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Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex

Sensory signals undergo substantial recoding when neural activity is relayed from sensors through pre-thalamic and thalamic nuclei to cortex. To explore how temporal dynamics and directional tuning are sculpted in hierarchical vestibular circuits, we compared responses of macaque otolith afferents w...

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Autores principales: Laurens, Jean, Liu, Sheng, Yu, Xiong-Jie, Chan, Raymond, Dickman, David, DeAngelis, Gregory C, Angelaki, Dora E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5226653/
https://www.ncbi.nlm.nih.gov/pubmed/28075326
http://dx.doi.org/10.7554/eLife.20787
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author Laurens, Jean
Liu, Sheng
Yu, Xiong-Jie
Chan, Raymond
Dickman, David
DeAngelis, Gregory C
Angelaki, Dora E
author_facet Laurens, Jean
Liu, Sheng
Yu, Xiong-Jie
Chan, Raymond
Dickman, David
DeAngelis, Gregory C
Angelaki, Dora E
author_sort Laurens, Jean
collection PubMed
description Sensory signals undergo substantial recoding when neural activity is relayed from sensors through pre-thalamic and thalamic nuclei to cortex. To explore how temporal dynamics and directional tuning are sculpted in hierarchical vestibular circuits, we compared responses of macaque otolith afferents with neurons in the vestibular and cerebellar nuclei, as well as five cortical areas, to identical three-dimensional translational motion. We demonstrate a remarkable spatio-temporal transformation: otolith afferents carry spatially aligned cosine-tuned translational acceleration and jerk signals. In contrast, brainstem and cerebellar neurons exhibit non-linear, mixed selectivity for translational velocity, acceleration, jerk and position. Furthermore, these components often show dissimilar spatial tuning. Moderate further transformation of translation signals occurs in the cortex, such that similar spatio-temporal properties are found in multiple cortical areas. These results suggest that the first synapse represents a key processing element in vestibular pathways, robustly shaping how self-motion is represented in central vestibular circuits and cortical areas. DOI: http://dx.doi.org/10.7554/eLife.20787.001
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spelling pubmed-52266532017-01-13 Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex Laurens, Jean Liu, Sheng Yu, Xiong-Jie Chan, Raymond Dickman, David DeAngelis, Gregory C Angelaki, Dora E eLife Neuroscience Sensory signals undergo substantial recoding when neural activity is relayed from sensors through pre-thalamic and thalamic nuclei to cortex. To explore how temporal dynamics and directional tuning are sculpted in hierarchical vestibular circuits, we compared responses of macaque otolith afferents with neurons in the vestibular and cerebellar nuclei, as well as five cortical areas, to identical three-dimensional translational motion. We demonstrate a remarkable spatio-temporal transformation: otolith afferents carry spatially aligned cosine-tuned translational acceleration and jerk signals. In contrast, brainstem and cerebellar neurons exhibit non-linear, mixed selectivity for translational velocity, acceleration, jerk and position. Furthermore, these components often show dissimilar spatial tuning. Moderate further transformation of translation signals occurs in the cortex, such that similar spatio-temporal properties are found in multiple cortical areas. These results suggest that the first synapse represents a key processing element in vestibular pathways, robustly shaping how self-motion is represented in central vestibular circuits and cortical areas. DOI: http://dx.doi.org/10.7554/eLife.20787.001 eLife Sciences Publications, Ltd 2017-01-11 /pmc/articles/PMC5226653/ /pubmed/28075326 http://dx.doi.org/10.7554/eLife.20787 Text en © 2017, Laurens et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Laurens, Jean
Liu, Sheng
Yu, Xiong-Jie
Chan, Raymond
Dickman, David
DeAngelis, Gregory C
Angelaki, Dora E
Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex
title Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex
title_full Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex
title_fullStr Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex
title_full_unstemmed Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex
title_short Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex
title_sort transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5226653/
https://www.ncbi.nlm.nih.gov/pubmed/28075326
http://dx.doi.org/10.7554/eLife.20787
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