VISUAL AND TACTILE ROD BISECTION IN UNILATERAL NEGLECT Haukur Hjaltason, Gorei Caneman and Richard Tegnt!r (Department of Neurology, Karolinska Hospital, Stockholm)
Unilateral spatial neglect is usually examined in the visual modality with tasks such as line bisection, various cancellation tasks, and figure copying. The modality-specific nature of neglect has been srressed by some authors and neglect has been attributed to defective oculomotor mechanisms (Kinsboume, 1970; Chedru, 1976). The occurrence of neglect in other modalities is therefore of relevance. Tactile neglect has attracted particular interest, but results from different studies conflict. Right-brain-damaged (RBD) patients with visual field defect (VFD) showed neglect for left hemispace when searching for a marble in a tactile maze hidden behind a curtain (De Renzi, Faglioni and Scotti, 1970). Caneman, Levander and Tegner (1992) reached a similar conclusion, while Villardita (1987) unexpectedly found that RBD patients with VFD actually preferred to explore left hemispace. Weintraub and Mesulam (1987) had subjects manually locate a bead fixed on a board and found that RBD patients had longer search times in left hemispace than in right. Chedru (1976) designed a test suitable for presentation in equivalent tactile and visual versions. Subjects were required, with and without blindfold, to tap the keys all over a Teletype keyboard as quickly as possible. RBD patients with VFD showed no impairment in tapping the left-sided keys when vision was precluded, while they preferred the right-sided keys with visual control. The test was later improved with increased searching demands, but then RBD patients with visual neglect preferred the right-sided keys both with and without visual control, although this ipsilateral preference was significantly less marked under the tactile condition (Gentilini, Barbieri, De Renzi et aI., 1989). Line bisection is a welh~stablished, highly sensitive neglect test seemingly suitable for comparison between tactile and visual modalities. In a recent study, RBD patients with visual neglect made large rightward errors in the visual task, while they did not differ from normal controls in the tactile task (Fujii, Fukatsu, Kimura et aI., 1991). These authors had, however, failed to control for differences in task demand between the conditions which we have tried to do in the present study. Cortex, (1993) 29, 583 c 588
H. Hjaltason, G. Caneman and R. Tegner
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MATERIAL AND METHODS
Patients
The study comprised 16 RBD patients with unilateral neglect, 10 RBD patients without neglect, 10 left-brain-damaged (LBD) patients without neglect, and 10 controls with spinal or peripheral nerve disorders. The patient groups will be referred to as RBD +, RBD - , and LBD -, respectively. Clinical data for patients with neglect are summarized in Table I. All patients had unilateral lesions due to cerebrovascular events. They were all right-handed. Motor and somatosensory impairment, and visual field defects were assessed using a standard procedure (Bisiach, Vallar, Perani et ai., 1986). The presence of neglect was determined by a line cancellation test (Albert, 1973) or a random letter cancellation test (Weintraub and Mesulam, 1987), figure copying (Gainotti, D'Erme, Monteleone et ai., 1986), and a reading task. The figure copying task uses a drawing with a house in the middle flanked by two trees on each side. Severity of neglect was rated as '+' if objects of the left side of the drawing were omitted, '+ +' if the entire left half of the drawing was ommitted, and as , + + +' if objects on the right half were also omitted. Neglect dyslexia was tested with 10 sentences of four words each; the number of sentences with left-sided omissions is shown in Table I. Mean age of the groups were (mean±SD): RBD+ 61.6±15.7 years, RBD- 67.9±8.4 years, LBD- 64.3±11.7 years, and controls 58.8±17.6 years. The brain-damaged patients were examined at a time after stroke when they were alert and cooperative. The interval between stroke and examination did not differ significantly between the groups (KruskalWallis test): RBD+ 18.2±20.48 days, RBD- 12.6±17.33 days, and LBD- 14.6±14.18 days (mean±SD). Tests and Procedure
Each stimulus consisted of a semi-circular plastic rod mounted on a 122 X 348 mm piece of cardboard. The rods were 10 mm in diameter and had lengths of 200 and 400 mm. The stimulus card was horizontally aligned directly in front of the subject at a distance of about
TABLE I
Age, Sex and Clinical Data of RBD Patients with Unilateral Neglect
Case
1 2 3 4 5 6 7 8 9 10 11
12 13 14 15 16
Age/Sex
94, 69, 60, 52, 74, 78, 66, 70, 45, 62, 50, 54, 74, 67, 80, 64,
M M M F F M M F M F F M M M M F
Lesion site and duration poststroke
VFD
PO, 10 d TO, T*, 14 d FTD, 16 d P, 17 d PD, D*, 57 d P,P*,79d POD, 21 d PTD, 5 d P, 9 d P, D*, 11 d P, 7 d P, D*, 18 d P, D*, 8 d P, 9 d D, 8 d P, P*, 2 d
+ + + + + + + + + + + +
P
S
+ + + + + + + + + + + + + + +
+ + + + + + + + + + + + + + +
FC
CA
R
NA
22/40 26/40
10/10 NA NA 7110 6/10
+
+ +++ +++ +++ +++ +++ +++ ++ ++ +++ ++ + +
11160
13/40 26/40 25/40 25/40 9/40 24/40 3/40 25/40 34/40 1/40 31/40 14/60 10/40
3110
NA NA
9110
4/10 9/10 NA NA 0/10 0110 9/10
F = frontal; P = parietal; T = temporal; 0 = occipital; D = deep; VFD = visual field defect; P = paresis; S = sensory loss; FC = figure copying; CA = number of omissions on line cancellation task (40 targets) or letter cancellation task (60 targets); R = numbers of error on reading test; NA = not available. * old lesion.
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45 cm. All subjects performed the task under three conditions. In the visual condition, subjects merely had to indicate the midpoint of the rod by pointing with their index finger. In the visuo-tactile (no blindfold) and tactile (blindfold) conditions, the task was to indicate the midpoint of the rod by running the index finger along the rod and stopping at the estimated midpoint. The examiner placed the subject's index finger on either the left or the right end of the rod. Each subject completed the three conditions in a Latin square with order of condition as the Latinized variable. There were 24 trials per condition. Within conditions, the two rod lengths occurred 12 times each in fixed random order. The starting point (right, left) was randomized and occurred equally often within the vi suo-tactile and tactile conditions. The task was untimed and there were no limitations on the number of times a subject was allowed to run his finger along the rod. All RBD patients and controls performed the task with their right hand; of the LBD patients, 5· used their left hand and 5 used their right hand. Deviations from objective midpoint were recorded to the nearest centimeter. Since accuracy of measurement is proportional to the square root of the number of replications, resolution within conditions and groups is approximately 0.5-0.6 mm. Positive sign denotes rightward error.
RESULTS
A 2-way ANOVA by Group (N = 4) and Condition (N = 3) was performed. A significant Group X Condition interaction (F = 6.36; d.f. = 6, 176; p
30 mTactile D Visuo-tactile
25 .-.. S S
.-.--s::: 0 ...... ~
~ 0
20
-Visual
15 10 5 0 -5 -10
RBD+
RBD-
LBD-
CONTROLS
Fig. 1 - Line bisection under three experimental conditions. Mean deviations from true midpoint. Positive sign denotes rightward error.
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H. Hjaltason, G. Caneman and R. Tegner
was due to a difference between the visual condition on the one hand and the vi suo-tactile and the tactile conditions on the other hand. The dissociation was supported by subsequent t-tests, where the only significant deviation from objective midpoint was found in the RBD + group for the visual condition. The effect of the starting point was tested with a 3-way ANOV A by Group (N = 4), Condition (N = 2) and Starting Point (N = 2). Only the RBD + group was sensitive to the starting point and made leftward errors with left start and rightward errors with right start (Group X Starting Point, F = 3.92, dJ. = 3, 126; p<0.02). Of relevance in this context is the fact that the Condition X Starting Point interaction was not significant (p>0.20), which means that the difference between right and left start was constant across conditions. In the RBD + group the mean displacements were: in the visuo-tactile condition + 14.4 mm with right start, and - 1.6 mm with left start, and in the tactile condition - 0.2 mm with right start, and - 11.8 mm with left start. DISCUSSION In a previous study, RBD patients with 'neglect were shown to make large rightward errors on a visual line bisection test while they performed normally on a tactile bisection test (Fujii et aI., 1991). As the authors point out, the two tasks differ in requirements such as "head and eye movements and motor programs". The tasks also differ in that only the tactile task demands rod exploration. To make the tasks more 'symmetrical' would require a condition where subjects visually explore the rods prior to bisection, but there is as yet no really satisfactory way to ensure this. One technique is to have subjects identify an object, for example a letter, at one or both ends of the line to bisect. Compared with a no-cue condition left neglect patients were shown to perform worse with a right-end letter and better with a left-end letter (Riddoch and Humphreys, 1983), The drawback is that letter identification does not ensure that the line is actually explored. We tried to overcome the difficulty by introducing a task with tactile rod exploration under visual guidance, and we found that rod exploration markedly reduced visual neglect. The performance was essentially the same in the vi suotactile and the tactile conditions with no significant deviations from objective midpoint. Barnes and Butter (1992) reached a similar conclusion when they compared the performance of left neglect patients on a tactile bisection task and a visual task where the subjects identified a colour at the ends of the line prior to bisection. A possible conclusion is that rod exploration reduces neglect to the point that, even if it had been present in some of our patients, it would not have shown up on the tactile bisection task. However, even if we have shown that rod exploration reduces visual neglect, it does not necessarily follow that it also reduces tactile neglect. An alternative explanation for the lack of neglect in the tactile modality is that our patient selection was biased. Frontal regions have been implicated in mediating an exploratory-motor component of spatial attention (Mesulam, 1981). It is possible
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that tactile rod bisection puts heavier demands on this component than does a visual bisection task. Only one of the RBD + patients in the present study had a frontal lesion, which may explain why we found no evidence of tactile neglect. An unexpected finding was that only RBD patients with neglect were sensitive to the starting point, making errors to the left with left start and to the right with right start. To our knowledge this has not been previously described. It is, however, uncertain if this constitutes a genuine part of the neglect syndrome, since the brain-damaged groups of the current study were not matched for lesion size, and RBD patients with neglect generally tend to have larger lesions (Levine, Warach, Benowitz et aI., 1986). More important in this context is that the difference between left and right start was constant across the conditions and does not confound our comparisons. Fujii et ai. (1991) used the actual midpoint as the starting point. If RBD patients are sensitive also to this starting point, the absolute magnitude of their errors would be reduced, making it more difficult to identify tactile neglect. ABSTRACT
A rod bisection task was performed by 16 RBD patients with visual neglect, 10 RBD and 10 LBD patients without visual neglect, and 10 normal controls. Three different conditions were used: tactile, where they explored the rod blindfolded; visuo-tactile, where they explored the rod manually without blindfold; and visual, where they pointed to the midpoint without prior manual exploration. Only within the RBD group with visual neglect was there a significant difference between the three conditions. These patients made large rightward errors under the visual condition but no significant deviations from actual midpoint under the visuo-tactile or the tactile condition. It is therefore possible that rod exploration, which is an integral part of tactile bisection, reduces neglect to such an extent that it is difficult to identify neglect in the tactile modality on this task. Acknowledgments The research was supported by the Swedish Council for Planning and Coordination of Research (Dnr 890258:2), the Swedish Medical Research Council (Dnr K9019P-093l8-0lA), and by the Swedish Society for Prevention of Stroke. We wish to thank Staffan Ekblom at the Institute of Actuarial Mathematics and Mathematical Statistics of the Univ~rsity of Stockholm for statistical advice, and two anonymous referees for helpful comments. REFERENCES ALBERT, M.L. A simple test of visual neglect. Neurology, Minneapolis, 23: 658-664, 1973. BARNES, L., and BUTTER, C.M. Visual versus tactile neglect in brain damaged patients: Is neglect a multimodal disorder? Poster presented at TENNET III, May 20-22, 1992, Montreal, Canada. BISIACH, E., VALLAR, G., PERANI, D., PAPAGNO, C., and BERTI, A. Unawareness of disease following lesions of the right hemisphere: anosognosia for hemiplegia and anosognosia for hemianopia. Neuropsychologia, 24: 471-482, 1986. CANEMAN, G, LEVANDER, M., and TEGNER R., A tactile maze test in unilateral spatial neglect: the influence of vision and recording technique. Journal of Neurology, 239: 273-276, 1992. CHEDRU, F. Space representation in unilateral spatial neglect. Journal of Neurology, Neurosurgery and Psychiatry,39: 1057-1061, 1976. DE RENzi, E., FAGLIONI, P., and SCOTTI, G. Hemispheric contribution to exploration of space through the visual and tactile modality. Cortex, 6: 191-203, 1970. FUJII, T., FUKATSU, R., KIMURA, I., SAO, S.-I., and KOGURE, K. Unilateral spatial neglect in visual and tactile modalities. Cortex, 27: 339-343, 1991. GAINOTTI, G., D'ERME, P., MONTELEONE, D., and SILVERI, M.C. Mechanisms of unilateral spatial
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neglect in relation to laterality of cerebral lesions. Brain, 109: 599-612, 1986. GENTILINI, M., BARBIERI, C., DE RENZI, E., and FAGLIONI, P. Space exploration with and without the aid of vision in hemisphere-damaged patients. Cortex, 25: 643-651, 1989. KiNSBOURNE, M. A model for the mechanism of unilateral neglect of space. Transactions of the American Neurological Association, 95: 143-146, 1970. LEVINE, D., WARACH, J., BENOWITZ, L., and CALVANIO, R. Left spatial neglect: Effects of lesion size and premorbid brain atrophy on severity and recovery following right cerebral infarction. Neurology, 36: 362-366, 1986. MESULAM, M.-M. A cortical network for directed attention and unilaterl neglect. Annals of Neurology, 10: 309-325, 1981. RIDDOCH, J., and HUMPHREYS, G.W. The effect of cueing on unilateral neglect. Neuropsychologia, 21: 589-599, 1983. VILLARDITA, C. Tactile exploration of space and visual neglect in brain-damaged patients. Journal of Neurology, 234: 292-297, 1987. WEINTRAUB, S., and MESULAM, M.-M. Right cerebral dominance in spatial attention. Archives of Neurology, 44: 621-625, 1987. Dr. Richard Tegn"r, Department of Neurology, Karolinska Hospital, 10401 Stockholm, Sweden. Fax 4687293757.