Vestibular heading discrimination and sensitivity to linear acceleration in head and world coordinates
Identifieur interne : 001C90 ( Pmc/Checkpoint ); précédent : 001C89; suivant : 001C91Vestibular heading discrimination and sensitivity to linear acceleration in head and world coordinates
Auteurs : Paul R. Macneilage [États-Unis] ; Martin S. Banks [États-Unis] ; Gregory C. Deangelis [États-Unis] ; Dora E. Angelaki [États-Unis]Source :
- The Journal of neuroscience : the official journal of the Society for Neuroscience [ 0270-6474 ] ; 2010.
Abstract
Effective navigation and locomotion depend critically on an observer’s ability to judge direction of linear self-motion, i.e., heading. The vestibular cue to heading is the direction of inertial acceleration that accompanies transient linear movements. This cue is transduced by the otolith organs. The otoliths also respond to gravitational acceleration, so vestibular heading discrimination could depend on: 1) the direction of movement in head coordinates (i.e., relative to the otoliths), 2) the direction of movement in world coordinates (i.e., relative to gravity), or 3) body orientation (i.e., the direction of gravity relative to the otoliths). To quantify these effects, we measured vestibular and visual discrimination of heading along azimuth and elevation dimensions with observers oriented both upright and side-down relative to gravity. We compared vestibular heading thresholds with corresponding measurements of sensitivity to linear motion along lateral and vertical axes of the head (coarse direction discrimination and amplitude discrimination). Neither heading nor coarse direction thresholds depended on movement direction in world coordinates, demonstrating that the nervous system compensates for gravity. Instead, they depended similarly on movement direction in head coordinates (better performance in the horizontal plane), and on body orientation (better performance in the upright orientation). Heading thresholds were correlated with, but significantly larger than, predictions based on sensitivity in the coarse discrimination task. Simulations of a neuron/anti-neuron pair with idealized cosine-tuning properties show that heading thresholds larger than those predicted from coarse direction discrimination could be accounted for by an amplitude-response nonlinearity in the neural representation of inertial motion.
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DOI: 10.1523/JNEUROSCI.1304-10.2010
PubMed: 20610742
PubMed Central: 2914270
Affiliations:
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<wicri:cityArea> Dept. of Anatomy & Neurobiology, Washington University School of Medicine, St. Louis</wicri:cityArea>
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<author><name sortKey="Banks, Martin S" sort="Banks, Martin S" uniqKey="Banks M" first="Martin S." last="Banks">Martin S. Banks</name>
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<author><name sortKey="Angelaki, Dora E" sort="Angelaki, Dora E" uniqKey="Angelaki D" first="Dora E." last="Angelaki">Dora E. Angelaki</name>
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<front><div type="abstract" xml:lang="en"><p id="P1">Effective navigation and locomotion depend critically on an observer’s ability to judge direction of linear self-motion, i.e., heading. The vestibular cue to heading is the direction of inertial acceleration that accompanies transient linear movements. This cue is transduced by the otolith organs. The otoliths also respond to gravitational acceleration, so vestibular heading discrimination could depend on: 1) the direction of movement in head coordinates (i.e., relative to the otoliths), 2) the direction of movement in world coordinates (i.e., relative to gravity), or 3) body orientation (i.e., the direction of gravity relative to the otoliths). To quantify these effects, we measured vestibular and visual discrimination of heading along azimuth and elevation dimensions with observers oriented both upright and side-down relative to gravity. We compared vestibular heading thresholds with corresponding measurements of sensitivity to linear motion along lateral and vertical axes of the head (coarse direction discrimination and amplitude discrimination). Neither heading nor coarse direction thresholds depended on movement direction in world coordinates, demonstrating that the nervous system compensates for gravity. Instead, they depended similarly on movement direction in head coordinates (better performance in the horizontal plane), and on body orientation (better performance in the upright orientation). Heading thresholds were correlated with, but significantly larger than, predictions based on sensitivity in the coarse discrimination task. Simulations of a neuron/anti-neuron pair with idealized cosine-tuning properties show that heading thresholds larger than those predicted from coarse direction discrimination could be accounted for by an amplitude-response nonlinearity in the neural representation of inertial motion.</p>
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Dept. of Anatomy & Neurobiology, Washington University School of Medicine, St. Louis, MO</aff>
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Vision Science Program, UC Berkeley, Berkeley, CA</aff>
<aff id="A3"><label>3</label>
Dept. of Brain and Cognitive Sciences, University of Rochester Medical Center, Rochester, NY</aff>
<author-notes><corresp id="FN1">Address for correspondence: Dr. Dora Angelaki (<email>angelaki@wustl.edu</email>
), Dept. of Anatomy & Neurobiology - Box 8108, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis MO 63110, Phone: 314-747-5529, Fax: 314-747-4370</corresp>
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<volume>30</volume>
<issue>27</issue>
<fpage>9084</fpage>
<lpage>9094</lpage>
<abstract><p id="P1">Effective navigation and locomotion depend critically on an observer’s ability to judge direction of linear self-motion, i.e., heading. The vestibular cue to heading is the direction of inertial acceleration that accompanies transient linear movements. This cue is transduced by the otolith organs. The otoliths also respond to gravitational acceleration, so vestibular heading discrimination could depend on: 1) the direction of movement in head coordinates (i.e., relative to the otoliths), 2) the direction of movement in world coordinates (i.e., relative to gravity), or 3) body orientation (i.e., the direction of gravity relative to the otoliths). To quantify these effects, we measured vestibular and visual discrimination of heading along azimuth and elevation dimensions with observers oriented both upright and side-down relative to gravity. We compared vestibular heading thresholds with corresponding measurements of sensitivity to linear motion along lateral and vertical axes of the head (coarse direction discrimination and amplitude discrimination). Neither heading nor coarse direction thresholds depended on movement direction in world coordinates, demonstrating that the nervous system compensates for gravity. Instead, they depended similarly on movement direction in head coordinates (better performance in the horizontal plane), and on body orientation (better performance in the upright orientation). Heading thresholds were correlated with, but significantly larger than, predictions based on sensitivity in the coarse discrimination task. Simulations of a neuron/anti-neuron pair with idealized cosine-tuning properties show that heading thresholds larger than those predicted from coarse direction discrimination could be accounted for by an amplitude-response nonlinearity in the neural representation of inertial motion.</p>
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