Effect of the Stimulus Duration on the Adaptation of the Optokinetic Afternystagmus

Observing a rotating visual pattern covering a large portion of the visual field induces optokinetic nystagmus (OKN). If the lights are suddenly switched off, optokinetic afternystagmus (OKAN) occurs. OKAN is hypothesized to originate in the velocity storage mechanism (VSM), a central processing net...

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Main Authors: Jan Gygli, Fausto Romano, Christopher J. Bockisch, Nina Feddermann-Demont, Dominik Straumann, Giovanni Bertolini
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2021.518133/full
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author Jan Gygli
Fausto Romano
Fausto Romano
Christopher J. Bockisch
Christopher J. Bockisch
Christopher J. Bockisch
Nina Feddermann-Demont
Nina Feddermann-Demont
Dominik Straumann
Dominik Straumann
Dominik Straumann
Giovanni Bertolini
Giovanni Bertolini
author_facet Jan Gygli
Fausto Romano
Fausto Romano
Christopher J. Bockisch
Christopher J. Bockisch
Christopher J. Bockisch
Nina Feddermann-Demont
Nina Feddermann-Demont
Dominik Straumann
Dominik Straumann
Dominik Straumann
Giovanni Bertolini
Giovanni Bertolini
author_sort Jan Gygli
collection DOAJ
description Observing a rotating visual pattern covering a large portion of the visual field induces optokinetic nystagmus (OKN). If the lights are suddenly switched off, optokinetic afternystagmus (OKAN) occurs. OKAN is hypothesized to originate in the velocity storage mechanism (VSM), a central processing network involved in multi-sensory integration. During a sustained visual rotation, the VSM builds up a velocity signal. After the lights are turned off, the VSM discharges slowly, with OKAN as the neurophysiological correlate. It has been reported that the initial afternystagmus in the direction of the preceding stimulus (OKAN-I) can be followed by a reversed one (OKAN-II), which increases with stimulus duration up to 15 min. In 11 healthy adults, we investigated OKAN following optokinetic stimulus lasting 30 s, 3-, 5-, and 10-min. Analysis of slow-phase cumulative eye position and velocity found OKAN-II in only 5/11 participants. Those participants presented it in over 70% of their trials with longer durations, but only in 10% of their 30 s trials. While this confirms that OKAN-II manifests predominantly after sustained stimuli, it suggests that its occurrence is subject-specific. We also did not observe further increases with stimulus duration. Conversely, OKAN-II onset occurred later as stimulus duration increased (p = 0.02), while OKAN-II occurrence and peak velocity did not differ between the three longest stimuli. Previous studies on OKAN-I, used negative saturation models to account for OKAN-II. As these approaches have no foundation in the OKAN-II literature, we evaluated if a simplified version of a rigorous model of OKAN adaptation could be used in humans. Slow-phase velocity following the trials with 3-, 5-, and 10-min stimuli was fitted with a sum of two decreasing exponential functions with opposite signs (one for OKAN-I and one for OKAN-II). The model assumes separate mechanisms for OKAN-I, representing VSM discharge, and OKAN-II, described as a slower adaptation phenomenon. Although the fit was qualitatively imperfect, this is not surprising given the limited reliability of OKAN in humans. The estimated adaptation time constant seems comparable to the one describing the reversal of the vestibulo-ocular reflex during sustained rotation, suggesting a possible shared adaptive mechanism.
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spelling doaj.art-5607436231604d9396ba73e6968b5f982022-12-21T19:52:57ZengFrontiers Media S.A.Frontiers in Neurology1664-22952021-03-011210.3389/fneur.2021.518133518133Effect of the Stimulus Duration on the Adaptation of the Optokinetic AfternystagmusJan Gygli0Fausto Romano1Fausto Romano2Christopher J. Bockisch3Christopher J. Bockisch4Christopher J. Bockisch5Nina Feddermann-Demont6Nina Feddermann-Demont7Dominik Straumann8Dominik Straumann9Dominik Straumann10Giovanni Bertolini11Giovanni Bertolini12Faculty of Medicine, University of Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, Zurich, SwitzerlandSwiss Concussion Center, Schulthess Clinic, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, Zurich, SwitzerlandSwiss Concussion Center, Schulthess Clinic, Zurich, SwitzerlandDepartments of Ophthalmology and Otorhinolaryngology, University Hospital Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, Zurich, SwitzerlandSwiss Concussion Center, Schulthess Clinic, Zurich, SwitzerlandFaculty of Medicine, University of Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, Zurich, SwitzerlandSwiss Concussion Center, Schulthess Clinic, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, Zurich, SwitzerlandSwiss Concussion Center, Schulthess Clinic, Zurich, SwitzerlandObserving a rotating visual pattern covering a large portion of the visual field induces optokinetic nystagmus (OKN). If the lights are suddenly switched off, optokinetic afternystagmus (OKAN) occurs. OKAN is hypothesized to originate in the velocity storage mechanism (VSM), a central processing network involved in multi-sensory integration. During a sustained visual rotation, the VSM builds up a velocity signal. After the lights are turned off, the VSM discharges slowly, with OKAN as the neurophysiological correlate. It has been reported that the initial afternystagmus in the direction of the preceding stimulus (OKAN-I) can be followed by a reversed one (OKAN-II), which increases with stimulus duration up to 15 min. In 11 healthy adults, we investigated OKAN following optokinetic stimulus lasting 30 s, 3-, 5-, and 10-min. Analysis of slow-phase cumulative eye position and velocity found OKAN-II in only 5/11 participants. Those participants presented it in over 70% of their trials with longer durations, but only in 10% of their 30 s trials. While this confirms that OKAN-II manifests predominantly after sustained stimuli, it suggests that its occurrence is subject-specific. We also did not observe further increases with stimulus duration. Conversely, OKAN-II onset occurred later as stimulus duration increased (p = 0.02), while OKAN-II occurrence and peak velocity did not differ between the three longest stimuli. Previous studies on OKAN-I, used negative saturation models to account for OKAN-II. As these approaches have no foundation in the OKAN-II literature, we evaluated if a simplified version of a rigorous model of OKAN adaptation could be used in humans. Slow-phase velocity following the trials with 3-, 5-, and 10-min stimuli was fitted with a sum of two decreasing exponential functions with opposite signs (one for OKAN-I and one for OKAN-II). The model assumes separate mechanisms for OKAN-I, representing VSM discharge, and OKAN-II, described as a slower adaptation phenomenon. Although the fit was qualitatively imperfect, this is not surprising given the limited reliability of OKAN in humans. The estimated adaptation time constant seems comparable to the one describing the reversal of the vestibulo-ocular reflex during sustained rotation, suggesting a possible shared adaptive mechanism.https://www.frontiersin.org/articles/10.3389/fneur.2021.518133/fullmodelingocular motor adaptationvelocity storage mechanismoptokinetic nystagmusoptokinetic afternystagmus
spellingShingle Jan Gygli
Fausto Romano
Fausto Romano
Christopher J. Bockisch
Christopher J. Bockisch
Christopher J. Bockisch
Nina Feddermann-Demont
Nina Feddermann-Demont
Dominik Straumann
Dominik Straumann
Dominik Straumann
Giovanni Bertolini
Giovanni Bertolini
Effect of the Stimulus Duration on the Adaptation of the Optokinetic Afternystagmus
Frontiers in Neurology
modeling
ocular motor adaptation
velocity storage mechanism
optokinetic nystagmus
optokinetic afternystagmus
title Effect of the Stimulus Duration on the Adaptation of the Optokinetic Afternystagmus
title_full Effect of the Stimulus Duration on the Adaptation of the Optokinetic Afternystagmus
title_fullStr Effect of the Stimulus Duration on the Adaptation of the Optokinetic Afternystagmus
title_full_unstemmed Effect of the Stimulus Duration on the Adaptation of the Optokinetic Afternystagmus
title_short Effect of the Stimulus Duration on the Adaptation of the Optokinetic Afternystagmus
title_sort effect of the stimulus duration on the adaptation of the optokinetic afternystagmus
topic modeling
ocular motor adaptation
velocity storage mechanism
optokinetic nystagmus
optokinetic afternystagmus
url https://www.frontiersin.org/articles/10.3389/fneur.2021.518133/full
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