Literature DB >> 28978765

Convergence of linear acceleration and yaw rotation signals on non-eye movement neurons in the vestibular nucleus of macaques.

Shawn D Newlands1,2, Ben Abbatematteo3, Min Wei1, Laurel H Carney3,2, Hongge Luan1.   

Abstract

Roughly half of all vestibular nucleus neurons without eye movement sensitivity respond to both angular rotation and linear acceleration. Linear acceleration signals arise from otolith organs, and rotation signals arise from semicircular canals. In the vestibular nerve, these signals are carried by different afferents. Vestibular nucleus neurons represent the first point of convergence for these distinct sensory signals. This study systematically evaluated how rotational and translational signals interact in single neurons in the vestibular nuclei: multisensory integration at the first opportunity for convergence between these two independent vestibular sensory signals. Single-unit recordings were made from the vestibular nuclei of awake macaques during yaw rotation, translation in the horizontal plane, and combinations of rotation and translation at different frequencies. The overall response magnitude of the combined translation and rotation was generally less than the sum of the magnitudes in responses to the stimuli applied independently. However, we found that under conditions in which the peaks of the rotational and translational responses were coincident these signals were approximately additive. With presentation of rotation and translation at different frequencies, rotation was attenuated more than translation, regardless of which was at a higher frequency. These data suggest a nonlinear interaction between these two sensory modalities in the vestibular nuclei, in which coincident peak responses are proportionally stronger than other, off-peak interactions. These results are similar to those reported for other forms of multisensory integration, such as audio-visual integration in the superior colliculus. NEW & NOTEWORTHY This is the first study to systematically explore the interaction of rotational and translational signals in the vestibular nuclei through independent manipulation. The results of this study demonstrate nonlinear integration leading to maximum response amplitude when the timing and direction of peak rotational and translational responses are coincident.

Entities:  

Keywords:  brain stem; multisensory integration; otolith; semicircular canal; single-unit recording

Mesh:

Year:  2017        PMID: 28978765      PMCID: PMC5866467          DOI: 10.1152/jn.00382.2017

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  50 in total

1.  Convergence of the horizontal semicircular canal and otolith afferents on cat single vestibular neurons.

Authors:  X Zhang; M Zakir; H Meng; H Sato; Y Uchino
Journal:  Exp Brain Res       Date:  2001-09       Impact factor: 1.972

2.  Vestibular convergence patterns in vestibular nuclei neurons of alert primates.

Authors:  J David Dickman; Dora E Angelaki
Journal:  J Neurophysiol       Date:  2002-12       Impact factor: 2.714

3.  Neurons compute internal models of the physical laws of motion.

Authors:  Dora E Angelaki; Aasef G Shaikh; Andrea M Green; J David Dickman
Journal:  Nature       Date:  2004-07-29       Impact factor: 49.962

4.  Response of vestibular neurons to head rotations in vertical planes. III. Response of vestibulocollic neurons to vestibular and neck stimulation.

Authors:  V J Wilson; Y Yamagata; B J Yates; R H Schor; S Nonaka
Journal:  J Neurophysiol       Date:  1990-12       Impact factor: 2.714

5.  Behavior of eye-movement-related cells in the vestibular nuclei during combined rotational and translational stimuli.

Authors:  K M McConville; R D Tomlinson; E Q NA
Journal:  J Neurophysiol       Date:  1996-11       Impact factor: 2.714

6.  Integration of canal and otolith inputs by central vestibular neurons is subadditive for both active and passive self-motion: implication for perception.

Authors:  Jerome Carriot; Mohsen Jamali; Jessica X Brooks; Kathleen E Cullen
Journal:  J Neurosci       Date:  2015-02-25       Impact factor: 6.167

7.  Statistics of the vestibular input experienced during natural self-motion: implications for neural processing.

Authors:  Jérome Carriot; Mohsen Jamali; Maurice J Chacron; Kathleen E Cullen
Journal:  J Neurosci       Date:  2014-06-11       Impact factor: 6.167

8.  Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. I. Natural stimulation.

Authors:  I S Curthoys; C H Markham
Journal:  Brain Res       Date:  1971-12-24       Impact factor: 3.252

9.  Responses of interneurons in the cat cervical cord to vestibular tilt stimulation.

Authors:  R H Schor; I Suzuki; S J Timerick; V J Wilson
Journal:  J Neurophysiol       Date:  1986-10       Impact factor: 2.714

10.  Encoding of head acceleration in vestibular neurons. I. Spatiotemporal response properties to linear acceleration.

Authors:  G A Bush; A A Perachio; D E Angelaki
Journal:  J Neurophysiol       Date:  1993-06       Impact factor: 2.714

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  3 in total

Review 1.  Vestibular System and Self-Motion.

Authors:  Zhixian Cheng; Yong Gu
Journal:  Front Cell Neurosci       Date:  2018-11-22       Impact factor: 5.505

2.  Adaptation of spatio-temporal convergent properties in central vestibular neurons in monkeys.

Authors:  Julia N Eron; Dmitri Ogorodnikov; Anja K E Horn; Sergei B Yakushin
Journal:  Physiol Rep       Date:  2018-09

Review 3.  Animal Models of Vestibular Evoked Myogenic Potentials: The Past, Present, and Future.

Authors:  Brian D Corneil; Aaron J Camp
Journal:  Front Neurol       Date:  2018-06-25       Impact factor: 4.003

  3 in total

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