(X)28-3932,93 S6.00+0.00 Pergamon Press Ltd
TO SEE OR NOT TO SEE: THE EFFECTS OF VISIBLE AND INVISIBLE CUES ON LINE BISECTION JUDGEMENTS IN UNILATERAL NEGLECT JASON
B. MATTINGLEY,*?
JANE
M.
and
PIERSON,~ JUDY
tDepartment of Psychology, Monash University, Psychology, University of Hertfordshire, (Received
1 December
JOHN
L. BRADSHAW,~
JAMES G.
PHILLIPS,?
A. BRADSHAWt Clayton, Victoria 3168, Australia; and IDepartment College Lane, Hatfield, Herts AL10 9AB, U.K. 1992; accepted
7 April
of
1993)
Abstract-Patients with left unilateral neglect and matched controls were tested in two experiments to examine the effects of lateralized cues on line bisection judgements. Unlike previous studies in which letter or number cues were placed beyond the endpoint(s) ofeach line, we adopted a procedure which maintained the perceptual point of balance in the horizontal axis of each line. We also related the cueing task more closely to the act of bisection by requiring subjects to place a small mark in direct alignment with the endpoint(s) of each line. In the first experiment, it was found that, for controls, the presence or absence of visible lateralized cues did not differentially affect the magnitude of bisection errors. However, the magnitude of bisection errors made by neglect patients was significantly reduced (and reversed) in the presence ofa visible left-sided cue, but remained well to the right of the midpoint in the absence ofsuch cues. In a second experiment, subjects engaged in an otherwise identical cueing procedure, except that no visible marks appeared on the stimulus lines. Neither subject group was affected by the presence or absence of right-sided cues. However, the presence of left-sided cues again reduced the magnitude of bisection errors in neglect patients, but not in controls. These results indicate that the extent of the attentional bias exhibited by neglect patients can be ameliorated even in the absence of lateralized visible cues.
STUDIES examining the performance of patients with unilateral neglect on tasks of line bisection have provided numerous insights into the mechanisms which may underlie the disorder. In the standard version of the task, subjects are required to place a mark at the midpoint of a horizontal line. Normal dextral controls show a tendency to err slightly to the left of the midpoint [4], though there would seem to be considerable individual variation in both the direction and extent of this bias [6, 161. In contrast, patients with right hemisphere lesions and left neglect consistently place their transections well to the right of the true midpoint [27]. Several explanations have been proposed to account for this rightward error, including failure adequately to represent the left side of line stimuli [3], existence of a left hemispatial memory disorder [ 121, and a deficit of intentional control, such that movements directed towards the left side of space are hypometric, i.e. fall short of the true midpoint [ 121. Most recent investigations, however, have invoked the notion of an attentional deficit (or bias) to explain the pattern of bisection errors made by both normal subjects and patients
*To whom correspondence
should
be addressed. 1201
1202
J. B. MATTINGLEYet al.
with unilateral neglect [23, 251. These explanations have, in part, been based on data obtained from experiments in which the magnitude of bisection errors was altered by requiring subjects to report cues positioned at either end of the line prior to making their judgement. More specifically, in patients with left neglect, a visual cue placed adjacent to the left end of each line has been consistently found to reduce the extent of rightward bisection error compared with conditions in which no cues or single right-sided cues were present [21, 24, 251. It has been suggested that the beneficial effects of left-sided cueing occur because patients are forced to direct their attention to a part of the line which they would otherwise neglect [25]. The patient is thereby afforded a more realistic percept of the spatial extent of the line and is better able to judge its true midpoint. In normal subjects, such cueing procedures have also been shown to influence subjects’judgements of the true midpoint of a line. MILNER et al. 1201 found that bisection errors were significantly biased away from the midpoint and towards the endpoint which had a visual cue. They concluded that an attentional bias operates on judgements of spatial extent, such that those parts of a stimulus receiving “less” attention are somehow reduced in perceived magnitude. In most previous studies, the “attention-getting” properties of the visual cues have been implied, rather than explicit. Subjects have typically been required to read out a letter or number positioned adjacent to the line end, prior to making their bisection judgement [ 12, 20, 21, 251. One potential problem with such procedures is that the cueing task (letter or number reading) is not related to the experimental task (line bisection). Under these conditions, subjects may report the cues but then disregard them completely when switching to the quite different and unrelated task of line bisection [S]. In the present study, we asked subjects to place a small, visible mark on either end (or both ends) of the line, prior to placing their bisection mark, and compared the performance in these conditions with that obtained when the bisection mark was placed Gthout prior cueing. We reasoned that the use of a technique where subjects must overtly identify the end, or ends, of the line itself may tie the cues to the line bisection task more closely than does the reading out of letters or numbers. A second, but equally important reason for adopting such a procedure, was to overcome a potential bias that may have influenced the results of some previous cueing experiments. In these earlier studies, visual cues were positioned beyond the true endpoints of the lines, thereby extending their horizontal extent by several millimetres. Such configurations are particularly problematic in cases of uniluterul cueing where, in addition to the purported attentional properties of the cues, the perceived (horizontal) magnitude of the combined line/cue stimulus is (artifactually) biased toward one side. Under such circumstances, it becomes impossible to separate the relative contributions of attentional manipulation from those arising as a consequence of the alteration in the perceptual “point of balance” of the stimulus in the horizontal plane. Thus, the apparent length of a line varies depending upon whether, as in a variant of the Miiller-Lyer illusion 1261, two small terminal squares occur within or outside the ends of a line. The potential effect of such a confounding factor assumes even more importance in studies where the size of the reported bisection error is of the same order of magnitude as the additional spatial extent added by the (unilateral) visual cue 120, 241. By ensuring that subjects placed their cue marks in precise alignment with either end of each line, we were able to eliminate the potential contribution of such perceptual biases. A third reason for adopting our procedure, which was explored in a second experiment, is that the procedure permits comparison between performance when the cue remains visible after placement, and when all other aspects remain constant except that no visible mark appears.
VISIBLF
ANV INVISIHLF
CUES OS
JIJVGEMENTS
IN CNILATERAL
NEGLECT
1203
1
EXPERIMENT
In Experiment 1, patients with left unilateral neglect and matched controls were asked to bisect lines of variable length, under four different cue conditions: a baseline condition in which bisections were made without prior cueing, unilateral left-sided cueing, unilateral right-sided cueing, and bilateral cueing. The cueing conditions involved the subjects placing a small, visible mark in direct alignment with one or other end of the line (or both ends) prior to placing their bisection mark. Method Suhjrc/.s. Six patients with left unilateral neglect and six individually age- and sex-matched healthy controls participated in the experiment. There was no significant difference between the mean age of patients (68.3 years) and controls (68.2 years). [F(I, lO)=O.OOl, ns.]. Patients had unilateral right hemisphere lesions as inferred from clinical examination and confirmed by cranial CT scan. Age, sex and clinical details for each patient are provided in Table 1. For all subjects, handedness was assessed by a IO item questionnaire which obtained information on familial handedness and hand preference for a variety of unimanual tasks [22]. All subjects were assessed as being right-handed. and none exhibited primary sensory or motor disturbances in this limb. Table
I. Age. sex and clinical details of left neglect patients
Case
Age (years). sex
Lesion
I 2 3 4 5 6
78. M 55. F 6X. M 86, M 62. M 61.F
FTPOS FP FTS FTPS FTPS s
I
in Experiment
Neglect test
F=frontal: O=occipital; homonymous hemianopia; + + =dense: + = mild; circle cancellation task; SC
Poststroke (days) 19 41 71 I5 54 16
VFA LHH NAD L sup. quad. LHH NAD LHH
Hemiplegia
AL
CC
SC
++ ++ ++ ++ + +
39 Y4 33 0 0 53
25 80 25 0 10 35
85 87 43 28 37 70
P=parietal: T= temporal: S=subcortical; VFA=visual field assessment; LHH =left L sup. quad. = left superior quadrantanopia; NAD = no abnormalities detected: = absent; AL = percentage omissions on Albert’s lines; CC = percentage omissions in = percentage omissions on Star Cancellation task.
S~~rc~iin~~/i)r uni/~/te~(~/neglrc~t. A screening protocol identical for all patients was performed immediately prtor to conducting the line bisection task. The procedure used to assess the presence ofvisual neglect has been described in detail elsewhere [ IY]. Briefly. it inv/olved the administration of a line cancellation task [I]. a circle cancellation task [5]. and the Star Cancellation task from the Behavioural Inattention Test 1301. Patients used their preferred (ipsilesional) hand to hold the pen. and each task was placed in front ofthe patient and centred at the body midline. The percentage of omissions made by patients on each of these tasks is shown in Table I. Mtrtrritrls. Ten black horizontal lines. each 2 mm in width. were printed on sheets of white A4 paper. Lines were centred on the narrow axis ofeach sheet and each line was separated by 30 mm. The lines varied in length from 80 to I70 mm in IO mm steps, and these lengths were pseudorandomly ordered from the top to the bottom ofthe sheet. A mask for the stimulus sheet was constructed from a piece of white cardboard measuring 239 mm in width and 353 mm in length. Halfway down the length ofthe mask, two narrow slits were cut. These were positioned centrally and I6 mm apart in order to form a viewing window through which each line could be presented. one at a time. to the subject. All subjects used a sharp HB lead pencil (0.5 mm diameter) to make their responses. Procr~du,r, Control subjects and most patients were seated at a table during the screening and experimental tasks. A small number of patients was tested while sitting upright in bed. with a height-adjustable table located at a comfortable distance in front of them. Subjects’ body position was monitored to ensure an upright posture. but no attempt was made to restrict head or eye movement. The stimulus sheets were placed beneath the mask and positioned in the horizontal plane directly opposite the body midline. Subjects, using their right hand. were asked to mark the midpoint of each line as it appeared in the viewing window. The examiner then moved the stimulus sheet through the mask to cover the prcv’ious response and expose the next line. Care was taken to ensure that the lines remained centred at the body midline. and that the table. mask, and stimulus sheets bore no marks which could be used by the subjects as extraneous reference points. Subjects completed IO lines in each of four conditions, giving a total of 40 lines per subject (240 lines per group).
1204
J. B. MATTINGL~Y rt (I/.
All subjects completed the “no cues” (bisect only) condition first to avoid possible carryover effects from the other three conditions in which cues were used. For the second set of 10 lines, subjects were instructed to place a pencil mark at both ends of each line before marking the midpoint. Subjects were asked to ensure that cue marks were e.uuctl!, aliyd with the line’s perceived endpoints. No constraints were placed on theend which was marked first. In the event, neglect patients invariably marked the right end first and, in many instances, needed to be reminded also to mark the left end. Controls usually marked the left end first, although this was by no means a consistent intra- or inter-subject bias. Subjects then completed two more sets of lines, one in which the left end was marked prior to bisection and the other in which the right end was marked prior to bisection. The order ofcompletion for each ofthc two unilateral cue conditions was counterbalanced across subjects. Errors were measured as the distance. to the nearest millimetre, between the subject’s bisection mark and the true (objective) midpoint of the lint. In accordance with established convention. errors to the right and left of the true midpoint were denoted as positive and negative. respectively. Datu mdysis. Since the major focus of this study was to examine the effects of lateralized visual cues. we adopted an N priori technique for distinguishing between the relative contributions made by the ~WWIW (or crhsrncr) of such cues. Signed error data representing the original cue conditions (i.e. no cues. dual cues, left cue and right cue) were divided into two separate factors, Right Cue and Left Cue, each ofwhich contained two levels (present. absent). The manner in which this transformation was achieved is presented in Table 2 (see KEPPEL [IS] for a full explanation of this design). Thus. data from all four of the original cue conditions were examined twice in the statistical analysis, once in relation to the left endpoint (Left Cue) and again in relation to the right endpoint (Right Cue). The presence or absence ofcues represented the two levels ofeach ofthesc factors. Signed errors for each subject were submitted to a four-way analysis of variance with Group (patients. controls) as a between-subjects factor and Left Cue (present. absent). Right Cue (present, absent) and Line Length (80 170 mm) as within-subjects factors.
Table 2. Transformation of original cueing conditions into factors for statistical analysis Factor
Lcvcl
Cut conditions
Left Cue
Present Absent
(left cue + dual cues) (no cues+ right cue)
Right Cue
Present Absent
(right cue+dual cues) (no cues + left cues)
Results For purposes of comparison with previous studies, Table 3 shows the mean bisection errors, in each of the four original cue conditions, for patients and controls. Mean bisection error in the “no cues” condition was to the right of the true midpoint for all left neglect patients. The direction of bisection error made by controls in the same condition was less consistent, although the group mean indicated a small deviation to the left of the true midpoint. The pattern of bisection errors associated with the presence/absence of left- and right-sided cues (as per our statistical analysis) is presented in Fig. 1. For simplicity, the effect of line length on bisection errors is presented in a separate figure. Analysis of mean, signed bisection errors revealed significant main effects of group [F (1,lO)=29.06, P
VlSlHLF
AND IYVISIHLE
CUES ON JUDGEMENTS
IN UNILATERAL
1205
NEGLECT
Table 3. Mean bisection error (in mm) of six left unilateral neglect patients and six matched controls in Experiment I No cues
Right only
Left only
Dual cues
Patient I 2 3 4 5 6
34.3 39.0 II.2 9.4 8.4 10.7
-12.2 -9.2 0.6 -1.5 5.4 -10.1
33.4 25.9 22.0 1.4 7.3 30.3
Mean S.D.
18.8 13.9
-4.5 7.0
21.0 11.3
-2.0 9.3
Control I 2 3 4 5 6
-0.8 - 1.6 1.2 -6.5 I .7 0.2
-0.2 - 1.2 1.4 -4.3 -2.0 1.3
I .o 0.2 2.0 -3.1 2.9 0.6
1.4 -2.1 2.1 -4.0 -0.9 1.7
Mean S.D.
~ 1.0 3.0
-0.8 2.2
0.6 2.1
-0.3 2.4
(a)
m
Cue
m
Cue absent
present
-20.1
I .2 1.3 1.2 6.7 -2.3
(b)
Left Laterality
of Cue
Laterelity
m
Cue
m
Cue absent
present
Right of Cue
Fig. I. Experiment 1. Mean bisection error as a function of cue laterality. Solid bars--cue present; hatched bars--cue absent. One standard error indicated. (a) Neglect patients, (b) controls.
and controls, the presence or absence of such a cue did not differentially affect mean bisection error. Two further analyses were conducted separately on data from each subject group in order to determine the effects of the factors Left Cue and Line Length, and the relationship between
1206
J. B. MATTINGLEY CItrl
them. While there were no significant main effects and no interaction for controls, the left neglect patients showed significant main effects of Left Cue [F (1, 5) = 9.87, PC O.OS] and Line Length [F(9,45)=7.49, P
For patients with left neglect, our results are similar to those reported in previous studies, insofar as they indicate that visual cues, placed on either end of a horizontal line, can influence the subsequent placement of bisection marks [21, 24, 251. More specifically, we have demonstrated that while the presence or absence of a right-sided cue did not differentially affect mean bisection error for either subject group, deviations from the true midpoint were significantly reduced in neglect patients (but not controls) in the presence of a left-sided cue. These results support the view that in the absence of visual cues, left neglect patients attend initially to the right end of the line and thereafter direct their attention (hypometrically) toward the true midpoint. This rightward bias is maintained (but not exacerbated) in the presence of a right-sided cue. In contrast, the presence of a left-sided cue (either in the unilateral left or dual cue conditions) explicitly directs attention to the otherwise “unattended” end of each line, thereby reducing and rcwrsing the subsequent bisection error. Indeed, the mean bisection error for patients in the Left Cue present condition was further to the lc$ of the true midpoint than that of controls in the same condition. Bisection errors made by neglect patients in the absence of a left-sided cue also showed a positive, linear relationship with line length. The slope of this function (Fig. 2) was shown to be significantly different from that obtained when left-sided cues were present. Indeed, in the presence of left-sided cues, the magnitude ofthe bisection error remained relatively consistent across the range of line lengths employed. These results are similar to those obtained in other studies which have examined the performance of left neglect patients on cued line bisection. Thus, NICHELLI et al. [21] found that a left-sided cue reduced the magnitude of bisection errors at all line lengths tested and that the slope of the function was shallower than in the “no cue” and “right cue” conditions. HALLIGAN and MARSHALI. [8, 91 reported similar results
VISIBLE
AND INVISIBLE
CUES ON JUDGEMENTS
LEFT
,
I
60
90
100
I
110 Line
Fig. 2. Experiment
I. Mean
CUE
1
120 length
IN UNILATERAL
PRESENT
A .
Ielk
<‘I,<’ rues
150
160
170
-1
I
130
1207
NEGLECT
140
(mm)
bisection error for neglect patients, plotted condition, as a function of’ line length.
separately
for each cue
using lines presented on a computer-controlled visual display. Their patients were required to move a cursor either from the left or right end of the line. Bisection errors were found to increase linearly with increasing line length, but the “left start”condition produced relatively smaller increments in bisection error compared to the “right start” condition. Unlike previous investigations on the effects of cueing in normal subjects 1203, our controls did not exhibit any significant changes in bisection error as a function of cue type or line length. This may be an age-related discrepancy (the subjects tested by MILNER et al. [20] were all young adults) or it may reflect the specific properties of our cueing paradigm, which itself circumvents potential artifacts that may occur when letter or digit cues are used. We adopted a cueing procedure which has at least two advantages over those used previously. Firstly, marking the end of a line would seem to be more explicitly related to the task of making bisection judgements than simply reading out a letter or number. Our procedure ensures that the respective extremities are attended to directly, a result which has only been inferred in previous studies. Secondly, and perhaps more importantly, in our paradigm the horizontal extent of each line remained constant across all cueing conditions, thereby eliminating the potential bias produced by letter or digit cues placed adjacent to line ends. In Experiment I, marks made by subjects in the cued conditions extended several millimetres beyond the top and bottom of the lines. It could be argued that the very existerrce of visual cues, regardless of their actual position with respect to the endpoints of the line, may still alter the perceptual salience of the stimulus as a whole. Indeed, several previous studies
1208
J. B. MATTLNGLEYrt ul.
have indicated that perceptual judgements made by neglect patients are exquisitely sensitive to apparently minor or irrelevant stimulus dimensions [ 10,17,28]. Moreover, evidence from several previous studies has suggested that even when subjects are not required to report or attend to visual cues, their presence nevertheless influences subsequent bisection errors [23-251. In Experiment 2, we adopted a paradigm which incorporated attentional cues without any visual referents.
EXPERIMENT
2
In this experiment, instead of asking subjects to place visible marks on each stimulus, we adopted an otherwise identical cueing paradigm except that no Cd& rnurks were left on the stimulus lines. By adopting this procedure, it was possible to unambiguously determine the effects of attentional cueing in the absence of extraneous visual information. Method Suhject.s. A further six patients
with left unilateral neglect and six individually age- and sex-matched healthy controls participated in the experiment. There was no significant difference between the mean age of patients (64.0 years) and controls (64.5 years) [F(l, 10)=0.75, n.s.1. As in Experiment I, all patients had unilateral right hemisphere lesions as inferred from clinical examination and confirmed by cranial CT scan. Age, sex, clinical details and performance on neglect screening tasks for each patient are provided in Table 4. All subjects were right-handed according to the handedness assessment procedures outlined in Experiment I. and none had primary sensory or motor impairments in this limb.
Table 4. Age, sex and clinical details of left neglect patients
in Experiment
2 Neglect test
Age Case I 2 3 4 5 6 See Table
(years). sex 61. 67, 72. 66. 52. 66,
M M F M F F
Lesion FP S TP FP TP P
Poststroke (days) 14 I0 31 423 9 5
VFA
Hemiplegia
AL
CC
SC
LHH LHH NAD NAD LHH LHH
++ ++ ++ ++
0 8 94 17 36 18
0 5 75 0 20 55
26 43 91 7 69 81
+
I for abbreviations
Mafurials. All materials were idcntlcal to those employed in Experiment I. with the important exception of the pen used by subjects to mark lines. This pen had a tapered, white plastic tip instead ofan inking nib. The plastic tip made an invisible impression on the stimulus sheet which could later be identified by placing the sheet over a light box. PWW/UW. The procedures adopted for data collection were identical to those employed in Experiment I. Once again. although a small number of patients was tested while sitting upright in bed. most subjects were seated at a table during the screening and experimental tasks. As in Experiment I. in the “dual cues” condition patients invariably marked the right end of the line first and occasionally had to bc reminded also to mark the left end, while controls showed a predominant (though not exclusive) tendency to mark the left end first. /Guru anul~sis. Slgned error data from the four levels of the Condition factor were again treated as two separate factors, namely, Right Cue and Left Cue, each containing two levels (present. absent). Signed error data were submitted to a four-way analysis of variance with group (patients, controls) as a between-subjects factor and Left Cue (present, absent). Right Cue (present. absent) and Line Length (80 170 mm) as within-subjects Factors.
Results
Table patients
5 shows the mean bisection error, in each of the four original cue conditions, for and controls. The overall bisection error for the six patients in the “no cues”
VISIBLE ANIl
condition “no cues” “no cues” bias, with
INVISIBLE CUES ON JUDGEMENTS
IN UNILATERAL
NEGLECT
1209
(22.7 mm) was comparable to that exhibited by our other neglect patients in the condition of Experiment 1. Once again, the performance of control subjects in the condition was more accurate, though less consistent in terms of the direction of an overall bisection error 0.3 mm to the left of the true midpoint.
Table 5. Mean bisection error (in mm) of six left unilateral neglect patients and six matched controls in Experiment 2 No cues
Left only
Right only
Dual cues
Patient
I 2 3 4 5 6
Il.2 16.5 33.1 5.x 15.5 54.2
0.0 1.5 -9.9 -7.5
Mean S.D.
30.2
7.3 7.9 31.4 1.3 22.3 50.4
1.3 2.2 -8.6 ~ 1.9 9.4 25.2
22.7 17.9
2.6 14.3
20.1 18.5
4.6 Il.7
Control I 2 3 4 5 6
-2.5 2.2 1.5 ~ 1.7 0.4 ~ I.5
~ 1.0 0.5 2.4 ~ I .4 -0.6 -0.8
-0.9 2.5 3.4 4.3 -0.1 ~ I .o
-2.1 2.8 2.2 -0.3 -0.2 -0.4
Mean S.D.
-0.3 I .9
-0.2 I .4
I .4 2.3
0.3
I .4
1.8
The pattern of bisection errors associated with the presence/absence ofleft- and right-sided cues is presented in Fig. 3. As before, the effect ofline length on bisection errors is presented in a separate figure. Analysis of mean, signed bisection errors revealed a near significant main effect of group [F (1, 10) =4.34, P=O.O6],and significant main effects of Left Cue [F(l, lo)= 11.60, PcO.011and Line Length [F(9, 90)=4.49, P
1210
J.
B.
MATTINGLEY
er rrl
(a) 25
Left Laterality
Right of
Cue
-a
Left Laterality
Right of
Cue
Fig. 3. Experiment 2. Mean blsection error as a function of cue laterahty. Solid bars- -cue present: hatched bars-cue absent. One standard error indicated. (a) Neglect patients. (b) controls.
and 170 mm) and at 90 and 120 mm. However, in the absence of left-sided cues, errors were to the right of the true midpoint for all but the three shortest line lengths (SO,90 and 100 mm). In contrast, for left neglect patients there were significant simple main effects of Left Cue [F (1, 5)= 11.08, P
The effects of invisible attentional cues were generally similar to those obtained in Experiment 1. Thus, bisection errors made by subjects in both groups were not affected by the presence or absence of an attentional cue on the right end of the lines. In contrast, for neglect patients, the presence of a left-sided attentional cue significantly reduced the
VISIIILI: AKD
INVISIBLE
(‘US
ON JUDCiEMENTS
LEFT
LEFT
CUE
CUE
IN UNILATERAL
PRESENT
ABSENT
A
left
0
dual
0
no
0
-10
cue cues cues
right
cue
j I
I
I
I
80
90
100
110 Line
Fig. 4. Experiment
1211
NEGLECT
/ 120 length
, 130
140
I
I
I
150
160
170
(mm)
2. Mean bisection error for neglect patients, plotted condition, as a function of line length.
separately
for each cue
magnitude of bisection error compared with those conditions where such a cue was absent. As in Experiment 1, there was a significant difference between the slopes of the Left Cue present and Left Cue absent functions relating patients’ bisection errors to line length (see Fig. 4). Thus, although there was a positive, linear relationship between bisection error and line length when left cues were absent, these errors remained relatively consistent across different line lengths when left cues were present. Normal controls again exhibited bisection errors that were unaffected by the presence or absence of left- or right-sided cues. Failure to find a significant effect of attentional cueing in both the “visible” and “invisible” versions of our paradigm further supports our original assertion, i.e. although normal individuals may exhibit a bisection bias when letter or digit cues are placed adjacent to line ends [20], this effect is reduced or absent (at least in older individuals) when such extraneous visual information is removed. Of course, the same argument cannot be applied to neglect patients, whose substantial bisection error in the absence of left-sided cues was markedly attenuated, even without lateralized visible cues, when their attention was drawn to the left. GENERAL
DISCUSSION
Previous studies of the effects of visual cues on line bisection performance have required subjects to report a letter or digit which is placed adjacent to either end of the line. This alters
1212
J.B.MATTINGLEY crcl/.
the horizontal extent of the stimuli and, in the case of unilateral cueing, produces a stimulus which is visually “lopsided”. Under these circumstances, the relative contributions of the visual attributes of the skzulus are confounded with their potential to draw attrrltim to a particular location on the stimulus figure [ 12, 20, 251. In Experiment 1, subjects generated visual cues which were aligned with the endpoints of each line, thereby maintaining the perceptual point of balance in the horizontal axis of the stimulus. The presence of left-sided cues resulted in a significant reduction in the magnitude of rightward bisection errors among left neglect patients. However, the presence of visual cues in any form may alter the perceptual qualities of the line. It is therefore possible that the effects of left-sided cues found in our first experiment were attributable to heightened perceptual salience afforded by the cue marks themselves. To control for this, in Experiment 2 subjects were required to attend to the appropriate end(s) of each line, but not to change its visual attributes in any way. Once again, left neglect patients exhibited a significant reduction in the extent of rightward bisection errors, even in the absence of visual information, when forced to attend to the left end of the line. In neither experiment were patients’ bisection errors differentially affected by the presence or absence of right-sided cues. Moreover, contrary to previous evidence, control subjects failed to exhibit any significant effects of leftor right-sided cues. Despite our finding that patients’ bisection errors can be influenced even in the absence of “explicit” visual cues, we would in no way wish to deny that the effect is reliant at some point upon visual information per se. Indeed, in both experiments subjects were forced to visuull? attend to the appropriate extremities of each line prior to placing their bisection mark. Moreover, subjects were free to draw upon their memory of visual cues that may have been (transiently) provided by the positioning of both responding hand and pen. Attentional
L’S spatiomotor
cueiny
In addition to any effects of visual attention, spatio-motor cueing may also have influenced subjects’ bisection performance. In a series of experiments conducted by HALLIGAN and colleagues [779]. the position (left or right) from which subjects approached the subjective midpoint of a line was found to influence subsequent bisection judgements of left neglect patients. In one of these experiments [7] the patient’s responding hand was positioned at one or other end of the line prior to being asked to place a bisection mark. Rightward bisection errors were significantly reduced in “left start” compared to “right start” conditions. regardless of which hand was used to respond. On the basis of these and other observations, it was suggested that, in the absence of cues, left neglect patients invariably direct their attention toward the midpoint from the right end of the line. They subsequently place their bisection mark short (i.e. to the right) of the true midpoint by a value corresponding to their “pathologically increased” Weber fraction for judging visual extents [7]. We do not know whether the subjects tested by HALLWAY et (I/. [7] were constrained to move their hand from its starting position to the perceived midpoint of the line, or, as in our experiments, were free to examine and move their hand over the stimulus line from any direction, after initial orientation to the end(s). Indeed, the question of what subjects (and particularly neglect patients) do qfter they have been cued remains vexed. It is possible that the same explanation as that proposed by Halligan and colleagues may account for the performances of our own neglect patients. In the Left cue absent conditions, patients may have adopted a right-to-left “scanpath”, resulting in rightward bisection errors. In contrast, the Left Cue present conditions may have induced a left-to-right scanpath, thereby
VlSlBLE
AND INVISIBLE
CUES ON JUDGEMEYTS
IN UNILATERAL
NEGLECT
1213
overcoming a prevailing attentional bias and reducing (or reversing) bisection errors. Interestingly, in Experiment 1, patients’ errors remained to the left of the true midpoint at most line lengths for both conditions in which left-sided cues were present. In contrast, bisection errors for the same two conditions in Experiment 2 remained predominantly to the right of the true midpoint, This result does not seem to be attributable to differences in overall severity of neglect between the two groups of patients, since their mean error scores in conditions without left cues were very similar. Since the spatio-motor aspects of the task remained identical across the two experiments, it would appear that the continued presence of a lateralized visible mark on the left end of the line provides a small additional bias toward the left side. While the explanation offered by Halligan and colleagues may explain the pattern of bisection errors exhibited by most of our neglect patients, it is difficult to see how it could account for the performance of Patient 6 in Experiment 2 (see Table 5). During testing, Patient 6 was reluctant to mark (invisibly) the left end of the stimulus lines and had to be encouraged to do so (either verbally or by physically moving her arm) on every occasion. Moreover, after marking the left end, she would consistently use the pen to trace along the length of the line to the right end and then move kftwurds (again) to place her transection mark. Insofar as this overt strategy reflected covert attentional scanning, it seems reasonable to conclude that she was approaching the perceived midpoint of each line from the right, regardless of the demands of our cueing procedure. The point of interest here is that, despite a consistent right-to-left approach toward the perceived midpoint, left-sided cueing still resulted in a substantial reduction in the magnitude of rightward bisection errors. This suggests that lateralized cues may influence the subsequent placement of bisections in a manner other than through manipulation of the probability of scanning a line from one end or the other. Perhaps such techniques assist in reducing an otherwise large “zone of indifference”. Alternatively, they may assist in the construction of a more veridical representation of the line. Correlutions
between line bisection und cancellation
tusk perfornzances
HALLIGAN and MARSHALL [I I] reported a classic double-dissociation [14] between performances of two patients with right hemisphere damage on line bisection and the Star Cancellation task from the Behavioural Inattention Test [30]. One patient was unimpaired on the cancellation task but showed a substantial rightward error on (standard) line bisection, while the other patient omitted many targets in the cancellation task but was unimpaired on line bisection. In a separate study, BINDER et ul. [2] examined the performances of 34 right hemisphere damaged patients on standard line bisection and a letter cancellation task [29]. The correlation between line bisection and cancellation task performances obtained from the subset of patients who exhibited unilateral neglect (defined as impaired performance on one or both tasks) was low (r = 0.39) and non-significant. On the basis of these findings, both HALLICAN and MARSHALL [ 1 l] and BINDER et ul. [2] proposed that the so-called “syndrome” of unilateral neglect may in fact be better conceptualized as dissociable phenomena which reflect disruption to quite separate neural mechanisms. Our own views [IS] are in full concordance with this proposition. We therefore performed correlational analyses, on data from our own patients (combined for Experiments 1 and 2), between line bisection errors in the “no cues” condition and omissions on the three cancellation tasks. Significant positive correlations (x=0.01) were obtained between line bisection scores and each of the three cancellation tasks (Albert’s lines,
1214
J. B. MATTINGLEY CTtrl.
=0.78; Circle Cancellation, r =0.77; Star Cancellation, r = 0.8 1). These results, which indicate that the tasks provided a similar index of “neglect severity”, appear to contradict those of BINDER er al. [2]. However, unlike these authors, we did not test patients with a normal line bisection performance, since the main purpose of our experiment was to examine the effects of attentional cues on patients with otherwise abnormal line bisection judgements. In fact, we reanalysed the data reported by BINDER et ul. [2], selecting only those cases where line bisection performance was c~hnormal, and obtained a significant positive correlation (r=0.76) between the tasks, which is comparable to those calculated from our own data. Clearly, the criteria used to select patients for analysis are important. We must therefore conclude (and see also Ref. [2]) that for patients showing abnormal line bisection performance, the number of omissions on cancellation tasks will usua/f~ (but not ~n~uri~zb~~) be impaired to a similar degree. The issue of whether the “neglect syndrome” is in fact, as recently claimed [I I], a “meaningless entity”, remains to be resolved. r
CONCLUSION It is clear that patients with left neglect have a persistent attentional bias to the right which, under appropriate circumstances, can be attenuated or reversed by left-sided spatio-motor and/or attentional cues. While cueing techniques such as those employed here are designed to exert an opposing attentional demand on patients’ prevailing orienting tendency, HJALTAS~N and TEGN~R [13] have recently shown that the extent of patients’ rightward bias on a line bisection task can also be significantly reduced (though not eliminated) by asking patients to bisect illuminated lines in the dark. It may be that under such conditions, extraneous visual information can no longer capture the neglect patient’s attention, and the extent of any rightward bisection error now reflects an “internal” attentional imbalance, free from “external” influences. It would be interesting to compare the performances of neglect patients under conditions of normal illumination and darkness using cueing techniques such as those reported here. Such a study may shed further light on the relative contributions of “internal” and “external” factors in the attentional bias exhibited by patients with neglect. Ackno~c/erlg~,n~,lts~ -WC gratcrully acknowledge the assiatnnce of administration and staB at the following institutions: Alfred Hospital. Austin Hospital, Hampton Rehabilitation Hospital. Heidelberg Repatriation Hospital. Kingston Centre, Monash Medical Ccntre and Royal Talbot Rehabilitation Hospital. This study was supported by ZI grant from the Australian Research Council.
REFERENCES I. ALBIX~. M. L. A simple tesl of VISLUI neglect. &‘~~u~o/o~g~~ 23, 65X 664. 1973. 2. BINIIEK, J.. MARSHALL. R.. LAZAK. R., BI~NJAMIN.J. nnd MOHK. J. P. Distinct syndromes ofhcmineglcct. Ar&. Xrurol. 49, 1187-I 194. 1992. 3. BISIACH, E.. BCLGAKELLI, c‘.. STLK71. R. and VALUK. G. Line bisection and cognitive placticity of unila~er;ll neglect of space. B&iz C;qnif. 2, 32 3X. 1983. 4. BKADSHAW. J. L.. N~TTLETON, N. C.. NATHAS. G. and WILSON;.L. Bisecting rods :md lines: ETTectsof hortzontztl and vertical posture on left side underestimation by normal subjects. N~,urop.\vc,ho/o(/itr 23, 421 425. 1985. 5. ELLIS, A. W.. FLIJLX R. M. and YOLNG, A. W. “Neglect Dyslexia” and the enriy visual processing of letters in words and nonwords. Cocq~~. ,~;:c,lr~op.\,ch~~/. 4, 439 464, 1987. 6. HALLGAY, P. W ~ MAYYIN<,, L. ;tnd MAKSHAI L, J. C. Indivldunl variation in line bisection: A study of four patienta with right hemisphere damage and normal controls. ,Yru,op,\?.c.h~,/o~itr 28, 1043 1051, 1990. I. HALLIGAN, P. W., MAI\xI~~. L. and MAKSHALL, J. C. Hemispheric activation vs spatio-motor cueing in visual neglect: A case study. ~Vru~~,p,\~~ho/oc/icr 29, I65 176, 199 I 8. HALLIGAN. P. W. and MAKSHALL. J. C. Two techniques for the :tsseasment of line bixction in visuo-spatial neglect: A single cast study. J. ,l;e~ool. &‘rur~\urcq. P.\,vc~hitrf52, 1300 1302.1989.
VISIHLEANL)INVISIHLECUES ON JUDGEMENTSIN UNILATERALNEGLECT
1215
9. HALLIC;.~N, P. W. and MAKSHALL, J. C. Perceptual cueing and perceptuo-motor compatibility in visuo-spatial neglect: A single case study. Cognit. Neuropsyckol. 6, 423-435, 1989. 10. HALLIC;AN, P. W. and MAKSHALL, J. C. Figural modulation of visuo-spatial neglect: A case study. Nruropsychologiu 29, 619 628, 1991. 11. HALLIC~AN,P W. and MARSHALL, J. C. Left v&IO-spatial neglect: A meaningless entity’? Cortex 28, 525 535, 1992. 12. HEILMAN. K. M. and VALCNS~FIN, E. Mechanisms underlying hemispatial neglect. Ann. Neural. 5, 166-170, 1979. 13. HJALTASOP;, H. and TEGN~K, R. Darkness improves line bisection in unilateral spatial neglect. Corrrr 28, 353 358, 1992. 14. JONES, Ci. V. On double dissociation of function. Neurops~~,hologiu 21, 397400, 1983. 15. KEPPEL, G. &sign and Anulgsis: A Researcher’.s Handbook, 2nd Edn. Prentice-Hall, Englewood Cliffs, NJ. 1982. 16. MANNING, L., HALLIGAN, P. W. and MARSHALL, J. C. Individual variation in line bisection: A study of normal subjects with application to the interpretation of visual neglect. Neuropsycholoqio 28, 647 655, 1990. 17. MAKSHALL, J. C. and HALLIC;AN, P. W. A study of plane bisection in four cases of visual neglect. Cortex 27, 277 284, 1991. IX. MA~TIN(;LEY, J. B., BKAL)SHAW,J. L. and PHILLIPS, J. G. Re-appraising unilateral neglect. Aust. J. Psycho/. 44, 163-169, 1992. 19. MATTI&(.;LEY,J. B., BRAUSHAW, J. L. and PHILLIPS, J. G. Impairments ofmovement initiation and execution in unilateral neglect: Directional hypokinesia and bradykinesia. Brai,l 11.5, 1849-l 874, 1992. 20. MILNER. A. D., BRECHMANN, M. and PAC;LIARINI, L. To halve and to halve not: An analysis of line bisection judgements in normal subjects. Neuropsychologiu 30, 515-526, 1992. 21. NICH~LLI, P., RINALDI, M. and CUB~LLI, R. Selective spatial attention and length representation in normal subjects and in patients with unilateral spatial neglect. Brain Cognit. 9, 57-70, 1989. 22. PATTERSON, K. and BRAI~SHAW,J. L. Differential hemispheric mediation of nonverbal visual stimuli. J. esp. f’sq’c’hol. Hum. Percrpl. Petj%n. 1, 246 252, 1975. 23. RFUTER-LOR~NZ. P. A., KINSROUKNE,M. and MOS~OVI~~H, M. Hemispheric control ofspatial attention. Bruin Cognit. 12, 24@~266, 1990. 24. RI:UTER-LOK~~NZ,P. A. and POSNEK,M. I. Components ofneglect from right-hemispheredamage: An analysisof line bisection. Nruropsychologia 28, 327 333, 1990. 25. RIDIXICH, J. M. and HUMPHREYS, G. W. The effect of cueing on unilateral neglect. Neurops~~holoUiu 21, 589 599, 1983. 26. ROCK, 1. An Introductim to Prrception. Macmillan, New York. 1975. 27. SCHFNKENHEKG,T., BKADFOKI), D. C. and AJAX, E. T. Line bisection and unilateral visual neglect in patients
with neurological impairment. Neuroloyy 30, 509 517, 1980. 28. TEGNI?R, R. and LEVANDEK, M. The influences of stimulus properties on visual neglect. J. Neural. Neuroswy. Psyrhiut. 54, 882 887, 1991. 29. WEINTRAUH, S. and MESIJLAM, M-M. Visual hemispatial inattention: Stimulus parameters and exploratory strategies. J. Nrurol. Nrurosttry. Psychiut. 51, 148 I-1488, 1988. 30. WILSON, B., CO(‘KBUKN, J. and HALLICAN, P. W. &hatGm/ Inatrentim Te.sr. Thames Valley Test Co., Titchfield, Hants, 1987.