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

Jean Laurens, Sheng Liu, Xiong Jie Yu, Raymond Chan, David Dickman, Gregory C. DeAngelis, Dora Angelaki

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
Article numbere20787
JournaleLife
Volume6
DOIs
StatePublished - Jan 11 2017

Fingerprint

Otolithic Membrane
Macaca
Neurons
Tuning
Networks (circuits)
Vestibular Nuclei
Afferent Neurons
Cerebellar Nuclei
Thalamic Nuclei
Synapses
Brain Stem
Sensors
Processing

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)

Cite this

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.

In: eLife, Vol. 6, e20787, 11.01.2017.

Research output: Contribution to journalArticle

Laurens, Jean ; Liu, Sheng ; Yu, Xiong Jie ; Chan, Raymond ; Dickman, David ; DeAngelis, Gregory C. ; Angelaki, Dora. / Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex. In: eLife. 2017 ; Vol. 6.
@article{0d9991af9a284bcc9813b23cef7a6578,
title = "Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex",
abstract = "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.",
author = "Jean Laurens and Sheng Liu and Yu, {Xiong Jie} and Raymond Chan and David Dickman and DeAngelis, {Gregory C.} and Dora Angelaki",
year = "2017",
month = "1",
day = "11",
doi = "10.7554/eLife.20787",
language = "English (US)",
volume = "6",
journal = "eLife",
issn = "2050-084X",
publisher = "eLife Sciences Publications",

}

TY - JOUR

T1 - Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex

AU - Laurens, Jean

AU - Liu, Sheng

AU - Yu, Xiong Jie

AU - Chan, Raymond

AU - Dickman, David

AU - DeAngelis, Gregory C.

AU - Angelaki, Dora

PY - 2017/1/11

Y1 - 2017/1/11

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85009458376&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85009458376&partnerID=8YFLogxK

U2 - 10.7554/eLife.20787

DO - 10.7554/eLife.20787

M3 - Article

VL - 6

JO - eLife

JF - eLife

SN - 2050-084X

M1 - e20787

ER -