NOTE HOMING IN ON NEGLECT: A CASE STUDY OF VISUAL SEARCH Peter W. Halligan and John C. Marshall (Rivennead Rehabilitation Centre, Abingdon Road, Oxford, and University Department of Clinical Neurology, Radcliffe Infinnary, Woodstock Road, Oxford, UK) INTRODUCTION It is well-known that the effects of left-sided cueing in patients with left neglect are both variable and transitory. With appropriate instructions and a sufficiently strong cue, it is usually possible to direct the patient's "attention" to stimuli on the left. In some cueing-paradigms one can be fairly certain that the patient has "seen" the full extent of the stimulus-array, but even in these circumstances the patient continues to "neglect" stimuli (or parts thereof) that have apparently been "perceived" (in some sense of the tenn). The phenomenon can be observed most clearly in studies of line bisection. In some investigations where the patient is required to report a letter placed at the left end of a stimulus line prior to bisection, no improvement over uncued trials is found (Heilman and Valenstein, 1979). In other studies, such cueing reduces but does not eliminate left neglect (Riddoch and Humphreys, 1983; Nichelli, Rinaldi and Cubelli, 1989). A similar effect may be found on cancellation tasks, although we are not aware of any study that has explicitly investigated the issue. Nonetheless, in the standard deployment of the Albert Test, the examiner is first required to draw over each of the 40 stimulus lines with a red pencil. The method thus calls "the subject's attention to all the lines and also explicitly (shows) the limits of the test" (Albert, 1973). In a modification employed by Fullerton, McSherry and Stout (1986), some of the lines are pointed out to the patient, "including those to extreme right and extreme left." Despite these manipulations, the patient with severe left neglect wi\l still fail to cancel stimuli on the left of the stimulus page. We now report the first systematic exploration of how much a patient with left neglect can "know" about the overall dimensions of a cancellation test whilst "neglecting" a substantial number of the smaller targets that he is required to cross out. The question at issue is whether a particular fonn of "panoramic" cueing to the full extent of a stimulus display has any effect upon the direction of attention to items within that display . CASE HISTORY R.B., a 50 year-old, left handed man (with right handed parents), was admitted to hospital on 16 December 1991, following a right hemisphere stroke. CT scan, on 17 December 1991, revealed a large right middle cerebral artery infarct (Figure 1). The infarct involved primarily the right parietal cortex. Admitted to Rivennead on 16 March, 1992, R.B.'s major problems included left hemiplegia, left homonymous hemianopia, left sensory loss, and gross left vi suo-spatial neglect. Although well oriented in time and place, R.B. had little insight into his neglect. On the six conventional subtests of the Behavioural Inattention Test (BIT} (Halligan, Cockburn and Wilson, 1991), R.B.'s score of 25/146 indicated severe left sided neglect. On the behavioural tests he failed to read the left side of telephone numbers and numbers located on the left side of a clockface. He also neglected the left side of words and Cortex, (1993) 29,167-174 168 P. W. Halligan and J.e. Marshall Fig. 1 - CT scan on 17 December 1991, showing a large right middle cerebral artery infarct (right is on the left of the image). sentences when reading or copying text. Visual acuity was 6/9 in both eyes (glasses corrected). Saccades were slightly hypometric and there was some difficulty in maintaining steady fixation. EXPERIMENT 1 Materials and Methods This experiment has 4 separate steps. Each step included the requirement that the patient cross out (cancel) all the targets of the line crossing test from the BIT (Halligan et aI., 1991). Head and eye movements were in no way constrained, but moving the stimulus sheet was not permitted. The targets consisted of 40 black lines of different orientations arrayed across an A4 page (279 X 210 mm); the stimulus sheet was centred on the sagittal midplane of the patient's head and trunk. The target lines (25 mm long by 1 mm wide) are distributed across the page in such a fashion that they can be scored as 7 "columns" from left to right. The central column (column 4) is composed of 4 target lines; all other columns contain 6 lines. The patient was seated at a comfortable distance from the test sheet displayed on the desk top. No knowledge of results was provided to the patient and no time pressure was imposed. The patient stopped when he was satisfied with his own performance. The (unaffected) right hand was always used and each step began with the right hand in its natural position to the right of the stimulus page. Unlike the standardised BIT condition of this task, the patient's attention was never drawn to the central columns. The experiment (all 4 steps) was repeated three times. The first step (standard condition) required the patient to cross out all the target lines he could see on the page. The second step was the same as the first except that immediately prior to the start of the task, the patient was asked to mark each comer of the stimulus page with a cross. The third step was the same as the first except that this time the patient was asked to indicate the comers of the stimulus page after he had completed crossing out all the lines he could see on the page. The fourth step was identical to the first step. If the two intermediary steps had any effect, this fourth step would Homing in on neglect 169 TABLE I Experiment 1: Number of Lines Crossed Out: Mean and Standard Deviation Standard Cross out lines Mark 4 corners/ Cross out lines Cross out lines/ Mark 4 corners Standard Cross out lines Left Right Left Right Left Right Left Right 0 (0) 13.0 0 (0) 12.3 (2.5) 0 (0) 11.3 0 (0) 10.3 (1.2) (1.7) (1.2) access whether or not there was a carry-over effect on performance. After this experiment had been repeated 3 times, the patient was required to indicate the size of the stimulus page on which the target lines had been displayed. Blank sheets of A4 (279 X 210 mm) and AS (148 X 210 mm) were presented one above the other and the patient was asked to indicate the sheet that was the same size as the stimulus page. The toplbottom position of the two sheets was randomly counterbalanced throughout 6 trials. Both stimulus sheets were centred near the patient's sagittal midplane and spatially aligned so that .the right edges were justified. Results Omission scores from the 4 presentations of line crossing were calculated. In each of the four conditions R.B. failed to cross out all the target lines located on the left side of the stimulus page. In steps 2 and 3, however, R.B. showed no difficulty in locating and marking the 4 comers of the stimulus page. The results (means of the three trials) are shown in Table 1. It is clear that R.B.'s apparent awareness of the spatial extent of the A4 stimulus page made no difference to his cancellation of the targets contained within the area whose comers he had accurately indicated. For the task requiring judgment of the stimulus page size, R.B. always chose the correct (A4) sheet (6/6). EXPERIMENT 2 Materials and Methods This experiment was similar to Experiment 1. The only difference was the size of the page on which the stimuli lines were displayed. The same spatial array of lines was used but transposed (centrally) onto a larger A3 (422 X 298 mm) page. The first step required the patient to cross out all the target lines as before. The second step was similar to the first except that immediately prior to the start of the task, the patient was asked to mark the comers of the stimulus sheet. The third step was identical to the first step. The fourth step required the patient to mark the extent of the spatial display of target lines (rather than the comers of the stimulus page) before cancelling the lines. The fifth step was identical to the first step. Finally, the sixth step required the patient to judge: (1) the size of the stimulus page on which the target lines were positioned; (2) the size of the space within which the target lines were contained. For this step, blank A3 (422X298 mm), A4 (279X21O mm) and AS (148X21O mm) sheets were presented one above the other and the patient was asked to indicate the stimulus sheet that corresponded to the two judgments required. All three stimulus sheets were centred near the patient's sagittal midplane and spatially aligned so that the right edges were justified. The vertical order of the three sheets was randomly counterbalanced over five trials for each type of judgement. P. W. Halligan and J.e. Marshall 170 Fig. 2 - An exampLe of R.B. 's peiformance on step four of Experiment 2. The patient indicated (with numbers) the extent of the spatial array of line targets that he couLd see on the A3 page. The array only is shown, not the full extent of the (A3) page. dYY ---r ~ \I v -/ "< --;---~ ./ G~ ~ Q ----- ----------- -- ----- ~ ~ y J- --I-- ~ \ / ~ / ~@ ~ ~ / ~ -- ~ ----- Results As in the first experiment, R.B. always correctly marked the comers of the stimulus page. He accordingly seems not to show the type of directional hypokinesia (or hypometria) reported in Bottini, Sterzi and Vallar (1992). Despite this, R.B. continued to neglect some 70% of the targets on the stimulus sheet (Table II). Requested in step four to mark the extent of the spatial array of target lines, R.B . marked the spatial array as smaller than it was. Figure 2 shows R.B.'s performance on step four. The patient indicated (with numbers) that the extent of the spatial array of line targets constituted the three rightmost columns of the spatial array. Even within this restricted space, however, there are omissions on two of the three columns that lie within the extent of the spatial array that the patient has marked. When requested (as in Experiment 1) to indicate the size of the stimulus page on which the spatial array of target line had been presented, R.B. consistently (SIS) chose the correct (A3) page. However, when requested to indicate the size of the spatial array of target lines from the three page sizes (A3, A4 and AS) R.B. chose the smaller (AS) page on 4/5 trials. On one trial, he chose the correct A4 page. EXPERIMENT 3 Materials and Methods A new line crossing task was devised. 42 target lines were presented on an A4 page. The targets were pseudo-randomly distributed but in such a fashion that they could be TABLE II Experiment 2: Number of Lines Crossed Out Standard Cross out lines Mark 4 comers/ Cross out lines Standard Cross out lines Mark edges of display/Cross out lines Standard Cross out lines Left Right Left Right Left Right Left Right Left Right o 9 o 12 o 12 o 15 o 13 171 Homing in on neglect scored as seven "columns" of six target lines each. Half the target lines were red and the other half were black. The red and black lines were pseudo-randomly placed so that there were equal numbers on the left and on the right; and to the top and bottom of the page. This experiment has six separate steps. The first step simply required the patient to cross out all the target lines on the page irrespective of colour. In the second step in order to establish that RB. could see the total number of target lines on the page he was asked to state the colour of each of the 42 lines when the examiner systematically pointed each one out (from the rightmost to the leftmost column). R.B. had no difficulty with this task and was very quick to name each colour correctly. Having traversed the total spatial extent of the target array, ยท the patient was requested as before to cancel all the target lines that he could see on the page. Step three then repeats the (un cued) first step. Step four replicated step two (naming the colours and then crossing out the targets). Step five was identical to the first step (uncued). Finally, step six required the patient to indicate first the size of the page on which the target lines were placed and second the size of the spatial array of lines contained on that page. The page sizes presented were the same as in Experiment 1. Results The purpose of Experiment 3 was again to ascertain whether after RB. had explicitly covered (and made an overt response to) the full extent of the spatial array of target lines, he would subsequently detect and cross out more of the target lines. As in the previous experiments R.B. could clearly respond to the full extent of the stimulus page when cued to do so. He had no difficulty in naming correctly the colour of the lines irrespective of spatial location when they were pointed out to him. However, the cancellation results (Table III) show that, after this cueing, RB. persisted in neglecting over 50% of the targets' located on his left. When requested (as in the previous experiments) to indicate the size of the stimulus page on which the black and red target lines had been presented, R.B. consistently chose the correct (A4) sheet (3/3). Requested to indicate the size of the spatial array contained on the stimulus page, RB. consistently chose the incorrect (AS) sheet (3/3). TABLE III Experiment 3: Number of Lines Crossed Out Standard Cross out lines Name colours/ Cross out lines Standard Cross out lines Name colours/ Cross out lines Standard Cross out lines Left Right Left Right Left Right Left Right Left Right o II o 22 o 17 o 15 o II DISCUSSION Experiment 1 shows that RB. can correctly mark the full extent of the A4 stimulus page both before (step 2) and after (step 3) he attempts to cancel the target lines. His manifest ability to do so, however, has little or no effect upon his inadequate performance on the cancellation task itself. RB. also "remembers" the size of the target display (step 5) when the display covers the full extent of the stimulus page. Experiment 2 shows that R.B. can correctly mark the full extent of a larger A3 (422 X 298 mm) stimulus page, and confirms that so doing has little or no effect upon cancellation performance (compare the results of steps 1, 2 and 3). But if required to mark the comers of the target display (when that display is smaller than the stimulus page), R.B. "neglects" a substantial part of the left extent of the target display in both 172 P. W. Halligan and J.e. Marshall the corner marking task itself and the subsequent cancellation task. He can "remember" the size (A3) of the stimulus page correctly (step 6), but apparently misremembers the size of the target display (A4) as the smaller size A3. This latter result is consistent with the size that R.B. marked as the target display when he viewed it in step 4. Experiment 3 confirms that R.B . can perceive all the targets scattered over an A4 page: when they are individually pointed out to him he correctly names the colour of each line. As in the previous experiments, however, he continued to "neglect" over 50% of the target lines when required to cross them out immediately after having named their colour. In the size judgement task (step 6), R.B . correctly "remembers" the size of the stimulus page (A4), as he had done in Experiments I and 2, but misremembers the size of the target display as smaller than it was (consistent with the results of Experiment 2). The data-pattern, then, is remarkably reliable and consistent across the three experiments. The interpretation of this pattern should, we propose, proceed along the following lines. In one current metaphor, visual attention has been likened to a "zoom lens" (Eriksen and St. James, 1986; Humphrey and Bruce, 1989). Such a system can be set to cover a wide range of field with poor resolution of detail, or a constricted field with good resolution (and all intervening ranges) . When R.B. is "looking for" the boundaries of one (fairly) large figure (an A3 or A4 page), he has no difficulty in detecting (and making a manual response to) the corners of that (relatively) "wide range" stimulus. There is no obvious perceptual or "hypokinetic" deficit in left space. Neither is there any gross memory failure for the size of that space. However, when the task demands that attention is focussed onto a smaller area (in order to resolve and cancel the individual line targets), the "lens" has a systematic bias to the right. This bias leads to failure to cancel left sided targets in all three experiments; and failure to mark correctly the top and bottom left corners of the target display in Experiment 2. Attention is initially weakly distribut\'!d over the largest (relevant) field; when any "focussing in" occurs, the rightward bias becomes manifest, and affects both corner marking and target cancellation. The "remembered" target field (Experiment 2) is then the extent of the narrowed and (right-) biased field. This latter effect still obtains even when objectively the spatial extent of the stimulus page and the target display are (almost) identical (Experiment 3). This result thus goes beyond the well established phenomenon that neglect gets worse with increasing demands on visual selective attention (Kaplan, Verfaellie, Meadows et aI. , 1991). Accordingly, these effects provide a theoretical link between unilateral neglect and simultanagnosia (Luria, 1959). As Bisiach and Rusconi (1990) and Young, Hellawell and Welch (1992) report, patients with left neglect may correctly trace the entirety of a line drawing of one object and thereby trace through another object situated on the left side of the first object without consciously "noticing" the presence of the second object. As Balint (1907) observed, a mild degree of such "simultanagnosia" is perfectly normal: "It is a well-known phenomenon that we do not notice anything happening in our surroundings while being absorbed in the inspection of something; focussing our attention on a certain object may happen to such an extent that we cannot perceive other objects placed in the peripheral parts of our visual field ... " (Translation by Husain and Stein, 1988). Gross clinical simultanagnosia (usually seen after bilateral occipito-parietal damage) differs from this normal constriction of attention in that one of two "objects" can be "neglected" even when they overlap and are "seen" in foveal vision. The report by Luria (1959) of a patient who could perceive at anyone instant only one of the two triangles that make up a Star-of-David is a convincing demonstration of pathological simultanagnosia in the above sense of the term. Our current conjecture is that it may be profitable to think of unilateral neglect as a form of lateralized simultanagnosia for objects represented at a "small" spatial scale (Farah, 1990). R.B. can see the global but not the local features of left space (Robertson and Lamb, 1991) unless, as in Experiment 3, his attention is specifically drawn to them. The patients reported by Bisiach and Rusconi (1990) can see the house but not the fire Homing in on neglect 173 in left space. As Humphreys and Bruce (1989) point out, the zoom lens metaphor captures " ... the way we can choose to see either a forest or leaves at different times". It seems to us that a zoom lens with a rightward bias captures at least one important aspect of the behaviours that have gone under the clinical label of left vi suo-spatial neglect. Consider, for example, neglect dyslexia (Ellis, Flude and Young, 1987). The most frequent error-type preserves the overall length of the word (measured in letters) but letter substitutions occur on the left (e.g. FACADE - "arcade"). Similarly, when drawing or copying a clock-face, the circle is usually complete but the numbers on the left may be missing. Line bisections are grossly skewed to the right but the centre of a square or circle may be correctly estimated (Halligan and Marshall, 1991). In all these examples, there is no "neglect" when the lens is set for a wide range of field; "left neglect" occurs when the field is narrowed in order to resolve a "small" stimulus (e.g. the end-point of a line). In "simultanagnosia" as traditionally understood, "higher" levels of perceptual analysis "select" one object and block the simultaneous perception of another. This is reminiscent of "extinction", but without the lateralized aspect thereof. In neglect, the whole can be perceived but "higher" levels of perceptual analysis can only "select" a lateralized subpart of the whole for processing in focal attention. Coslett and Saffran (1991) note that "the most puzzling aspect of the performance of patients with simultanagnosia" is this: "When confronted with a complex visual array these patients often report 'seeing' only a single item, yet when confronted with a large depiction of a single 'object' that is co-existensive with the multi-item array, such as a drawing of an elephant, subjects generally report seeing the entire object rather than components of the object (e.g., an ear, trunk, etc.) despite the fact that many of the components may be in themselves 'objects'?". A similar (but not identical) puzzle may be one aspect of neglect. Our patient R.B. can "see" the whole array but only a lateralized subportion of the "objects" that make up the array. ABSTRACT We report three studies of visual search in a patient with left neglect after a right parietal infarct. 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