta Phase Lag Coordination of Hippocampal Cell Assemblies.

ABSTRACT: Hippocampal theta oscillations coordinate neuronal firing to support memory and spatial navigation. The medial septum (MS) is critical in theta generation by two possible mechanisms: either a unitary "pacemaker" timing signal is imposed on the hippocampal system, or it may assist in organizing target subcircuits within the phase space of theta oscillations. We used temperature manipulation of the MS to test these models. Cooling of the MS reduced both theta frequency and power and was associated with an enhanced incidence of errors in a spatial navigation task, but it did not affect spatial correlates of neurons. MS cooling decreased theta frequency oscillations of place cells and reduced distance-time compression but preserved distance-phase compression of place field sequences within the theta cycle. Thus, the septum is critical for sustaining precise theta phase coordination of cell assemblies in the hippocampal system, a mechanism needed for spatial memory.

SUBMITTER: Petersen PC

PROVIDER: S-EPMC7442698 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Cooling of Medial Septum Reveals Theta Phase Lag Coordination of Hippocampal Cell Assemblies.

Petersen Peter Christian PC Buzsáki György G

Neuron 20200610 4

Hippocampal theta oscillations coordinate neuronal firing to support memory and spatial navigation. The medial septum (MS) is critical in theta generation by two possible mechanisms: either a unitary "pacemaker" timing signal is imposed on the hippocampal system, or it may assist in organizing target subcircuits within the phase space of theta oscillations. We used temperature manipulation of the MS to test these models. Cooling of the MS reduced both theta frequency and power and was associated ...[more]

PMID: 32526196

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Project description:The medial septum (MS) plays an essential role in rhythmogenesis in the hippocampus (HIPP); theta-rhythmic bursts of MS neurons are believed to drive theta oscillations in rats' HIPP. The MS theta pacemaker hypothesis has solid foundation but the MS-hippocampal interactions during different behavioral states are poorly understood. The MS and the HIPP have reciprocal connections and it is not clear in particular what role, if any, the strong HIPP to MS projection plays in theta generation. To study the functional interactions between MS and HIPP during different behavioral states, this study investigated the relationship between MS single-unit activity and HIPP field potential oscillations during theta states of active waking and REM sleep and non-theta states of slow wave sleep (SWS) and quiet waking (QW), i.e., sleep-wake states that comprise the full behavioral repertoire of undisturbed, freely moving rats. We used non-parametric Granger causality (GC) to decompose the MS-HIPP synchrony into its directional components, MS→HIPP and HIPP→MS, and to examine the causal interactions between them within the theta frequency band. We found a significant unidirectional MS→HIPP influence in non-theta states which switches to bidirectional theta drive during theta states with MS→HIPP and HIPP→MS GC being of equal magnitude. In non-theta states, unidirectional MS→HIPP influence was accompanied by significant MS-HIPP coherence, but no signs of theta oscillations in the HIPP. In theta states of active waking and REM sleep, sharp theta coherence and strong theta power in both structures was associated with a rise in HIPP→MS to the level of the MS→HIPP drive. Thus, striking differences between waking and REM sleep theta states and non-theta states of SWS and QW were primarily observed in activation of theta influence carried by the descending HIPP→MS pathway associated with more regular rhythmic bursts in the MS and sharper MS→HIPP GC spectra without a significant increase in MS→HIPP GC magnitude. The results of this study suggest an essential role of descending HIPP to MS projections in theta generation.

Dataset Information

Cooling of Medial Septum Reveals Theta Phase Lag Coordination of Hippocampal Cell Assemblies.

Publications

Cooling of Medial Septum Reveals Theta Phase Lag Coordination of Hippocampal Cell Assemblies.

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