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      Temporal synchrony and gamma to theta power conversion in the dendrites of CA1 pyramidal neurons

      1 , 2 , 2

      Nature neuroscience

      HCN, synchrony, theta, gamma

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          Abstract

          Timing is a crucial aspect of synaptic integration. For pyramidal neurons that integrate thousands of synaptic inputs spread across hundreds of microns, it is thus a challenge to maintain the timing of incoming inputs at the axo-somatic integration site. Here we show that pyramidal neurons in the rodent hippocampus use a gradient of inductance in the form of HCN channels as an active mechanism to counteract location-dependent temporal differences of dendritic inputs at the soma. Using simultaneous multi-site whole cell recordings complemented by computational modeling, we find that this intrinsic biophysical mechanism produces temporal synchrony of rhythmic inputs in the theta and gamma frequency ranges across wide regions of the dendritic tree. While gamma and theta oscillations are known to synchronize activity across space in neuronal networks, our results identify a novel mechanism by which this synchrony extends to activity within single pyramidal neurons with complex dendritic arbors.

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          Most cited references 39

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          Dynamic predictions: oscillations and synchrony in top-down processing.

          Classical theories of sensory processing view the brain as a passive, stimulus-driven device. By contrast, more recent approaches emphasize the constructive nature of perception, viewing it as an active and highly selective process. Indeed, there is ample evidence that the processing of stimuli is controlled by top-down influences that strongly shape the intrinsic dynamics of thalamocortical networks and constantly create predictions about forthcoming sensory events. We discuss recent experiments indicating that such predictions might be embodied in the temporal structure of both stimulus-evoked and ongoing activity, and that synchronous oscillations are particularly important in this process. Coherence among subthreshold membrane potential fluctuations could be exploited to express selective functional relationships during states of expectancy or attention, and these dynamic patterns could allow the grouping and selection of distributed neuronal responses for further processing.
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            Memory, navigation and theta rhythm in the hippocampal-entorhinal system.

            Theories on the functions of the hippocampal system are based largely on two fundamental discoveries: the amnestic consequences of removing the hippocampus and associated structures in the famous patient H.M. and the observation that spiking activity of hippocampal neurons is associated with the spatial position of the rat. In the footsteps of these discoveries, many attempts were made to reconcile these seemingly disparate functions. Here we propose that mechanisms of memory and planning have evolved from mechanisms of navigation in the physical world and hypothesize that the neuronal algorithms underlying navigation in real and mental space are fundamentally the same. We review experimental data in support of this hypothesis and discuss how specific firing patterns and oscillatory dynamics in the entorhinal cortex and hippocampus can support both navigation and memory.
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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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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                11 March 2014
                03 November 2013
                December 2013
                01 June 2014
                : 16
                : 12
                : 1812-1820
                Affiliations
                [1 ]Institute for Neuroscience Graduate Program, The University of Texas at Austin, Austin, TX 78712
                [2 ]Center for Learning and Memory, The University of Texas at Austin, Austin, TX 78712
                Author notes
                Corresponding Author: Daniel Johnston, Ph.D., Center for Learning and Memory, The University of Texas at Austin, 1, University Station C7000, Austin, TX 78712-0805, 512-232-6564 (Voice), 512-475-8000 (Fax), djohnston@ 123456mail.clm.utexas.edu
                Article
                NIHMS560017
                10.1038/nn.3562
                3958963
                24185428
                Categories
                Article

                Neurosciences

                hcn, gamma, theta, synchrony

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