Strategies for Gaze Stabilization Critically Depend on Locomotor Speed

Locomotion involves complex combinations of translational and rotational head movements. For gaze stability, this necessitates the interplay of angular and linear vestibulo-ocular reflexes (VOR) as well as the integration of visual feedback about the desired viewing distance. Furthermore, gaze stabi...

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Published in:Neuroscience Vol. 408; pp. 418 - 429
Main Authors: Dietrich, H., Wuehr, M.
Format: Journal Article
Language:English
Published: United States Elsevier Ltd 01-06-2019
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Abstract Locomotion involves complex combinations of translational and rotational head movements. For gaze stability, this necessitates the interplay of angular and linear vestibulo-ocular reflexes (VOR) as well as the integration of visual feedback about the desired viewing distance. Furthermore, gaze stabilizing systems must be able to cope with vast differences in head motion brought about by changing locomotor speeds and patterns (walking vs. running). The present study investigated horizontal and vertical angular VOR (aVOR) and linear gaze stabilization (lGS) as well as compensation for linear head movements by angular counter rotation of the head during treadmill walking and running at different velocities (0.4 to 2.4 m/s) while fixating either a close (0.5 m) or distant (2.0 m) target. In the horizontal plane, the aVOR predominated throughout all locomotor speeds, whereas the compensation of linear translations was highly variable and generally insufficient. In contrast, in the vertical plane, eye and angular head motion steadily became more in phase with increasing locomotor speed, which served to optimize linear motion compensation. Furthermore, the timing of the vertical aVOR became more automated and independent of visual feedback during faster locomotion. Thus, horizontal and vertical gaze stabilization strategies appear to be considerably different. Whereas horizontal gaze control is likely governed by passive sensorimotor reflexes throughout all locomotor speeds, vertical gaze stabilization switches to an automated feed-forward control at faster locomotion. This switch is presumably driven by efference copies from spinal locomotor commands that were previously shown to govern gaze stabilization in animal models during stereotypic locomotion. •Gaze stabilization during locomotion depends on locomotor speed, dimension, and target distance.•Gaze stabilization in the horizontal dimension is mediated by sensory feedback independent of locomotor speed.•In contrast, gaze stabilization in the vertical plane undergoes a major transformation from slow to fast locomotion.•These changes in vertical gaze stabilization are presumably governed by feed-forward signals from the locomotor command.
AbstractList Locomotion involves complex combinations of translational and rotational head movements. For gaze stability, this necessitates the interplay of angular and linear vestibulo-ocular reflexes (VOR) as well as the integration of visual feedback about the desired viewing distance. Furthermore, gaze stabilizing systems must be able to cope with vast differences in head motion brought about by changing locomotor speeds and patterns (walking vs. running). The present study investigated horizontal and vertical angular VOR (aVOR) and linear gaze stabilization (lGS) as well as compensation for linear head movements by angular counter rotation of the head during treadmill walking and running at different velocities (0.4 to 2.4 m/s) while fixating either a close (0.5 m) or distant (2.0 m) target. In the horizontal plane, the aVOR predominated throughout all locomotor speeds, whereas the compensation of linear translations was highly variable and generally insufficient. In contrast, in the vertical plane, eye and angular head motion steadily became more in phase with increasing locomotor speed, which served to optimize linear motion compensation. Furthermore, the timing of the vertical aVOR became more automated and independent of visual feedback during faster locomotion. Thus, horizontal and vertical gaze stabilization strategies appear to be considerably different. Whereas horizontal gaze control is likely governed by passive sensorimotor reflexes throughout all locomotor speeds, vertical gaze stabilization switches to an automated feed-forward control at faster locomotion. This switch is presumably driven by efference copies from spinal locomotor commands that were previously shown to govern gaze stabilization in animal models during stereotypic locomotion.
Locomotion involves complex combinations of translational and rotational head movements. For gaze stability, this necessitates the interplay of angular and linear vestibulo-ocular reflexes (VOR) as well as the integration of visual feedback about the desired viewing distance. Furthermore, gaze stabilizing systems must be able to cope with vast differences in head motion brought about by changing locomotor speeds and patterns (walking vs. running). The present study investigated horizontal and vertical angular VOR (aVOR) and linear gaze stabilization (lGS) as well as compensation for linear head movements by angular counter rotation of the head during treadmill walking and running at different velocities (0.4 to 2.4 m/s) while fixating either a close (0.5 m) or distant (2.0 m) target. In the horizontal plane, the aVOR predominated throughout all locomotor speeds, whereas the compensation of linear translations was highly variable and generally insufficient. In contrast, in the vertical plane, eye and angular head motion steadily became more in phase with increasing locomotor speed, which served to optimize linear motion compensation. Furthermore, the timing of the vertical aVOR became more automated and independent of visual feedback during faster locomotion. Thus, horizontal and vertical gaze stabilization strategies appear to be considerably different. Whereas horizontal gaze control is likely governed by passive sensorimotor reflexes throughout all locomotor speeds, vertical gaze stabilization switches to an automated feed-forward control at faster locomotion. This switch is presumably driven by efference copies from spinal locomotor commands that were previously shown to govern gaze stabilization in animal models during stereotypic locomotion. •Gaze stabilization during locomotion depends on locomotor speed, dimension, and target distance.•Gaze stabilization in the horizontal dimension is mediated by sensory feedback independent of locomotor speed.•In contrast, gaze stabilization in the vertical plane undergoes a major transformation from slow to fast locomotion.•These changes in vertical gaze stabilization are presumably governed by feed-forward signals from the locomotor command.
Author Dietrich, H.
Wuehr, M.
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Keywords COP
locomotion
HFD
eye movements
vestibulo-ocular reflex
aVOR
aHead
lHead
VOR
efference copy
lGS
GRF
gaze stabilization
lVOR
Language English
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Snippet Locomotion involves complex combinations of translational and rotational head movements. For gaze stability, this necessitates the interplay of angular and...
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SubjectTerms Adult
efference copy
eye movements
Female
Fixation, Ocular - physiology
gaze stabilization
Head Movements - physiology
Humans
locomotion
Locomotion - physiology
Male
Reflex, Vestibulo-Ocular - physiology
vestibulo-ocular reflex
Young Adult
Title Strategies for Gaze Stabilization Critically Depend on Locomotor Speed
URI https://dx.doi.org/10.1016/j.neuroscience.2019.01.025
https://www.ncbi.nlm.nih.gov/pubmed/30703510
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