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How Long is a Piece of String? A Study of Line Bisection in a Case of Visual Neglect
NOTE
HOW LONG IS A PIECE OF STRING? A STUDY OF LINE BISECTION IN A CASE OF VISUAL NEGLECT Peter W. Halligan and John C. Marshall
(Rivermead Rehabilitation Centre, Oxford, and Neuropsychology Unit, The Radcliffe Infirmary, Oxford)
INTRODUCTION
Line bisection is a traditional task in common use in clinical and experimental studies of unilateral visual neglect (Bisiach, Capitani, Colombo and Spinnler, 1976; Bradshaw, Nettleton, Pierson, Wilson and Nathan, 1987; Schenkenberg, Bradford and Ajax, 1980). Patients with right posterior brain damage are particularly liable to bisect lines significantly to the right of the objective midpoint as one symptom of an underlying tendency to 'neglect' stimuli in the left half of space (De Renzi, 1982); less severe manifestations of the converse phenomenon (right neglect) can be seen in some patients with left hemisphere damage, and may be especially prevalent with anterior pathology (Ogden, 1985). Bisiach, Bulgarelli, Sterzi and Vallar (1983) have, however, noted that "the clinical syndrome of unilateral neglect is qualitatively less homogenous than might be expected", a conclusion that supports the ever increasing evidence for the variability of all the symptom-complexes of classical behavioural neurology (Marshall, 1982). In the specific case of 'unilateral visual neglect', it would seem that this variation from patient to patient extends to the apparently simple task of line bisection, with comparatively few possibilities for functional decomposition. Thus some of the patients reported by Bisiach et al. (1983), case R.G., for example, produce a far larger right displacement the longer the line presented for bisection; other patients (e.g. c.c.) show a right displacement which appears to be relatively independent of line length. The issue of the underlying relationships between line length and magnitude of displacement is, however, still somewhat contentious, as can be seen from the differing interpretations of Bruyer (1984) and Bisiach and Vallar (1984). Nonetheless, R.G.'s performance is particularly interesting. If one extrapolates his (tested) performance (on line lengths of 600,400, and 200 mm) to even smaller lines (not tested), it would appear that the patient's subjective midpoint will cross over from a rightwards to a leftwards displacement. That is, he will be relatively accurate with lines of circa 100 mm and will then show significant 'right neglect' rather than left on lines smaller than circa 50 mm. This argument does, of course, depend upon performing a linear extrapolation from Bisiach et al.'s data. Such extrapolation is fraught with potentially misleading properties and would only be convincing if confirmed by hard empirical evidence. We now report (with appropriate control subjects) a single-case study of a patient with left neglect who appears to be similar to R.G. We investigate the patient's bisection performance on lines which vary from 279 mm (11") to 25 mm (1") in order to see if such linear extrapolation from Bisiach et al.'s results is indeed justifiable.
MATERIALS AND METHODS
Subjects
1 - P.B., a 54 year old, right-handed retail manager, was admitted to the Radcliffe Cortex, (1988) 24, 321-328
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Peter W Halligan and John C. Marshall ,
Infirmary on 26 February, 1986, after the gradual onset of left sided weakness. He had suffered one episode of angina five years previously and had been treated for hypertension in the preceding five months. On admission, neurological examination disclosed homonymous hemianopia with left sided neglect, sluggish pupils, and complete left hemiplegia. Reflexes were brisk on the left with left up going plantar. A CT-scan performed on 27 February 1986 showed widespread infarction of the right middle cerebral artery territory. There was moderate compression of the right lateral ventricle and some shift of the midline (see Figure 1).
Fig. 1 - CT-scan of patient P.B., showing infarction of the right middle cerebral artery territory, with some sparing of the frontal poles and occipital regions.
P.B. was admitted to Rivermead Rehabilitation Centre on 21 April, 1986 with gross motor and perceptual problems, including florid neglect of the left side. He was fully alert, well-oriented and cooperative. Speech was fluent and often highly articulate. There was no evidence of either expressive or receptive aphasia. Assessed on the National Adult Reading Test (Nelson, 1982), his estimated premorbid IQ was in the high average range. Visual neglect was assessed with a comprehensive battery of standard behavioural tests, together with an extensive Perceptual Assessment Battery used in rehabilitation (Whiting, Lincoln, Bhavnani and Cockburn, 1985). The conventional neglect tests included a modified Albert's test (Albert, 1973), two cancellation tasks, line bisection, free drawing and copying of simple objects. All these tasks clearly indicated gross neglect of the left side of working space. P.B.'s aggregate omission score on these tests was 77/146. The behavioural tests of neglect, currently being developed at Rivermead, included such practically relevant tasks as telephone dialling, newspaper reading, copying an address, scanning a picture, discriminating between coins, telling the time from a clock, and following a simple map (Wilson, Cockburn and Halligan, 1987). These tests, which correlate well with therapists' evaluations of functional disability, revealed significant deficits of left sided omission. On a tactile search task that involved taking pegs out of holes the blindfolded patient showed no evidence of hemineglect or hemihypokinesia.
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323
Thus, unlike the patients discussed in Bisiach, Capitani and Porta (1985), P.B. did not present with neglect in two modalities (visual and tactile). Dissociations comparable to those of P.B. have been reported by Halsband, Gruhn and Ettlinger (1985). However, when asked to name British towns in orderly sequence on imaginary trips from north to south and south to north, P.B. reported more west coast towns on the former and more east coast towns on the latter trajectory (see Bisiach and Luzzatti, 1978). Over the next six months, P.B. consistently showed a classical, gross and durable hemispatial visual neglect. The incongruous nature of the neglect was highlighted by the patient's ability to discuss dispassionately features of his neglect while at the same time appearing incapable of translating this verbal insight into appropriate compensatory behaviours. Reminded by therapists that he was always bumping into object on the left hand side, P.B. would agree but was incapable to taking any action to avoid so doing. 2 - D.W., a 63 year old, right-handed, retired police officer, had sustained a stroke following quadruple coronary by-pass surgery in the U.S.A. in September 1986. Following his return to England he was admitted to Rivermead Rehabilitation Centre on 22 February, 1987_ He presented with a mild left hemiparesis, left homonymous hemianopia and features of neglect. In unfamiliar surroundings he would occasionally bump into objects on his left side. The CT-scan, read in the U.S.A., indicated infarction of the right temporo-parietal region. On formal testing, D.W. showed no evidence of aphasia and scored within the high average range of intellectual ability on the National Reading Test (Nelson, 1982). Using the same battery of traditional and behavioural tests of neglect employed with P.B., D.W. exhibited left visual neglect on a wide range of tasks. His aggregate omission score on the traditional tests was 36/146. However, he rarely made incomplete drawings and had no difficulty in imagining and locating the major east and west coast cities of the U.S.A. Furthermore, D.W., unlike P.B., showed considerable insight into his neglect, and often endeavoured to use compensatory strategies. For example, he learned to position a ruler on the left hand side of pages for reading; this was then used as an 'anchor-point' for returning to the beginning of lines. 3 - As normal controls, ten staff members of Rivermead Rehabilitation Centre were recruited. Their mean age was 41.6 years (range 32 to 60), with a standard deviation of 8.4. Six were female and four male; all save one were right-handed.
Stimuli and Procedure Eleven horizontal black lines were individually drawn on sheets of white paper (208 X 298 mm). Each line was approximately 1 mm wide. The lines varied in length from 1" (25 mm) to 11" (279 mm) in steps of 1". Each line was presented on a separate sheet in pseudo-random order, and positioned on the desk so that the objective midpoint lay in the sagittal midplane of the subjects' trunk. The subjects were instructed to mark the midpoint of each line with a pencil, using the preferred hand. The entire set of stimuli was repeated at least 8 times with P.B.; on some occasions, particular lines were repeated (randomly) within a trial. D.W. performed the task twice; the controls once each. RESULTS
The distance to the right of each transection was measured to the nearest millimetre and subtracted from the distance to the right of the objective midpoint. The resultant difference represents the extent to which there was a leftwards bias if the sign is negative, or arightwards bias with positive sign. The data for P.B., D.W. and the normal controls are shown in Table I. Figure 2 shows graphically the mean performance of P.B. and D.W. at all line lengths. As can clearly be seen, P.B. shows an approximately linear increase of the rightward displacement of the subjective midpoint as a function of line-length. This is precisely the result that Bisiach et al. (1983) found for their patient R.G. The corollary of our finding,
Peter W. Halligan and John C. Marshall
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TABLE I
Mean Displacements of Line Bisection Performance in P.B., D.W. and Ten Normal Controls
Line length 279 mm / II" 254 mm / 10" 228 mm / 9" 203 mm /8" 178 mm / 7" 152 mm /6" 127 mm / 5" 102 mm / 4" 77 mm /3" 51mm/2" 25 mm / 1"
Mean displacement ( + SD)
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
+62.0 -13.5 -1.0 +50.5 -6.5 -0.9 +54.0 +3.5 -0.6 +45.2 +3.0 +0.5 +36.3 +7.0 0 +27.0 +4.5 + 1.9 +16.3 + 1.5 -0.8 + 11.6 +15.0 +0.4 +4.0 +5.5 +0.5 +0.2 -0.5 -0.3 -4.4 -4.0 +0.1
(19.5) (6.4) (4.5) (13.6) (0.7) (4.3) (17.4) (2.1) (3.5) (10.2) (1.4) (3.5) (12.4) (1.4) (3.2) (8.4) (0.7) (4.0) (11.7) (0.7) (2.1) (9.0) (1.4) (2.9) (11.7) (0.7) (1.8) (5.5) (0.7) (0.9) (5.6) (0.0) (0.6)
N
Range +38 -18 -8 +31 -7 -7 +23 +2 -6 +34 +2 -4 +22 +6 -5 +17 +4 -2
~ ~ ~
~ ~ ~
~
-+ ~
~ ~ ~
~ ~ ~
~ ~ ~
o~
+1~ -5 ~
-2 +14 -4 -21 +5 -2 -11
~
~ ~ ~
~ ~ ~
-1~
-1~
-18 -4
~ ~
-1~
+100 -9 +6 +73 -6 +5 +74 +5 +4 +67 +4 +5 +51 +8 +5 +39 +5 +10 +31 . +2 +1 +24 +16 +7 +16 +6 +4 +7 0 +2 0 -4 +1
9 2 10
11
2 10
11
2 10 11
2 10
11
2 10 11
2 10 8 2 10 8 2 10 9 2 10 10 2 10 12 2 10
however, is that, for lines shorter than those used by Bisiach et al. (200 - 600 rnrn), our patient is more accurate with lines of 2" (51 rnrn), and does indeed show 'right neglect' (i.e. a consistent leftward displacement of the subjective midpoint) at line length I" (25 rnrn). This is exactly the 'anomalous' result that we had predicted from our extrapolation of the original data of Bisiach et al.'s patient R.G. Comparison with the data obtained from normal controls (Table I) shows that for line lengths 4" to II", P.B.'s mean displacement (to the right) is outside the range of scores obtained by any normal subject (N = 10). For line lengths 3" and 2", P.B.'s mean is within the normal range. Indeed at line length 2" (= 51 rnrn), P.B.'s mean displacement ( + 0.2) is marginally closer to the objective midpoint than is the comparison mean of the controls ( 0.3). However, for line length I" (= 25 rnrn), P.B.'s mean displacement (- 4.4) is once again outside the range of the normal controls (Mean = + 0.1; range - 1.0 to + 1.0), albeit in the opposite direction from his performance with the longer lines. Although the striking linear relationship between displacement and line length found in P.B. does not manifest itself in D.W.'s performance (see Figure 2), it is nonetheless notable that D.W.'s bisection is most accurate at the two smallest lengths (I" and 2"). Likewise, the leftwards displacement that D.W. shows on the I" line ( - 4.0) is outside the range of the normal controls (- I to + 1). Confusingly, his leftwards displacement on the longest line, 11" (- 13.5)is also outside the normal range ( - 8 to + 6). For the majority of line lengths, however, D.W. does show convincing right displacement (7111) and hence mild left neglect. .
How long is a piece of string? A study of visual neglect
11" 10"
mm)
D.W.
325
P.B.
(254m_m-'-)~~~~~~~~~~~l%+---,-r+-__~~~~-f-~~~~~~~_
g" (228 mm)
~~~~~~~~~-l:7%~~-l+-~~~~~+-~~~~~-
S" (203 mm) 7""(178 mm) 6" (152 ml)1) 5" (127 mm)
4" (102 mm) 3" (77 mm) 2"(51 mm) 1"(25 mm)
Fig. 2 - Graphical presentation of mean line bisections by patients P.B. and D. W; the shadowed area on the left represents the mean and SD for the hypothesized 'attentional boundary' manifested by P.B.
DISCUSSION
We appear, then, to have confirmed a strikingly counter-intuitive prediction derived from an earlier study by Bisiach et al. (1983). Namely: patients (or more precisely a patient) with classical left neglect can show 'right neglect' on a bisection task when the lines are sufficiently small. That P.B.'s performance with smaller lines is more accurate than with longer ones confirms standard clinical wisdom that large lines should be employed when testing for the presence of neglect. But we know of no previous evidence that bisection performance can actually 'cross over' when small lines are employed; nor do we know of any theory of neglect in line bisection that would make this prediction. Yet the phenomenon (if reliable in some patients) would seem to place constraints upon the interpretation of (some forms of) unilateral visual neglect. How, then, should we look at P.B.'s performance? The presence of hemianopia per se does not explain the pattern of P.B.'s bisection displacement. Although the hemianopic patient D.W. does show a tendency to leftwards displacement at our smallest line length, he does not manifest the powerful relationship between length and magnitude of displacement seen in P.B. One possible explanation springs from the fact that the leftmost point of P.B.'s 'subjective' line (calculated as distance between P.B.'s transection and the right most point of the objective line X 2) is approximately constant. For the eleven line lengths (from largest to smallest), the distances between the objective point of bisection and the leftmost point of the 'subjective' lines are: 15.5; 26.0; 6.0; 11.1; 16.4; 22.0; 30.9; 27.8; 30.5; 25.1; 21.3. The mean is 21.1 mm (SD = 8.0). Imagine, then, that a boundary, approximately, 21 millimetres to the left of centre, constitutes the limit beyond which P.B. cannot further direct his attention leftwards. The 'perceived' line is then the line to the right of this attentional boundary. And it is this line that the patient bisects. Clearly, this account suffices to interpret the majority of our data, although the 'cross-over' to 'right neglect' at
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Peter W. Halligan and John C. Marshall
length I" (= 25 mm) requires further explanation. Following the work of Warrington (1962) and Bisiach and Vallar (1984), we would speculate that this is an instance of 'pathological completion' provoked by the conditions of testing. For all lines except the I" line, the objective stimulus does indeed extend to our hypothesized attentional boundary. I t is thus not unreasonable to suppose that under such constraints 'completion' of a line to that boundary can take place. Before accepting such a hypothesis, one should, however, consider the possibility that P.B.'s performance on the I" line is normal. For line lengths 80 to 170 mm, Bradshaw, Nettleton, Nathan and Wilson (1985) have shown that normal subjects asked to bisect a line placed across the midline consistently transect to the left of centre. They interpret the phenomenon by arguing that "It is as if such subjects see the extent to the left of center as larger than it really is, possibly because of the greater visuospatial processing power of the right hemisphere ... and so in compensation make the left side slightly smaller to seem equal to the right" (Bradshaw, Nettleton, Pierson, Wilson and Nathan, 1987). Our own control data (N = 10) do not show this effect (see Table I), but this is perhaps due to small sample size. On a larger sample of normal controls (N = 48), we have confirmed the results of Bradshaw et al. for a line length of 8" ( = 203 mm). The mean error found on the 8" line was 2.0% to the left of the midpoint (- 2.0 mm) with a standard deviation of 3.9. Bradshaw, Nathan, Nettleton, Wilson and Pierson (1987) confirmed the results of Bradshaw et al. (1985), using a rod bisection task. Similar results (with normal subjects) have also been found by Scarisbrick, Tweedy and Kuslansky (1987) for visual line bisection, and by Bowers and Heilman (1980) with tactile bisection. The average magnitude of normal left displacement from the true midpoint found by Bradshaw et al. (1985) was - 1.02 mm (1.6%). For our I" (= 25 mm) lines, P.B. showed a mean left displacement of 4.4 mm. The individual figures for the twelve trials were ranked as follows: - 18; - 14; - 4; - 4; -4; - 3; - 2; - 2; - 1; - 1; 0; o. Eight of these twelve reading show larger left displacements than the mean reported by Bradshaw et al. (who do not report ranges and standard deviations for their data). Six readings are beyond the mean absolute displacements of our own controls with a line of 8". Thus even if the direction of P.B.'s displacements (at line length I") is normal, the magnitude of the displacement is four-fold over that of Bradshaw et al.'s (normal) subjects. P.B.'s performance on the smallest of our lines is thus emphatically deviant. One further possibility, of course, is that P.B.'s left displacement is normal in direction but exaggerated by problems due to visuo-motor co-ordination or dyspraxia. We can, however, rule out this hypothesis with some confidence. The figures just quoted for P.B.'s twelve trials with the I" line do not show random swings around a displaced subjective midpoint; rather the transections are systematically displaced to the left. Further evidence against a visuo-motor coordination hypothesis comes from P.B.'s performance on the earlier described cancellation tasks. When crossing out stars or individual letters (with horizontal and vertical extention of approximately 6 mm), P.B. never motorically missed any stimulus he was cancelling. Yet on two occasions, when performing the I" (25 mm) line bisection task, P.B.'s displacement placed the 'perceived' midpoint further left than the left endpoint of the actual line. This, then, looks like a dramatic confirmation of P.B.'s 'completion' of this line into empty space. It is consistent with this hypothesis that P.B. does indeeed complete on other tasks in free vision. For example, presented with chimerics of human faces (one side female, the other male), P.B. consistently named the right side, and even upon intensive questioning could see nothing odd about the stimuli. Similar results were found with side views of chimeric animals (e.g. half elephant and half cow). We thus agree with Bisiach et al. (1983) that representational completion is "critical for an adequate understanding of unilateral neglect". On the other hand, the type of line completion that is in question with our patient cannot be interpreted as mere verbal confabulation filling a representational vacuum. Such an account may be possible in the case of objects that have an intrinsic symmetry (e.g. front views of faces), or in the case of words (where only a limited number of left sided completions will transform a letter sequence into an attested word). With line completion, however, the stimulus has no a priori length over and above the length of the seen stimulus. In this case, then, completion must in some sense be perceptual completion to the
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hypothesized 'attentional boundary'. That is, P.B. has incorporated the space to the attentional boundary into his represention of the (objectively) 25 nun line. He thus bisects (on some trials) a space that is devoid of sensory information but is filled in by an 'internally represented' line. ABSTRACT
We report a case of severe left visual neglect consequent upon extensive infarction in the territory of the right middle cerebral artery. A detailed analysis is given of the patient's performance on line bisection. The stimuli cover a wider range of lengths than is usually employed in such studies (11" to 1"). The magnitude of the patient's rightward displacement of his transections is linearly related to the length of the stimulus line, such that the longer the line, the greater the left 'neglect'. At line length 2", the patient's transections are relatively accurate, and at length 1", the transections cross the objective midpoint to give a reliable left displacement (= 'right neglect'). On some occasions, these latter transections are placed beyond the leftmost point of the stimulus line. We interpret the data in terms of two constructs: (a) an 'attentional boundary' placed slightly to the left of the objective midline; (b) 'representational completion' that extends to the attentional boundary. Acknowledgements. Peter Halligan's work was supported by grants 85/17 from Oxford Regional Health Authority (to Dr. Barbara Wilson), and 6/87 from the Chest, Heart, and Stroke Association (to Mr Peter Halligan and Drs. Derick Wade and John C. Marshall). The Neuropsychology Unit is supported by Medical Research Council grant PG 7301443 to Drs. Freda Newcombe and John C. Marshall. REFERENCES
ALBERT, M.L. A simple test of visual neglect. Neurology,: 23: 258-264, 1973. BISIACH, E., and LUZZATTI, C. Unilateral neglect of representation space. Cortex, 14: 129-133, 1978. BISIACH, E., and VALLAR, G. Pathological completion of hemineglect: A reply to Bruyer. Brain and Cognition, 3: 235-237, 1984. BISIACH, E., CAPITAN I, E., and PORTA, E. Two basic properties of space representation in the brain: evidence from unilateral neglect. Journal of Neurology, Neurosurgery, and Psychiatry, 48: 141-144, 1985. BISIACH, E., BULGARELLI, C., STERZI, R., and VALLAR, G. Line bisection and cognitive plasticity of unilateral neglect of space. Brain and Cognition, 2: 32-38, 1983. BISIACH, E., CAPITANI, E. COLOMBO, A., and SPINNLER, H. Halving a horizontal segment: A study on hemisphere-damaged patients with cerebral focal lesions. Archives Suisses de Neurologie, Neurochirurgie et de Psychiatrie, 118: 199-206, 1976. BOWERS, D., and HEILMAN, K.M. Pseudoneglect: effects of hemispace on tactile line bisection task. Neuropsychologia, 18: 491-498, 1980. BRADSHAW, J.L., NATHAN, G., NETTLETON, N.C., WILSON, L., and PIERSON, J. Why is there a left side underestimation in rod bisection? Neuropsychologia, 25: 735-738, 1987. BRADSHAW, J. L., NETTLETON, N.C., NATHAN, G, and WILSON, L.E. Bisecting rods and lines: Effects of horizontal and vertical posture on left side underestimation by normal subjects. Neuropsychologia, 23: 421-436. 1985. BRADSHAW, J.L., NETTLETON, N.C., PIERSON, J.M., WILSON, L.E., and NATHAN, G. Coordinates of extracorporeal space. In M. Jeannerod (Ed.), Neurophysiological and Neuropsychological Aspects of Spatial Neglect. Amsterdam: North-Holland, 1987. BRUYER, R. Neglects in hemineglect: A comment on the study of Bisiach et al. (1983). Brain and Cognition, 3: 231-234, 1984. DE RENZI, E. Disorders of Space Exploration and Cognition. New York: Wiley, 1982. HALSBAND, u., GRUHN, S., and ETTLINGER, G. Unilateral spatial neglect and defective performance in one half of space. International Journal of Neuroscience, 28: 173-195, 1985. JEANNEROD, M. (Ed.) Neurophysiological and Neuropsychological Aspects of Spatial Neglect. Amsterdam: North-Holland, 1987.
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MARSHALL, J.e. What is a symptom-complex? In M.A. Arbib, D. Caplan and J.e. Marshall (Eds.), Neural Models of Language Processes. New York: Academic Press 1982, pp. 389-409. 1982. NELSON, H.E. The National Adult Reading Test. Windsor, England: NFER-Nelson Publishing Co. .. Ltd., 1982. OGDEN, J.A. Anterior-posterior interhemispheric differences in the loci of lesions producing visual hemineglect. Brain and Cognition, 4: 59-75, 1985. SCARISBRICK, D.J., TwEEDY, J.R., and KUSLANSKY, G. Hand preference and performance effects on line bisection. Neuropsychologia, 25: 695-699, 1987. SCHENKENBERG, T., BRADFORD, D.e., and AJAX, E.T. Line bisection and unilateral visual neglect in patients with neurological impairment. Neurology, 30: 509-517, 1980. WARRINGTON, E.K. The completion of visual forms across hemianopic field defects. Journal of Neurology, Neurosurgery, and Psychiatry, 25: 208-218, 1962. WHITING, S. LINCOLN, N., BHAVNANI, G., and COCKBURN, J. Rivermead Perceptual Assessment Battery. Windsor, England: NFER-Nelson Publishing Co. Ltd., 1985. WILSON, B., COCKBURN, J., and HALLIGAN, P.W. Development of a behavioural test of visuospatial neglect. Archives of Physical Medicine and Rehabilitation, 68: 98-102, 1987. Peter W. Halligan, Rivermead Rehabilitation Centre, Abingdon Road, Oxford OXI 4XD, U.K. John C. Marshall, Neuropsychology Unit, The Radcliffe Infirmary, Woodstock Road, Oxford OX2 6HE, U.K.
HOW LONG IS A PIECE OF STRING? A STUDY OF LINE BISECTION IN A CASE OF VISUAL NEGLECT Peter W. Halligan and John C. Marshall
(Rivermead Rehabilitation Centre, Oxford, and Neuropsychology Unit, The Radcliffe Infirmary, Oxford)
INTRODUCTION
Line bisection is a traditional task in common use in clinical and experimental studies of unilateral visual neglect (Bisiach, Capitani, Colombo and Spinnler, 1976; Bradshaw, Nettleton, Pierson, Wilson and Nathan, 1987; Schenkenberg, Bradford and Ajax, 1980). Patients with right posterior brain damage are particularly liable to bisect lines significantly to the right of the objective midpoint as one symptom of an underlying tendency to 'neglect' stimuli in the left half of space (De Renzi, 1982); less severe manifestations of the converse phenomenon (right neglect) can be seen in some patients with left hemisphere damage, and may be especially prevalent with anterior pathology (Ogden, 1985). Bisiach, Bulgarelli, Sterzi and Vallar (1983) have, however, noted that "the clinical syndrome of unilateral neglect is qualitatively less homogenous than might be expected", a conclusion that supports the ever increasing evidence for the variability of all the symptom-complexes of classical behavioural neurology (Marshall, 1982). In the specific case of 'unilateral visual neglect', it would seem that this variation from patient to patient extends to the apparently simple task of line bisection, with comparatively few possibilities for functional decomposition. Thus some of the patients reported by Bisiach et al. (1983), case R.G., for example, produce a far larger right displacement the longer the line presented for bisection; other patients (e.g. c.c.) show a right displacement which appears to be relatively independent of line length. The issue of the underlying relationships between line length and magnitude of displacement is, however, still somewhat contentious, as can be seen from the differing interpretations of Bruyer (1984) and Bisiach and Vallar (1984). Nonetheless, R.G.'s performance is particularly interesting. If one extrapolates his (tested) performance (on line lengths of 600,400, and 200 mm) to even smaller lines (not tested), it would appear that the patient's subjective midpoint will cross over from a rightwards to a leftwards displacement. That is, he will be relatively accurate with lines of circa 100 mm and will then show significant 'right neglect' rather than left on lines smaller than circa 50 mm. This argument does, of course, depend upon performing a linear extrapolation from Bisiach et al.'s data. Such extrapolation is fraught with potentially misleading properties and would only be convincing if confirmed by hard empirical evidence. We now report (with appropriate control subjects) a single-case study of a patient with left neglect who appears to be similar to R.G. We investigate the patient's bisection performance on lines which vary from 279 mm (11") to 25 mm (1") in order to see if such linear extrapolation from Bisiach et al.'s results is indeed justifiable.
MATERIALS AND METHODS
Subjects
1 - P.B., a 54 year old, right-handed retail manager, was admitted to the Radcliffe Cortex, (1988) 24, 321-328
322
Peter W Halligan and John C. Marshall ,
Infirmary on 26 February, 1986, after the gradual onset of left sided weakness. He had suffered one episode of angina five years previously and had been treated for hypertension in the preceding five months. On admission, neurological examination disclosed homonymous hemianopia with left sided neglect, sluggish pupils, and complete left hemiplegia. Reflexes were brisk on the left with left up going plantar. A CT-scan performed on 27 February 1986 showed widespread infarction of the right middle cerebral artery territory. There was moderate compression of the right lateral ventricle and some shift of the midline (see Figure 1).
Fig. 1 - CT-scan of patient P.B., showing infarction of the right middle cerebral artery territory, with some sparing of the frontal poles and occipital regions.
P.B. was admitted to Rivermead Rehabilitation Centre on 21 April, 1986 with gross motor and perceptual problems, including florid neglect of the left side. He was fully alert, well-oriented and cooperative. Speech was fluent and often highly articulate. There was no evidence of either expressive or receptive aphasia. Assessed on the National Adult Reading Test (Nelson, 1982), his estimated premorbid IQ was in the high average range. Visual neglect was assessed with a comprehensive battery of standard behavioural tests, together with an extensive Perceptual Assessment Battery used in rehabilitation (Whiting, Lincoln, Bhavnani and Cockburn, 1985). The conventional neglect tests included a modified Albert's test (Albert, 1973), two cancellation tasks, line bisection, free drawing and copying of simple objects. All these tasks clearly indicated gross neglect of the left side of working space. P.B.'s aggregate omission score on these tests was 77/146. The behavioural tests of neglect, currently being developed at Rivermead, included such practically relevant tasks as telephone dialling, newspaper reading, copying an address, scanning a picture, discriminating between coins, telling the time from a clock, and following a simple map (Wilson, Cockburn and Halligan, 1987). These tests, which correlate well with therapists' evaluations of functional disability, revealed significant deficits of left sided omission. On a tactile search task that involved taking pegs out of holes the blindfolded patient showed no evidence of hemineglect or hemihypokinesia.
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Thus, unlike the patients discussed in Bisiach, Capitani and Porta (1985), P.B. did not present with neglect in two modalities (visual and tactile). Dissociations comparable to those of P.B. have been reported by Halsband, Gruhn and Ettlinger (1985). However, when asked to name British towns in orderly sequence on imaginary trips from north to south and south to north, P.B. reported more west coast towns on the former and more east coast towns on the latter trajectory (see Bisiach and Luzzatti, 1978). Over the next six months, P.B. consistently showed a classical, gross and durable hemispatial visual neglect. The incongruous nature of the neglect was highlighted by the patient's ability to discuss dispassionately features of his neglect while at the same time appearing incapable of translating this verbal insight into appropriate compensatory behaviours. Reminded by therapists that he was always bumping into object on the left hand side, P.B. would agree but was incapable to taking any action to avoid so doing. 2 - D.W., a 63 year old, right-handed, retired police officer, had sustained a stroke following quadruple coronary by-pass surgery in the U.S.A. in September 1986. Following his return to England he was admitted to Rivermead Rehabilitation Centre on 22 February, 1987_ He presented with a mild left hemiparesis, left homonymous hemianopia and features of neglect. In unfamiliar surroundings he would occasionally bump into objects on his left side. The CT-scan, read in the U.S.A., indicated infarction of the right temporo-parietal region. On formal testing, D.W. showed no evidence of aphasia and scored within the high average range of intellectual ability on the National Reading Test (Nelson, 1982). Using the same battery of traditional and behavioural tests of neglect employed with P.B., D.W. exhibited left visual neglect on a wide range of tasks. His aggregate omission score on the traditional tests was 36/146. However, he rarely made incomplete drawings and had no difficulty in imagining and locating the major east and west coast cities of the U.S.A. Furthermore, D.W., unlike P.B., showed considerable insight into his neglect, and often endeavoured to use compensatory strategies. For example, he learned to position a ruler on the left hand side of pages for reading; this was then used as an 'anchor-point' for returning to the beginning of lines. 3 - As normal controls, ten staff members of Rivermead Rehabilitation Centre were recruited. Their mean age was 41.6 years (range 32 to 60), with a standard deviation of 8.4. Six were female and four male; all save one were right-handed.
Stimuli and Procedure Eleven horizontal black lines were individually drawn on sheets of white paper (208 X 298 mm). Each line was approximately 1 mm wide. The lines varied in length from 1" (25 mm) to 11" (279 mm) in steps of 1". Each line was presented on a separate sheet in pseudo-random order, and positioned on the desk so that the objective midpoint lay in the sagittal midplane of the subjects' trunk. The subjects were instructed to mark the midpoint of each line with a pencil, using the preferred hand. The entire set of stimuli was repeated at least 8 times with P.B.; on some occasions, particular lines were repeated (randomly) within a trial. D.W. performed the task twice; the controls once each. RESULTS
The distance to the right of each transection was measured to the nearest millimetre and subtracted from the distance to the right of the objective midpoint. The resultant difference represents the extent to which there was a leftwards bias if the sign is negative, or arightwards bias with positive sign. The data for P.B., D.W. and the normal controls are shown in Table I. Figure 2 shows graphically the mean performance of P.B. and D.W. at all line lengths. As can clearly be seen, P.B. shows an approximately linear increase of the rightward displacement of the subjective midpoint as a function of line-length. This is precisely the result that Bisiach et al. (1983) found for their patient R.G. The corollary of our finding,
Peter W. Halligan and John C. Marshall
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TABLE I
Mean Displacements of Line Bisection Performance in P.B., D.W. and Ten Normal Controls
Line length 279 mm / II" 254 mm / 10" 228 mm / 9" 203 mm /8" 178 mm / 7" 152 mm /6" 127 mm / 5" 102 mm / 4" 77 mm /3" 51mm/2" 25 mm / 1"
Mean displacement ( + SD)
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
P.B.
D.W. Controls
+62.0 -13.5 -1.0 +50.5 -6.5 -0.9 +54.0 +3.5 -0.6 +45.2 +3.0 +0.5 +36.3 +7.0 0 +27.0 +4.5 + 1.9 +16.3 + 1.5 -0.8 + 11.6 +15.0 +0.4 +4.0 +5.5 +0.5 +0.2 -0.5 -0.3 -4.4 -4.0 +0.1
(19.5) (6.4) (4.5) (13.6) (0.7) (4.3) (17.4) (2.1) (3.5) (10.2) (1.4) (3.5) (12.4) (1.4) (3.2) (8.4) (0.7) (4.0) (11.7) (0.7) (2.1) (9.0) (1.4) (2.9) (11.7) (0.7) (1.8) (5.5) (0.7) (0.9) (5.6) (0.0) (0.6)
N
Range +38 -18 -8 +31 -7 -7 +23 +2 -6 +34 +2 -4 +22 +6 -5 +17 +4 -2
~ ~ ~
~ ~ ~
~
-+ ~
~ ~ ~
~ ~ ~
~ ~ ~
o~
+1~ -5 ~
-2 +14 -4 -21 +5 -2 -11
~
~ ~ ~
~ ~ ~
-1~
-1~
-18 -4
~ ~
-1~
+100 -9 +6 +73 -6 +5 +74 +5 +4 +67 +4 +5 +51 +8 +5 +39 +5 +10 +31 . +2 +1 +24 +16 +7 +16 +6 +4 +7 0 +2 0 -4 +1
9 2 10
11
2 10
11
2 10 11
2 10
11
2 10 11
2 10 8 2 10 8 2 10 9 2 10 10 2 10 12 2 10
however, is that, for lines shorter than those used by Bisiach et al. (200 - 600 rnrn), our patient is more accurate with lines of 2" (51 rnrn), and does indeed show 'right neglect' (i.e. a consistent leftward displacement of the subjective midpoint) at line length I" (25 rnrn). This is exactly the 'anomalous' result that we had predicted from our extrapolation of the original data of Bisiach et al.'s patient R.G. Comparison with the data obtained from normal controls (Table I) shows that for line lengths 4" to II", P.B.'s mean displacement (to the right) is outside the range of scores obtained by any normal subject (N = 10). For line lengths 3" and 2", P.B.'s mean is within the normal range. Indeed at line length 2" (= 51 rnrn), P.B.'s mean displacement ( + 0.2) is marginally closer to the objective midpoint than is the comparison mean of the controls ( 0.3). However, for line length I" (= 25 rnrn), P.B.'s mean displacement (- 4.4) is once again outside the range of the normal controls (Mean = + 0.1; range - 1.0 to + 1.0), albeit in the opposite direction from his performance with the longer lines. Although the striking linear relationship between displacement and line length found in P.B. does not manifest itself in D.W.'s performance (see Figure 2), it is nonetheless notable that D.W.'s bisection is most accurate at the two smallest lengths (I" and 2"). Likewise, the leftwards displacement that D.W. shows on the I" line ( - 4.0) is outside the range of the normal controls (- I to + 1). Confusingly, his leftwards displacement on the longest line, 11" (- 13.5)is also outside the normal range ( - 8 to + 6). For the majority of line lengths, however, D.W. does show convincing right displacement (7111) and hence mild left neglect. .
How long is a piece of string? A study of visual neglect
11" 10"
mm)
D.W.
325
P.B.
(254m_m-'-)~~~~~~~~~~~l%+---,-r+-__~~~~-f-~~~~~~~_
g" (228 mm)
~~~~~~~~~-l:7%~~-l+-~~~~~+-~~~~~-
S" (203 mm) 7""(178 mm) 6" (152 ml)1) 5" (127 mm)
4" (102 mm) 3" (77 mm) 2"(51 mm) 1"(25 mm)
Fig. 2 - Graphical presentation of mean line bisections by patients P.B. and D. W; the shadowed area on the left represents the mean and SD for the hypothesized 'attentional boundary' manifested by P.B.
DISCUSSION
We appear, then, to have confirmed a strikingly counter-intuitive prediction derived from an earlier study by Bisiach et al. (1983). Namely: patients (or more precisely a patient) with classical left neglect can show 'right neglect' on a bisection task when the lines are sufficiently small. That P.B.'s performance with smaller lines is more accurate than with longer ones confirms standard clinical wisdom that large lines should be employed when testing for the presence of neglect. But we know of no previous evidence that bisection performance can actually 'cross over' when small lines are employed; nor do we know of any theory of neglect in line bisection that would make this prediction. Yet the phenomenon (if reliable in some patients) would seem to place constraints upon the interpretation of (some forms of) unilateral visual neglect. How, then, should we look at P.B.'s performance? The presence of hemianopia per se does not explain the pattern of P.B.'s bisection displacement. Although the hemianopic patient D.W. does show a tendency to leftwards displacement at our smallest line length, he does not manifest the powerful relationship between length and magnitude of displacement seen in P.B. One possible explanation springs from the fact that the leftmost point of P.B.'s 'subjective' line (calculated as distance between P.B.'s transection and the right most point of the objective line X 2) is approximately constant. For the eleven line lengths (from largest to smallest), the distances between the objective point of bisection and the leftmost point of the 'subjective' lines are: 15.5; 26.0; 6.0; 11.1; 16.4; 22.0; 30.9; 27.8; 30.5; 25.1; 21.3. The mean is 21.1 mm (SD = 8.0). Imagine, then, that a boundary, approximately, 21 millimetres to the left of centre, constitutes the limit beyond which P.B. cannot further direct his attention leftwards. The 'perceived' line is then the line to the right of this attentional boundary. And it is this line that the patient bisects. Clearly, this account suffices to interpret the majority of our data, although the 'cross-over' to 'right neglect' at
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Peter W. Halligan and John C. Marshall
length I" (= 25 mm) requires further explanation. Following the work of Warrington (1962) and Bisiach and Vallar (1984), we would speculate that this is an instance of 'pathological completion' provoked by the conditions of testing. For all lines except the I" line, the objective stimulus does indeed extend to our hypothesized attentional boundary. I t is thus not unreasonable to suppose that under such constraints 'completion' of a line to that boundary can take place. Before accepting such a hypothesis, one should, however, consider the possibility that P.B.'s performance on the I" line is normal. For line lengths 80 to 170 mm, Bradshaw, Nettleton, Nathan and Wilson (1985) have shown that normal subjects asked to bisect a line placed across the midline consistently transect to the left of centre. They interpret the phenomenon by arguing that "It is as if such subjects see the extent to the left of center as larger than it really is, possibly because of the greater visuospatial processing power of the right hemisphere ... and so in compensation make the left side slightly smaller to seem equal to the right" (Bradshaw, Nettleton, Pierson, Wilson and Nathan, 1987). Our own control data (N = 10) do not show this effect (see Table I), but this is perhaps due to small sample size. On a larger sample of normal controls (N = 48), we have confirmed the results of Bradshaw et al. for a line length of 8" ( = 203 mm). The mean error found on the 8" line was 2.0% to the left of the midpoint (- 2.0 mm) with a standard deviation of 3.9. Bradshaw, Nathan, Nettleton, Wilson and Pierson (1987) confirmed the results of Bradshaw et al. (1985), using a rod bisection task. Similar results (with normal subjects) have also been found by Scarisbrick, Tweedy and Kuslansky (1987) for visual line bisection, and by Bowers and Heilman (1980) with tactile bisection. The average magnitude of normal left displacement from the true midpoint found by Bradshaw et al. (1985) was - 1.02 mm (1.6%). For our I" (= 25 mm) lines, P.B. showed a mean left displacement of 4.4 mm. The individual figures for the twelve trials were ranked as follows: - 18; - 14; - 4; - 4; -4; - 3; - 2; - 2; - 1; - 1; 0; o. Eight of these twelve reading show larger left displacements than the mean reported by Bradshaw et al. (who do not report ranges and standard deviations for their data). Six readings are beyond the mean absolute displacements of our own controls with a line of 8". Thus even if the direction of P.B.'s displacements (at line length I") is normal, the magnitude of the displacement is four-fold over that of Bradshaw et al.'s (normal) subjects. P.B.'s performance on the smallest of our lines is thus emphatically deviant. One further possibility, of course, is that P.B.'s left displacement is normal in direction but exaggerated by problems due to visuo-motor co-ordination or dyspraxia. We can, however, rule out this hypothesis with some confidence. The figures just quoted for P.B.'s twelve trials with the I" line do not show random swings around a displaced subjective midpoint; rather the transections are systematically displaced to the left. Further evidence against a visuo-motor coordination hypothesis comes from P.B.'s performance on the earlier described cancellation tasks. When crossing out stars or individual letters (with horizontal and vertical extention of approximately 6 mm), P.B. never motorically missed any stimulus he was cancelling. Yet on two occasions, when performing the I" (25 mm) line bisection task, P.B.'s displacement placed the 'perceived' midpoint further left than the left endpoint of the actual line. This, then, looks like a dramatic confirmation of P.B.'s 'completion' of this line into empty space. It is consistent with this hypothesis that P.B. does indeeed complete on other tasks in free vision. For example, presented with chimerics of human faces (one side female, the other male), P.B. consistently named the right side, and even upon intensive questioning could see nothing odd about the stimuli. Similar results were found with side views of chimeric animals (e.g. half elephant and half cow). We thus agree with Bisiach et al. (1983) that representational completion is "critical for an adequate understanding of unilateral neglect". On the other hand, the type of line completion that is in question with our patient cannot be interpreted as mere verbal confabulation filling a representational vacuum. Such an account may be possible in the case of objects that have an intrinsic symmetry (e.g. front views of faces), or in the case of words (where only a limited number of left sided completions will transform a letter sequence into an attested word). With line completion, however, the stimulus has no a priori length over and above the length of the seen stimulus. In this case, then, completion must in some sense be perceptual completion to the
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hypothesized 'attentional boundary'. That is, P.B. has incorporated the space to the attentional boundary into his represention of the (objectively) 25 nun line. He thus bisects (on some trials) a space that is devoid of sensory information but is filled in by an 'internally represented' line. ABSTRACT
We report a case of severe left visual neglect consequent upon extensive infarction in the territory of the right middle cerebral artery. A detailed analysis is given of the patient's performance on line bisection. The stimuli cover a wider range of lengths than is usually employed in such studies (11" to 1"). The magnitude of the patient's rightward displacement of his transections is linearly related to the length of the stimulus line, such that the longer the line, the greater the left 'neglect'. At line length 2", the patient's transections are relatively accurate, and at length 1", the transections cross the objective midpoint to give a reliable left displacement (= 'right neglect'). On some occasions, these latter transections are placed beyond the leftmost point of the stimulus line. We interpret the data in terms of two constructs: (a) an 'attentional boundary' placed slightly to the left of the objective midline; (b) 'representational completion' that extends to the attentional boundary. Acknowledgements. Peter Halligan's work was supported by grants 85/17 from Oxford Regional Health Authority (to Dr. Barbara Wilson), and 6/87 from the Chest, Heart, and Stroke Association (to Mr Peter Halligan and Drs. Derick Wade and John C. Marshall). The Neuropsychology Unit is supported by Medical Research Council grant PG 7301443 to Drs. Freda Newcombe and John C. Marshall. REFERENCES
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MARSHALL, J.e. What is a symptom-complex? In M.A. Arbib, D. Caplan and J.e. Marshall (Eds.), Neural Models of Language Processes. New York: Academic Press 1982, pp. 389-409. 1982. NELSON, H.E. The National Adult Reading Test. Windsor, England: NFER-Nelson Publishing Co. .. Ltd., 1982. OGDEN, J.A. Anterior-posterior interhemispheric differences in the loci of lesions producing visual hemineglect. Brain and Cognition, 4: 59-75, 1985. SCARISBRICK, D.J., TwEEDY, J.R., and KUSLANSKY, G. Hand preference and performance effects on line bisection. Neuropsychologia, 25: 695-699, 1987. SCHENKENBERG, T., BRADFORD, D.e., and AJAX, E.T. Line bisection and unilateral visual neglect in patients with neurological impairment. Neurology, 30: 509-517, 1980. WARRINGTON, E.K. The completion of visual forms across hemianopic field defects. Journal of Neurology, Neurosurgery, and Psychiatry, 25: 208-218, 1962. WHITING, S. LINCOLN, N., BHAVNANI, G., and COCKBURN, J. Rivermead Perceptual Assessment Battery. Windsor, England: NFER-Nelson Publishing Co. Ltd., 1985. WILSON, B., COCKBURN, J., and HALLIGAN, P.W. Development of a behavioural test of visuospatial neglect. Archives of Physical Medicine and Rehabilitation, 68: 98-102, 1987. Peter W. Halligan, Rivermead Rehabilitation Centre, Abingdon Road, Oxford OXI 4XD, U.K. John C. Marshall, Neuropsychology Unit, The Radcliffe Infirmary, Woodstock Road, Oxford OX2 6HE, U.K.