Perception of Verticality After Recent Cerebral Hemispheric Stroke

Subjects

The patients included had recently experienced their first and only cerebral hemispheric stroke, resulting at least in initial motor and balance impairment. The time since stroke was not longer than 3 months (13 weeks). Patients were excluded if they had perturbed vigilance, a history of neurological disturbances, vertigo or vestibular dysfunction, amblyopia or diplopia, or severe aphasia. Before testing, we performed a complete neurological examination in which the following were evaluated: motricity, using the Collin and Wade scale¹⁸; visual field, assessed at the bedside and confirmed by Goldmann campimetry when hemianopia was suspected; visuospatial neglect, using Albert’s test¹⁹ and Bergego’s scale, ²⁰ a test assessing daily behavior during meals, washing, and ambulation; balance, as estimated by the Postural Assessment Scale for Stroke²¹; and functional independence, according to the Functional Independence Measure.²²

Forty consecutive patients were studied (Table 1), 20 with a right hemispheric lesion (RHL) and 20 with a left hemispheric lesion (LHL). The stroke was hemorrhagic in 11 patients and ischemic in 29. Among the ischemic lesions, posterior cerebral artery territory was never involved. Anterior cerebral artery territory was affected in 1 case, anterior choroidal artery territory in 7 cases (it was the only territory affected in 3), and middle cerebral artery territory in 28. Age, sex, etiology, and time since stroke did not differ in RHL and LHL patients. All patients suffered from hemiplegia. A visual field defect was observed in 6 RHL and 3 LHL patients. Visuospatial neglect, considered to be present when Albert’s test was different from zero or Bergego’s score exceeded 2, was noted in 13 RHL and 3 LHL patients. Visuospatial neglect and a visual field defect were associated in all 6 RHL patients and 2 of the 3 LHL patients.

The control group was composed of 20 healthy subjects, 9 men and 11 women, with a mean age of 42.9±5.8 years.

Procedure

The experiment was performed in a dark room with the subjects sitting in a wheelchair or normal chair. A 30-cm-long luminous rod was placed directly in front of each one at a distance of 2 meters. Subjects were asked to adjust the rod to the vertical position by manipulating a box held in the healthy hand, with 2 switches easily handled by the thumb; there was no time limit. As in previous studies, SVV was assessed with binocular and monocular vision.^7,14,16⇓⇓ The head was not fixed but freely held upright. The manipulation of vestibular and somatosensory input by tilting the head affects the SVV in a way that, as already explained, depends on the angle of the tilt.^6–8⇓⇓ We therefore assessed SVV with the head tilted to observe the possible effects of this sensory stimulation. The investigator stood behind the patient, with 1 hand on the patient’s head, to help her or him to sustain a tilt of approximately 20°. Two series of measurements were made in all cases: for the first, the rod was initially tilted 60° to the left of the vertical objective, and the patient had to adjust it with a clockwise movement; for the second, the rod was initially tilted 60° to the right of the vertical objective for a counterclockwise adjustment. The measures were then repeated with the head in the upright, right-tilted, and left-tilted positions, and after each positioning, the observer read the deviation in degrees (clockwise deviation, +; counterclockwise deviation, −). The relatively few trials conducted were chosen to avoid distortion of the results due to fatigue, since patients were deliberately examined in a subacute stage after stroke. The following data were analyzed: mean SVV (V value) for the clockwise and counterclockwise measurements in each position, and the range of uncertainty (U value), defined as the maximum difference between the clockwise and counterclockwise adjustments. Because the binocular and monocular V and U values with the head held upright were not different for controls and hemiplegic patients, the data were combined and recorded as V_upright and U_upright. With the head tilted, SVV was only measured with binocular vision. Therefore, V_upright and U_upright refer to upright head data, V_{right tilt} and U_{right tilt} refer to rightward-tilted head data, and V_{left tilt} and U_{left tilt} refer to leftward-tilted head data.

Identification of Site of Lesion

The site of the lesion was determined on CT scans to explore possible correlations between the abnormalities recorded and particular lesion sites. CT scans were done with a Picker unit, with a slice thickness of 4 mm up to the midbrain and 8 mm more rostrally. The stereotaxic baseline was used according to the Duvernoy atlas.²³ If the imaging plane was not parallel to the anterior/posterior commissure plane, we attempted to optimize the localization of the projected lesion. Anatomic lesions were noted, with particular attention focused on the recognized regions of interest in the vestibular cortex. These regions are the parietoinsular vestibular cortex and areas 2v, 3a, and 7, as described by Brandt et al.¹⁶ The parietoinsular vestibular cortex lies deep in the posterior part of the insula, area 2v is located at the tip of the interparietal sulcus, area 3a at the anterior bank of the central sulcus, and area 7 at the inferior parietal cortex. The main cerebral areas involved are given in Table 2.

Statistical Analysis

Since the distribution of the variables studied was nongaussian, data were summarized by median, interquartile distance (IQD), and extreme values. Comparisons were made by distribution-free tests, ie, the Mann-Whitney and Wilcoxon tests for unpaired and paired groups, respectively. All tests were 2-sided; significance level was adjusted with the use of the Bonferroni procedure according to the number of comparisons made for each hypothesis tested. Thus, because 4 comparisons were made to analyze the possible changes of deviation or uncertainty from the upright position, the significance level was fixed at P=0.0125 for these types of comparisons. Because 3 comparisons between groups were made for each position, the significance level was fixed at P=0.0166 for these types of comparisons. All tests were done with the use of StatXact from Cytel Software.

Controls

For the controls, no significant difference was observed between binocular, right eye, and left eye vision (0.2° [IQD 1.1°], 0.2° [IQD 0.8°], and 0° [IQD 0.9°], respectively). The median tilt of the SVV with the head upright (V_upright) was 0.35° (Table 3). Maximal individual deviations were 2.9° on the left and 2.2° on the right. Consequently, the results for each patient were considered different from control values when the deviation exceeded 3° for V_upright, which was clearly larger than the deviation for the controls, and similar to the normal range previously reported.¹⁴ The median range of uncertainty for U_upright was 1.9° (IQD 1.3°), and the maximum intraindividual difference was 6°. Therefore, for U_upright, 8° was considered significantly abnormal. With the head tilted, the E effect was observed: thus, the SVV setting was significantly tilted to the opposite side, and V_{right tilt} and V_{left tilt} were −2° and 1.2°, respectively. Differences between V_{right tilt} and V_upright reached the adjusted significance level (P=0.0048) but not those between V_{left tilt} and V_upright (P=0.023). The ranges of uncertainty for U_{right tilt} and U_{left tilt} did not differ from U_upright.

Patients

As in the controls, no significant difference was observed between binocular or monocular vision (Table 3).

Right Hemispheric Lesions

Values outside the normal range were recorded for 13 of 20 RHL patients (65%): this was the case for both V_upright and U_upright in 5 patients, for V_upright in 3, and for U_upright in 5. SVV was significantly tilted toward the side contralateral to the lesion (P<0.007 for V_upright). Of greater interest was the range of uncertainty, which was dramatically higher in patients than controls (P<0.001 for U_upright, P=0.05 for U_{right tilt}, and P<0.001 for U_{left tilt}). Seven patients were very disturbed by the initial position of the rod and were unable to adjust it to the vertical: thus, U_upright reached 47.5° for 1 of them and 44°, 25.4°, 22.5°, 13°, 12.7°, and 9.7° for the 6 others. As in the controls, the E effect was observed when the head was tilted toward the side opposite to the lesion, ie, for right-side lesions, the leftward tilt of the head tended to compensate for the leftward shift of the SVV: V_{left tilt} differed significantly from V_upright (P<0.003). There was no difference between the ranges of uncertainty U_{left tilt} and U_upright. But with the head tilted rightward, no change in V_{right tilt} or U_{right tilt} was observed in relation to the upright position, and there was apparently no E effect.

Left Hemispheric Lesions

Values outside the normal range were recorded for 10 of 20 LHL patients (50%); this was the case for both V_upright and U_upright in 2 patients, for V_upright in 6, and for U_upright in 2. SVV was significantly tilted toward the side contralateral to the lesion (P=0.001 for V_upright). The range of uncertainty was wider than for the controls, for U_upright (P<0.001) and U_{right tilt} (P=0.002). Head tilts tended to produce the same effect in LHL as RHL patients; as in the controls, the E effect was observed when the head was tilted toward the side opposite to the lesion, ie, for left-side lesions, the rightward tilt of the head tended to compensate for the rightward shift of the SVV: V_{right tilt} differed, but not significantly, from V_upright. There was no difference between the ranges of uncertainty U_{right tilt} and U_upright. But with the head tilted leftward, no change in V_{left tilt} or U_{left tilt} was observed in relation to the upright position, and again the E effect was apparently absent.

Differences Between Right and Left Hemispheric Lesions

The apparent difference between V_upright values in the RHL and LHL groups (SVV was tilted to the left for RHL patients and to the right for LHL patients) was not a real difference when expressed in absolute values. The range of uncertainty, U_upright, was wider in RHL than LHL patients (median, 7.6° versus 4.7°), but the difference did not reach significance. U_upright was >8° for 10 RHL patients (mean, 20.3°) but for only 4 LHL patients (mean, 16.9°). U_upright was >20° for 4 RHL patients and 1 LHL patient and >10° for 7 RHL and 3 LHL patients.

Role of Visual Field Defect

Statistical analysis showed that a visual field defect had no effect on V_upright or U_upright, irrespective of the side of the lesion. Nevertheless, among RHL patients, V_upright tended to be greater when visual field defect was present, and U_upright was >8 for 5 of the 6 patients with visual field defect compared with 5 of the 14 patients without visual field defect. Note that all the RHL patients with visual field defect and all but 1 of the LHL patients with visual field defect also had visuospatial neglect.

Role of Visuospatial Neglect

When all 40 patients were considered together, visuospatial neglect was strongly correlated with low V_upright and U_upright values (P=0.002 and P=0.003, respectively). The effect of visuospatial neglect seemed to be the same whichever the side of the lesion, but no statistical analysis could be conducted separately for LHL patients with visuospatial neglect because they were so few. None of the 16 patients with visuospatial neglect had a normal SVV setting. Two RHL and 4 LHL patients without visuospatial neglect exhibited a tilt of the SVV, but it was always mild, as V_upright was <7 and U_upright was <16.

Role of Site of Lesion

The frontal lobule was affected by the stroke in 12 patients; the lesion was localized in the frontal areas alone in only 2 of these patients, who did not exhibit an abnormal SVV setting; the remaining 10 had large lesions of the middle cerebral artery, and only 2 of them had normal data. The thalamus was involved in only 2 patients, 1 of them with perturbed SVV, especially for the range of uncertainty (44°) and the values for both the leftward- and rightward-tilted head positions (V_{right tilt}= −24°; V_{left tilt}=+16.9°). Lenticular nuclei were affected by the lesion in 24 patients; 7 of them had an isolated lenticular lesion, 2 had abnormal SVV with the head upright and tilted, and 2 others only had abnormal SVV with the head tilted. The internal capsule was affected in 18 patients, 5 of whom had an isolated lesion and 2 of whom had slightly perturbed SVV. The occipital cortex was never affected. The vestibular cortex was affected in 12 patients, who included 7 RHL and 5 LHL patients. None of the lesions was limited to the vestibular cortex. The deviation of the SVV was not significantly different when the vestibular cortex was involved and when it was not (V_upright=3.0° and 2.3°, respectively), and the same applied to the range of uncertainty (U_upright=8.3° and 4.7°, respectively). This was because strong perturbations were also observed in some patients with lesions at other sites. In fact, the vestibular cortex was only involved in 6 of the 11 patients with strong perturbations for the range of uncertainty (U >10). The other lesion sites were the lenticular nuclei in 3 patients and the thalamus and internal capsule in 1 patient each.