The interpretation of the verticality of the environment is crucial for a proper body balance. The subjective visual vertical test (SVV) is a widely used method to determine the visual perception of the verticality, whose alteration has been related with poor functional status.
OBJECTIVE:
To analyze the visual perception of the verticality in neurological patients in comparison with healthy controls.
METHODS:
We searched PubMed, Scopus, and Scielo from the start of the databases until October 2017 and manually searched the reference lists of studies comparing SVV values between neurological patients and controls. Standardized mean difference (SMD) and subgroup analysis were used to analyze differences between neurological patients and healthy subjects and between stroke and non-stroke patients, respectively.
RESULTS:
A total of 1,916 subjects from 31 studies were included. Neurological patients misestimate the true vertical in comparison with controls (SMD = 1.05; 95% CI: 0.81, 1.28). The misperception of the verticality was higher in stroke patients (SMD = 1.35; 95% CI: 1.02, 1.68) than in patients with other neurological conditions (SMD = 0.48; 95% CI: 0.29, 0.68).
CONCLUSIONS:
Neurological patients showed a misperception of the verticality, estimated using the SVV. The neurological pathology that most alters the SVV is stroke.
Anastasopoulos,D., Bronstein,A., Haslwanter,T., Fetter,M., Dichgans,J. (1999). The role of somatosensory input for the perception of verticality, Ann N Y Acad Sci871, 379–383.
2.
Asai,M., Aoki,M., Hayashi,H., Yamada,N., Mizuta,K., Ito,Y. (2009). Subclinical deviation of the subjective visual vertical in patients affected by a primary headache, Acta Oto-Laryngologica129(1), 30–35. doi: 10.1080/00016480802032785
3.
Baggio,J. A., Mazin,S. S., Alessio-Alves,F. F., Barros,C. G., Carneiro,A. A., Leite,J. P., ... Santos-PontelliT. E. (2016). Verticality perceptions associate with postural control and functionality in stroke patients, PloS One11(3), e0150754. doi: 10.1371/journal.pone.015075
4.
Baier,B., Suchan,J., Karnath,H. O., Dieterich,M. (2012). Neural correlates of disturbed perception of verticality, Neurology78(10), 728–735. doi: 10.1212/WNL.0b013e318248e544
5.
Barbieri,G., Gissot,A. S., Fouque,F., Casillas,J. M., Pozzo,T., Perennou,D. (2008). Does proprioception contribute to the sense of verticality?Exp Brain Res185(4), 545–552. doi: 10.1007/s00221-007-1177-8
6.
Barnett-Cowan,M., Dyde,R. T., Fox,S. H., Moro,E., Hutchison,W. D., Harris,L. R. (2010). Multisensory determinants of orientation perception in parkinson’s disease, Neuroscience167(4), 1138–1150. doi: 10.1016/j.neuroscience.2010.02.065
7.
Barra,J., Benaim,C., Chauvineau,V., Ohlmann,T., Gresty,M., Perennou,D. (2008). Are rotations in perceived visual vertical and body axis after stroke caused by the same mechanism?Stroke39(11), 3099–3101. doi: 10.1161/STROKEAHA.108.515247 [doi]
8.
Barra,J., Marquer,A., Joassin,R., Reymond,C., Metge,L., Chauvineau,V., Perennou,D. (2010). Humans use internal models to construct and update a sense of verticality, Brain133(Pt 12), 3552–3563. doi: 10.1093/brain/awq311
9.
Blomsterwall,E., Frisén,L., Wikkelsö,C. (2011). Postural function and subjective eye level in patients with idiopathic normal pressure hydrocephalus, J Neurol258(7), 1341–1346. doi: 10.1007/s00415-011-5943-y
10.
Bonan,I. V., Leman,M. C., Legargasson,J. F., Guichard,J. P., Yelnik,A. P. (2006). Evolution of subjective visual vertical perturbation after stroke, Neurorehabil Neural Repair20(4), 484–491. doi:20/4/484
11.
Bonan,I., Derighetti,F., Gellez-Leman,M.C., BradaÏ,N., Yelnik,A. (2006). Visual dependence after recent stroke, Annales de readaptation et de medecine physique49(4), 166–171. doi: 10.1016/j.annrm2006.01.010
12.
Bonan,I. V., Guettard,E., Leman,M. C., Colle,F. M., Yelnik,A. P. (2006). Subjective visual vertical perception relates to balance in acute stroke, Arch Phys Med Rehabil87(5), 642–646. doi: 10.1016/j.apmr.2006.01.019
13.
Bonan,I. V., Hubeaux,K., Gellez-Leman,M. C., Guichard,J. P., Vicaut,E., Yelnik,A. P. (2007). Influence of subjective visual vertical misperception on balance recovery after stroke, J Neurol Neurosurg Psychiatry78(1), 49–55. doi: 10.1136/jnn2006.087791
14.
Braem,B., Honore,J., Rousseaux,M., Saj,A., Coello,Y. (2014). Integration of visual and haptic informations in the perception of the vertical in young and old healthy adults and right brain-damaged patients, Clin Neurophysiol44(1), 41–48. doi: 10.1016/j.neucli.2013.10.137
15.
Cohen,A. H. (2013). Vision rehabilitation for visual-vestibular dysfunction: The role of the neuro-optometrist, NeuroRehabilitation32(3), 483–92. doi: 10.3233/NRE-130871
16.
Cooper,H., Hedges,L. V., Valentine,J. C. (2009). The handbook of research synthesis and meta-analysis 2nd edition, In The Hand. of Res. Synthesis and Meta-Analysis, 2nd Ed (pp. 1–615). Russell Sage Foundation.
17.
Crevits,L., Vanacker,L., Verraes,A. (2012). Patients with migraine correctly estimate the visual verticality, Clin Neurol Neurosurg114(4), 313–315. doi: 10.1016/j.clineuro.2011.10.025
18.
Crevits,L., Venhovens,J., Vanoutrive,J., Debruyne,J. (2007). False perception of visual verticality in multiple sclerosis, Eur J Neurol14(2), 228–232. doi: ENE1636
19.
Chandrakumar,M., Blakeman,A., Goltz,H. C., Sharpe,J. A., Wong,A. M. (2011). Static ocular counterroll reflex in skew deviation, Neurology77(7), 638–644. doi: 10.1212/WNL.0b013e3182299f71
20.
Chetana,N., Jayesh,R. (2015). Subjective visual vertical in various vestibular disorders by using a simple bucket test, Indian J Otolaryngol Head Neck Surg67(2), 180–184. doi: 10.1007/s12070-014-0760-0
21.
Cho,K., Lee,G. (2013). Impaired dynamic balance is associated with falling in post-stroke patients, Tohoku J Exp Med230(4), 233–239. doi: DN/JST.JSTAGE/tjem/230.233
22.
da Fonseca,B. A., Pereira,C. B., Jorge,F., Simm,R., Apostolos-Pereira,S., Callegaro,D. (2016). A disturbed processing of graviceptive pathways may be involved in the pathophysiology of balance disorders in patients with multiple sclerosis, Arq Neuropsiquiatr74(2), 106–111. doi: 10.1590/0004-282X20160004
23.
de Groot,M. H., van der Jagt-Willems,H. C., van Campen,J. P., Lems,W. F., Beijnen,J. H., Lamoth,C. J. (2014). A flexed posture in elderly patients is associated with impairments in postural control during walking, Gait Posture39(2), 767–772. doi: 10.1016/j.gaitpost.2013.10.015
24.
Duval,S., Tweedie,R. (2000). Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis, Biometrics56(2), 455–463.
25.
Frisén,L. (2010). Deviations of the visual upright in three dimensions in disorders of the brainstem: A clinical exploration, Brain133(12), 3541–3551. doi: 10.1093/brain/awq241
26.
Funk,J., Finke,K., Muller,H. J., Utz,K. S., Kerkhoff,G. (2011). Visual context modulates the subjective vertical in neglect: Evidence for an increased rod-and-frame-effect, Neuroscience173, 124–134. doi: 10.1016/j.neuroscience.2010.10.067
27.
Funk,J., Finke,K., Müller,H. J., Utz,K. S., Kerkhoff,G. (2010). Effects of lateral head inclination on multimodal spatial orientation judgments in neglect: Evidence for impaired spatial orientation constancy, Neuropsychologia48(6), 1616–1627. doi: 10.1016/j.neuropsychologia.2010.01.029
28.
GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. (2016). Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990-2015: A systematic analysis for the global burden of disease study 2015, Lancet (London, England),388(10053), 1545–1602. doi: S0140-6736(16)31678-6
29.
Gor-Garcia-Fogeda,M. D., Cano de la Cuerda,R., Carratala Tejada,M., Alguacil-Diego,I. M., Molina-Rueda,F. (2016). Observational gait assessments in people with neurological disorders: A systematic review, Arch Phys Med97(1), 131–140. doi: 10.1016/j.apmr.2015.07.018
30.
Guerraz,M., Bronstein,A. M. (2008). Ocular versus extraocular control of posture and equilibrium, Neurophysiol Clin38(6), 391–398. doi: 10.1016/j.neucli.2008.09.007
31.
Higgins,J. P., Altman,D. G., Gotzsche,P. C., Juni,P., Moher,D., Oxman,A. D., ... Cochrane Statistical Methods Group. (2011). The cochrane collaboration’s tool for assessing risk of bias in randomised trials, BMJ (Clinical Research Ed.)343, d5928. doi: 10.1136/bmj.d5928
32.
Hubner,P. P., Khan,S. I., Migliaccio,A. A. (2017). The mammalian efferent vestibular system plays a crucial role in vestibulo-ocular reflex compensation after unilateral labyrinthectomy, J Neurophysiol117(4), 1553–1568. doi: 10.1152/jn.01049.2015
33.
Ishikura,K. (1999). Relations between biased tonicity of the body and vertical judgement in poststroke hemiplegic persons, Percept Mot Skills88(3 Pt 1), 952–956. doi: 10.2466/pms.1999.88.3.952
34.
Johannsen,L., Fruhmann Berger,M., Karnath,H. O. (2006). Subjective visual vertical (SVV) determined in a representative sample of 15 patients with pusher syndrome, J Neurol253(10), 1367–1369. doi: 10.1007/s00415-006-0216-x
35.
Khattab,A., Docherty,S., Bagust,J., Willington,R., Thomas,P., Amar,K. (2012). Subjective visual vertical perception and sense of smell in parkinson disease, J Rehabi Res Dev49(6), 961–969.
36.
Lopez,C., Lacour,M., Ahmadi,A. E., Magnan,J., Borel,L. (2007). Changes of visual vertical perception: A long-term sign of unilateral and bilateral vestibular loss, Neuropsychologia45(9), 2025–2037. doi: S0028-3932(07)00063-2
37.
Lucertini,M., De Angelis,C., Martelli,M., Zolesi,V., Tomao,E. (2011). Subjective visual vertical in erect/supine subjects and under microgravity: Effects of lower body negative pressure, Eur Arch Otorhinolaryngol268(7), 1067–1075. doi: 10.1007/s00405-011-1493-2
38.
Mansfield,A., Fraser,L., Rajachandrakumar,R., Danells,C. J., Knorr,S., Campos,J. (2015). Is perception of vertical impaired in individuals with chronic stroke with a history of ‘pushing’?Neurosci Let590, 172–177. doi: 10.1016/j.neulet.2015.02.007
39.
Martin-Sanz,E., Rueda,A., Esteban-Sanchez,J., Yanes,J., Rey-Martinez,J., Sanz-Fernandez,R. (2017). Vestibular restoration and adaptation in vestibular neuritis and ramsay hunt syndrome with vertigo, Otol Neurotol38(7), e203–e208. doi: 10.1097/MAO.0000000000001468
40.
Pereira,C. B., Kanashiro,A. K., Maia,F. M., Barbosa,E. R. (2014). Correlation of impaired subjective visual vertical and postural instability in parkinson’s disease, J Neurol Sci346(1-2), 60–65. doi: 10.1016/j.jns.2014.07.057
41.
Perennou,D. A., Mazibrada,G., Chauvineau,V., Greenwood,R., Rothwell,J., Gresty,M. A., Bronstein,A. M. (2008). Lateropulsion, pushing and verticality perception in hemisphere stroke: A causal relationship?Brain: A Journal of Neurology131(Pt 9), 2401–2413. doi: 10.1093/brain/awn170
42.
Pinar,H. S., Ardic,F. N., Topuz,B., Kara,C. O. (2005). Subjective visual vertical and subjective visual horizontal measures in patients with chronic dizziness, J Otolaryngol34(2), 121–125.
43.
Piscicelli,C., Perennou,D. (2017). Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization, Ann Phys Rehabil Med60(3), 208–216. doi: S1877-0657(16)00042-7
44.
Piscicelli,C., Barra,J., Sibille,B., Bourdillon,C., Guerraz,M., Perennou,D. A. (2016). Maintaining trunk and head upright optimizes visual vertical measurement after stroke, Neurorehabil Neural Repair30(1), 9–18. doi: 10.1177/1545968315583722
45.
Saj,A., Honore,J., Rousseaux,M. (2006). Perception of the vertical in patients with right hemispheric lesion: Effect of galvanic vestibular stimulation, Neuropsychologia44(8), 1509–1512. doi: S0028-3932(05)00382-9
46.
Saj,A., Honore,J., Bernati,T., Rousseaux,M. (2012). Influence of spatial neglect, hemianopia and hemispace on the subjective vertical, Eur Neurol68(4), 240–246. doi: 10.1159/000339266
47.
Saj,A., Honore,J., Coello,Y., Rousseaux,M. (2005). The visual vertical in the pusher syndrome: Influence of hemispace and body position, J Neurol252(8), 885–891. doi: 10.1007/s00415-005-0716-0
Snowdon,N., Scott,O. (2005). Perception of vertical and postural control following stroke: A clinical study, Physiotherapy91(3), 165–170. doi: 10.1016/j.physio.2004.11.008
50.
Tarnutzer,A. A., Marti,S., Straumann,D. (2008). Gravity perception in cerebellar patients, Prog Brain Res171, 369–372. doi: 10.1016/S0079-6123(08)00654-7
51.
Tarnutzer,A. A., Shaikh,A. G., Palla,A., Straumann,D., Marti,S. (2011). Vestibulo-cerebellar disease impairs the central representation of self-orientation, Front Neurol2, 11. doi: 10.3389/fneur.2011.00011
52.
Tesio,L., Longo,S., Rota,V. (2011). The subjective visual vertical: Validation of a simple test, Int J Rehabil Res34(4), 307–315. doi: 10.1097/MRR.0b013e32834c45bc
53.
Utz,K. S., Keller,I., Artinger,F., Stumpf,O., Funk,J., Kerkhoff,G. (2011). Multimodal and multispatial deficits of verticality perception in hemispatial neglect, Neuroscience188, 68–79. doi: 10.1016/j.neuroscience.2011.04.068
54.
Vaugoyeau,M., Hakam,H., Azulay,J. P. (2011). Proprioceptive impairment and postural orientation control in parkinson’s disease, Hum Mov Sci30(2), 405–414. doi: 10.1016/j.humov.2010.10.006
55.
Venhovens,J., Meulstee,J., Bloem,B. R., Verhagen,W. I. (2016). Neurovestibular analysis and falls in parkinson’s disease and atypical parkinsonism, Eur J Neurosci43(12), 1636–1646. doi: 10.1111/ejn.13253
56.
Yelnik,A. P., Lebreton,F. O., Bonan,I. V., Colle,F. M., Meurin,F. A., Guichard,J. P., Vicaut,E. (2002). Perception of verticality after recent cerebral hemispheric stroke, Stroke33(9), 2247–2253.
57.
Yeo,S. S., Jang,S. H., Kwon,J. W. (2017). Central vestibular disorder due to ischemic injury on the parieto-insular vestibular cortex in patients with middle cerebral artery territory infarction: Observational study. e, Medicine96(51), 9349. doi: 10.1097/MD.0000000000009349
