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      Theta oscillations represent collective dynamics of multineuronal membrane potentials of murine hippocampal pyramidal cells

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          Abstract

          Theta (θ) oscillations are one of the characteristic local field potentials (LFPs) in the hippocampus that emerge during spatial navigation, exploratory sniffing, and rapid eye movement sleep. LFPs are thought to summarize multineuronal events, including synaptic currents and action potentials. However, no in vivo study to date has directly interrelated θ oscillations with the membrane potentials ( Vm) of multiple neurons, and it remains unclear whether LFPs can be predicted from multineuronal Vms. Here, we simultaneously patch-clamp up to three CA1 pyramidal neurons in awake or anesthetized mice and find that the temporal evolution of the power and frequency of θ oscillations in Vms (θ Vm s) are weakly but significantly correlate with LFP θ oscillations (θ LFP) such that a deep neural network could predict the θ LFP waveforms based on the θ Vm traces of three neurons. Therefore, individual neurons are loosely interdependent to ensure freedom of activity, but they partially share information to collectively produce θ LFP.

          Abstract

          A deep neural network model predicts theta oscillations in the mouse hippocampal CA1 area based on in vivo membrane potentials of as few as three pyramidal cells.

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          Most cited references64

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          Theta oscillations in the hippocampus.

          Theta oscillations represent the "on-line" state of the hippocampus. The extracellular currents underlying theta waves are generated mainly by the entorhinal input, CA3 (Schaffer) collaterals, and voltage-dependent Ca(2+) currents in pyramidal cell dendrites. The rhythm is believed to be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights. Nevertheless, numerous critical issues regarding both the generation of theta oscillations and their functional significance remain challenges for future research.
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            The origin of extracellular fields and currents--EEG, ECoG, LFP and spikes.

            Neuronal activity in the brain gives rise to transmembrane currents that can be measured in the extracellular medium. Although the major contributor of the extracellular signal is the synaptic transmembrane current, other sources--including Na(+) and Ca(2+) spikes, ionic fluxes through voltage- and ligand-gated channels, and intrinsic membrane oscillations--can substantially shape the extracellular field. High-density recordings of field activity in animals and subdural grid recordings in humans, combined with recently developed data processing tools and computational modelling, can provide insight into the cooperative behaviour of neurons, their average synaptic input and their spiking output, and can increase our understanding of how these processes contribute to the extracellular signal.
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              Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning

              ABSTRACT Sharp wave ripples (SPW‐Rs) represent the most synchronous population pattern in the mammalian brain. Their excitatory output affects a wide area of the cortex and several subcortical nuclei. SPW‐Rs occur during “off‐line” states of the brain, associated with consummatory behaviors and non‐REM sleep, and are influenced by numerous neurotransmitters and neuromodulators. They arise from the excitatory recurrent system of the CA3 region and the SPW‐induced excitation brings about a fast network oscillation (ripple) in CA1. The spike content of SPW‐Rs is temporally and spatially coordinated by a consortium of interneurons to replay fragments of waking neuronal sequences in a compressed format. SPW‐Rs assist in transferring this compressed hippocampal representation to distributed circuits to support memory consolidation; selective disruption of SPW‐Rs interferes with memory. Recently acquired and pre‐existing information are combined during SPW‐R replay to influence decisions, plan actions and, potentially, allow for creative thoughts. In addition to the widely studied contribution to memory, SPW‐Rs may also affect endocrine function via activation of hypothalamic circuits. Alteration of the physiological mechanisms supporting SPW‐Rs leads to their pathological conversion, “p‐ripples,” which are a marker of epileptogenic tissue and can be observed in rodent models of schizophrenia and Alzheimer's Disease. Mechanisms for SPW‐R genesis and function are discussed in this review. © 2015 The Authors Hippocampus Published by Wiley Periodicals, Inc.
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                Author and article information

                Contributors
                asakonoguchi.an@gmail.com
                Journal
                Commun Biol
                Commun Biol
                Communications Biology
                Nature Publishing Group UK (London )
                2399-3642
                12 April 2023
                12 April 2023
                2023
                : 6
                : 398
                Affiliations
                [1 ]GRID grid.26999.3d, ISNI 0000 0001 2151 536X, Graduate School of Pharmaceutical Sciences, , The University of Tokyo, ; Tokyo, 113-0033 Japan
                [2 ]GRID grid.26999.3d, ISNI 0000 0001 2151 536X, Institute for AI and Beyond, , The University of Tokyo, ; Tokyo, 113-0033 Japan
                [3 ]GRID grid.28312.3a, ISNI 0000 0001 0590 0962, Center for Information and Neural Networks, National Institute of Information and Communications Technology, Suita City, ; Osaka, 565-0871 Japan
                Author information
                http://orcid.org/0000-0001-9823-8188
                http://orcid.org/0000-0002-0426-9416
                http://orcid.org/0000-0003-2260-8191
                Article
                4719
                10.1038/s42003-023-04719-z
                10097823
                37045975
                153906db-9b64-4513-89a4-cad53ed98c99
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 21 September 2022
                : 16 March 2023
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                © The Author(s) 2023

                neural circuits,membrane potential
                neural circuits, membrane potential

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