Absence of Anti-Compensatory Saccades Despite Normal VOR Gain: A New Indicator of Central Vestibular Dysfunction in Neurological Disorders

preprint OA: closed
Full text JSON View at publisher

Abstract

Introduction: The Suppression Head Impulse Paradigm (SHIMP) is a valuable tool for assessing vestibulo-ocular reflex (VOR) function by eliciting anti-compensatory saccades (ACs) in individuals with intact angular VOR (aVOR). While previous studies have extensively examined VOR gain in neurological disorders, the absence of ACs in patients with preserved VOR gain has not been described. This study investigated whether the absence of ACs during SHIMP is a distinguishing feature of central vestibular dysfunction. Methods This cross-sectional study included 119 patients with multiple sclerosis (PwMS), severe traumatic brain injury (PwTBI), stroke (PwS), and Parkinson’s disease (PwPD). The video Head Impulse Test (vHIT) was performed to assess the VOR gain across all semicircular canals using both the HIMP and SHIMP paradigms. The presence, absence, or delay of ACs was systematically recorded. Results Among the 119 patients evaluated (238 semicircular canals), 24 (20%) demonstrated normal aVOR gain but failed to generate ACs during SHIMP. The absence of ACs was observed in seven PwMS, five with PwTBI, six with PwS, and six with PwPD. Conclusion The absence of ACs despite normal VOR gain suggests a potential impairment in the central pathways controlling saccadic responses, independent of peripheral vestibular function. These findings underscore the clinical relevance of integrating the SHIMP into vestibular assessments to improve the identification of central vestibular dysfunction in neurological disorders.
Full text 31,541 characters · extracted from preprint-html · click to expand
Absence of Anti-Compensatory Saccades Despite Normal VOR Gain: A New Indicator of Central Vestibular Dysfunction in Neurological Disorders | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL This is a preprint and has not been peer reviewed. Data may be preliminary. 18 March 2025 V1 Latest version Share on Absence of Anti-Compensatory Saccades Despite Normal VOR Gain: A New Indicator of Central Vestibular Dysfunction in Neurological Disorders Authors : Marco Tramontano 0000-0001-6034-0638 [email protected] , Laura Casagrande Conti , and Leonardo Manzari Authors Info & Affiliations https://doi.org/10.22541/au.174228506.63667276/v1 273 views 134 downloads Contents Abstract Supplementary Material Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract Introduction The Suppression Head Impulse Paradigm (SHIMP) is a valuable tool for assessing vestibulo-ocular reflex (VOR) function by eliciting anti-compensatory saccades (ACs) in individuals with intact angular VOR (aVOR). While previous studies have extensively examined VOR gain in neurological disorders, the absence of ACs in patients with preserved VOR gain has not been described. This study investigated whether the absence of ACs during SHIMP is a distinguishing feature of central vestibular dysfunction. Methods This cross-sectional study included 119 patients with multiple sclerosis (PwMS), severe traumatic brain injury (PwTBI), stroke (PwS), and Parkinson’s disease (PwPD). The video Head Impulse Test (vHIT) was performed to assess the VOR gain across all semicircular canals using both the HIMP and SHIMP paradigms. The presence, absence, or delay of ACs was systematically recorded. Results Among the 119 patients evaluated (238 semicircular canals), 24 (20%) demonstrated normal aVOR gain but failed to generate ACs during SHIMP. The absence of ACs was observed in seven PwMS, five with PwTBI, six with PwS, and six with PwPD. Conclusion The absence of ACs despite normal VOR gain suggests a potential impairment in the central pathways controlling saccadic responses, independent of peripheral vestibular function. These findings underscore the clinical relevance of integrating the SHIMP into vestibular assessments to improve the identification of central vestibular dysfunction in neurological disorders. Absence of Anti-Compensatory Saccades Despite Normal VOR Gain: A New Indicator of Central Vestibular Dysfunction in Neurological Disorders Introduction The Suppression Head Impulse Paradigm (SHIMP) is a valuable tool for assessing vestibulo-ocular reflex (VOR) function by eliciting anti-compensatory saccades (ACs) in individuals with intact angular VOR (aVOR). While previous studies have extensively examined VOR gain in neurological disorders, the absence of ACs in patients with preserved VOR gain has not been described. This study investigated whether the absence of ACs during SHIMP is a distinguishing feature of central vestibular dysfunction. Methods This cross-sectional study included 119 patients with multiple sclerosis (PwMS), severe traumatic brain injury (PwTBI), stroke (PwS), and Parkinson’s disease (PwPD). The video Head Impulse Test (vHIT) was performed to assess the VOR gain across all semicircular canals using both the HIMP and SHIMP paradigms. The presence, absence, or delay of ACs was systematically recorded. Results Among the 119 patients evaluated (238 semicircular canals), 24 (20%) demonstrated normal aVOR gain but failed to generate ACs during SHIMP. The absence of ACs was observed in seven PwMS, five with PwTBI, six with PwS, and six with PwPD. Conclusion The absence of ACs despite normal VOR gain suggests a potential impairment in the central pathways controlling saccadic responses, independent of peripheral vestibular function. These findings underscore the clinical relevance of integrating the SHIMP into vestibular assessments to improve the identification of central vestibular dysfunction in neurological disorders. Key Points: • The Suppression Head Impulse Paradigm (SHIMP) is a valuable tool for assessing vestibulo-ocular reflex (VOR) function. • People with neurological disorders may present with dysfunction of the vestibulo-ocular reflex (VOR). • The absence of anti-compensatory saccades (ACs) is generally associated with a reduction in VOR gain during SHIMP in people with vestibular hypofunction. • The mechanisms of VOR suppression are mediated by the central nervous system. • The absence of ACs during SHIMP despite normal VOR gain could represent a new indicator of central vestibular dysfunction. Keywords: Vestibulo-ocular reflex, anti-compensatory saccades, neurological disorders, SHIMP, vHIT, central vestibular dysfunction. Introduction The Suppression Head Impulse Paradigm (SHIMP) is a variant of the Head Impulse Test (HIT) designed to evaluate the functionality of the angular Vestibulo-Ocular Reflex (aVOR ) in a more nuanced manner [1]. VOR is crucial for maintaining visual stability during rapid head movements by generating compensatory eye movements in the opposite direction of head motion [2]. Traditional HIT focuses on detecting overt saccades when VOR fails [3]; however, it introduces a novel approach by requiring patients to fixate on a moving target during head impulses, eliciting anti-compensatory saccades in people with normal aVOR [4]. In recent years, evidence has supported the presence of semi-circular canal dysfunction in people with neurological disorders. Recent studies have shown that people with stroke (PwS) [5], multiple sclerosis (PwMS) [6], severe traumatic brain injury (PwTBI) [7], and Parkinson’s disease (PwPD) [8] can present aVOR alterations during the HIMP and SHIMP paradigms. In patients with unilateral or bilateral vestibular hypofunction, the expected anti-compensatory saccades (ACs) may be absent or delayed despite a normal aVOR [9,10]. This phenomenon suggests a disruption of the central pathways responsible for the initiation of saccades [11]. Understanding the implications of absent ACs during SHIMP could significantly enhance diagnostic accuracy and clinical assessment, more than VOR gain, particularly in patients with central vestibular lesions [12]. The ability to differentiate between peripheral and central vestibular dysfunction based on vHIT results can be particularly valuable in managing these populations [13]. Previous studies evaluating VOR gain in individuals with neurological disorders have primarily focused on quantitative assessment. While some studies [11,12,14] have analyzed compensatory saccades, none have specifically described the absence of ACs in the presence of physiological VOR gain. We hypothesized that this phenomenon may be present in patients with neurological disorders, suggesting a potential dysfunction in the central pathways responsible for saccadic initiation. This study aimed to investigate whether the absence of ACs during the SHIMP paradigm occurs in patients with neurological disorders despite preserved VOR gain. By identifying this phenomenon, we sought to enhance our understanding of central vestibular dysfunction and improve the diagnostic accuracy of vestibular assessment in these populations. Methods This cross-sectional study received approval from the Local Independent Ethics Committee under protocol number Prot. CE/2022_011. All procedures adhered to ethical standards outlined by national and institutional guidelines on human experimentation, the World Medical Association Declaration of Helsinki, and the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines [15]. Written informed consent was obtained from all participants for the publication of results derived from their clinical examinations and instrumental tests. Participants Patients with multiple sclerosis (MS), severe traumatic brain injury (sTBI), Parkinson’s disease (PD), and stroke were recruited based on consecutive sampling at the hospital between March 2022 and July 2023. Participants diagnosed with MS according to the McDonald criteria [16] were included if they presented a diagnosis of relapsing–remitting (RRMS) or secondary-progressive (SPMS) MS confirmed by a certified neurologist, an age of 18 years or older, and an Expanded Disability Status Scale (EDSS) score between 1 and 6 [17]. Exclusion criteria included the presence of psychiatric or neurological disorders other than MS, other pathological conditions and/or clinical disorders severe enough to interfere with cognitive functioning or the performance of motor or cognitive tasks, the occurrence of a clinical relapse in the three months prior to enrollment, steroid therapy administered in the 30 days preceding enrollment, a lower extremity fracture within three months prior to enrollment, or other medical conditions that could interfere with study procedures. A history of vestibular disorders was also considered an exclusion criterion. Participants with sTBI were included if they were between 18 and 65 years old, had a Glasgow Coma Scale (GCS) score of ≤8 at the time of injury, had a Level of Cognitive Functioning of 7 or higher [18], presented with disturbances in static and dynamic balance, and were able to understand verbal commands. Participants were also required to be able to walk without continuous physical assistance, with a Functional Ambulation Classification score greater than 3. Participants with PD were included if they had no dementia, as indicated by a Mini-Mental State Examination score of greater than 25, had a Hoehn & Yahr stage of 2 or 3, and were able to walk without a device or without the need for continuous physical assistance (Functional Ambulation Classification > 3). Exclusion criteria included cognitive deficits affecting the ability to understand task instructions, severe vision impairment preventing the ability to focus on visual targets or impairing eye movements, history of ear surgery, chronic otitis media, deafness, vertigo, limited neck movement due to a neck injury, or the presence of neurological, orthopedic, or cardiac comorbidities. Participants with first-ever stroke and unilateral hemiparesis were included if they were able to walk with or without a device and did not require continuous physical assistance, as indicated by a Functional Ambulation Classification score greater than 3 [19]. Exclusion criteria included cognitive deficits preventing task comprehension, defined as a Mini-Mental State Examination score lower than 24, severe unilateral spatial neglect, severe aphasia, and the presence of other neurological, orthopedic, or cardiac comorbidities. Assessment The video Head Impulse Test (vHIT) (ICS Impulse, Otometrics/Natus, Denmark) was used to evaluate the angular VOR (aVOR) gain for movements stimulating the six semicircular canals, assessing both the HIMP (Head Impulse Paradigm) and SHIMP paradigms. The assessment protocol was designed to minimize variability and ensure accurate and reliable data collection. Evaluations were conducted by expert clinicians specializing in the vestibular field. During the HIMP paradigm, patients were instructed to fixate on a point on the wall 1 meter in front of them. Approximately 14 rapid, horizontal head turns (head impulses) were applied unpredictably to each side, with specific parameters: Eye and head velocities were recorded for each impulse, with a normal VOR gain range defined as 0.76-1.29 for vertical canals and 0.80-1.29 for horizontal canals [20] Head movements for vertical canal testing were adjusted to align with the RALP (Right Anterior-Left Posterior) and LARP (Left Anterior-Right Posterior) planes [3]. In the SHIMP paradigm, patients followed a red dot generated by a laser attached to their head during head impulses. Under physiological conditions, anti-compensatory saccades in the opposite direction to the aVOR are expected after a short latency [9]. A normal VOR gain range in the SHIMP paradigm was defined as 0.66-1.29. VOR gain outside these ranges was classified as hypo-gain or hyper-gain based on direction [20]. Statistical Analysis To evaluate the absence of ACs, each raw data entry was screened by two experts in the field for the presence or absence of saccades, ensuring accuracy in classification. Statistical analyses were conducted to evaluate differences in SHIMP VOR gain among the four neurological conditions and to assess correlations between SHIMP gain and the absence of ACs. A one-way analysis of variance (ANOVA) was performed to determine whether SHIMP horizontal left and right gain differed significantly among the groups. Post-hoc pairwise comparisons were conducted using Tukey’s Honestly Significant Difference test to identify specific differences between conditions. Additionally, Pearson correlation analysis was used to assess the relationship between SHIMP horizontal gain and the absence of ACs. Results One-hundred nineteen patients were evaluated in this study, encompassing 238 semicircular canals assessed using the SHIMP paradigm. Twenty-seven PwMS (mean age 47.93 ± 8.5), 22 PwTBI, 36 with stroke (mean 55.11 ± 15.09), and 35 PwPD (mean age 69.9 ± 8.4), clinical and demographic characteristics are reported in table 1. Table 1. Demographic and clinical characteristics of participants across neurological conditions Sample Size (n) 27 22 36 35 Age (years, mean ± SD) 47.93 ± 8.51 42 ± 15.02 55.11 ± 15.09 69.9 ± 8.4 Sex (Female, %) 66.67% 14.3% 30.5% 31.4% HIMP aVOR Gain (mean ± SD) Left Anterior 0.78 ± 0.22 0.81 ± 0.15 0.81 ± 0.20 0.79 ± 0.19 Right Anterior 0.86 ± 0.14 0.71 ± 0.18 0.83 ± 0.26 0.85 ± 0.25 Horizontal Left 0.92 ± 0.19 0.87 ± 0.15 0.9 ± 0.12 0.94 ± 0.16 Horizontal Right 0.98 ± 0.24 0.97 ± 0.21 0.98 ± 0.14 0.99 ± 0.20 Left Posterior 0.82 ± 0.12 0.86 ± 0.15 0.91 ± 0.16 0.85 ± 0.22 Right Posterior 0.76 ± 0.17 0.91 ± 0.25 0.79 ± 0.12 0.79 ± 0.19 SHIMP aVOR Gain (mean ± SD) Horizontal Left 0.78 ± 0.21 0.81 ± 0.26 0.88 ± 0.20 0.85 ± 0.19 Horizontal Right 0.87 ± 0.23 0.74 ± 0.23 0.77 ± 0.19 0.85± 0.2 The results revealed that 24 out of 119 patients (20%) demonstrated a normal aVOR gain in the SHIMP paradigm but did not exhibit any ACs. Among those with absent ACs, 7 were PwMS, 5 sTBI, 6 stroke and 6 PwPD (exemplificative cases are reported in Figure 1). The ANOVA for the SHIMP horizontal left gain yielded a statistically significant result (p=0.041), indicating differences among the groups. The ANOVA for the SHIMP VOR gain of the right horizontal semicircular canal showed no significant differences (p=0.067). Post-hoc analysis using Tukey’s test revealed that for SHIMP VOR gain on the left side, PwMS had a significantly higher gain than PwTBI (p<0.05), and stroke patients had a significantly higher gain than PwTBI (p<0.05). No significant differences were found between the PwPD group and the other groups. For SHIMP VOR gain on the right side, PwTBI had a significantly lower gain compared to PwMS (p<0.05) and stroke patients (p<0.05), whereas no significant differences were found for PD compared to other groups. No correlations were found between the SHIMP VOR gain on either side and the absence of ACs (right side: r = -0.42, p = 0.012; left side: r = -0.36, p = 0.038). Figure 1. Suppressed Head Impulse Paradigm in People with Neurological disorders Red arrow indicates the lack of Anti-compensatory saccades in normal VOR gain during the SHIMP paradigm. An exemplificative case for each disease. Discussion This study identified the absence of ACs in individuals with neurological disorders who demonstrated normal aVOR gain during the SHIMP paradigm. The findings revealed that 20% of the evaluated patients (24 119) did not exhibit ACs despite a preserved aVOR gain. This phenomenon has been observed across different neurological conditions, including MS, sTBI, stroke, and PD. These results align with previous evidence indicating that saccadic abnormalities can occur in neurological disorders even when the vestibular reflex is functionally intact [21]. In particular, the absence of ACs suggests a possible disruption of the central pathways responsible for saccadic generation, which may not be directly reflected in VOR gain measurements alone.The SHIMP paradigm was designed as an alternative to the HIMP (Head Impulse Paradigm) to provide additional information about saccadic function in individuals with preserved vestibular function. Under normal conditions, aVOR suppression should lead to the generation of ACs, but in the present study, a significant proportion of patients with neurological disorders failed to exhibit these responses. Hawkins and colleagues [14], showed that individuals with PD exhibited reduced peak AC velocities and prolonged latencies compared to healthy controls, despite no significant difference in VOR gain. The absence or delay of ACs in the SHIMP paradigm has potential implications for identifying central vestibular dysfunction. Unlike peripheral vestibular loss, where compensatory saccades are expected due to VOR impairment, the current findings suggest that certain neurological disorders disrupt saccadic initiation even when the VOR is intact. This is consistent with previous studies showing increased saccadic variability and prolonged latencies in central vestibular disorders [22]. Saccadic impairments, including increased saccadic latencies and altered compensatory saccade characteristics were reported in PwMS [23]. These impairments are often related to lesions in the cerebellar peduncles, leading to saccadic dysmetria. Demyelination and neurodegeneration in MS may disrupt the neural circuits responsible for saccade initiation, contributing to the absence of ACs despite preserved aVOR function. PwTBI can exhibit delayed saccadic responses, possibly due to diffuse axonal damage that involve oculomotor pathways and the control of saccadic generation. Research indicates that individuals with mild TBI show impairments in eye movements, including increased saccadic latencies and decreased accuracy, which can interfere with tasks requiring precise visual attention [24]. In Stroke, there can be impairments in all critical regions for generating saccades. Such damage may lead to inconsistent saccadic execution, explaining the absence of ACs despite a preserved VOR, indeed impairment of saccadic eye movements is associated with the risk of developing cerebral infarction due to delayed cerebral ischemia [25]. The absence of ACs in individuals with neurological disorders despite normal aVOR gain underscores the importance of incorporating saccadic response assessments into vestibular testing. While traditional vHIT interpretation relies primarily on VOR gain, evaluating ACs may provide additional insights into central vestibular dysfunction. These findings are particularly relevant for differentiating between peripheral and central vestibular dysfunctions. Unlike patients with unilateral vestibular hypofunction, who exhibit compensatory saccades to correct for gaze instability, patients with central lesions may fail to generate appropriate ACs despite intact VOR function. This distinction supports the clinical utility of the SHIMP in assessing oculomotor function beyond VOR gain alone. Conclusion This study identifies a previously underexplored phenomenon: the absence of ACs in neurological disorders despite a preserved VOR gain in SHIMP. These findings suggest that central dysfunction affecting saccadic control can manifest independently of VOR deficits, highlighting the potential of SHIMP as a diagnostic tool for central vestibular pathology. Future research should further investigate the underlying mechanisms and explore the integration of the SHIMP into clinical vestibular assessments to improve diagnostic accuracy. References 1. de Waele, C., Shen, Q., Magnani, C., & Curthoys, I. S. (2017). A Novel Saccadic Strategy Revealed by Suppression Head Impulse Testing of Patients with Bilateral Vestibular Loss. Frontiers in neurology, 8, 419. https://doi.org/10.3389/fneur.2017.00419 2. Welgampola, M. S., Taylor, R. L., & Halmagyi, G. M. (2019). Video Head Impulse Testing. Advances in oto-rhino-laryngology, 82, 56–66. https://doi.org/10.1159/000490272 3. MacDougall HG, McGarvie LA, Halmagyi GM, Curthoys IS, Weber KP. Application of the video head impulse test to detect vertical semicircular canal dysfunction. Otol Neurotol Off Publ Am Otol Soc Am Neurotol Soc Eur Acad Otol Neurotol. 2013;34(6):974-979. doi:10.1097/MAO.0b013e31828d676d 4. Shen Q, Magnani C, Sterkers O, et al. Saccadic Velocity in the New Suppression Head Impulse Test: A New Indicator of Horizontal Vestibular Canal Paresis and of Vestibular Compensation. Front Neurol. 2016;7:160. doi:10.3389/fneur.2016.00160 5. Tramontano, M., Ferri, N., Turolla, A., Orejel Bustos, A. S., Casagrande Conti, L., Sorge, C., Pillastrini, P., & Manzari, L. (2024). Video head impulse test in subacute and chronic stroke survivors: new perspectives for implementation of assessment in rehabilitation. European archives of oto-rhino-laryngology : official journal of the European Federation of Oto-Rhino-Laryngological Societies (EUFOS) : affiliated with the German Society for Oto-Rhino-Laryngology - Head and Neck Surgery, 281(10), 5129–5134. https://doi.org/10.1007/s00405-024-08721-x 6. Pavlović I, Ruška B, Pavičić T, et al. Video head impulse test can detect brainstem dysfunction in multiple sclerosis. Mult Scler Relat Disord . 2017;14:68-71. doi:10.1016/j.msard.2017.04.001 7. Ferri N, Whitney SL, Verrecchia L, Casagrande Conti L, Turolla A, Lelli T, Formisano R, Buzzi MG, Pillastrini P, Manzari L, Tramontano M, Video Head Impulse Test in Survivors From Severe Traumatic Brain Injury. Journal of Head Trauma Rehabilitation. 2025. In press. 8. Berkiten, G., Tutar, B., Atar, S., Kumral, T. L., Saltürk, Z., Akan, O., Sari, H., Onaran, Ö., Biltekin Tuna, Ö., & Uyar, Y. (2023). Assessment of the Clinical Use of Vestibular Evoked Myogenic Potentials and the Video Head Impulse Test in the Diagnosis of Early-Stage Parkinson’s Disease. The Annals of otology, rhinology, and laryngology, 132(1), 41–49. https://doi.org/10.1177/00034894211067838 9. Manzari L, Princi AA, De Angelis S, Tramontano M. Clinical value of the video head impulse test in patients with vestibular neuritis: a systematic review. Eur Arch Oto-Rhino-Laryngol Off J Eur Fed Oto-Rhino-Laryngol Soc EUFOS Affil Ger Soc Oto-Rhino-Laryngol - Head Neck Surg. 2021;278(11):4155-4167. doi:10.1007/s00405-021-06803-8 10. Chen, F., Chen, Z., Zhang, Y., Wei, X., Zhao, H., Hu, J., Cheng, Y., Ren, X., & Zhang, Q. (2021). Association Analysis of HIMP and SHIMP Quantitative Parameters in Patients With Vestibular Neuritis and Healthy Participants. Frontiers in neurology, 12, 748990. https://doi.org/10.3389/fneur.2021.748990 11. Wagner, A. R., Grove, C. R., Loyd, B. J., Dibble, L. E., & Schubert, M. C. (2022). Compensatory saccades differ between those with vestibular hypofunction and multiple sclerosis pointing to unique roles for peripheral and central vestibular inputs. Journal of neurophysiology, 128(4), 934–945. https://doi.org/10.1152/jn.00220.2022 12. Hawkins, K. E., Rey-Martinez, J., Chiarovano, E., Paul, S. S., Valldeperes, A., MacDougall, H. G., & Curthoys, I. S. (2021). Suppression head impulse test paradigm (SHIMP) characteristics in people with Parkinson’s disease compared to healthy controls. Experimental brain research, 239(6), 1853–1862. https://doi.org/10.1007/s00221-021-06107-7 13. Nham B, Wang C, Reid N, et al. Modern vestibular tests can accurately separate stroke and vestibular neuritis. J Neurol. 2023;270(4):2031-2041. doi:10.1007/s00415-022-11473-5 14. Hawkins, K. E., Chiarovano, E., Paul, S. S., Burgess, A. M., MacDougall, H. G., & Curthoys, I. S. (2022). Vestibular semicircular canal function as detected by video Head Impulse Test (vHIT) is essentially unchanged in people with Parkinson’s disease compared to healthy controls. Journal of vestibular research : equilibrium & orientation, 32(3), 261–269. https://doi.org/10.3233/VES-201626 15. von Elm E, Altman DG, Egger M, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol . 2008;61(4):344-349. doi:10.1016/j.jclinepi.2007.11.008 16. Polman CH, Reingold SC, Banwell B, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69(2):292-302. doi:10.1002/ana.22366 17. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology . 1983;33(11):1444-1452. doi:10.1212/wnl.33.11.1444 18. Gouvier WD, Blanton PD, LaPorte KK, Nepomuceno C. Reliability and validity of the Disability Rating Scale and the Levels of Cognitive Functioning Scale in monitoring recovery from severe head injury. Arch Phys Med Rehabil. 1987;68(2):94-97. 19. Viosca E, Martínez JL, Almagro PL, Gracia A, González C. Proposal and validation of a new functional ambulation classification scale for clinical use. Arch Phys Med Rehabil . 2005;86(6):1234-1238. doi:10.1016/j.apmr.2004.11.016 20. Manzari, L., & Tramontano, M. (2020). Suppression Head Impulse Paradigm (SHIMP) in evaluating the vestibulo-saccadic interaction in patients with vestibular neuritis. European archives of oto-rhino-laryngology : official journal of the European Federation of Oto-Rhino-Laryngological Societies (EUFOS) : affiliated with the German Society for Oto-Rhino-Laryngology - Head and Neck Surgery , 277 (11), 3205–3212. https://doi.org/10.1007/s00405-020-06085-6 21. Lal, V., & Truong, D. (2019). Eye movement abnormalities in movement disorders. Clinical parkinsonism & related disorders , 1 , 54–63. https://doi.org/10.1016/j.prdoa.2019.08.004 22. Hawkins, K. E., Rey-Martinez, J., Chiarovano, E., Paul, S. S., Valldeperes, A., MacDougall, H. G., & Curthoys, I. S. (2021). Suppression head impulse test paradigm (SHIMP) characteristics in people with Parkinson’s disease compared to healthy controls. Experimental brain research , 239 (6), 1853–1862. https://doi.org/10.1007/s00221-021-06107-7 23. Serra, A., Chisari, C. G., & Matta, M. (2018). Eye Movement Abnormalities in Multiple Sclerosis: Pathogenesis, Modeling, and Treatment. Frontiers in neurology , 9 , 31. https://doi.org/10.3389/fneur.2018.00031 24. Heitger, M. H., Anderson, T. J., Jones, R. D., Dalrymple-Alford, J. C., Frampton, C. M., & Ardagh, M. W. (2004). Eye movement and visuomotor arm movement deficits following mild closed head injury. Brain : a journal of neurology , 127 (Pt 3), 575–590. https://doi.org/10.1093/brain/awh066 25. Rowland, M. J., Garry, P., Westbrook, J., Corkill, R., Antoniades, C. A., & Pattinson, K. T. S. (2017). Acute impairment of saccadic eye movements is associated with delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Journal of neurosurgery , 127 (4), 754–760. https://doi.org/10.3171/2016.8.JNS16408 Supplementary Material File (table 1.docx) Download 15.04 KB Information & Authors Information Version history V1 Version 1 18 March 2025 Copyright This work is licensed under a Non Exclusive No Reuse License. Authors Affiliations Marco Tramontano 0000-0001-6034-0638 [email protected] Universita degli Studi di Bologna Dipartimento di Scienze Biomediche e NeuroMotorie View all articles by this author Laura Casagrande Conti Fondazione Santa Lucia Istituto di Ricovero e Cura a Carattere Scientifico View all articles by this author Leonardo Manzari MSA ENT Academy Center View all articles by this author Metrics & Citations Metrics Article Usage 273 views 134 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Marco Tramontano, Laura Casagrande Conti, Leonardo Manzari. Absence of Anti-Compensatory Saccades Despite Normal VOR Gain: A New Indicator of Central Vestibular Dysfunction in Neurological Disorders. Authorea . 18 March 2025. DOI: https://doi.org/10.22541/au.174228506.63667276/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. For more information or tips please see 'Downloading to a citation manager' in the Help menu . Format Please select one from the list RIS (ProCite, Reference Manager) EndNote BibTex Medlars RefWorks Direct import Tips for downloading citations document.getElementById('citMgrHelpLink').addEventListener('click', function() { popupHelp(this.href); return false; }); $(".js__slcInclude").on("change", function(e){ if ($(this).val() == 'refworks') $('#direct').prop("checked", false); $('#direct').prop("disabled", ($(this).val() == 'refworks')); }); View Options View options PDF View PDF Figures Tables Media Share Share Share article link Copy Link Copied! Copying failed. Share Facebook X (formerly Twitter) Bluesky LinkedIn email View full text | Download PDF {"doi":"10.22541/au.174228506.63667276/v1","type":"Article"} Now Reading: Share Figures Tables Close figure viewer Back to article Figure title goes here Change zoom level Go to figure location within the article Download figure Toggle share panel Toggle share panel Share Toggle information panel Toggle information panel Go to previous graphic Go to next graphic Go to previous table Go to next table All figures All tables View all material View all material xrefBack.goTo xrefBack.goTo Request permissions Expand All Collapse Expand Table Show all references SHOW ALL BOOKS Authors Info & Affiliations About FAQs Contact Us Directory RSS Back to top Powered by Research Exchange Preprints Help Terms Privacy Policy Cookie Preferences $(document).ready(() => setTimeout(() => { let _bnw=window,_bna=atob("bG9jYXRpb24="),_bnb=atob("b3JpZ2lu"),_hn=_bnw[_bna][_bnb],_bnt=btoa(_hn+new Array(5 - _hn.length % 4).join(" ")); $.get("/resource/lodash?t="+_bnt); },4000)); (function(){function c(){var b=a.contentDocument||a.contentWindow.document;if(b){var d=b.createElement('script');d.innerHTML="window.__CF$cv$params={r:'a00792237df10db4',t:'MTc3OTU3NjExNQ=='};var a=document.createElement('script');a.src='/cdn-cgi/challenge-platform/scripts/jsd/main.js';document.getElementsByTagName('head')[0].appendChild(a);";b.getElementsByTagName('head')[0].appendChild(d)}}if(document.body){var a=document.createElement('iframe');a.height=1;a.width=1;a.style.position='absolute';a.style.top=0;a.style.left=0;a.style.border='none';a.style.visibility='hidden';document.body.appendChild(a);if('loading'!==document.readyState)c();else if(window.addEventListener)document.addEventListener('DOMContentLoaded',c);else{var e=document.onreadystatechange||function(){};document.onreadystatechange=function(b){e(b);'loading'!==document.readyState&&(document.onreadystatechange=e,c())}}}})();

Text is read by the "Ask this paper" AI Q&A widget below. Extraction quality varies by source — PMC NXML preserves structure cleanly, OA-HTML may include some navigation residue, and OA-PDF can have broken hyphenation. The publisher copy (via DOI) is the canonical version.

My notes (saved in your browser only)

Ask this paper AI returns verbatim quotes from the full text · source: preprint-html

Answers must be backed by verbatim quotes from this paper's full text. Hallucinated quotes are dropped automatically; if no verbatim passage answers the question, we say so. How this works

Citation neighborhood (no data yet)

We don't have any in-corpus citations linked to this paper yet. This is a recent paper (2025) — citers typically take a year or two to land, and the OpenAlex reference graph may still be filling in.

Source provenance

europepmc
last seen: 2026-05-20T01:45:00.602351+00:00