Neuronal detection thresholds during vestibular compensation: contributions of response variability and sensory substitution

Key points Unilateral vestibular injury impairs our ability to detect motion. However, before this study the neural mechanisms underlying this impairment had not yet been established. We found that the detection thresholds of neurons at the first central stage of vestibular processing (i.e. vestibul...

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Published inThe Journal of physiology Vol. 592; no. 7; pp. 1565 - 1580
Main Authors Jamali, Mohsen, Mitchell, Diana E., Dale, Alexis, Carriot, Jerome, Sadeghi, Soroush G., Cullen, Kathleen E.
Format Journal Article
LanguageEnglish
Published England Wiley Subscription Services, Inc 01.04.2014
BlackWell publishing Ltd
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Online AccessGet full text
ISSN0022-3751
1469-7793
1469-7793
DOI10.1113/jphysiol.2013.267534

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Abstract Key points Unilateral vestibular injury impairs our ability to detect motion. However, before this study the neural mechanisms underlying this impairment had not yet been established. We found that the detection thresholds of neurons at the first central stage of vestibular processing (i.e. vestibular nuclei) dramatically increase immediately post‐lesion, and despite some recovery remain elevated even after 1 month, following the trend reported for vestibular patients’ perception. After the lesion, parallel changes in neuronal trial‐to‐trial variability and sensitivity account for consistently elevated thresholds, thus providing a neural correlate for impaired behavioural performance. In a subset of neurons, sensory substitution with extravestibular (i.e. proprioceptive) inputs after the lesion combined with residual vestibular information serves to improve neuronal detection thresholds for head‐on‐body motion. Our results provide a neural correlate for rehabilitation approaches that take advantage of the convergence of proprioceptive and vestibular inputs to improve patient outcomes. The vestibular system is responsible for processing self‐motion, allowing normal subjects to discriminate the direction of rotational movements as slow as 1–2 deg s−1. After unilateral vestibular injury patients’ direction–discrimination thresholds worsen to ∼20 deg s−1, and despite some improvement thresholds remain substantially elevated following compensation. To date, however, the underlying neural mechanisms of this recovery have not been addressed. Here, we recorded from first‐order central neurons in the macaque monkey that provide vestibular information to higher brain areas for self‐motion perception. Immediately following unilateral labyrinthectomy, neuronal detection thresholds increased by more than two‐fold (from 14 to 30 deg s−1). While thresholds showed slight improvement by week 3 (25 deg s−1), they never recovered to control values – a trend mirroring the time course of perceptual thresholds in patients. We further discovered that changes in neuronal response variability paralleled changes in sensitivity for vestibular stimulation during compensation, thereby causing detection thresholds to remain elevated over time. However, we found that in a subset of neurons, the emergence of neck proprioceptive responses combined with residual vestibular modulation during head‐on‐body motion led to better neuronal detection thresholds. Taken together, our results emphasize that increases in response variability to vestibular inputs ultimately constrain neural thresholds and provide evidence that sensory substitution with extravestibular (i.e. proprioceptive) inputs at the first central stage of vestibular processing is a neural substrate for improvements in self‐motion perception following vestibular loss. Thus, our results provide a neural correlate for the patient benefits provided by rehabilitative strategies that take advantage of the convergence of these multisensory cues.
AbstractList The vestibular system is responsible for processing self-motion, allowing normal subjects to discriminate the direction of rotational movements as slow as 1-2 deg s(-1). After unilateral vestibular injury patients' direction-discrimination thresholds worsen to ∼20 deg s(-1), and despite some improvement thresholds remain substantially elevated following compensation. To date, however, the underlying neural mechanisms of this recovery have not been addressed. Here, we recorded from first-order central neurons in the macaque monkey that provide vestibular information to higher brain areas for self-motion perception. Immediately following unilateral labyrinthectomy, neuronal detection thresholds increased by more than two-fold (from 14 to 30 deg s(-1)). While thresholds showed slight improvement by week 3 (25 deg s(-1)), they never recovered to control values - a trend mirroring the time course of perceptual thresholds in patients. We further discovered that changes in neuronal response variability paralleled changes in sensitivity for vestibular stimulation during compensation, thereby causing detection thresholds to remain elevated over time. However, we found that in a subset of neurons, the emergence of neck proprioceptive responses combined with residual vestibular modulation during head-on-body motion led to better neuronal detection thresholds. Taken together, our results emphasize that increases in response variability to vestibular inputs ultimately constrain neural thresholds and provide evidence that sensory substitution with extravestibular (i.e. proprioceptive) inputs at the first central stage of vestibular processing is a neural substrate for improvements in self-motion perception following vestibular loss. Thus, our results provide a neural correlate for the patient benefits provided by rehabilitative strategies that take advantage of the convergence of these multisensory cues.The vestibular system is responsible for processing self-motion, allowing normal subjects to discriminate the direction of rotational movements as slow as 1-2 deg s(-1). After unilateral vestibular injury patients' direction-discrimination thresholds worsen to ∼20 deg s(-1), and despite some improvement thresholds remain substantially elevated following compensation. To date, however, the underlying neural mechanisms of this recovery have not been addressed. Here, we recorded from first-order central neurons in the macaque monkey that provide vestibular information to higher brain areas for self-motion perception. Immediately following unilateral labyrinthectomy, neuronal detection thresholds increased by more than two-fold (from 14 to 30 deg s(-1)). While thresholds showed slight improvement by week 3 (25 deg s(-1)), they never recovered to control values - a trend mirroring the time course of perceptual thresholds in patients. We further discovered that changes in neuronal response variability paralleled changes in sensitivity for vestibular stimulation during compensation, thereby causing detection thresholds to remain elevated over time. However, we found that in a subset of neurons, the emergence of neck proprioceptive responses combined with residual vestibular modulation during head-on-body motion led to better neuronal detection thresholds. Taken together, our results emphasize that increases in response variability to vestibular inputs ultimately constrain neural thresholds and provide evidence that sensory substitution with extravestibular (i.e. proprioceptive) inputs at the first central stage of vestibular processing is a neural substrate for improvements in self-motion perception following vestibular loss. Thus, our results provide a neural correlate for the patient benefits provided by rehabilitative strategies that take advantage of the convergence of these multisensory cues.
The vestibular system is responsible for processing self-motion, allowing normal subjects to discriminate the direction of rotational movements as slow as 1-2 deg s(-1). After unilateral vestibular injury patients' direction-discrimination thresholds worsen to ∼20 deg s(-1), and despite some improvement thresholds remain substantially elevated following compensation. To date, however, the underlying neural mechanisms of this recovery have not been addressed. Here, we recorded from first-order central neurons in the macaque monkey that provide vestibular information to higher brain areas for self-motion perception. Immediately following unilateral labyrinthectomy, neuronal detection thresholds increased by more than two-fold (from 14 to 30 deg s(-1)). While thresholds showed slight improvement by week 3 (25 deg s(-1)), they never recovered to control values - a trend mirroring the time course of perceptual thresholds in patients. We further discovered that changes in neuronal response variability paralleled changes in sensitivity for vestibular stimulation during compensation, thereby causing detection thresholds to remain elevated over time. However, we found that in a subset of neurons, the emergence of neck proprioceptive responses combined with residual vestibular modulation during head-on-body motion led to better neuronal detection thresholds. Taken together, our results emphasize that increases in response variability to vestibular inputs ultimately constrain neural thresholds and provide evidence that sensory substitution with extravestibular (i.e. proprioceptive) inputs at the first central stage of vestibular processing is a neural substrate for improvements in self-motion perception following vestibular loss. Thus, our results provide a neural correlate for the patient benefits provided by rehabilitative strategies that take advantage of the convergence of these multisensory cues.
The vestibular system is responsible for processing self-motion, allowing normal subjects to discriminate the direction of rotational movements as slow as 1–2 deg s −1 . After unilateral vestibular injury patients’ direction–discrimination thresholds worsen to ∼20 deg s −1 , and despite some improvement thresholds remain substantially elevated following compensation. To date, however, the underlying neural mechanisms of this recovery have not been addressed. Here, we recorded from first-order central neurons in the macaque monkey that provide vestibular information to higher brain areas for self-motion perception. Immediately following unilateral labyrinthectomy, neuronal detection thresholds increased by more than two-fold (from 14 to 30 deg s −1 ). While thresholds showed slight improvement by week 3 (25 deg s −1 ), they never recovered to control values – a trend mirroring the time course of perceptual thresholds in patients. We further discovered that changes in neuronal response variability paralleled changes in sensitivity for vestibular stimulation during compensation, thereby causing detection thresholds to remain elevated over time. However, we found that in a subset of neurons, the emergence of neck proprioceptive responses combined with residual vestibular modulation during head-on-body motion led to better neuronal detection thresholds. Taken together, our results emphasize that increases in response variability to vestibular inputs ultimately constrain neural thresholds and provide evidence that sensory substitution with extravestibular (i.e. proprioceptive) inputs at the first central stage of vestibular processing is a neural substrate for improvements in self-motion perception following vestibular loss. Thus, our results provide a neural correlate for the patient benefits provided by rehabilitative strategies that take advantage of the convergence of these multisensory cues.
Key points Unilateral vestibular injury impairs our ability to detect motion. However, before this study the neural mechanisms underlying this impairment had not yet been established. We found that the detection thresholds of neurons at the first central stage of vestibular processing (i.e. vestibular nuclei) dramatically increase immediately post‐lesion, and despite some recovery remain elevated even after 1 month, following the trend reported for vestibular patients’ perception. After the lesion, parallel changes in neuronal trial‐to‐trial variability and sensitivity account for consistently elevated thresholds, thus providing a neural correlate for impaired behavioural performance. In a subset of neurons, sensory substitution with extravestibular (i.e. proprioceptive) inputs after the lesion combined with residual vestibular information serves to improve neuronal detection thresholds for head‐on‐body motion. Our results provide a neural correlate for rehabilitation approaches that take advantage of the convergence of proprioceptive and vestibular inputs to improve patient outcomes. The vestibular system is responsible for processing self‐motion, allowing normal subjects to discriminate the direction of rotational movements as slow as 1–2 deg s−1. After unilateral vestibular injury patients’ direction–discrimination thresholds worsen to ∼20 deg s−1, and despite some improvement thresholds remain substantially elevated following compensation. To date, however, the underlying neural mechanisms of this recovery have not been addressed. Here, we recorded from first‐order central neurons in the macaque monkey that provide vestibular information to higher brain areas for self‐motion perception. Immediately following unilateral labyrinthectomy, neuronal detection thresholds increased by more than two‐fold (from 14 to 30 deg s−1). While thresholds showed slight improvement by week 3 (25 deg s−1), they never recovered to control values – a trend mirroring the time course of perceptual thresholds in patients. We further discovered that changes in neuronal response variability paralleled changes in sensitivity for vestibular stimulation during compensation, thereby causing detection thresholds to remain elevated over time. However, we found that in a subset of neurons, the emergence of neck proprioceptive responses combined with residual vestibular modulation during head‐on‐body motion led to better neuronal detection thresholds. Taken together, our results emphasize that increases in response variability to vestibular inputs ultimately constrain neural thresholds and provide evidence that sensory substitution with extravestibular (i.e. proprioceptive) inputs at the first central stage of vestibular processing is a neural substrate for improvements in self‐motion perception following vestibular loss. Thus, our results provide a neural correlate for the patient benefits provided by rehabilitative strategies that take advantage of the convergence of these multisensory cues.
Key points Unilateral vestibular injury impairs our ability to detect motion. However, before this study the neural mechanisms underlying this impairment had not yet been established. We found that the detection thresholds of neurons at the first central stage of vestibular processing (i.e. vestibular nuclei) dramatically increase immediately post-lesion, and despite some recovery remain elevated even after 1 month, following the trend reported for vestibular patients' perception. After the lesion, parallel changes in neuronal trial-to-trial variability and sensitivity account for consistently elevated thresholds, thus providing a neural correlate for impaired behavioural performance. In a subset of neurons, sensory substitution with extravestibular (i.e. proprioceptive) inputs after the lesion combined with residual vestibular information serves to improve neuronal detection thresholds for head-on-body motion. Our results provide a neural correlate for rehabilitation approaches that take advantage of the convergence of proprioceptive and vestibular inputs to improve patient outcomes. The vestibular system is responsible for processing self-motion, allowing normal subjects to discriminate the direction of rotational movements as slow as 1-2 deg s-1. After unilateral vestibular injury patients' direction-discrimination thresholds worsen to 20 deg s-1, and despite some improvement thresholds remain substantially elevated following compensation. To date, however, the underlying neural mechanisms of this recovery have not been addressed. Here, we recorded from first-order central neurons in the macaque monkey that provide vestibular information to higher brain areas for self-motion perception. Immediately following unilateral labyrinthectomy, neuronal detection thresholds increased by more than two-fold (from 14 to 30 deg s-1). While thresholds showed slight improvement by week 3 (25 deg s-1), they never recovered to control values - a trend mirroring the time course of perceptual thresholds in patients. We further discovered that changes in neuronal response variability paralleled changes in sensitivity for vestibular stimulation during compensation, thereby causing detection thresholds to remain elevated over time. However, we found that in a subset of neurons, the emergence of neck proprioceptive responses combined with residual vestibular modulation during head-on-body motion led to better neuronal detection thresholds. Taken together, our results emphasize that increases in response variability to vestibular inputs ultimately constrain neural thresholds and provide evidence that sensory substitution with extravestibular (i.e. proprioceptive) inputs at the first central stage of vestibular processing is a neural substrate for improvements in self-motion perception following vestibular loss. Thus, our results provide a neural correlate for the patient benefits provided by rehabilitative strategies that take advantage of the convergence of these multisensory cues. [PUBLICATION ABSTRACT]
Unilateral vestibular injury impairs our ability to detect motion. However, before this study the neural mechanisms underlying this impairment had not yet been established.We found that the detection thresholds of neurons at the first central stage of vestibular processing (i.e. vestibular nuclei) dramatically increase immediately post-lesion, and despite some recovery remain elevated even after 1 month, following the trend reported for vestibular patients' perception.After the lesion, parallel changes in neuronal trial-to-trial variability and sensitivity account for consistently elevated thresholds, thus providing a neural correlate for impaired behavioural performance.In a subset of neurons, sensory substitution with extravestibular (i.e. proprioceptive) inputs after the lesion combined with residual vestibular information serves to improve neuronal detection thresholds for head-on-body motion.Our results provide a neural correlate for rehabilitation approaches that take advantage of the convergence of proprioceptive and vestibular inputs to improve patient outcomes. The vestibular system is responsible for processing self-motion, allowing normal subjects to discriminate the direction of rotational movements as slow as 1-2 deg s-1. After unilateral vestibular injury patients' direction-discrimination thresholds worsen to similar to 20 deg s-1, and despite some improvement thresholds remain substantially elevated following compensation. To date, however, the underlying neural mechanisms of this recovery have not been addressed. Here, we recorded from first-order central neurons in the macaque monkey that provide vestibular information to higher brain areas for self-motion perception. Immediately following unilateral labyrinthectomy, neuronal detection thresholds increased by more than two-fold (from 14 to 30 deg s-1). While thresholds showed slight improvement by week 3 (25 deg s-1), they never recovered to control values - a trend mirroring the time course of perceptual thresholds in patients. We further discovered that changes in neuronal response variability paralleled changes in sensitivity for vestibular stimulation during compensation, thereby causing detection thresholds to remain elevated over time. However, we found that in a subset of neurons, the emergence of neck proprioceptive responses combined with residual vestibular modulation during head-on-body motion led to better neuronal detection thresholds. Taken together, our results emphasize that increases in response variability to vestibular inputs ultimately constrain neural thresholds and provide evidence that sensory substitution with extravestibular (i.e. proprioceptive) inputs at the first central stage of vestibular processing is a neural substrate for improvements in self-motion perception following vestibular loss. Thus, our results provide a neural correlate for the patient benefits provided by rehabilitative strategies that take advantage of the convergence of these multisensory cues.
Author Dale, Alexis
Sadeghi, Soroush G.
Mitchell, Diana E.
Carriot, Jerome
Jamali, Mohsen
Cullen, Kathleen E.
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  surname: Jamali
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  givenname: Diana E.
  surname: Mitchell
  fullname: Mitchell, Diana E.
  organization: McGill University
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  givenname: Alexis
  surname: Dale
  fullname: Dale, Alexis
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  fullname: Carriot, Jerome
  organization: McGill University
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  givenname: Soroush G.
  surname: Sadeghi
  fullname: Sadeghi, Soroush G.
  organization: The State University of New York
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  givenname: Kathleen E.
  surname: Cullen
  fullname: Cullen, Kathleen E.
  organization: McGill University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24366259$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2014 The Authors. The Journal of Physiology © 2014 The Physiological Society
2014 The Physiological Society
2014 The Authors. The Journal of Physiology © 2014 The Physiological Society 2014
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SSID ssj0013099
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Snippet Key points Unilateral vestibular injury impairs our ability to detect motion. However, before this study the neural mechanisms underlying this impairment had...
The vestibular system is responsible for processing self-motion, allowing normal subjects to discriminate the direction of rotational movements as slow as...
Key points Unilateral vestibular injury impairs our ability to detect motion. However, before this study the neural mechanisms underlying this impairment had...
The vestibular system is responsible for processing self-motion, allowing normal subjects to discriminate the direction of rotational movements as slow as 1-2...
Unilateral vestibular injury impairs our ability to detect motion. However, before this study the neural mechanisms underlying this impairment had not yet been...
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proquest
pubmed
crossref
wiley
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 1565
SubjectTerms Action Potentials
Animals
Cues
Disease Models, Animal
Head Movements
Macaca
Macaca mulatta
Motion Perception
Neurons - pathology
Neuroscience: Development/Plasticity/Repair
Proprioception
Recovery of Function
Sensory Thresholds
Time Factors
Vestibular Diseases - pathology
Vestibular Diseases - physiopathology
Vestibular Diseases - psychology
Vestibule, Labyrinth - pathology
Vestibule, Labyrinth - physiopathology
Title Neuronal detection thresholds during vestibular compensation: contributions of response variability and sensory substitution
URI https://onlinelibrary.wiley.com/doi/abs/10.1113%2Fjphysiol.2013.267534
https://www.ncbi.nlm.nih.gov/pubmed/24366259
https://www.proquest.com/docview/1511378341
https://www.proquest.com/docview/1512558998
https://www.proquest.com/docview/1544012164
https://pubmed.ncbi.nlm.nih.gov/PMC3979612
Volume 592
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