In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.

Previous studies have shown that neurons within the vestibular nuclei (VN) can faithfully encode the time course of sensory input through changes in firing rate in vivo. However, studies performed in vitro have shown that these same VN neurons often display nonlinear synchronization (i.e. phase lock...

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Autores principales:	Adam D Schneider, Kathleen E Cullen, Maurice J Chacron
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/40fe02b465504c8894f1d86ec827d73a
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spelling	oai:doaj.org-article:40fe02b465504c8894f1d86ec827d73a2021-11-18T05:50:24ZIn vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.1553-734X1553-735810.1371/journal.pcbi.1002120https://doaj.org/article/40fe02b465504c8894f1d86ec827d73a2011-07-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21814508/?tool=EBIhttps://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Previous studies have shown that neurons within the vestibular nuclei (VN) can faithfully encode the time course of sensory input through changes in firing rate in vivo. However, studies performed in vitro have shown that these same VN neurons often display nonlinear synchronization (i.e. phase locking) in their spiking activity to the local maxima of sensory input, thereby severely limiting their capacity for faithful encoding of said input through changes in firing rate. We investigated this apparent discrepancy by studying the effects of in vivo conditions on VN neuron activity in vitro using a simple, physiologically based, model of cellular dynamics. We found that membrane potential oscillations were evoked both in response to step and zap current injection for a wide range of channel conductance values. These oscillations gave rise to a resonance in the spiking activity that causes synchronization to sinusoidal current injection at frequencies below 25 Hz. We hypothesized that the apparent discrepancy between VN response dynamics measured in in vitro conditions (i.e., consistent with our modeling results) and the dynamics measured in vivo conditions could be explained by an increase in trial-to-trial variability under in vivo vs. in vitro conditions. Accordingly, we mimicked more physiologically realistic conditions in our model by introducing a noise current to match the levels of resting discharge variability seen in vivo as quantified by the coefficient of variation (CV). While low noise intensities corresponding to CV values in the range 0.04-0.24 only eliminated synchronization for low (<8 Hz) frequency stimulation but not high (>12 Hz) frequency stimulation, higher noise intensities corresponding to CV values in the range 0.5-0.7 almost completely eliminated synchronization for all frequencies. Our results thus predict that, under natural (i.e. in vivo) conditions, the vestibular system uses increased variability to promote fidelity of encoding by single neurons. This prediction can be tested experimentally in vitro.Adam D SchneiderKathleen E CullenMaurice J ChacronPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 7, Iss 7, p e1002120 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Adam D Schneider Kathleen E Cullen Maurice J Chacron In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.
description	Previous studies have shown that neurons within the vestibular nuclei (VN) can faithfully encode the time course of sensory input through changes in firing rate in vivo. However, studies performed in vitro have shown that these same VN neurons often display nonlinear synchronization (i.e. phase locking) in their spiking activity to the local maxima of sensory input, thereby severely limiting their capacity for faithful encoding of said input through changes in firing rate. We investigated this apparent discrepancy by studying the effects of in vivo conditions on VN neuron activity in vitro using a simple, physiologically based, model of cellular dynamics. We found that membrane potential oscillations were evoked both in response to step and zap current injection for a wide range of channel conductance values. These oscillations gave rise to a resonance in the spiking activity that causes synchronization to sinusoidal current injection at frequencies below 25 Hz. We hypothesized that the apparent discrepancy between VN response dynamics measured in in vitro conditions (i.e., consistent with our modeling results) and the dynamics measured in vivo conditions could be explained by an increase in trial-to-trial variability under in vivo vs. in vitro conditions. Accordingly, we mimicked more physiologically realistic conditions in our model by introducing a noise current to match the levels of resting discharge variability seen in vivo as quantified by the coefficient of variation (CV). While low noise intensities corresponding to CV values in the range 0.04-0.24 only eliminated synchronization for low (<8 Hz) frequency stimulation but not high (>12 Hz) frequency stimulation, higher noise intensities corresponding to CV values in the range 0.5-0.7 almost completely eliminated synchronization for all frequencies. Our results thus predict that, under natural (i.e. in vivo) conditions, the vestibular system uses increased variability to promote fidelity of encoding by single neurons. This prediction can be tested experimentally in vitro.
format	article
author	Adam D Schneider Kathleen E Cullen Maurice J Chacron
author_facet	Adam D Schneider Kathleen E Cullen Maurice J Chacron
author_sort	Adam D Schneider
title	In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.
title_short	In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.
title_full	In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.
title_fullStr	In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.
title_full_unstemmed	In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.
title_sort	in vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/40fe02b465504c8894f1d86ec827d73a
work_keys_str_mv	AT adamdschneider invivoconditionsinducefaithfulencodingofstimulibyreducingnonlinearsynchronizationinvestibularsensoryneurons AT kathleenecullen invivoconditionsinducefaithfulencodingofstimulibyreducingnonlinearsynchronizationinvestibularsensoryneurons AT mauricejchacron invivoconditionsinducefaithfulencodingofstimulibyreducingnonlinearsynchronizationinvestibularsensoryneurons
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In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.

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