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NeuroRehabilitation 44 (2019) 379–388 379

DOI:10.3233/NRE-182642
IOS Press

Misperception of the subjective visual


vertical in neurological patients with
or without stroke: A meta-analysis
Francisco Molinaa , Rafael Lomas-Vegaa,∗ , Esteban Obrero-Gaitána , Alma Rusb ,
Daniel Rodrı́guez Almagroa and Rafael del-Pino-Casadoc
a Department of Health Science, University of Jaén, Paraje Las Lagunillas s/n, Jaén, Spain
b Department of Cell Biology, University of Granada, Campus Fuentenueva, Granada, Spain
c Department of Nursing, University of Jaén, Paraje Las Lagunillas s/n, Jaén, Spain

Abstract.
BACKGROUND: 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.

Keywords: Stroke, neurological disorders, gravity perception, subjective visual vertical, balance

1. Introduction gies course with a myriad of symptoms and signs that


generate a great disability in patients, the main goal of
The Global Burden Diseases (GBD) assessment neurorehabilitation is to increase the independence of
in 2016 largely attributed increases in the number of the subjects with neurological diseases. To reach this
years lived with disability (YLDs) with neurological goal, the rehabilitation protocols pay special attention
disorders such as stroke, Alzheimer’s disease, Parkin- to the gait pattern and balance.
son’s disease, migraine, and multiple sclerosis (GBD Some of the most frequent symptoms experienced
2015 Disease and Injury Incidence and Prevalence by neurological patients are difficulty maintaining
Collaborators, 2016). Because neurological patholo- correct posture and absence of an adequate body
∗ Address
balance (Gor-Garcı́a-Fogeda, Cano-de-la-Cuerda,
for correspondence: Rafael Lomas Vega, PhD,
Carratala-Tejada, Alguacil-Diego, & Molina-Rueda,
Department of Health Sciences (Building B3-205), University of
Jaén, Campus Las Lagunillas s/n, 23071 Jaén, Spain. Tel.: +34 2016). Scientific literature suggests that the visual
953 212918; Fax: +34 953 211875; E-mail: rlomas@ujaen.es. information is essential for maintaining a correct

ISSN 1053-8135/19/$35.00 © 2019 – IOS Press and the authors. All rights reserved
380 F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke

standing balance (Venhovens, Meulstee, Bloem, & 2. Materials and methods


Verhagen, 2016). The visual verticality emerges as
a key concept to understand how the brain creates 2.1. Sources
the perception of the body verticality and then of
the body balance. The visual verticality is the abil- The MOOSE statement was used to perform the
ity of the brain to judge if something is aligned with present review and its report. Relevant literature up
the true vertical (gravity line). To keep an adequate to October 2017 was searched in PubMed, SciELO,
standing balance under normal conditions, the brain and Scopus databases and in the reference lists of the
creates a virtual map of the position of the body in retrieved full-text articles and other reviews. A sen-
a concrete environment. In this scenario, the visual sitive search was carried out in PubMed using the
cues, together with the information sent from the following strategy search: (SVV[tiab] OR verticality
extraocular muscles (EOM) (Guerraz & Bronstein, perception[tiab] OR subjective visual vertical[tiab]
2008), the musculoskeletal proprioceptors and the OR visual vertical[tiab]) AND (Nervous System Dis-
vestibular organs (Chetana & Jayesh, 2015; Lopez, eases[mh]OR stroke[mh] OR stroke[tiab] OR Brain
Lacour, Ahmadi, Magnan, & Borel, 2007), gener- Diseases[mh] OR Brain diseases[tiab]). The search
ate the sense of verticality. Several brain diseases, in Scopus and SciELO databases was performed
such as stroke, may damage one or more areas of the using the terms “subjective visual vertical”, “nervous
visual and vestibular central nervous system (CNS) system diseases” and “stroke”. No language or pub-
that are involved in the sense of verticality. This lication date restrictions were set. The search was
damage may lead to a miscalculation of both the performed by two independent investigators (F.M.O.
body and environment verticality, thereby promoting and R.L.V.).
loss of balance (Baier, Suchan, Karnath, & Dieterich,
2012). 2.2. Study selection
The most commonly used method to estimate
the visual verticality is the subjective visual verti- The inclusion criteria were 1) observational stud-
cal (SVV) test. The SVV test is a validated method to ies as cross-sectional, case-control and cohort studies
determine the ability of the subject to evaluate if a rod 2) that analyze the ability of the neurological patients
is aligned with the real vertical position (gravity line), to estimate the SVV 3) in a standing or upright sitting
without any external visual reference (Tesio, Longo, position and 4) in comparison with healthy sub-
& Rota, 2011). Healthy subjects can align a line with jects. Two independent reviewers (F.M. and E.O.G.)
an error less than 2.5º from the vertical (Piscielli & revised and selected the studies. The discrepant stud-
Perennou, 2017). Deviations in the SVV have been ies were re-evaluated by each reviewer, and the
related to risk of falling in patients with multiple scle- disagreements were resolved by consensus discus-
rosis (da Fonseca, et al., 2016) and are used to analyze sion.
vestibular dysfunction in patients with Parkinson’s
disease (Venhovens, et al., 2016). 2.3. Data extraction and synthesis
Several studies have compared SVV values
between neurological patients and healthy subjects Two independent reviewers (F.M. and E.O.G.)
showing controversial results, probably due to the compiled the characteristics of the participants and
variety of procedure protocols used and the own the intervention outcomes of each trial using a stan-
characteristics of the participants. To the best of our dardized data-collection form. Mean and standard
knowledge, there are no meta-analyses analyzing the deviation of the SVV values were extracted from
ability of neurological patients to estimate the SVV both the non-exposed group (healthy subjects) and
in comparison to healthy subjects nor any investigat- the exposed group (patients with neurological disor-
ing possible differences among patients with different ders). We only analyzed the SVV values obtained
neurological conditions. Therefore, the aim of the when the body and the head of the participant
present systematic review and meta-analysis is to were in upright position (not tilted or rolled). The
analyze, for the first time, the visual perception of data from clinical trials were extracted at baseline.
the verticality in neurological patients in compar- Other characteristics of the study population were
ison with healthy controls as well as the eventual also collected, including type of neurological lesion
differences among patients suffering from different (vascular/non-vascular), localization of the lesion
neurological pathologies. (brain/brainstem-medulla/mixed), time of progres-
F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke 381

sion (weeks from the damage), protocol for SVV inconsistency (I2 ) of Higgins et al., 2011. Publication
measurement (SVV Upstanding/SVV Sitting/Rod bias was assessed by the funnel plot, and the pooled
and Frame), presence/absence of hemispatial neglect, effect was estimated (taking into account any possible
and presence/absence of stroke. Disagreements publication bias) by the Trim and Fill method (Duval
between reviewers were solved by consensus. The & Tweedie, 2000). Sensitivity analyses were con-
pooled effect was calculated as standardized mean ducted to assess the contribution of the studies to the
difference (SMD). pooled estimate in the meta-analysis (leave-one-out
method) (Cooper et al., 2009). The Newcastle-Ottawa
2.4. Analyses Scale (NOS) was used to assess the quality of the
Analyses were performed using the Com- studies included in the meta-analysis.
prehensive Meta-analysis 3.3.070. Following the
recommendations of Cooper et al., 2009, the random- 3. Results
effects model was used for estimating the pooled
effects and their 95% confidence interval (CI) to The 31 studies included in the present meta-
improve the generalization of the study findings to analysis were comprised of 54 samples with 54
any exposed or non-exposed subject. The Q test independent comparisons. The study selection pro-
was used for performing the heterogeneity analysis, cess is summarized in the PRISMA flow chart
which was completed by calculating the degree of (Fig. 1). The total number of participants was 1,916

Fig. 1. PRISMA flow diagram of the selection process of studies.


382 F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke

Table 1
Characteristics of the studies included in the meta-analysis
Samples N Location Vascular Stroke
Anastasopoulus et al. 1999 1 38 Mixed Yes Yes
Asai et al. 2009 1 33 Brain Yes No
Barnett-Cowan et al. 2010 2 44 Brain No No
Barra et al. 2010 1 50 Brain Yes Yes
Blomsterwall et al. 2011 1 26 Brain No No
Bonan et al. 2006a 2 70 Brain Yes Yes
Bonan et al. 2006b 1 53 Brain Yes Yes
Bonan et al. 2007 1 48 Brain Yes Yes
Braem et al. 2014 2 32 Brain Yes Yes
Chandrakumar et al. 2010 1 35 Mixed Yes Yes
Crevits et al. 2007 1 47 Brain Yes No
Crevits et al. 2012 1 143 Brain Yes No
Frisen et al. 2010 4 201 Brain No No
Funk et al. 2010 3 48 Brain Yes Yes
Funk et al. 2011 3 72 Brain Yes Yes
Ishikura et al. 1999 1 28 Brain Yes Yes
Johannsen et al. 2006 2 35 Brain Yes Yes
Khattab et al. 2012 1 94 Brain No No
Mansfield et al. 2015 2 34 Mixed Yes Yes
Pereira et al. 2014 1 90 Brain No No
Pérennou et al. 2008 4 275 Brain / Mixed Yes Yes
Pinar et al. 2005 1 33 Brain Yes No
Saj et al. 2005 3 34 Brain Yes Yes
Saj et al. 2006 2 28 Brain Yes Yes
Saj et al. 2012 4 89 Brain Yes Yes
Scocco et al. 2014 1 27 Brain No No
Snowdown et al. 2005 1 21 Brain Yes Yes
Tarnutzer et al. 2008 1 20 Brain No No
Tarnutzer et al. 2011 1 22 Mixed No No
Utz et al. 2011 2 66 Brain Yes Yes
Yelnik et al. 2002 2 80 Brain Yes Yes
Abbreviations: N: sample size; Mixed: Several regions of the Central Nervous System.

(mean per sample: 35.5). Table 1 summarizes the (Anastasopoulos, Bronstein, Haslwanter, Fetter, &
main characteristics of the studies. In 48 of the 54 Dichgans, 1999; Chandrakumar, Blakeman, Goltz,
samples, the neurological lesions were located in the Sharpe, & Wong, 2011; Mansfield, et al., 2015; Peren-
brain (Asai, et al., 2009; Barnet-Cowan, et al., 2010; nou, et al., 2008; Tarnutzer, Shaikh, Palla, Straumann,
Barra, et al., 2010; Blomsterwall, Frisén, & Wikkelso, & Marti, 2011), included mixed lesions (brain and
2011; Bonan, Derighetti, Guellez-Leman, BradaÏ, & brainstem-medulla). Concerning the origin of the
Yelnik, 2006; Bonan, Guettard, Leman, Colle, & lesions, vascular injuries were analyzed in 42 sam-
Yelnik, 2006; Bonan, et al., 2007; Braem, Honore, ples (Asai et al., 2009; Barra et al., 2010; Bonan et al.,
Rousseaux, Saj, & Coello, 2014; Crevits, Vanacker, 2006; Bonan et al., 2006; Bonan et al., 2007; Braem
& Verraes, 2012; Crevits, Venhovens, Vanoutrive, et al., 2014; Crevits et al., 2012; Crevits et al., 2007;
& Debruyne, 2007; Frisén, 2010; Funk, Finke, Funk et al., 2011; Funk et al., 2010; Ishikura, 1999;
Muller, Utz, & Kerkhoff, 2011; Funk, Finke, Muller, Johannsen et al., 2006; Pinar et al., 2005; Saj et al.,
Utz, & Kerkhoff, 2010; Ishikura, 1999; Johannsen, 2012; Saj et al., 2005; Saj et al., (2006); Snowdon
Fruhmann-Berger, & Karnath, 2006; Khattab, et al., & Scott, 2005; Utz et al., 2011; Yelnik et al., 2002;
2012; Pereira, Kanashiro, Maia, & Barbosa, 2014; Anastosopoulos et al., 1999; Chandrakumar et al.,
Pinar, Ardic, Topuz, & Kara, 2005; Saj, Honore, 2011; Mansfield et al., 2015; Perennou et al., 2008).
Bernati, & Rousseaux, 2012; Saj, Honore, Coello, The most common neurological disorder was stroke
& Rousseaux, 2005; Saj, Honore, & Rousseaux, (38 samples) (Barra et al., 2010; Bonan et al., 2006;
2006; Scocco, Wagner, Racosta, Chade, & Gershanik, Bonan et al., 2006; Bonan et al., 2007; Braem et al.,
2014; Snowdon & Scott, 2005; Tarnutzer, Marti, & 2014; Funk et al., 2011; Funk et al., 2010; Ishikura,
Straumann, 2008; Utz, et al., 2011; Yelnik, et al., 1999; Johannsen et al., 2006; Saj et al., 2012; Saj
2002). The other 6 samples, obtained from 5 studies et al., 2005; Saj et al., (2006); Snowdon & Scott, 2005;
F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke 383

Table 2 plot showing the results of the studies is displayed in


Newcastle-Ottawa Scale (NOS) for assessing the quality of the Fig. 2. The funnel plot (Fig. 3) was clearly asymmetri-
studies included in the meta-analysis
cal, suggesting a publication bias that was confirmed
S1 S2 S3 S4 C1 E1 E2 E3 Total by the Egger’s test (p = 0.00003). However, the SMD
Anastasopoulus et al. 1999 – – – – – – – – 0
value corrected by the Trim and Fill test varied by
Asai et al. 2009 – – – – ** – – * 3 9.5% (SMD = 1.15). The sensitivity analysis, per-
Barnett-Cowan et al. 2010 – – * * – – – * 3 formed by eliminating one study each time, showed
Barra et al. 2010 – * – – * * – * 4 SMD values between 0.98 (6.1% variation) and 1.07
Blomsterwall et al. 2011 – * – – – * – – 2 (1.9% variation).
Bonan et al. 2006a * – – – – * – * 3 When the meta-regression was performed using
Bonan et al. 2006b * – – – ** * – * 5 the “presence of stroke” as the moderating vari-
Bonan et al. 2007 * – – – * * – * 4 able, the model explained 18% of the heterogeneity.
Braem et al. 2014 * – – * – * – * 4 The scatterplots of the meta-regression are shown
Chandrakumar et al 2010 * – – * * * – * 5
in Fig. 4. The variable “type of SVV measurement”
Crevits et al. 2007 – – – – ** – – * 3
(SVV Upstanding, SVV Sitting, and Rod and Frame)
Crevits et al. 2012 – – – * – – – * 2
Frisen et al. 2010 * – * – – * * – 4
did not explain any percentage of the heterogeneity
Funk et al. 2010 * – – – ** * – * 5 (p = 0.42).
Funk et al. 2011 * – – – ** * – * 5 When the subgroups were analyzed according to
Ishikura et al. 1999 – – – * – – – * 2 the moderating variable (presence or absence of
Johannsen et al. 2006 * * – * – * – * 5 stroke), the SMD was significantly higher in the
Khattab et al. 2012 – – * * ** – – * 5 “stroke” subgroup than in the “non-stroke” sub-
Mansfield et al. 2015 * – * * * * – * 6 group (Table 3). The heterogeneity was low in the
Pereira et al. 2014 – – – * ** – – * 4 “non-stroke” subgroup, while it was moderate in the
Pérennou et al. 2008 * * – – ** * – * 6 “stroke” group. Regarding the publication bias, the
Pinar et al. 2005 – * – * – – – * 3
funnel plot of the “stroke” subgroup (Fig. 5) was
Saj et al. 2005 * – – – – * – * 3
clearly asymmetrical, and the result of the Egger test
Saj et al. 2006 * – – – ** * – * 5
Saj et al. 2012 * – – – ** * – * 5
confirmed the risk of publication bias. The Trim and
Scocco et al. 2014 – – * – ** – – * 4 Fill test showed a higher SMD value (1.45), which
Snowdown et al. 2005 * – * – * * – * 5 means a slight correction (7.4%) in respect to the orig-
Tarnutzer et al. 2008 – – – – * – – * 2 inal SMD value. The funnel plot of the “non-stroke”
Tarnutzer et al. 2011 * – – – * * – – 3 subgroup was somewhat asymmetrical (Fig. 6). The
Utz et al. 2011 * – – – * * – * 3 results of the Egger test ruled out the risk of publica-
Yelnik et al. 2002 * * – – * * – * 5 tion bias, and the Trim and Fill test showed a lower
Each study can be awarded a maximum of one star for each num- SMD value (0.45), which is a small correction (6.3%)
bered item within the Selection (S) and Exposure (E) categories. in respect to the initial SMD value.
A maximum of two stars can be given for Comparability (C).
S1: Adequate case definition; S2: Representativeness of the cases;
S3: Selection of controls; S4: Definition of controls; C1: Com-
parability of cases and controls; E1: Ascertainment of Exposure;
4. Discussion
E2: Same method of ascertainment for cases and controls; E3:
Non-Response rate. Several neurological diseases may alter the
processing of exteroceptive and proprioceptive infor-
mation, leading to blindness, hearing loss or
Utz et al., 2011; Yelnik et al., 2002; Anastosopoulos hemispatial neglect, due to neurological damage in
et al., 1999; Chandrakumar et al., 2011; Mansfield some CNS areas. One of the most frequently associ-
et al., 2015; Perennou et al., 2008) and the mean age ated symptoms in neurological patients is difficulty
of the participants ranged from 45 to 75 years old. keeping a stable standing position or a proper gait
The quality of the studies, assessed by the NOS, was pattern. To maintain correct vertical body posture,
low to moderate (Table 2). the CNS uses vestibular, proprioceptive and visual
The mean deviation of the SVV from the true ver- information. Such information, provided by several
tical was higher in the exposed subjects, showing receptors, must be congruent. When information
an SMD of 1.05 (95% CI: 0.81, 1.28) and a low from the vestibular and/or musculoskeletal organs
to moderate heterogeneity (I2 = 38.9 %). The forest is altered or disabled (due to neural damage), visual
384 F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke

Fig. 2. Forest plot for subjective visual vertical deviation from the true vertical (effect sizes are expressed as standardized mean difference).

cues play a critical role in determining the vertical- Our main finding is that patients with neurologi-
ity of the environment and of the subject. The SVV cal diseases misestimated the SVV in comparison to
test is widely used to estimate the visual perception healthy subjects. Such deviation from the true vertical
of verticality in neurological patients. However, the in neurological patients suggests that neural damage
scientific literature shows controversial results on the may cause a visual deficient interpretation of the ver-
perception of the verticality in these patients. ticality, leading to a misalignment of the head and
F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke 385

Fig. 3. Funnel Plot. Fig. 5. Funnel Plot of the “stroke” subgroup.

Fig. 4. Scatterplots.
Fig. 6. Funnel Plot of the “non-stroke” subgroup.
of the body axis (Perennou et al., 2008; Barra, et al.,
2008). This abnormal body position may trigger sev- perception of the verticality to improve their balance
eral additional symptoms and co-morbidities as a (Cohen, 2013).
higher risk of falling (de Groot, et al., 2014). Along Our data also showed that stroke patients mis-
this line, recent studies have reported that the SVV perceived the SVV to a greater extent than patients
deviation detected in subjects with multiple sclero- suffering from other neurological disorders, suggest-
sis (da Fonseca et al., 2016) and Parkinson’s disease ing that stroke patients may be at higher risk of falls
(Pereira et al., 2014) is correlated with a higher risk (Cho & Lee, 2013) than patients with other neuro-
of falling. logical pathologies due to a greater misperception of
As stated above, the sense of verticality is the result the verticality (Baggio, et al., 2016). However, fur-
of the function of several CNS areas distributed over ther research is needed to confirm this hypothesis
the brainstem, brain and cerebellum, among others. before proposing the determination of the SVV as
Consequently, an injury in one or more of these areas a predictor of the risk of falling in stroke patients.
may alter the perception of the verticality. Our results The differences found in the SVV estimation between
have shown that all the neurological patients failed stroke and non-stroke patients may be explained by
to estimate the SVV in comparison with the healthy considering the temporary phase of the neurologi-
controls and that the most frequently damaged area in cal damage. The majority of stroke patients were
these patients was the brain, supporting the hypoth- recruited during the acute or sub-acute phase of the
esis that any CNS damage may alter the perception disease (<6 months) in most of the studies included
of the verticality. Therefore, patients with any neu- in the present review. In contrast, the non-stroke
rological condition should be retrained in the visual patients suffered from chronic neurological condi-
386 F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke

Table 3
Subgroup analysis
k N Point Lower Upper I2 Egger Trim and
estimate Limit Limit test Fill
(SMD) (p value) (% of variation)
“Stroke” subgroup 38 1136 1.35 1.02 1.68 33.7 % 0.0007 7.4 %
“Non-stroke” subgroup 16 780 0.48 0.29 0.68 10.4 % 0.39 6.3 %
Abbreviations: k: number of studies; N: total sample size; SMD: Standardised Mean Difference.

tions (hydrocephalus, multiple sclerosis, Parkinson’s on the visual perception of the verticality (Lucertini
disease, migraine), i.e., with a longer time of dis- et al., 2011).
ease progression. In this sense, it is well established The present systematic review and meta-analysis
that the CNS may mitigate the severity of the initial has some limitations. Some of the studies found dur-
symptoms of a neural injury due to the neuroplasticity ing the searching process were not included in this
phenomena. Thus, adaptive or compensatory mech- meta-analysis for not expressing the SVV data of the
anisms have been widely described in patients with control group in numerical values. On the other hand,
vestibular disorders (Hubner, Khan, & Migliaccio, the disease features were not always available, which
2017; Martin-Saez, et al., 2017). Stroke also triggers limited the scope of the findings of this review. More-
the neuroplasticity process, improving the SVV esti- over, there was great variability in the protocols used
mation at 3 months from the lesion (Lucertini, De by the selected studies for determining the SVV. For
Angelis, Martelli, Zolesi, & Tomao, 2011). However, future research, we recommend a standardization of
meta-regression using the moderating variable “time the SVV protocol following the recommendations
of progression” did not explain a significant percent- of Piscicelli et al., 2016, to obtain a reliable tool
age of the variability, probably because only 24 of for determining the misperception of the verticality
the 46 comparisons analyzed indicated the time of in patients with different pathologies. Correlations
disease progression. On the other hand, stroke fre- among the SVV, time of disease progression and risk
quently occurs in the middle cerebral artery area and of falling should be investigated in stroke patients.
may cause acute and focal damage to balance and In summary, this study is the first meta-analysis
eye-control-related brain areas (eg: insula, temporal that investigates the visual perception of the verti-
and parietal lobe, middle frontal gyrus) (Yeo, Jang, & cality in neurological patients. The findings of the
Kwon, 2017), while the other neurological diseases present systematic review evidence that the visual
usually cause diffuse damage. In addition, the major- perception of the verticality, determined using the
ity of the studies analyzed recruited patients with right SVV test, is altered in patients with neurological dis-
hemisphere stroke, which could explain our results eases. The neurological pathology that most alters
since right hemispheric lesions are associated with the SVV is stroke. Although we did not find any
poorer recovery of the verticality perception than left difference when determining the SVV using diverse
hemispheric lesions (Bonan, Leman, Legargasson, experimental procedures, a standardized protocol
Guichard, & Yelnik, 2006). should be established and used in future research to
Our results did not show any effect of the type simplify the comparison of the results from different
of protocol used for determining the SVV, suggest- studies. The time of progression of neurological dis-
ing that there are no difference when estimating the eases should also be considered in future studies to
SVV in an upright position versus a sitting position. determine the real effect of the neuroplasticity pro-
This is an interesting result because it contradicts cess on the recovery/retrain of the visual perception
the hypothesis of some researchers that lower limb of the verticality. Further research is needed to con-
proprioception may be decisive in determining the firm the effectiveness of the SVV determination as a
verticality perception of body and head (Barbieri, prognosis method for recovery and risk of falling in
et al., 2008; Vaugoyeau, Hakam, & Azulay, 2011) stroke patients.
and, consequently, the visual perception of the verti-
cality. However, our results suggest that lower limb
proprioceptive information does not influence the Conflict of interest
verticality perception. In agree with our results, other
authors failed to find any implication of body posture The authors declare no conflict of interest.
F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke 387

References Cohen, A. H. (2013). Vision rehabilitation for visual-vestibular


dysfunction: The role of the neuro-optometrist. NeuroReha-
bilitation, 32(3), 483-92. doi:10.3233/NRE-130871
Anastasopoulos, D., Bronstein, A., Haslwanter, T., Fetter, M., &
Cooper, H., Hedges, L. V., & Valentine, J. C. (2009). The handbook
Dichgans, J. (1999). The role of somatosensory input for the
of research synthesis and meta-analysis 2nd edition. In The
perception of verticality. Ann N Y Acad Sci, 871, 379-383.
Hand. of Res. Synthesis and Meta-Analysis, 2nd Ed. (pp. 1-
Asai, M., Aoki, M., Hayashi, H., Yamada, N., Mizuta, K.,
615). Russell Sage Foundation.
& Ito, Y. (2009). Subclinical deviation of the subjec-
Crevits, L., Vanacker, L., & Verraes, A. (2012). Patients
tive visual vertical in patients affected by a primary
with migraine correctly estimate the visual ver-
headache. Acta Oto-Laryngologica, 129(1), 30-35. doi:
ticality. Clin Neurol Neurosurg, 114(4), 313-315.
10.1080/00016480802032785
doi:10.1016/j.clineuro.2011.10.025
Baggio, J. A., Mazin, S. S., Alessio-Alves, F. F., Barros, C. G.,
Crevits, L., Venhovens, J., Vanoutrive, J., & Debruyne, J. (2007).
Carneiro, A. A., Leite, J. P.,...& Santos-Pontelli, T. E. (2016).
False perception of visual verticality in multiple sclerosis. Eur
Verticality perceptions associate with postural control and
J Neurol, 14(2), 228-232. doi:ENE1636
functionality in stroke patients. PloS One, 11(3), e0150754.
Chandrakumar, M., Blakeman, A., Goltz, H. C., Sharpe,
doi:10.1371/journal.pone.015075
J. A., & Wong, A. M. (2011). Static ocular counter-
Baier, B., Suchan, J., Karnath, H. O., & Dieterich, M. (2012) Neu-
roll reflex in skew deviation. Neurology, 77(7), 638-644.
ral correlates of disturbed perception of verticality. Neurology,
doi:10.1212/WNL.0b013e3182299f71
78(10), 728-735. doi:10.1212/WNL.0b013e318248e544
Chetana, N., & Jayesh, R. (2015). Subjective visual vertical
Barbieri, G., Gissot, A. S., Fouque, F., Casillas, J. M., Pozzo,
in various vestibular disorders by using a simple bucket
T., & Perennou, D. (2008). Does proprioception contribute
test. Indian J Otolaryngol Head Neck Surg, 67(2), 180-184.
to the sense of verticality? Exp Brain Res, 185(4), 545-552.
doi:10.1007/s12070-014-0760-0
doi:10.1007/s00221-007-1177-8
Cho, K., & Lee, G. (2013). Impaired dynamic balance is associated
Barnett-Cowan, M., Dyde, R. T., Fox, S. H., Moro, E., Hutchison,
with falling in post-stroke patients. Tohoku J Exp Med, 230(4),
W. D., & Harris, L. R. (2010). Multisensory determinants of
233-239. doi:DN/JST.JSTAGE/tjem/230.233
orientation perception in parkinson’s disease. Neuroscience,
da Fonseca, B. A., Pereira, C. B., Jorge, F., Simm, R.,
167(4), 1138-1150. doi:10.1016/j.neuroscience.2010.02.065
Apostolos-Pereira, & S., Callegaro, D. (2016). A dis-
Barra, J., Benaim, C., Chauvineau, V., Ohlmann, T., Gresty,
turbed processing of graviceptive pathways may be involved
M., & Perennou, D. (2008). Are rotations in per-
in the pathophysiology of balance disorders in patients
ceived visual vertical and body axis after stroke caused
with multiple sclerosis. Arq Neuropsiquiatr, 74(2), 106-111.
by the same mechanism? Stroke, 39(11), 3099-3101.
doi:10.1590/0004-282X20160004
doi:10.1161/STROKEAHA.108.515247 [doi]
de Groot, M. H., van der Jagt-Willems, H. C., van Campen, J. P.,
Barra, J., Marquer, A., Joassin, R., Reymond, C., Metge, L., Chau-
Lems, W. F., Beijnen, J. H., & Lamoth, C. J. (2014). A flexed
vineau, V., & Perennou, D. (2010). Humans use internal models
posture in elderly patients is associated with impairments in
to construct and update a sense of verticality. Brain, 133(Pt 12),
postural control during walking. Gait Posture, 39(2), 767-772.
3552-3563. doi:10.1093/brain/awq311
doi:10.1016/j.gaitpost.2013.10.015
Blomsterwall, E., Frisén, L., & Wikkelsö, C. (2011). Postural
Duval, S., & Tweedie, R. (2000). Trim and fill: A simple funnel-
function and subjective eye level in patients with idiopathic
plot-based method of testing and adjusting for publication bias
normal pressure hydrocephalus. J Neurol, 258(7), 1341-1346.
in meta-analysis. Biometrics, 56(2), 455-463.
doi:10.1007/s00415-011-5943-y
Frisén, L. (2010). Deviations of the visual upright in three dimen-
Bonan, I. V., Leman, M. C., Legargasson, J. F., Guichard, J. P.,
sions in disorders of the brainstem: A clinical exploration.
& Yelnik, A. P. (2006). Evolution of subjective visual vertical
Brain, 133(12), 3541-3551. doi:10.1093/brain/awq241
perturbation after stroke. Neurorehabil Neural Repair, 20(4),
Funk, J., Finke, K., Muller, H. J., Utz, K. S., & Kerkhoff, G. (2011).
484-491. doi:20/4/484
Visual context modulates the subjective vertical in neglect:
Bonan, I., Derighetti, F., Gellez-Leman, M.C., BradaÏ, N., & Yel-
Evidence for an increased rod-and-frame-effect. Neuroscience,
nik, A. (2006). Visual dependence after recent stroke. Annales
173, 124-134. doi:10.1016/j.neuroscience.2010.10.067
de readaptation et de medecine physique, 49(4), 166-171.
Funk, J., Finke, K., Müller, H. J., Utz, K. S., & Kerkhoff, G. (2010).
Doi:10.1016/j.annrmp.2006.01.010
Effects of lateral head inclination on multimodal spatial ori-
Bonan, I. V., Guettard, E., Leman, M. C., Colle, F. M., & Yelnik,
entation judgments in neglect: Evidence for impaired spatial
A. P. (2006). Subjective visual vertical perception relates to
orientation constancy. Neuropsychologia, 48(6), 1616-1627.
balance in acute stroke. Arch Phys Med Rehabil, 87(5), 642-
doi:10.1016/j.neuropsychologia.2010.01.029
646. doi:10.1016/j.apmr.2006.01.019
GBD 2015 Disease and Injury Incidence and Prevalence Col-
Bonan, I. V., Hubeaux, K., Gellez-Leman, M. C., Guichard, J.
laborators. (2016). Global, regional, and national incidence,
P., Vicaut, E., & Yelnik, A. P. (2007). Influence of sub-
prevalence, and years lived with disability for 310 diseases
jective visual vertical misperception on balance recovery
and injuries, 1990-2015: A systematic analysis for the global
after stroke. J Neurol Neurosurg Psychiatry, 78(1), 49-55.
burden of disease study 2015. Lancet (London, England), 388
doi:10.1136/jnnp.2006.087791
(10053), 1545-1602. doi:S0140-6736(16)31678-6.
Braem, B., Honore, J., Rousseaux, M., Saj, A., & Coello, Y.
Gor-Garcia-Fogeda, M. D., Cano de la Cuerda, R., Carratala
(2014). Integration of visual and haptic informations in the
Tejada, M., Alguacil-Diego, I. M., & Molina-Rueda, F. (2016).
perception of the vertical in young and old healthy adults and
Observational gait assessments in people with neurological dis-
right brain-damaged patients. Clin Neurophysiol, 44(1), 41-48.
orders: A systematic review. Arch Phys Med, 97(1), 131-140.
doi:10.1016/j.neucli.2013.10.137
doi:10.1016/j.apmr.2015.07.018
388 F. Molina et al. / Misperception of the subjective visual vertical in neurological patients with or without stroke

Guerraz, M., & Bronstein, A. M. (2008). Ocular versus extraocular approaches and suggestions for standardization. Ann Phys
control of posture and equilibrium. Neurophysiol Clin, 38(6), Rehabil Med, 60(3), 208-216. doi:S1877-0657(16)00042-7
391-398. doi:10.1016/j.neucli.2008.09.007 Piscicelli, C., Barra, J., Sibille, B., Bourdillon, C., Guer-
Higgins, J. P., Altman, D. G., Gotzsche, P. C., Juni, P., Moher, D., raz, M., & Perennou, D. A. (2016). Maintaining trunk
Oxman, A. D.,... Cochrane Statistical Methods Group. (2011). and head upright optimizes visual vertical measurement
The cochrane collaboration’s tool for assessing risk of bias in after stroke. Neurorehabil Neural Repair, 30(1), 9-18.
randomised trials. BMJ (Clinical Research Ed.), 343, d5928. doi:10.1177/1545968315583722
doi:10.1136/bmj.d5928 Saj, A., Honore, J., & Rousseaux, M. (2006). Perception of
Hubner, P. P., Khan, S. I., & Migliaccio, A. A. (2017). the vertical in patients with right hemispheric lesion: Effect
The mammalian efferent vestibular system plays a crucial of galvanic vestibular stimulation. Neuropsychologia, 44(8),
role in vestibulo-ocular reflex compensation after unilat- 1509-1512. doi:S0028-3932(05)00382-9
eral labyrinthectomy. J Neurophysiol, 117(4), 1553-1568. Saj, A., Honore, J., Bernati, T., & Rousseaux, M. (2012). Influence
doi:10.1152/jn.01049.2015 of spatial neglect, hemianopia and hemispace on the subjective
Ishikura, K. (1999). Relations between biased tonicity of vertical. Eur Neurol, 68(4), 240-246. doi:10.1159/000339266
the body and vertical judgement in poststroke hemi- Saj, A., Honore, J., Coello, Y., & Rousseaux, M. (2005). The visual
plegic persons. Percept Mot Skills, 88(3 Pt 1), 952-956. vertical in the pusher syndrome: Influence of hemispace and
doi:10.2466/pms.1999.88.3.952 body position. J Neurol, 252(8), 885-891. doi:10.1007/s00415-
Johannsen, L., Fruhmann Berger, M., & Karnath, H. O. (2006). 005-0716-0
Subjective visual vertical (SVV) determined in a representative Scocco, D. H., Wagner, J. N., Racosta, J., Chade, A., &
sample of 15 patients with pusher syndrome. J Neurol, 253(10), Gershanik, O. S. (2014). Subjective visual vertical in
1367-1369. doi:10.1007/s00415-006-0216-x pisa syndrome. Parkinsonism Relat Disord, 20(8), 878-883.
Khattab, A., Docherty, S., Bagust, J., Willington, R., Thomas, P., doi:10.1016/j.parkreldis.2014.04.030
& Amar, K. (2012). Subjective visual vertical perception and Snowdon, N., & Scott, O. (2005). Perception of vertical and pos-
sense of smell in parkinson disease. J Rehabi Res Dev, 49(6), tural control following stroke: A clinical study. Physiotherapy,
961-969. 91(3), 165-170. doi:10.1016/j.physio.2004.11.008
Lopez, C., Lacour, M., Ahmadi, A. E., Magnan, J., & Borel, L. Tarnutzer, A. A., Marti, S., & Straumann, D. (2008). Gravity per-
(2007). Changes of visual vertical perception: A long-term sign ception in cerebellar patients. Prog Brain Res, 171, 369-372.
of unilateral and bilateral vestibular loss. Neuropsychologia, doi:10.1016/S0079-6123(08)00654-7
45(9), 2025-2037. doi:S0028-3932(07)00063-2 Tarnutzer, A. A., Shaikh, A. G., Palla, A., Straumann, D., &
Lucertini, M., De Angelis, C., Martelli, M., Zolesi, V., & Tomao, Marti, S. (2011). Vestibulo-cerebellar disease impairs the cen-
E. (2011). Subjective visual vertical in erect/supine sub- tral representation of self-orientation. Front Neurol, 2, 11.
jects and under microgravity: Effects of lower body negative doi:10.3389/fneur.2011.00011
pressure. Eur Arch Otorhinolaryngol, 268(7), 1067-1075. Tesio, L., Longo, S., & Rota, V. (2011). The subjective visual
doi:10.1007/s00405-011-1493-2 vertical: Validation of a simple test. Int J Rehabil Res, 34(4),
Mansfield, A., Fraser, L., Rajachandrakumar, R., Danells, 307-315. doi:10.1097/MRR.0b013e32834c45bc
C. J., Knorr, S., & Campos, J. (2015). Is perception Utz, K. S., Keller, I., Artinger, F., Stumpf, O., Funk, J., & Kerkhoff,
of vertical impaired in individuals with chronic stroke G. (2011). Multimodal and multispatial deficits of verticality
with a history of ‘pushing’? Neurosci Let, 590, 172-177. perception in hemispatial neglect. Neuroscience, 188, 68-79.
doi:10.1016/j.neulet.2015.02.007 doi:10.1016/j.neuroscience.2011.04.068
Martin-Sanz, E., Rueda, A., Esteban-Sanchez, J., Yanes, J., Vaugoyeau, M., Hakam, H., & Azulay, J. P. (2011). Pro-
Rey-Martinez, J., & Sanz-Fernandez, R. (2017). Vestibular prioceptive impairment and postural orientation control
restoration and adaptation in vestibular neuritis and ramsay in parkinson’s disease. Hum Mov Sci, 30(2), 405-414.
hunt syndrome with vertigo. Otol Neurotol, 38(7), e203-e208. doi:10.1016/j.humov.2010.10.006
doi:10.1097/MAO.0000000000001468 Venhovens, J., Meulstee, J., Bloem, B. R., & Verhagen, W.
Pereira, C. B., Kanashiro, A. K., Maia, F. M., & Barbosa, E. R. I. (2016). Neurovestibular analysis and falls in parkinson’s
(2014). Correlation of impaired subjective visual vertical and disease and atypical parkinsonism. Eur J Neurosci, 43(12),
postural instability in parkinson’s disease. J Neurol Sci, 346(1- 1636-1646. doi:10.1111/ejn.13253
2), 60-65. doi:10.1016/j.jns.2014.07.057 Yelnik, A. P., Lebreton, F. O., Bonan, I. V., Colle, F. M., Meurin,
Perennou, D. A., Mazibrada, G., Chauvineau, V., Greenwood, R., F. A., Guichard, J. P., & Vicaut, E. (2002). Perception of ver-
Rothwell, J., Gresty, M. A., & Bronstein, A. M. (2008). Lat- ticality after recent cerebral hemispheric stroke. Stroke, 33(9),
eropulsion, pushing and verticality perception in hemisphere 2247-2253.
stroke: A causal relationship? Brain : A Journal of Neurology, Yeo, S. S., Jang, S. H., & Kwon, J. W. (2017). Central vestibu-
131(Pt 9), 2401-2413. doi:10.1093/brain/awn170 lar disorder due to ischemic injury on the parieto-insular
Pinar, H. S., Ardic, F. N., Topuz, B., & Kara, C. O. (2005). Subjec- vestibular cortex in patients with middle cerebral artery terri-
tive visual vertical and subjective visual horizontal measures in tory infarction: Observational study. Medicine, 96(51), e9349.
patients with chronic dizziness. J Otolaryngol, 34(2), 121-125. doi:10.1097/MD.0000000000009349
Piscicelli, C., & Perennou, D. (2017). Visual verticality per-
ception after stroke: A systematic review of methodological

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