Objectives
The occurrence of direction-reversing nystagmus during positional testing in patients with benign paroxysmal positional vertigo (BPPV) is not uncommon. Further in-depth analysis of the characteristics and possible mechanisms of direction-reversing nystagmus will help us to diagnose and treat BPPV more precisely. The study aimed to analyze the incidence and characteristics of direction-reversing nystagmus during positional testing in BPPV patients, evaluate the outcomes of canalith repositioning procedure for these patients, and further explore the possible mechanism of reversal nystagmus in BPPV patients.
Study design
Retrospective study.
Setting
Single-center study.
Patients
A total of 575 patients with BPPV who visited the Vertigo Clinic of our hospital between April 2017 and June 2021 were enrolled.
Main outcome measures
Dix-Hallpike and supine roll tests were performed. The nystagmus was recorded using videonystagmography. The characteristics of direction-reversing nystagmus and the possible underlying mechanism were analyzed.
Results
Patients with BPPV who showed reversal nystagmus accounted for 9.39% (54 of 575) of all BPPV patients visiting our hospital during the same period, of which 5.57% (32 of 575) had horizontal semicircular canal BPPV (HC-BPPV), and 3.83% (22 of 575) had posterior semicircular canal BPPV (PC-BPPV). The maximum slow-phase velocities (mSPVs) of the first-phase nystagmus were greater in HC-BPPV and PC-BPPV patients with reversal nystagmus than those without (p = 0.04 and p = 0.01, respectively). In all HC-BPPV and PC-BPPV patients with reversal nystagmus, the mSPV of the first-phase nystagmus was greater than that of the second-phase nystagmus (p < 0.01). The duration of the second-phase nystagmus was longer than 60 seconds in 93.75% (30 of 32) of the HC-BPPV patients and 77.27% (17 of 22) of the PC-BPPV patients (p = 0.107, Fisher exact test). HC-BPPV and PC-BPPV patients with reversal nystagmus both required more than one canalith repositioning procedure compared with those without (HC-BPPV: 75 versus 28.13%, p < 0.001; PC-BPPV: 59.09 versus 13.64%, p = 0.002).
Conclusions
The cause of second-phase nystagmus in BPPV patients with direction-reversing nystagmus may be related to the involvement of central adaptation mechanisms secondary to the overpowering mSPV of the first-phase nystagmus.
Key Words: Benign paroxysmal positional vertigo, Central adaptation mechanism, Positional nystagmus, Semicircular canal, Spontaneous reversal nystagmus
INTRODUCTION
Benign paroxysmal positional vertigo (BPPV) is characterized by transient episodes of vertigo triggered by specific changes in head position. About 90% of positional vertigo is caused by BPPV, which is the most common peripheral vestibular disorder (1). The mechanism of BPPV is that the otoliths are dislodged from the original position within the otolith organs because of head trauma and local structural degeneration of otoliths in the elderly people, then the detached otolith debris floats freely in the semicircular canals (canalolithiasis) or is adherent to the cupula of a semicircular canal (cupulolithiasis) (2). In 2015, the Committee for the Classification of Vestibular Disorders of the Bárány Society produced an expert consensus document on the diagnostic criteria for BPPV (3), which provides a detailed description of various types of BPPV.
BPPV with atypical nystagmus is sometimes encountered in clinical work. For example, during the diagnosis of horizontal semicircular canal BPPV (HC-BPPV) by using the supine roll test, when a patient lying in the supine position is turned 90 degrees to the lateral position, first-phase geotropic nystagmus occurs on the affected side, which lasts for a few seconds and then subsides. Then the nystagmus changes direction after an interval of a few seconds, second-phase apogeotropic nystagmus occurs spontaneously on the affected side, and the duration is longer than the 60 seconds. A similar phenomenon can be found when performing the Dix-Hallpike test in patients with posterior semicircular canal BPPV (PC-BPPV); that is, spontaneous direction reversal of positional nystagmus occurred on the affected side during the Dix-Hallpike test in these patients.
Stahle and Terins (4) first reported the phenomenon of spontaneous direction reversal of positional nystagmus in BPPV in 1965 and provided a detailed analysis of the etiology and nystagmus characteristics in these patients, but they did not report the pathogenic mechanism of reversal nystagmus. Baloh et al. (5) further described the characteristics of reversal nystagmus in patients with HC-BPPV in 1993 and found that the second-phase apogeotropic nystagmus was easily induced when the slow-phase velocity (SPV) of first-phase geotropic nystagmus was greater than 50 deg/s. Lee et al. (6) analyzed the clinical features of 21 patients with HC-BPPV who showed reversal nystagmus, and found that reversal was unilateral in 16 patients and bilateral in 5 patients, and the authors also suggest that the occurrence of unilateral reversal nystagmus may be due to that when the patient's head is turned during positional testing, the nystagmus intensity exceeds a certain threshold could inhibit the ampullary nerve, thus leading to the increase of perilymphatic potassium (K+) concentrations and the activation of Na+-K+-ATPase, that is, the adaptive mechanism of the peripheral vestibular system, resulting in the generation of the second-phase nystagmus. However, this cannot explain the occurrence of bilateral reversal nystagmus. In 2015, Ogawa et al. (7) proposed that the coexistence of cupulolithiasis and canalolithiasis may be a mechanism that could explain the generation of bilateral reversal nystagmus. In 2020, Choi et al. (8) proposed central adaptation mechanism to elucidate the generation of reversal nystagmus. Since the phenomenon of reversal nystagmus in BPPV was discovered, several mechanistic hypotheses have been proposed; however, no theory can explain the occurrence of reversal nystagmus perfectly.
Given this background, in this study, we analyzed the characteristics of reversal nystagmus in 54 patients with BPPV, evaluated the intensity and duration of the nystagmus and the outcomes of canalith repositioning procedures (CRPs) for these patients, and further explored the possible mechanisms of reversal nystagmus. We hope the findings will provide references for clinicians and make contributions to the diagnosis and treatment of BPPV patients with reversal nystagmus.
METHODS
Subjects
We retrospective recruited 575 patients with BPPV who visited the Vertigo Clinic of Aerospace Center Hospital between April 2017 and June 2021. According to the nystagmus recorded using videonystagmography (Interacoustics, Middelfart, Denmark), reversal nystagmus was observed in 54 patients, including 32 patients with HC-BPPV and 22 with PC-BPPV. All patients met the diagnostic criteria for BPPV proposed by the International Bárány Society (3): positional nystagmus and vertigo were evoked by the Dix-Hallpike and supine roll tests. To confirm the diagnosis of HC-BPPV and PC-BPPV, each position should be maintained for more than 1 minute to record the changes in nystagmus. All patients underwent eye movement tests, including gaze, saccade, smooth pursuit, and optokinetic nystagmus tests. Magnetic resonance imaging was performed for all patients to exclude central lesions. Results of the eye movement test and magnetic resonance imaging findings were normal in all patients. All the aforementioned patients' data were analyzed anonymously.
Nystagmus was recorded binocularly with video-oculography (Interacoustics). To induce positional nystagmus, the patients lay supine from sitting (lying-down nystagmus) and turned their heads to either side while in the supine position (supine head-roll test). Then the patients were moved from a supine to a sitting position, and the head was bent down (head-bending nystagmus). Patients were also subjected to right and left Hallpike maneuvers. At each step during the test, the examiners kept the head position and observed the nystagmus at least for 1 minute and then transited to the next step.
The barbecue roll maneuver was used for treatment of HC-BPPV (9), and Epley maneuver was used for the treatment of PC-BPPV (10). The treatment efficacy was classified into three categories: cured (disappearance of both vertigo symptoms and nystagmus), effective (the reduction of either vertigo symptoms or nystagmus), and ineffective (the absence of any change in either vertigo symptoms or nystagmus).
Statistical Analysis
Measurement data were expressed as mean ± standard deviation, and comparisons for normally distributed data between groups were performed by using an independent-sample t test. The counting data were expressed as percentages, and comparisons between groups were performed using the χ2 test with Yates continuity correction or Fisher exact test, as appropriate. All reported p values are two-tailed, and a p < 0.05 was considered statistically significant. All statistical analyses were performed with SPSS 20.0 software (IBM, Armonk, NY).
The measures of positional nystagmus for analysis were the maximum SPV (mSPV), duration, and time constant (Tc). The Tc of positional nystagmus was calculated with a nonlinear regression test (9). Because the SPVs of positional nystagmus exponentially decreased, we use the following nonlinear regression equation: SPVs = A × e−t/τ + C (11), where A is the amplitude of mSPV, t is the duration time of nystagmus, C is offset indicating the constant SPVs, and τ is Tc. The values of A and C were arranged to 1 and 0 (11).
RESULTS
Patients' Clinical Characteristics
Among 575 patients with BPPV who visited the vertigo clinic during the same period, 9.39% (54 of 575) of the patients showed reversal nystagmus. There were 149 patients with HC-BPPV and 358 with PC-BPPV; 21.48% (32 of 149) of patients with HC-BPPV and 6.1% (22 of 358) of patients with PC-BPPV showed reversal nystagmus.
Two of the 32 patients with HC-BPPV showed bilateral reversal nystagmus during the supine roll test, and the remaining 30 patients showed unilateral reversal nystagmus. All patients with PC-BPPV both had unilateral reversal nystagmus. In all patients with unilateral reversal nystagmus, the reversal occurred on the affected side.
The average age of HC-BPPV patients with and without reversal nystagmus was 61.44 ± 12.50 and 57.19 ± 15.85 years, respectively; there was no statistically significant difference between these patients (t = 1.191, p = 0.238). In addition, there was also no statistically significant difference in the average age between PC-BPPV patients with and without reversal nystagmus (56.47 ± 16.78 versus 57.74 ± 15.29 yr, t = −0.086, p = 0.932; Table 1).
TABLE 1.
Comparison of clinical characteristics of patients with BPPV with and without reversal
| HC-BPPV | PC-BPPV | |||||||
|---|---|---|---|---|---|---|---|---|
| Total (n = 64) | With Reversal (n = 32) | Without Reversal (n = 32) | p | Total (n = 44) | With Reversal (n = 22) | Without Reversal (n = 22) | p | |
| Age, mean ± SD, yr | 58.95 ± 14.58 | 61.44 ± 12.50 | 57.19 ± 15.85 | 0.24a | 57.80 ± 15.64 | 56.47 ± 16.78 | 57.74 ± 15.29 | 0.93a |
| Male, n (%) | 22 (40.63) | 11 (34.4) | 15 (46.9) | 1.24b | 15 (34.09) | 7 (31.8) | 8 (36.4) | 0.10b |
| Lesion side, left, n (%) | 17 (28.33) | 9 (28.1) | 8 (25.0) | 0.20b | 27 (61.36) | 13 (57.9) | 14 (63.2) | 0.10b |
| CRP times, mean (SD) | 1.59 (0.64) | 1.88 (0.61) | 1.31 (0.54) | <0.001b | 1.45 (0.71) | 1.82 (0.80) | 1.05 (0.22) | 0.002b |
ap Values are estimated by rank-sum test.
bp Values are estimated by t test.
BPPV indicates benign paroxysmal positional vertigo; CRP, canalith repositioning procedure; HC-BPPV, horizontal canal BPPV; PC-BPPV, posterior canal BPPV; SD, standard deviation.
Nystagmus Characteristics
The average mSPVs of first-phase nystagmus were significantly greater in HC-BPPV patients with reversal nystagmus than those without (51.28 ± 17.76 versus 41.78± 19.21 deg/s, t = 2.05, p = 0.04). The average mSPV of first-phase nystagmus was also significantly greater in PC-BPPV patients with reversal nystagmus than those without (26.82 ± 13.90 versus 17.82 ± 7.76 deg/s, t = 2.65, p = 0.01; Table 2).
TABLE 2.
Analysis of positional nystagmus during the first phase
| HC-BPPV | PC-BPPV | |||||
|---|---|---|---|---|---|---|
| mSPV, Mean ± SD), deg/s | Duration Mean ± SD, s |
Tc, Mean ± SD, s | mSPV, Mean ± SD, deg/s | Duration, Mean ± SD, s | Tc, Mean ± SD, s | |
| Without reversal | 41.78 ± 19.21 | 20.59 ± 7.51 | 5.70 ± 1.79 | 17.82 ± 7.76 | 12.86 ± 3.92 | 4.66 ± 1.53 |
| With reversal | 51.28 ± 17.76 | 19.16 ± 6.48 | 4.91 ± 1.53 | 26.82 ± 13.90 | 14.23 ± 5.16 | 4.59 ± 1.32 |
| t | 2.05 | −0.82 | 1.71 | 2.65 | 0.99 | −1.45 |
| p | 0.04 | 0.42 | 0.09 | 0.01 | 0.33 | 0.89 |
BPPV indicates benign paroxysmal positional vertigo; HC-BPPV, horizontal canal BPPV; mSPV, maximum slow-phase velocity; PC-BPPV, posterior canal BPPV; SD, standard deviation; Tc, time constant.
The duration of first-phase nystagmus was 19.16 ± 6.48 and 20.59 ± 7.51 s, respectively, in HC-BPPV patients with and without reversal nystagmus (t = −0.82, p = 0.42). In addition, there was also no statistically significant difference in the duration of first-phase nystagmus between PC-BPPV patients with and without reversal nystagmus (14.23 ± 5.16 versus 12.86 ± 3.92, t = 0.99, p = 0.33; Table 2).
No statistically significant difference was found in the Tc of the first-phase nystagmus between HC-BPPV patients with and without reversal nystagmus (4.91 ± 1.53 versus 5.70 ± 1.79 s, t = 1.71, p = 0.09), as well as between PC-BPPV patients with and without reversal HC-BPPV (4.59 ± 1.32 versus 4.66 ± 1.53 s, t = −1.45, p = 0.89; Table 2, Fig. 1). The mean value of Tc for the second-phase nystagmus in patients with HC-BPPV with reversal nystagmus was 27.70 seconds (range, 15.58–43.28 s), respectively. The mean value of Tc for the second-phase nystagmus in patients with HC-BPPV with reversal nystagmus was 24.06 seconds (range, 12.5–43 s).
FIG. 1.
Comparison of the treatment outcomes between BPPV patients with and without spontaneous direction reversal of positional nystagmus. The number in the box indicates the number of patients. BPPV indicates benign paroxysmal positional vertigo; HC-BPPV, horizontal canal BPPV; PC-BPPV, posterior canal BPPV.
In the second-phase nystagmus, the average mSPV was 18.16 ± 11.88 deg/s in HC-BPPV patients with reversal nystagmus and 11.14 ± 4.73 deg/s in PC-BPPV patients with reversal nystagmus.
The duration of the second-phase nystagmus was longer than the 60 seconds in 93.75% (30 of 32) of the patients with HC-BPPV and 77.27% (17 of 22) of the patients with PC-BPPV.
Treatment Outcomes
Among HC-BPPV patients with reversal nystagmus, 25% (8 of 32) of the patients were cured after only one CRP, and 75% (24 of 32) of the patients required more than one CRP. Among HC-BPPV patients without reversal nystagmus, 71.88% (23 of 32) of the patients were cured after only one CRP, and 28.13% (9 of 32) of the patients required more than one CRP. There was statistical significance in the treatment outcomes between HC-BPPV patients with and without reversal nystagmus (t = 14.08, p < 0.001; Fig. 2).
FIG. 2.
Comparison of mSPVs of the first-phase nystagmus between BPPV patients with and without spontaneous direction reversal of positional nystagmus. The mSPVs of the first-phase nystagmus were stronger in HC-BPPV and PC-BPPV with reversal nystagmus than those without (p = 0.04 and p = 0.01, respectively). Reversal (+) represents patients with spontaneous direction reversal of positional nystagmus; reversal (−) represents patients without spontaneous direction reversal of positional nystagmus. BPPV indicates benign paroxysmal positional vertigo; HC-BPPV, horizontal canal BPPV; mSPVs, maximal slow-phase velocities; PC-BPPV, posterior canal BPPV.
Among PC-BPPV patients with reversal nystagmus, 40.91% (9 of 22) of the patients were cured after only one CRP, and 59.09% (13 of 22) of the patients required more than one CRP. Among PC-BPPV patients without reversal nystagmus, 86.36% (19 of 22) of the patients were cured after only one CRP, and 13.64% (3 of 22) of the patients required more than one CRP. There was statistical significance in the treatment outcomes between PC-BPPV patients with and without reversal nystagmus (t = 9.82, p = 0.002; Fig. 2). After initial CRP, canal conversion form AC to PC was observed in 18.75% (6 of 32) of HC-BPPV patients with reversal nystagmus, and canal conversion was observed in 13.63% (3 of 22) of PC-BPPV patients with reversal nystagmus, including from PC to AC in two-thirds of patients, from PC to HC in one-third of patients.
DISCUSSION
In this study, among 575 consecutive patients with benign paroxysmal positional vertigo, 54 of 575 (9.39%) patients with reversal nystagmus were identified, of which 5.56%(32 of 575) had horizontal semicircular canal BPPV and 3.82% (22 of 575) had posterior semicircular canal BPPV. Compared with previous studies (the incidence of patients with horizontal semicircular canal BPPV reversal nystagmus was 73%)(8,12), the incidence of reversal nystagmus in BPPV observed in our study was lower (68%). However, a similar result was reported in a study from Japan showing that the incidence of reversal nystagmus in patients with horizontal semicircular canal BPPV was 10% (7). We speculate that this may be because patients admitted to medical centers of different levels have different disease severity.
According to Ewald's law (13), the first-phase nystagmus in canalolithiasis of the posterior arm of the horizontal canal canalolithiasis is considered to be induced by the flow of endolymph toward the ampulla of the horizontal semicircular canal and the excitation of hair cells due to rapid movement of the otoliths under the action of gravity when the patient's head is turned. However, the mechanism responsible for the second-phase nystagmus in patients with BPPV is still unclear. Several mechanisms have been proposed to explain the occurrence of reversal nystagmus in BPPV: 1) simultaneous coexistence of canalolithiasis and cupulolithiasis (7), 2) the inertia of the otoliths (endolymphatic reflux mechanism) (14), 3) sensory adaptation of peripheral vestibular organs (6), and 4) short-term central adaptation of the vestibulo-ocular reflex (VOR) (8). Our study showed that the first-phase nystagmus was significantly stronger than the second-phase nystagmus in patients with BPPV reversal nystagmus, presumably due to excessive or oversized aggregated otolith particles, which drive endolymphatic fluid toward the ampulla under the effect of gravity, thereby producing strong first-phase nystagmus, when the central adaptation mechanism of VOR comes into play and produces second-phase nystagmus.
The central adaptation mechanism of VOR may be mediated through a velocity storage mechanism to produce second-phase nystagmus in patients with BPPV reversal nystagmus. In this study, most patients with reversal nystagmus had intense first-phase nystagmus with short duration (<60 s) and less intense second-phase nystagmus with long duration (>60 s). The Tc values of the first-phase nystagmus were 5.70 ± 1.79 and 4.66 ± 1.53 seconds, respectively, in HC-BPPV and PC-BPPV patients with reversal nystagmus, whereas the mean Tc values of the second-phase nystagmus were 27.7 and 24.06 seconds, respectively, in these patients. From the aforementioned results, we can find that the Tc of the second-phase nystagmus in this study is significantly longer than that of the second phase. Previous studies have shown that the Tc of the semicircular canal is estimated to be 4 to 7 seconds (15–18). There is a central brainstem mechanism, known as the velocity storage mechanism, which can prolong the process of rapid canal-cupula adaptation, causing the signals driving VOR to outlast the peripheral signal generated by head rotation alone. The velocity storage mechanism can prolong the Tc of VOR to 15 to 20 seconds (19,20). The Tc of the second-phase nystagmus in BPPV patients with reversal nystagmus found in the present study is similar to the aforementioned previous studies. The prolongation of the cupula time constant caused by the velocity storage mechanism may be mediated by the central vestibular feedback pathway (21), which is also known as the central adaptation mechanism (8). This central adaptation mechanism may play a pivotal role in the production of direction-reversing nystagmus. In addition, the short-term central adaptation of the VOR is also thought to underlie the second phase of biphasic headshaking nystagmus (22), optokinetic nystagmus (23), or rebound caloric nystagmus (24), and the generation of the second-phase nystagmus both due to the development of central adaptation caused by the intense nystagmus produced during the first phase.
In addition, in this study, 6.3% (2 of 32) of the patients with HC-BPPV showed bilateral reversal nystagmus during the supine roll test. Bilateral reversal nystagmus rarely occurs in patients with BPPV. Ogawa et al. (7) included seven patients with BPPV who showed reversal nystagmus (including five bilateral and two unilateral) and explored the mechanism of reversal nystagmus; the authors suggest that the coexistence of cupulolithiasis and canalolithiasis may be the mechanism responsible for the bilateral reversal of nystagmus in BPPV. During the positional testing, the movement of the otolith debris causes the flow of lymph fluid toward the ampulla, which leads to the displacement of the crista ampullaris, resulting in the occurrence of the first-phase geotropic nystagmus. When the otoliths stop moving, the geotropic nystagmus is attenuated, then the otoliths are adherent to the cupula under the action of gravity, and the displaced crista ampullari returns to the semicircular canal, causing the second-phase apogeotropic nystagmus. This may be the mechanism responsible for the bilateral reverse nystagmus in BPPV observed in this study.
The clinical significance of reversal nystagmus in patients with BPPV may be to help clinicians identify the affected side, because reversal nystagmus occurs on the affected side. In this study, we found that compared with BPPV patients without reversal nystagmus, patients with reversal nystagmus required more than one CRP treatment. This result is somewhat similar to a previous study conducted by Jeong et al. (12). Although statistical significance was not achieved (p = 0.059), a higher proportion of BPPV patients without reversal nystagmus recovered after only one CRP compared with those with reversal nystagmus (82% [14 of 17] versus 57% [26 of 46]). We assumed that the vigorous first-phase nystagmus can be induced by the accumulation of large numbers of otolith particles within the semicircular canals, and some otolith particles may not be repositioned after a CRP, so repeated CRP is required. A previous study conducted by Choi et al. (8) revealed no significant difference in the treatment response between BPPV patients with and without reversal nystagmus after receiving same treatment. We speculate that the reason for these contradictory results is the difference in the patient population included. The majority of the patients included in our study visited the hospital for the first time, whereas in the study of Choi et al., data of patients were obtained from tertiary referral centers.
These patients are also more likely to develop canal conversion after CRPs, indicating that patients with BPPV who showed reversal nystagmus have too many otolith debris aggregated and may require several CRPs. A previous study on BPPV patients who showed exhibited canal conversion (25) showed that the incidence of reversal nystagmus was significantly higher in the canal conversion group than in the noncanal conversion group (31.4% versus 4.3%, p < 0.001). This may be due to the presence of excessive accumulation of otoliths in the semicircular canals, and the otolith particles may translocate during CRP.
The study has certain limitations. The duration of second-phase nystagmus in patients with HC and PC-BPPV reversal nystagmus in this study was recorded only to more than 60 seconds. The duration of nystagmus disappearance was not fully recorded, so the duration of second-phase nystagmus was recorded as the 60 seconds in some patients, so the Tc of the second phase is an estimated value. However, the intensity of second-phase nystagmus in most of the patients in this study had become weak beyond the 60 seconds, so the estimated Tc of the second phase was not significantly different from the standard value. Sample size in future studies should be expanded to record complete second-phase nystagmus durations.
CONCLUSIONS
The cause of second-phase nystagmus in BPPV patients with direction-reversing nystagmus is most consistent with involvement of central adaptation mechanisms secondary to the overpowering mSPV of the first-phase nystagmus.
Footnotes
X.L. and L.S. contributed equally to this work.
Sources of support and disclosure of funding: The study was supported by Aerospace Center Hospital (grant no. YN202106).
Contributions: X.L.: methodology, data curation, formal analysis, visualization, writing original draft; L.S.: investigation, data curation, formal analysis, writing – review & editing; NS: methodology, formal analysis, investigation; Y.W.: methodology, formal analysis, investigation; M.Z.: methodology, formal analysis, investigation; Y.F.: methodology, formal analysis, investigation; T.Z.: methodology, formal analysis, investigation; X.Y.: conceptualization, supervision, writing – review and editing.
The authors disclose no conflicts of interest.
Contributor Information
Xiang Li, Email: lencholeee@163.com.
Lihong Si, Email: slh931554199@163.com.
Ning Song, Email: songning0506@163.com.
Yuexia Wu, Email: zmooner@163.com.
Menglu Zhang, Email: Monroe__Zhang@163.com.
Yufei Feng, Email: ciguangfifi@163.com.
REFERENCES
- 1.Brandt T, Dieterich M. The dizzy patient: Don't forget disorders of the central vestibular system. Nat Rev Neurol 2017;13:352–62. [DOI] [PubMed] [Google Scholar]
- 2.Schuknecht HF. Cupulolithiasis. Arch Otolaryngol 1969;90:765–78. [DOI] [PubMed] [Google Scholar]
- 3.von Brevern M Bertholon P Brandt T, et al. Benign paroxysmal positional vertigo: Diagnostic criteria. J Vestib Res 2015;25(3–4):105–17. [DOI] [PubMed] [Google Scholar]
- 4.Stahle J, Terins J. Paroxysmal positional nystagmus; an electronystagmographic and clinical study. Ann Otol Rhinol Laryngol 1965;74:69–83. [DOI] [PubMed] [Google Scholar]
- 5.Baloh RW, Jacobson K, Honrubia V. Horizontal semicircular canal variant of benign positional vertigo. Neurology 1993;43:2542–9. [DOI] [PubMed] [Google Scholar]
- 6.Lee SH, Kim MK, Cho KH, Kim JS. Reversal of initial positioning nystagmus in benign paroxysmal positional vertigo involving the horizontal canal. Ann N Y Acad Sci 2009;1:406–8. [DOI] [PubMed] [Google Scholar]
- 7.Ogawa Y Ichimura A Otsuka K, et al. Spontaneous inversion of nystagmus without a positional change in the horizontal canal variant of benign paroxysmal positional vertigo. J Vestib Res 2015;25(3–4):169–75. [DOI] [PubMed] [Google Scholar]
- 8.Choi SY, Lee MJ, Oh EH, Choi JH, Choi KD. Short-term central adaptation in benign paroxysmal positional vertigo. Front Neurol 2020;11:260. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Lempert T. Horizontal benign positional vertigo. Neurology 1994;44:2213–4. [DOI] [PubMed] [Google Scholar]
- 10.Hilton M, Pinder D. The Epley (canalith repositioning) maneuver for benign paroxysmal positional vertigo. Cochrane Database Syst Rev 2004;(2):CD003162. [DOI] [PubMed] [Google Scholar]
- 11.Choi JY Jung I Jung JM, et al. Characteristics and mechanism of perverted head-shaking nystagmus in central lesions: Video-oculography analysis. Clin Neurophysiol 2016;127:2973–8. [DOI] [PubMed] [Google Scholar]
- 12.Jeong KH, Shin JE, Shin DH, Kim CH. Direction-reversing nystagmus in horizontal and posterior semicircular canal canalolithiasis. Otol Neurotol 2016;37:767–71. [DOI] [PubMed] [Google Scholar]
- 13.Jongkees LB. J. R. Ewald. Arch Otolaryngol 1966;83:615–9. [PubMed] [Google Scholar]
- 14.Pagnini P, Nuti D, Vannucchi P. Benign paroxysmal vertigo of the horizontal canal. ORL J Otorhinolaryngol Relat Spec 1989;51:161–70. [DOI] [PubMed] [Google Scholar]
- 15.Katsarkas A, Smith H, Galiana H. Head-shaking nystagmus (HSN): The theoretical explanation and the experimental proof. Acta Otolaryngol 2000;120:177–81. [DOI] [PubMed] [Google Scholar]
- 16.Kim CH, Shin JE, Song CI, Yoo MH, Park HJ. Vertical components of head-shaking nystagmus in vestibular neuritis, Menière's disease and migrainous vertigo. Clin Otolaryngol 2014;39:261–5. [DOI] [PubMed] [Google Scholar]
- 17.Igarashi M, Ishii M, Chae S, Himi T. Second-phase optokinetic after-nystagmus and vestibular compensation. Acta Otolaryngol Suppl 1989;468:145–8. [DOI] [PubMed] [Google Scholar]
- 18.Kumar A, Pieri A, Krol G. Rebound caloric nystagmus. Laryngoscope 1993;103(11 Pt 1):1205–13. [DOI] [PubMed] [Google Scholar]
- 19.Furman JM, Koizuka I, Schor RH. Characteristics of secondary phase post-rotatory nystagmus following off-vertical axis rotation in humans. J Vestib Res 2000;10:143–50. [PubMed] [Google Scholar]
- 20.Jareonsettasin P Otero-Millan J Ward BK, et al. Multiple time courses of vestibular set-point adaptation revealed by sustained magnetic field stimulation of the labyrinth. Curr Biol 2016;26:1359–66. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Roberts DC Marcelli V Gillen JS, et al. MRI magnetic field stimulates rotational sensors of the brain. Curr Biol 2011;21:1635–40. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Ward BK, Roberts DC, Otero-Millan J, Zee DS. A decade of magnetic vestibular stimulation: From serendipity to physics to the clinic. J Neurophysiol 2019;121:2013–9. [DOI] [PubMed] [Google Scholar]
- 23.Zee DS, Jareonsettasin P, Leigh RJ. Ocular stability and set-point adaptation. Philos Trans R Soc Lond B Biol Sci 2017;372:20160199. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Ward BK Otero-Millan J Jareonsettasin P, et al. Magnetic vestibular stimulation (MVS) as a technique for understanding the normal and diseased labyrinth. Front Neurol 2017;8:122. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Wu Y Song N Ling X, et al. Canal switch in benign paroxysmal positional vertigo: Clinical characteristics and possible mechanisms. Front Neurol 2022;13:1049828. [DOI] [PMC free article] [PubMed] [Google Scholar]