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      Network mechanisms of theta related neuronal activity in hippocampal CA1 pyramidal neurons

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          Abstract

          Although hippocampal theta oscillations represent a prime example of temporal coding in the mammalian brain, little is known about the specific biophysical mechanisms. Intracellular recordings implicate a particular abstract oscillatory interference model of hippocampal theta activity; the soma-dendrite interference model. To gain insight into the cellular and circuit level mechanisms of theta activity we implemented a similar form of interference using the actual hippocampal network in mice in vitro. We found that pairing increasing levels of phasic dendritic excitation with phasic stimulation of perisomatic projecting inhibitory interneurons induced a somatic polarization and action potential timing profile that reproduced most common features. Alterations in the temporal profile of inhibition were required to fully capture all features. These data suggest that theta-related place cell activity is generated through an interaction between a phasic dendritic excitation and a phasic perisomatic shunting inhibition delivered by interneurons; a subset of which undergo activity-dependent presynaptic modulation.

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          Most cited references38

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          The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat.

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            Intracellular dynamics of hippocampal place cells during virtual navigation

            Hippocampal place cells encode spatial information in rate and temporal codes. To examine the mechanisms underlying hippocampal coding, we measured the intracellular dynamics of place cells by combining in vivo whole cell recordings with a virtual reality system. Head-restrained mice, running on a spherical treadmill, interacted with a computer-generated visual environment to perform spatial behaviors. Robust place cell activity was present during movement along a virtual linear track. From whole cell recordings, we identified three subthreshold signatures of place fields: (1) an asymmetric ramp-like depolarization of the baseline membrane potential; (2) an increase in the amplitude of intracellular theta oscillations; and, (3) a phase precession of the intracellular theta oscillation relative to the extracellularly-recorded theta rhythm. These intracellular dynamics underlie the primary features of place cell rate and temporal codes. The virtual reality system developed here will enable new experimental approaches to study the neural circuits underlying navigation.
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              Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop.

              Theta oscillations are believed to play an important role in the coordination of neuronal firing in the entorhinal (EC)-hippocampal system but the underlying mechanisms are not known. We simultaneously recorded from neurons in multiple regions of the EC-hippocampal loop and examined their temporal relationships. Theta-coordinated synchronous spiking of EC neuronal populations predicted the timing of current sinks in target layers in the hippocampus. However, the temporal delays between population activities in successive anatomical stages were longer (typically by a half theta cycle) than expected from axon conduction velocities and passive synaptic integration of feed-forward excitatory inputs. We hypothesize that the temporal windows set by the theta cycles allow for local circuit interactions and thus a considerable degree of computational independence in subdivisions of the EC-hippocampal loop.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nature neuroscience
                1097-6256
                1546-1726
                30 July 2010
                18 July 2010
                August 2010
                1 February 2011
                : 13
                : 8
                : 967-972
                Affiliations
                [1 ] Columbia University, Department of Neuroscience, New York, NY, USA
                [2 ] Howard Hughes Medical Institute, Janelia Farm Research, Campus, Ashburn, VA, USA
                Author notes
                Correspondence to: Jeffrey C. Magee, Howard Hughes Medical Institute, Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, VA, USA, mageej@ 123456janelia.hhmi.org
                [*]

                these authors contributed equally

                Article
                hhmipa214312
                10.1038/nn.2597
                2921679
                20639875
                74b59107-b1ce-409d-bb0c-a765a14b7526

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                History
                Funding
                Funded by: Howard Hughes Medical Institute
                Award ID: ||HHMI_
                Categories
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                Neurosciences
                Neurosciences

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