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      Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning

      research-article
      1 ,
      Hippocampus
      John Wiley and Sons Inc.
      memory, imagining, planning, epilepsy, learning

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          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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          Most cited references680

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          Neural networks and physical systems with emergent collective computational abilities.

          J Hopfield (1982)
          Computational properties of use of biological organisms or to the construction of computers can emerge as collective properties of systems having a large number of simple equivalent components (or neurons). The physical meaning of content-addressable memory is described by an appropriate phase space flow of the state of a system. A model of such a system is given, based on aspects of neurobiology but readily adapted to integrated circuits. The collective properties of this model produce a content-addressable memory which correctly yields an entire memory from any subpart of sufficient size. The algorithm for the time evolution of the state of the system is based on asynchronous parallel processing. Additional emergent collective properties include some capacity for generalization, familiarity recognition, categorization, error correction, and time sequence retention. The collective properties are only weakly sensitive to details of the modeling or the failure of individual devices.
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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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              Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs.

              Activity-driven modifications in synaptic connections between neurons in the neocortex may occur during development and learning. In dual whole-cell voltage recordings from pyramidal neurons, the coincidence of postsynaptic action potentials (APs) and unitary excitatory postsynaptic potentials (EPSPs) was found to induce changes in EPSPs. Their average amplitudes were differentially up- or down-regulated, depending on the precise timing of postsynaptic APs relative to EPSPs. These observations suggest that APs propagating back into dendrites serve to modify single active synaptic connections, depending on the pattern of electrical activity in the pre- and postsynaptic neurons.
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                Author and article information

                Journal
                Hippocampus
                Hippocampus
                10.1002/(ISSN)1098-1063
                HIPO
                Hippocampus
                John Wiley and Sons Inc. (Hoboken )
                1050-9631
                1098-1063
                26 September 2015
                October 2015
                : 25
                : 10 , Hippocampal Sharp Waves ( doiID: 10.1002/hipo.v25.10 )
                : 1073-1188
                Affiliations
                [ 1 ]The Neuroscience Institute, School of Medicine and Center for Neural Science, New York University New York New York
                Author notes
                [*] [* ]Correspondence to: György Buzsáki, The Neuroscience Institute, New York University, School of Medicine East Rivers Science Park, 450 East 29th Street, 9th Floor New York, NY 10016, USA. E‐mail: gyorgy.Buzsáki@nyumc.org
                Article
                HIPO22488
                10.1002/hipo.22488
                4648295
                26135716
                d7028d2a-c75f-4d8d-83e0-45a7b6c92ae6
                © 2015 The Authors Hippocampus Published by Wiley Periodicals, Inc.

                This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial‐NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 26 June 2015
                : 30 June 2015
                Page count
                Pages: 116
                Funding
                Funded by: National Institutes of Health
                Award ID: NS075015
                Award ID: MH54671
                Award ID: MH107396
                Award ID: 5U01NS090583
                Funded by: NSF
                Award ID: SBE 0542013
                Funded by: Human Frontiers Science Program and the G. Harold and Leila Y. Mathers Foundation
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                hipo22488
                October 2015
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:12.09.2016

                Neurology
                memory,imagining,planning,epilepsy,learning
                Neurology
                memory, imagining, planning, epilepsy, learning

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