A New Suppression Index Calculation Using the Visually Enhanced Vestibulo-Ocular Reflex and Vestibulo-Ocular Reflex Suppression Paradigms in the Video Head Impulse Test
Abstract
:1. Introduction
2. Materials and Methods
2.1. Recording of Sinusoidal Tests (qVVOR and qVORS)
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- Maintain a smooth and continuous movement.
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- Avoid prolonged stops at extreme head positions, aiming for a sinusoidal movement as much as possible.
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- Avoid dominance, bias, and asymmetry to the right and left during oscillations.
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- Perform oscillations describing a symmetrical arc of about 30–40° amplitude centered at the front.
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- Two 17 s recordings were obtained per subject (qVVOR, qVORS).
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- During the qVVOR recording, the fixation point was stable on the wall, but during the qVORS, it was displayed from the goggles, and in this test, the examiner repeatedly instructed the subject throughout not to lose sight of the moving laser point on the wall, aiming to achieve a paradigm with cognitive reinforcement according to the work of Soriano Reixach [17].
2.2. Mathematical Analysis and Gain Quantification of qVVOR and qVORS
2.3. Calculation of the Suppression Index (SI)
3. Results
3.1. Expected Frequency vs. Obtained Frequency (qVVOR and qVORS)
3.2. Calculation of the Suppression Index (SI) for Normal Subjects
3.2.1. Calculation of the Unilateral SI
3.2.2. Calculation of the Bilateral SI
3.2.3. Calculation of SI Stratified by Sex and Age
Differences in SI by Sex
Differences in SI by Age
4. Discussion
4.1. Sinusoidal Tests: VVOR/VORS
4.2. Impulsive vs. Sinusoidal Rotatory Stimulus
4.3. Suppression Index (SI)
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Halmagyi, G.M.; Gresty, M.A. Clinical signs of visual-vestibular interaction. J. Neurol. Neurosurg. Psychiatry 1979, 42, 934–939. [Google Scholar] [CrossRef] [PubMed]
- Kheradmand, A.; Zee, D.S. The bedside examination of the vestibulo-ocular reflex (VOR): An update. Rev. Neurol. 2012, 168, 710–719. [Google Scholar] [CrossRef]
- Daye, P.M.; Roberts, D.C.; Zee, D.S.; Optican, L.M. Vestibulo-ocular reflex suppression during head-fixed saccades reveals gaze feedback control. J. Neurosci. 2015, 35, 1192–1198. [Google Scholar] [CrossRef]
- Shen, Q.; Magnani, C.; Sterkers, O.; Lamas, G.; Vidal, P.P.; Sadoun, J.; Curthoys, I.S.; de Waele, C. 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, 106. [Google Scholar] [CrossRef]
- Della Santina, C.C.; Cremer, P.D.; Carey, J.P.; Minor, L.B. Comparison ot head thrust test with head autorotation test reveals that the vestibulo-ocular reflex is enhanced during voluntary head movements. Arch. Otolaryngol.-Head Neck Surg. 2002, 128, 1044–1054. [Google Scholar] [CrossRef]
- Johnston, J.L.; Daye, P.M.; Thomson, G.T.D. Inaccurate saccades and enhanced vestibulo-ocular reflex suppression during combined eye-head movements in patients with chronic neck pain: Possible implications for cervical vertigo. Front. Neurol. 2017, 8, 23. [Google Scholar] [CrossRef]
- Halmagyi, G.M.; Chen, L.; MacDougall, H.G.; Weber, K.P.; McGarvie, L.A.; Curthoys, I.S. The video head impulse test. Front. Neurol. 2017, 8, 258. [Google Scholar] [CrossRef] [PubMed]
- MacDougall, H.G.; McGarvie, L.A.; Halmagyi, G.M.; Curthoys, I.S.; Weber, K.P. The video Head Impulse Test (vHIT) detects vertical semicircular canal dysfunction. PLoS ONE 2013, 8, e61488. [Google Scholar] [CrossRef]
- An, S.Y.; Kim, B.J.; Suh, M.W.; Rhee, C.K.; Jung, J.Y. Clinical roles of fixation suppression failure in dizzy patients in the ENT clinic. Acta Otolaryngol. 2014, 134, 1134–1139. [Google Scholar] [CrossRef]
- Kingma, H.; van de Berg, R. Anatomy, Physiology, and Physics of the Peripheral Vestibular System, 1st ed.; Elsevier B.V.: Amsterdam, The Netherlands, 2016; Volume 137. [Google Scholar] [CrossRef]
- Murai, N.; Oda, N.; Hori, I.; Shabana, M.; Kurozawa, Y.; Funabiki, K. The relationship between cerebral T2 hyperintensity and fixation suppression of vestibulo-ocular reflex in elderly patients with dysequilibrium symptoms. Auris Nasus Larynx 2007, 34, 165–171. [Google Scholar] [CrossRef] [PubMed]
- Rey-Martinez, J.; Thomas-Arrizabalaga, I.; Espinosa-Sanchez, J.M.; Batuecas-Caletrio, A.; Trinidad-Ruiz, G.; Matiño-Soler, E.; Perez-Fernandez, N. Vestibulo-ocular reflex gain values in the suppression head impulse test of healthy subjects. Laryngoscope 2018, 128, 2383–2389. [Google Scholar] [CrossRef] [PubMed]
- Ramos, B.F.; Cal, R.; Carmona, S.; Weber, K.P.; Zuma E Maia, F. Corrective Saccades in Unilateral and Bilateral Vestibular Hypofunction During Slow Rotation Expressed by Visually Enhanced VOR and VOR Suppression: Role of the Cerebellum. Cerebellum 2021, 20, 673–677. [Google Scholar] [CrossRef] [PubMed]
- Rey-Martinez, J.; Batuecas-Caletrio, A.; Matiño, E.; Trinidad-Ruiz, G.; Altuna, X.; Perez-Fernandez, N. Mathematical methods for measuring the visually enhanced vestibulo-Ocular reflex and preliminary results from healthy subjects and patient groups. Front. Neurol. 2018, 9, 69. [Google Scholar] [CrossRef]
- Rey-Martinez, J.; Batuecas-Caletrio, A.; Matiño, E.; Fernandez, N.P. HITCal: A software tool for analysis of video head impulse test responses. Acta Otolaryngol. 2015, 135, 886–894. [Google Scholar] [CrossRef]
- Rey-Martinez, J.; Ninchritz, E.; Palicio, I.; Goiburu, M.; Casado, C.M.; Altuna, X. Clinical Validity of Quantified Visually Enhanced Vestibulo-ocular Reflex Test to Detect Horizontal Semicircular Canal Hypofunction. Otol. Neurotol. 2019, 40, 365–371. [Google Scholar] [CrossRef]
- Soriano-Reixach, M.M.; Prieto-Matos, C.; Perez-Fernandez, N.; Rey-Martinez, J. Effects of parameters of video head impulse testing on visually enhanced vestibulo-ocular reflex and vestibulo-ocular reflex suppression. Clin. Neurophysiol. 2020, 131, 1839–1847. [Google Scholar] [CrossRef] [PubMed]
- Soriano-Reixach, M.M.; Rey-Martínez, J.A.; Garcia-Martin, M.; Trinidad-Ruiz, G.; Altuna, X. A New Method for Gain Calculation in Quantified Visuo-vestibular Interaction Test. Laryngoscope 2023, 133, 3554–3563. [Google Scholar] [CrossRef] [PubMed]
- Kato, I.; Kimura, Y.; Aoyagi, M.; Mizukoshi, K.; Kawasaki, T. Visual suppression of caloric nystagmus in normal individuals. Acta Otolaryngol. 1977, 83, 245–251. [Google Scholar] [CrossRef]
- Kato, I.; Sato, Y.; Aoyagi, M.; Mizukoshi, K.; Kimura, Y.; Koike, Y.; Hayano, N. Caloric pattern test with special reference to failure of fixation-suppression. Acta Otolaryngol. 1979, 88, 97–104. [Google Scholar] [CrossRef]
- Kato, I.; Nakamura, T.; Koike, Y.; Watanabe, Y. Computer analysis of fixation-suppression of caloric nystagmus. Orl 1982, 44, 277–287. [Google Scholar] [CrossRef]
- Kato, I.; Watanabe, J.; Nakamura, T.; Koike, Y. Visual fixation of caloric nystagmus with special reference to a new index. ORL J. Otorhinolaryngol. Relat. Spec. 1984, 46, 7–16. [Google Scholar] [CrossRef]
- Pola, J.; Wyatt, H.J.; Lustgarten, M. Visual Fixation of a Target and Suppression of Optokinetic Nystagmus: Effects of Varying Target Feedback. Vis. Res. 1995, 35, 1079–1087. [Google Scholar] [CrossRef]
- Wyatt, H.J.; Pola, J.; Lustgarten, M.; Aksionoff, E. Optokinetic Nystagmus (OKN) Suppression by Fixation of a Stabilized Target: The Effect of OKN-stimulus Predictability. Vis. Res. 1995, 35, 2903–2910. [Google Scholar] [CrossRef]
- de Waele, C.; Shen, Q.; Magnani, C.; Curthoys, I.S. A novel saccadic strategy revealed by suppression head impulse testing of patients with bilateral vestibular loss. Front. Neurol. 2017, 8, 419. [Google Scholar] [CrossRef]
- Demanez, J.P. Influence of ocular fixation on postcaloric nystagmus. Its measurement. Its semiological importance. Acta Oto-Rhino-Laryngol. Belg. 1968, 22, 739–754. Available online: https://pubmed.ncbi.nlm.nih.gov/5746347/ (accessed on 25 June 2024).
- Demanez, J.P.; Ledoux, A. The index of ocular fixation in caloric tests. Rev. Laryngol. Otol. Rhinol. 1974, 95, 420–421. Available online: https://pubmed.ncbi.nlm.nih.gov/4445647/ (accessed on 23 October 2023).
- Matiño-Soler, E.; Esteller-More, E.; Martin-Sanchez, J.C.; Martinez-Sanchez, J.M.; Perez-Fernandez, N. Normative data on angular vestibulo-ocular responses in the yaw axis measured using the video head impulse test. Otol. Neurotol. 2015, 36, 466–471. [Google Scholar] [CrossRef]
- Halmagyi, G.M.; Curthoys, I.S. A Clinical Sign of Canal Paresis. Arch. Neurol. 1988, 45, 737–739. [Google Scholar] [CrossRef]
- Macdougall, H.G.; Weber, K.P.; Mcgarvie, L.A.; Halmagyi, M.G.M.; Curthoys, I.S. The Video Head Impulse Test Diagnostic Accuracy in Peripheral Vestibulopathy. 2009. Available online: www.neurology.org (accessed on 23 October 2023).
- MacDougall, H.G.; McGarvie, L.A.; Halmagyi, G.M.; Rogers, S.J.; Manzari, L.; Burgess, A.M.; Curthoys, I.S.; Weber, K.P. A new saccadic indicator of peripheral vestibular function based on the video head impulse test. Neurology 2016, 87, 410–418. [Google Scholar] [CrossRef]
- Rey-Martinez, J. Validity of wavelet transforms for analysis of video head impulse test (vHIT) results. Eur. Arch. Oto-Rhino-Laryngol. 2017, 274, 4241–4249. [Google Scholar] [CrossRef]
- Korda, A.; Sauter, T.C.; Caversaccio, M.D.; Mantokoudis, G. Quantifying a Learning Curve for Video Head Impulse Test: Pitfalls and Pearls. Front. Neurol. 2021, 11, 615651. [Google Scholar] [CrossRef] [PubMed]
- Tan, G.X.; Schoo, D.P.; Della Santina, C.C.; Rahman, M.A.; Valentin Contreras, N.S.; Sun, C.H.; Chiang, B. Automated head motion system improves reliability and lessens operator dependence for head impulse testing of vestibular reflexes. IEEE Int. Symp. Med. Meas. Appl. 2017, 2017, 94–99. [Google Scholar] [CrossRef]
- Crane, B.T.; Demer, J.L. Latency of voluntary cancellation of the human vestibulo-ocular reflex during transient yaw rotation. Exp. Brain Res. 1999, 127, 67–74. [Google Scholar] [CrossRef] [PubMed]
- Hawkins, K.E.; Rey-Martinez, J.; Chiarovano, E.; Paul, S.S.; Valldeperes, A.; MacDougall, H.G.; Curthoys, I.S. Suppression head impulse test paradigm (SHIMP) characteristics in people with Parkinson’s disease compared to healthy controls. Exp. Brain Res. 2021, 239, 1853–1862. [Google Scholar] [CrossRef] [PubMed]
- Boniver, R.; Demanez, J.P. Interest of the study of the influence of ocular fixation during caloric tests in pontocerebellar tumors. Orl 1977, 39, 203–208. [Google Scholar] [CrossRef]
- Jahn, K.; Strupp, M.; Krafczyk, S.; Schüler, O.; Glasauer, S.; Brandt, T. Suppression of eye movements improves balance. Brain 2002, 125, 2005–2011. [Google Scholar] [CrossRef]
Age | Freq (%) |
---|---|
≤20 | 8 (4.9) |
21–30 | 19 (11.6) |
31–40 | 9 (5.9) |
41–50 | 11 (6.7) |
51–60 | 10 (6.1) |
61–70 | 15 (9.1) |
71–80 | 9 (5.9) |
>80 | 2 (1.2) |
Gain | Ranges | |
---|---|---|
HIMPr | 1.008 ± 0.099 | 0.77–1.27 |
HIMPl | 0.940 ± 0.096 | 0.70–1.37 |
SHIMPr | 0.939 ± 0.116 | 0.71–1.40 |
SHIMPl | 0.877 ± 0.104 | 0.65–1.32 |
qVVORr | 0.981 ± 0.070 | 0.791–1.177 |
qVVORl | 0.978 ± 0.077 | 0.789–1.204 |
qVORSr | 0.334 ± 0.112 | 0.140–0.694 |
qVORSl | 0.353 ± 0.110 | 0.142–0.615 |
Percentile | Left SI | Right SI | Bilateral SI |
---|---|---|---|
p5 | 0.202 | 0.182 | 0.141 |
p10 | 0.224 | 0.225 | 0.181 |
p25 | 0.287 | 0.254 | 0.224 |
p50 (Median) | 0.354 | 0.325 | 0.283 |
p75 | 0.412 | 0.390 | 0.348 |
p90 | 0.530 | 0.529 | 0.451 |
p95 | 0.584 | 0.610 | 0.540 |
Age (Ranges) | SI |
---|---|
≤20 | 0.283 ± 0.081 |
21–30 | 0.299 ± 0.116 |
31–40 | 0.279 ± 0.101 |
41–50 | 0.273 ± 0.052 |
51–60 | 0.259 ± 0.103 |
61–70 | 0.295 ± 0.107 |
71–80 | 0.344 ± 0.125 |
>80 | 0.446 ± 0.163 |
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Prieto-Matos, C.; Rey-Martínez, J.; Pérez-Fernández, N. A New Suppression Index Calculation Using the Visually Enhanced Vestibulo-Ocular Reflex and Vestibulo-Ocular Reflex Suppression Paradigms in the Video Head Impulse Test. Audiol. Res. 2024, 14, 747-759. https://doi.org/10.3390/audiolres14040063
Prieto-Matos C, Rey-Martínez J, Pérez-Fernández N. A New Suppression Index Calculation Using the Visually Enhanced Vestibulo-Ocular Reflex and Vestibulo-Ocular Reflex Suppression Paradigms in the Video Head Impulse Test. Audiology Research. 2024; 14(4):747-759. https://doi.org/10.3390/audiolres14040063
Chicago/Turabian StylePrieto-Matos, Carlos, Jorge Rey-Martínez, and Nicolás Pérez-Fernández. 2024. "A New Suppression Index Calculation Using the Visually Enhanced Vestibulo-Ocular Reflex and Vestibulo-Ocular Reflex Suppression Paradigms in the Video Head Impulse Test" Audiology Research 14, no. 4: 747-759. https://doi.org/10.3390/audiolres14040063