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      Radiate and Planar Multipolar Neurons of the Mouse Anteroventral Cochlear Nucleus: Intrinsic Excitability and Characterization of their Auditory Nerve Input

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          Abstract

          Radiate and planar neurons are the two major types of multipolar neurons in the ventral cochlear nucleus (VCN). Both cell types receive monosynaptic excitatory synaptic inputs from the auditory nerve, but have different responses to sound and project to different target regions and cells. Although the intrinsic physiology and synaptic inputs to planar neurons have been previously characterized, the radiate neurons are less common and have not been as well studied. We studied both types of multipolar neurons and characterized their properties including intrinsic excitability, synaptic dynamics of their auditory nerve inputs, as well as their neural firing properties to auditory nerve stimulation. Radiate neurons had a faster member time constant and higher threshold current to fire spikes than planar neurons, but the maximal firing rate is the same for both cell types upon large current injections. Compared to planar neurons, radiate neurons showed spontaneous postsynaptic currents with smaller size, and slower but variable kinetics. Auditory nerve stimulation progressively recruited synaptic inputs that were smaller and slower in radiate neurons, over a broader range of stimulus strength. Synaptic inputs to radiate neurons showed less depression than planar neurons during low rates of repetitive activity, but the synaptic depression at higher rates was similar between two cell types. However, due to the slow kinetics of the synaptic inputs, synaptic transmission in radiate neurons showed prominent temporal summation that contributed to greater synaptic depolarization and a higher firing rate for repetitive auditory nerve stimulation at high rates. Taken together, these results show that radiate multipolar neurons integrate a large number of weak synaptic inputs over a broad dynamic range, and have intrinsic and synaptic properties that are distinct from planar multipolar neurons. These properties enable radiate neurons to generate powerful inhibitory inputs to target neurons during high levels of afferent activity. Such robust inhibition is expected to dynamically modulate the excitability of many cell types in the cochlear nuclear complex.

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          Most cited references74

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          Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization.

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            Response properties of single auditory nerve fibers in the mouse.

            The availability of transgenic and mutant lines makes the mouse a valuable model for study of the inner ear, and a powerful window into cochlear function can be obtained by recordings from single auditory nerve (AN) fibers. This study provides the first systematic description of spontaneous and sound-evoked discharge properties of AN fibers in mouse, specifically in CBA/CaJ and C57BL/6 strains, both commonly used in auditory research. Response properties of 196 AN fibers from CBA/CaJ and 58 from C57BL/6 were analyzed, including spontaneous rates (SR), tuning curves, rate versus level functions, dynamic range, response adaptation, phase-locking, and the relation between SR and these response properties. The only significant interstrain difference was the elevation of high-frequency thresholds in C57BL/6. In general, mouse AN fibers showed similar responses to other mammals: sharpness of tuning increased with characteristic frequency, which ranged from 2.5 to 70 kHz; SRs ranged from 0 to 120 sp/s, and fibers with low SR (<1 sp/s) had higher thresholds, and wider dynamic ranges than fibers with high SR. Dynamic ranges for mouse high-SR fibers were smaller (<20 dB) than those seen in other mammals. Phase-locking was seen for tone frequencies <4 kHz. Maximum synchronization indices were lower than those in cat but similar to those found in guinea pig.
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              Direct measurement of somatic voltage clamp errors in central neurons.

              The somatic voltage clamp technique has revolutionized understanding of synaptic physiology and the excitability of neurons. Although computer simulations have indicated that the somatic voltage clamp poorly controls voltage in the dendritic tree of neurons, where the majority of synaptic contacts are made, there has not been an experimental description of the performance of the somatic voltage clamp. Here, we directly quantify errors in the measurement of dendritic synaptic input by the somatic voltage clamp using simultaneous whole-cell recordings from the soma and apical dendrite of rat neocortical pyramidal neurons. The somatic voltage clamp did not control voltage at sites other than the soma and distorted measurement of the amplitude, kinetics, slope conductance and reversal potential of synaptic inputs in a dendritic distance-dependent manner. These errors question the use of the somatic voltage clamp as a quantitative tool in dendritic neurons.
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                Author and article information

                Contributors
                Journal
                Front Neural Circuits
                Front Neural Circuits
                Front. Neural Circuits
                Frontiers in Neural Circuits
                Frontiers Media S.A.
                1662-5110
                18 October 2017
                2017
                : 11
                : 77
                Affiliations
                [1] 1Department of Neurosciences, University of Toledo , Toledo, OH, United States
                [2] 2Department of Otolaryngology/Head and Neck Surgery, University of North Carolina at Chapel Hill , Chapel Hill, NC, United States
                [3] 3Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill , Chapel Hill, NC, United States
                Author notes

                Edited by: Catherine Carr, University of Maryland, College Park, United States

                Reviewed by: Michael Thomas Roberts, University of Michigan, United States; R. Michael Burger, Lehigh University, United States; Yong Lu, Northeast Ohio Medical University, United States; Ian Michael Winter, University of Cambridge, United Kingdom

                *Correspondence: Ruili Xie ruili.xie@ 123456utoledo.edu
                Article
                10.3389/fncir.2017.00077
                5651243
                29093666
                208c69a9-9d9f-43a2-9da8-d7afc5a3e4eb
                Copyright © 2017 Xie and Manis.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 27 June 2017
                : 02 October 2017
                Page count
                Figures: 6, Tables: 0, Equations: 1, References: 77, Pages: 17, Words: 13837
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: R01DC004551, R03DC013396
                Categories
                Neuroscience
                Original Research

                Neurosciences
                cochlear nucleus,inhibition,stellate neuron,radiate,planar,auditory nerve input,excitatory synaptic transmission,synaptic dynamics

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