The Effect of Vestibulo-Ocular Reflex Deficits and Covert Saccades on Dynamic Vision in Opioid-Induced Vestibular Dysfunction
Patients with bilateral vestibular dysfunction cannot fully compensate passive head rotations with eye movements, and experience disturbing oscillopsia. To compensate for the deficient vestibulo-ocular reflex (VOR), they have to rely on re-fixation saccades. Some can trigger "covert" sacca...
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| Published in | PloS one Vol. 9; no. 10; p. e110322 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
20.10.2014
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0110322 |
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| Abstract | Patients with bilateral vestibular dysfunction cannot fully compensate passive head rotations with eye movements, and experience disturbing oscillopsia. To compensate for the deficient vestibulo-ocular reflex (VOR), they have to rely on re-fixation saccades. Some can trigger "covert" saccades while the head still moves; others only initiate saccades afterwards. Due to their shorter latency, it has been hypothesized that covert saccades are particularly beneficial to improve dynamic visual acuity, reducing oscillopsia. Here, we investigate the combined effect of covert saccades and the VOR on clear vision, using the Head Impulse Testing Device-Functional Test (HITD-FT), which quantifies reading ability during passive high-acceleration head movements. To reversibly decrease VOR function, fourteen healthy men (median age 26 years, range 21-31) were continuously administrated the opioid remifentanil intravenously (0.15 µg/kg/min). VOR gain was assessed with the video head-impulse test, functional performance (i.e. reading) with the HITD-FT. Before opioid application, VOR and dynamic reading were intact (head-impulse gain: 0.87±0.08, mean±SD; HITD-FT rate of correct answers: 90±9%). Remifentanil induced impairment in dynamic reading (HITD-FT 26±15%) in 12/14 subjects, with transient bilateral vestibular dysfunction (head-impulse gain 0.63±0.19). HITD-FT score correlated with head-impulse gain (R = 0.63, p = 0.03) and with gain difference (before/with remifentanil, R = -0.64, p = 0.02). One subject had a non-pathological head-impulse gain (0.82±0.03) and a high HITD-FT score (92%). One subject triggered covert saccades in 60% of the head movements and could read during passive head movements (HITD-FT 93%) despite a pathological head-impulse gain (0.59±0.03) whereas none of the 12 subjects without covert saccades reached such high performance. In summary, early catch-up saccades may improve dynamic visual function. HITD-FT is an appropriate method to assess the combined gaze stabilization effect of both VOR and covert saccades (overall dynamic vision), e.g., to document performance and progress during vestibular rehabilitation. |
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| AbstractList | Patients with bilateral vestibular dysfunction cannot fully compensate passive head rotations with eye movements, and experience disturbing oscillopsia. To compensate for the deficient vestibulo-ocular reflex (VOR), they have to rely on re-fixation saccades. Some can trigger "covert" saccades while the head still moves; others only initiate saccades afterwards. Due to their shorter latency, it has been hypothesized that covert saccades are particularly beneficial to improve dynamic visual acuity, reducing oscillopsia. Here, we investigate the combined effect of covert saccades and the VOR on clear vision, using the Head Impulse Testing Device-Functional Test (HITD-FT), which quantifies reading ability during passive high-acceleration head movements. To reversibly decrease VOR function, fourteen healthy men (median age 26 years, range 21-31) were continuously administrated the opioid remifentanil intravenously (0.15 µg/kg/min). VOR gain was assessed with the video head-impulse test, functional performance (i.e. reading) with the HITD-FT. Before opioid application, VOR and dynamic reading were intact (head-impulse gain: 0.87±0.08, mean±SD; HITD-FT rate of correct answers: 90±9%). Remifentanil induced impairment in dynamic reading (HITD-FT 26±15%) in 12/14 subjects, with transient bilateral vestibular dysfunction (head-impulse gain 0.63±0.19). HITD-FT score correlated with head-impulse gain (R = 0.63, p = 0.03) and with gain difference (before/with remifentanil, R = -0.64, p = 0.02). One subject had a non-pathological head-impulse gain (0.82±0.03) and a high HITD-FT score (92%). One subject triggered covert saccades in 60% of the head movements and could read during passive head movements (HITD-FT 93%) despite a pathological head-impulse gain (0.59±0.03) whereas none of the 12 subjects without covert saccades reached such high performance. In summary, early catch-up saccades may improve dynamic visual function. HITD-FT is an appropriate method to assess the combined gaze stabilization effect of both VOR and covert saccades (overall dynamic vision), e.g., to document performance and progress during vestibular rehabilitation.Patients with bilateral vestibular dysfunction cannot fully compensate passive head rotations with eye movements, and experience disturbing oscillopsia. To compensate for the deficient vestibulo-ocular reflex (VOR), they have to rely on re-fixation saccades. Some can trigger "covert" saccades while the head still moves; others only initiate saccades afterwards. Due to their shorter latency, it has been hypothesized that covert saccades are particularly beneficial to improve dynamic visual acuity, reducing oscillopsia. Here, we investigate the combined effect of covert saccades and the VOR on clear vision, using the Head Impulse Testing Device-Functional Test (HITD-FT), which quantifies reading ability during passive high-acceleration head movements. To reversibly decrease VOR function, fourteen healthy men (median age 26 years, range 21-31) were continuously administrated the opioid remifentanil intravenously (0.15 µg/kg/min). VOR gain was assessed with the video head-impulse test, functional performance (i.e. reading) with the HITD-FT. Before opioid application, VOR and dynamic reading were intact (head-impulse gain: 0.87±0.08, mean±SD; HITD-FT rate of correct answers: 90±9%). Remifentanil induced impairment in dynamic reading (HITD-FT 26±15%) in 12/14 subjects, with transient bilateral vestibular dysfunction (head-impulse gain 0.63±0.19). HITD-FT score correlated with head-impulse gain (R = 0.63, p = 0.03) and with gain difference (before/with remifentanil, R = -0.64, p = 0.02). One subject had a non-pathological head-impulse gain (0.82±0.03) and a high HITD-FT score (92%). One subject triggered covert saccades in 60% of the head movements and could read during passive head movements (HITD-FT 93%) despite a pathological head-impulse gain (0.59±0.03) whereas none of the 12 subjects without covert saccades reached such high performance. In summary, early catch-up saccades may improve dynamic visual function. HITD-FT is an appropriate method to assess the combined gaze stabilization effect of both VOR and covert saccades (overall dynamic vision), e.g., to document performance and progress during vestibular rehabilitation. Patients with bilateral vestibular dysfunction cannot fully compensate passive head rotations with eye movements, and experience disturbing oscillopsia. To compensate for the deficient vestibulo-ocular reflex (VOR), they have to rely on re-fixation saccades. Some can trigger “covert” saccades while the head still moves; others only initiate saccades afterwards. Due to their shorter latency, it has been hypothesized that covert saccades are particularly beneficial to improve dynamic visual acuity, reducing oscillopsia. Here, we investigate the combined effect of covert saccades and the VOR on clear vision, using the Head Impulse Testing Device – Functional Test (HITD-FT), which quantifies reading ability during passive high-acceleration head movements. To reversibly decrease VOR function, fourteen healthy men (median age 26 years, range 21–31) were continuously administrated the opioid remifentanil intravenously (0.15 µg/kg/min). VOR gain was assessed with the video head-impulse test, functional performance (i.e. reading) with the HITD-FT. Before opioid application, VOR and dynamic reading were intact (head-impulse gain: 0.87±0.08, mean±SD; HITD-FT rate of correct answers: 90±9%). Remifentanil induced impairment in dynamic reading (HITD-FT 26±15%) in 12/14 subjects, with transient bilateral vestibular dysfunction (head-impulse gain 0.63±0.19). HITD-FT score correlated with head-impulse gain (R = 0.63, p = 0.03) and with gain difference (before/with remifentanil, R = −0.64, p = 0.02). One subject had a non-pathological head-impulse gain (0.82±0.03) and a high HITD-FT score (92%). One subject triggered covert saccades in 60% of the head movements and could read during passive head movements (HITD-FT 93%) despite a pathological head-impulse gain (0.59±0.03) whereas none of the 12 subjects without covert saccades reached such high performance. In summary, early catch-up saccades may improve dynamic visual function. HITD-FT is an appropriate method to assess the combined gaze stabilization effect of both VOR and covert saccades (overall dynamic vision), e.g., to document performance and progress during vestibular rehabilitation. Patients with bilateral vestibular dysfunction cannot fully compensate passive head rotations with eye movements, and experience disturbing oscillopsia. To compensate for the deficient vestibulo-ocular reflex (VOR), they have to rely on re-fixation saccades. Some can trigger "covert" saccades while the head still moves; others only initiate saccades afterwards. Due to their shorter latency, it has been hypothesized that covert saccades are particularly beneficial to improve dynamic visual acuity, reducing oscillopsia. Here, we investigate the combined effect of covert saccades and the VOR on clear vision, using the Head Impulse Testing Device-Functional Test (HITD-FT), which quantifies reading ability during passive high-acceleration head movements. To reversibly decrease VOR function, fourteen healthy men (median age 26 years, range 21-31) were continuously administrated the opioid remifentanil intravenously (0.15 µg/kg/min). VOR gain was assessed with the video head-impulse test, functional performance (i.e. reading) with the HITD-FT. Before opioid application, VOR and dynamic reading were intact (head-impulse gain: 0.87±0.08, mean±SD; HITD-FT rate of correct answers: 90±9%). Remifentanil induced impairment in dynamic reading (HITD-FT 26±15%) in 12/14 subjects, with transient bilateral vestibular dysfunction (head-impulse gain 0.63±0.19). HITD-FT score correlated with head-impulse gain (R = 0.63, p = 0.03) and with gain difference (before/with remifentanil, R = -0.64, p = 0.02). One subject had a non-pathological head-impulse gain (0.82±0.03) and a high HITD-FT score (92%). One subject triggered covert saccades in 60% of the head movements and could read during passive head movements (HITD-FT 93%) despite a pathological head-impulse gain (0.59±0.03) whereas none of the 12 subjects without covert saccades reached such high performance. In summary, early catch-up saccades may improve dynamic visual function. HITD-FT is an appropriate method to assess the combined gaze stabilization effect of both VOR and covert saccades (overall dynamic vision), e.g., to document performance and progress during vestibular rehabilitation. Patients with bilateral vestibular dysfunction cannot fully compensate passive head rotations with eye movements, and experience disturbing oscillopsia. To compensate for the deficient vestibulo-ocular reflex (VOR), they have to rely on re-fixation saccades. Some can trigger "covert" saccades while the head still moves; others only initiate saccades afterwards. Due to their shorter latency, it has been hypothesized that covert saccades are particularly beneficial to improve dynamic visual acuity, reducing oscillopsia. Here, we investigate the combined effect of covert saccades and the VOR on clear vision, using the Head Impulse Testing Device - Functional Test (HITD-FT), which quantifies reading ability during passive high-acceleration head movements. To reversibly decrease VOR function, fourteen healthy men (median age 26 years, range 21-31) were continuously administrated the opioid remifentanil intravenously (0.15 [micro]g/kg/min). VOR gain was assessed with the video head-impulse test, functional performance (i.e. reading) with the HITD-FT. Before opioid application, VOR and dynamic reading were intact (head-impulse gain: 0.87±0.08, mean±SD; HITD-FT rate of correct answers: 90±9%). Remifentanil induced impairment in dynamic reading (HITD-FT 26±15%) in 12/14 subjects, with transient bilateral vestibular dysfunction (head-impulse gain 0.63±0.19). HITD-FT score correlated with head-impulse gain (R = 0.63, p = 0.03) and with gain difference (before/with remifentanil, R = -0.64, p = 0.02). One subject had a non-pathological head-impulse gain (0.82±0.03) and a high HITD-FT score (92%). One subject triggered covert saccades in 60% of the head movements and could read during passive head movements (HITD-FT 93%) despite a pathological head-impulse gain (0.59±0.03) whereas none of the 12 subjects without covert saccades reached such high performance. In summary, early catch-up saccades may improve dynamic visual function. HITD-FT is an appropriate method to assess the combined gaze stabilization effect of both VOR and covert saccades (overall dynamic vision), e.g., to document performance and progress during vestibular rehabilitation. |
| Audience | Academic |
| Author | Schneider, Erich Sağlam, Murat Ramaioli, Cecilia Ramat, Stefano Colagiorgio, Paolo Heuser, Fabian Lehnen, Nadine |
| AuthorAffiliation | UMR8194, France 4 Clinical Neurosciences, Munich University Hospital, Munich, Germany 6 Department of Neurology, Munich University Hospital, Munich, Germany 1 German Center for Vertigo and Balance Disorders, Munich University Hospital, Munich, Germany 5 Brandenburg University of Technology, Cottbus-Senftenberg, Germany 2 Department of Electrical, Computer and Biomedical Engineering, University of Pavia, Pavia, Italy 3 Department of Anesthesiology, Klinikum rechts der Isar, TU Munich, Munich, Germany |
| AuthorAffiliation_xml | – name: UMR8194, France – name: 3 Department of Anesthesiology, Klinikum rechts der Isar, TU Munich, Munich, Germany – name: 4 Clinical Neurosciences, Munich University Hospital, Munich, Germany – name: 1 German Center for Vertigo and Balance Disorders, Munich University Hospital, Munich, Germany – name: 2 Department of Electrical, Computer and Biomedical Engineering, University of Pavia, Pavia, Italy – name: 6 Department of Neurology, Munich University Hospital, Munich, Germany – name: 5 Brandenburg University of Technology, Cottbus-Senftenberg, Germany |
| Author_xml | – sequence: 1 givenname: Cecilia surname: Ramaioli fullname: Ramaioli, Cecilia – sequence: 2 givenname: Paolo surname: Colagiorgio fullname: Colagiorgio, Paolo – sequence: 3 givenname: Murat surname: Sağlam fullname: Sağlam, Murat – sequence: 4 givenname: Fabian surname: Heuser fullname: Heuser, Fabian – sequence: 5 givenname: Erich surname: Schneider fullname: Schneider, Erich – sequence: 6 givenname: Stefano surname: Ramat fullname: Ramat, Stefano – sequence: 7 givenname: Nadine surname: Lehnen fullname: Lehnen, Nadine |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25329150$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2014 Public Library of Science 2014 Ramaioli et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2014 Ramaioli et al 2014 Ramaioli et al |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 ObjectType-Article-2 ObjectType-Feature-1 content type line 23 Competing Interests: ES is the managing director and a shareholder of EyeSeeTec GmbH. NL received speaker honoraria and compensation for travel expenses from Interacoustics, Autronic Reglersysteme GmbH, and Meytec GmbH Medizinsysteme, and research support from the German Federal Ministry of Education and Research (BMBF), the Faculty of Medicine of the University of Munich, and the Friedrich-Baur Foundation. She is a shareholder and paid consultant of EyeSeeTec GmbH. SR has the European patent on head impulse testing device for assessing the functionality of the semicircular canals and for the rehabilitation of vestibular loss (ep 2398377, Stefano Ramat, Marco Mandalà, 2011/12/28). CR, PC, MS, FH have no competing interests to report. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials. Conceived and designed the experiments: CR FH NL. Performed the experiments: CR FH. Analyzed the data: CR MS SR NL. Contributed reagents/materials/analysis tools: CR PC MS SR ES. Contributed to the writing of the manuscript: CR MS NL SR ES. |
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| References_xml | – volume: 136 start-page: 686 year: 2010 ident: ref13 article-title: A new dynamic visual acuity test to assess peripheral vestibular function publication-title: Arch Otolaryngol Head Neck Surg doi: 10.1001/archoto.2010.99 – volume: 79 start-page: 893 year: 1993 ident: ref18 article-title: Pharmacokinetics of remifentanil (GI87084B) and its major metabolite (GI90291) in patients undergoing elective inpatient surgery publication-title: Anesthesiology doi: 10.1097/00000542-199311000-00005 – ident: ref7 doi: 10.1212/WNL.0b013e3182a08d36 – volume: 35 start-page: 148 year: 2014 ident: ref21 article-title: Early adaptation and compensation of clinical vestibular responses after unilateral vestibular deafferentation surgery publication-title: Otol neurotol doi: 10.1097/MAO.0b013e3182956196 – volume: 18 start-page: 147 year: 2008 ident: ref14 article-title: Effect of vestibular rehabilitation on passive dynamic visual acuity publication-title: J Vestib Res doi: 10.3233/VES-2008-182-308 – volume: 103 start-page: 273 year: 1987 ident: ref15 article-title: The dynamic illegible E-test. A technique for assessing the vestibulo-ocular reflex publication-title: Acta Otolaryngol doi: 10.3109/00016488709107283 – volume: 3 start-page: 1 year: 2012 ident: ref16 article-title: A Device for the Functional Evaluation of the VOR in Clinical Settings publication-title: Front Neurol doi: 10.3389/fneur.2012.00039 – volume: 34 start-page: 8347 year: 2014 ident: ref19 article-title: Statistics of the Vestibular Input Experienced during Natural Self-Motion: Implications for Neural Processing publication-title: J Neurosci doi: 10.1523/JNEUROSCI.0692-14.2014 – volume: 127 start-page: 117 year: 1999 ident: ref20 article-title: Effects of walking velocity on vertical head and body movements during locomotion publication-title: Exp Brain Res doi: 10.1007/s002210050781 – volume: 72 start-page: 421 year: 1941 ident: ref3 article-title: The surgical treatment of Meniere’s disease publication-title: Surg Gynecol Obstet – volume: 4 start-page: 165 year: 2013 ident: ref17 article-title: A New Tool for Investigating the Functional Testing of the VOR publication-title: Front Neurol doi: 10.3389/fneur.2013.00165 – volume: 76 start-page: 4021 year: 1996 ident: ref9 article-title: Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. II. Responses in subjects with unilateral vestibular loss and selective semicircular canal occlusion publication-title: J Neurophysiol doi: 10.1152/jn.1996.76.6.4021 – volume: 1164 start-page: 331 year: 2009 ident: ref10 article-title: Head impulse testing using video-oculography publication-title: Ann N Y Acad Sci doi: 10.1111/j.1749-6632.2009.03850.x – volume: 34 start-page: 1894 year: 1993 ident: ref5 article-title: Dynamic visual acuity of normal subjects during vertical optotype and head motion publication-title: Invest Ophthalmol Vis Sci – volume: 82 start-page: 4009 year: 1996 ident: ref8 article-title: Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. I. Responses in normal subjects publication-title: J Neurophysiol – volume: 139 start-page: 803 year: 2013 ident: ref2 article-title: Prevalence and impact of bilateral vestibular hypofunction: results from the 2008 US National Health Interview Survey publication-title: JAMA Otolaryngol Head Neck Surg doi: 10.1001/jamaoto.2013.3913 – volume: 70 start-page: 454 year: 2008 ident: ref6 article-title: Head impulse test in unilateral vestibular loss Vestibulo-ocular reflex and catch-up saccades publication-title: Neurology doi: 10.1212/01.wnl.0000299117.48935.2e – volume: 73 start-page: 1134 year: 2009 ident: ref11 article-title: The video head impulse test: diagnostic accuracy in peripheral vestibulopathy publication-title: Neurology doi: 10.1212/WNL.0b013e3181bacf85 – volume: 45 start-page: 737 year: 1988 ident: ref12 article-title: A clinical sign of canal paresis publication-title: Arch Neurol doi: 10.1001/archneur.1988.00520310043015 – volume: 36 start-page: 129 year: 1994 ident: ref4 article-title: Treatment of abnormal eye movements that impair vision: strategies based on current concepts of physiology and pharmacology publication-title: Annals of neurology doi: 10.1002/ana.410360204 – volume: 138 start-page: 301 year: 2012 ident: ref1 article-title: Visual acuity while walking and oscillopsia severity in healthy subjects and patients with unilateral and bilateral vestibular function loss publication-title: Arch otolaryngol head neck surg doi: 10.1001/archoto.2012.4 |
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| SubjectTerms | Acuity Adult Analgesics, Opioid - pharmacology Anesthesiology Biology and Life Sciences Biomedical engineering Correlation analysis Diagnostic tests Eye movements Head Head - physiology Head movement Humans Language Latency Male Medicine and Health Sciences Movement - drug effects Narcotics Neurology Opioids Piperidines - pharmacology Quality of life Reflex, Vestibulo-Ocular - drug effects Reflex, Vestibulo-Ocular - physiology Rehabilitation Remifentanil Saccades - drug effects Velocity Vertigo Vestibular Nuclei - drug effects Vestibular Nuclei - physiopathology Vestibular system Vestibulo-ocular reflex Vision Vision, Ocular - drug effects Vision, Ocular - physiology Visual acuity Visual perception Young Adult |
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| Title | The Effect of Vestibulo-Ocular Reflex Deficits and Covert Saccades on Dynamic Vision in Opioid-Induced Vestibular Dysfunction |
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