International Journal of Neuroscience
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Attentional Load and Visual Neglect Ian Robertson & Rita Frasca To cite this article: Ian Robertson & Rita Frasca (1991) Attentional Load and Visual Neglect, International Journal of Neuroscience, 62:1-2, 45-56, DOI: 10.3109/00207459108999756 To link to this article: http://dx.doi.org/10.3109/00207459108999756
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Intern. J . Neuroscience, 1992, Vol. 62, pp. 45-56 Reprints available directly from the publisher Photocopying permitted by license only
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ATTENTIONAL LOAD AND VISUAL NEGLECT IAN ROBERTSON Medical Research Council Applied Psychology Unit, 15 Chaucer Road, Cambridge, U . K .
RITA FRASCA
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Centro Richerche, Clinica S Lucia, Roma, Italy. (Received April 26, 1991)
Ten subjects suffering from left unilateral neglect carried out a letter cancellation task under normal conditions, while counting forward, and when generating random numbers, respectively. The index of neglect increased with each of these conditions, though only the normal-random difference was statistically significant. In a second study, four left unilateral neglect subjects and four right brain-damaged controls carried out a simple reaction time task, with stimuli appearing randomly to the left and right, with and without the simultaneous performance of a secondary task (counting backward in threes from 100). The discrepancy between left versus right latencies increased significantly in the secondary task condition for two patients in the neglect group but not for the other two. None of the control group showed this effect. Theoretical implications of these findings for understanding neglect are discussed. Keywords: Attention, neglect, vision.
The question of nonlateralized attentional difficulties in unilateral left visual neglect has been raised by a number of different authors. Rapcsak, Verfaellie, Fleet and Heilman (1989) showed that in a cancellation task, increasing the complexity of the task increased the degree of neglect. They argued that neglect may be a function of a selective attentional process. Mark, Kooistra and Heilman (1988) reported that subjects carrying out a cancellation task showed less left neglect when they cancelled lines by erasure than when they cancelled them by the more normal method of stroking through them with a pencil. This suggested a role for attentional processes on the nonneglected side in the neglect process. Lecours, Mehler, Parente et al. (1987) studied brain-damaged illiterates and found that left brain-damaged patients who explored both sides of space when tested with simple linguistic stimuli tended to restrict visual search to the left side of space when syntactically more complex sentences were used. Right brain-damaged patients were unaffected by sentence complexity in their visual search. This research was supported by the Medical Research Council of Great Britain in the form of a travelling fellowship to the first author. The second author was supported by the Research Committee of the Clinica S Lucia, Rome, Italy. We would like to thank Professor Pizzamiglio, University of Rome, for his help and support in carrying out this research, and also the Clinica S Lucia, Rome, for providing us with the facilities and support for carrying out the research. Many thanks also to all our colleagues at the Centro Ricerche at Clinica S Lucia. Thanks are also due to Professors Daniel Bub and Teren Gum of the Montreal Neurological Institute for allowing us to use their PsychLab software in the preparation of the experiment in Study 2, as well as to Professor Yves Joanette of the Centre de Recherche du Centre hospitalier CGte des Neiges, Montreal, who was also instrumental in allowing us access to the software. 45
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Weintraub and Mesulam ( 1 987) analyzed cancellation scores and found that right brain-damaged patients not only made more left-sided omissions than controls and left brain-damaged patients, but also made more right-sided omissions than either of these groups. Robertson (1989) also proposed a nonlateralized attentional deficit in unilateral left visual neglect, and predicted that one result of this would be a significant increase in right-sided omissions as compared with controls when left neglect patients were cued to the left during the presentation of rapid single of double stimuli. This prediction was substantiated, with left cueing resulting in the equalizing of left versus right errors among the left neglect patients. In a second paper, Robertson (1990) found that degree of neglect was highly correlated with the disparity between forward and backward digit span, which is often taken as an index of capacity for serial information processing. Other indices of possible mental deterioration such as verbal memory or perseveration were uncorrelated with degree of neglect, and the digit span-neglect relationship remained even when the effects of visuo-spatial efficiency were partialled out. This latter finding argues against the view that poor ability to represent the digits spatially in backward span underlies both the span performance and the neglect. Other studies also provide indirect evidence that nonlateralized attentional load affects lateralized neglect. Karnath ( 1988) presented unilateral and bilateral stimuli tachistoscopally to three patients with right brain damage. The degree of extinction of information on the left in bilateral conditions could be reduced by reducing the degree of information analysis required to be done by the subject in the right visual field. Karnath postulates three components underlying neglect and extention-two affecting covert orienting and lateralized attentional shifts, and the other “affecting the directionally nonspecific processing of information by sequential analysis. ” Volpe, Ledoux and Gazzaniga (1979) have shown the presence of pre-attentive processing of stimuli of which there was no awareness in the extinguished field of brain-damaged patients, and more recently Marshall and Halligan (1988) have demonstrated this process more dramatically in a single neglect patient. Pillon (198 1 ) has also shown how decreasing the complexity of the Rey complex figure reduces the amount of neglect shown for the left half of the figure, even though the retinal size of the total shape to be copied remained the same. The theoretical explanations for these diverse findings vary widely: What is in common to them all is the notion that more than just attention to one side of space is impaired in neglect. Hence, the hypothesis tested in this paper is that increasing the nonvisual serial processing demands on neglect patients while they are engaged in a letter-cancellation task should increase the degree of lateralized attentional loss. The first experiment was based on the assumption that if neglect is caused by deficits in a perceptual process which depends upon a limited capacity serial attentional system, then engaging that system with a demanding secondary task while the subject is carrying out a visual task sensitive to neglect should increase the degree of unilateral neglect observed. More specifically, it was predicted that, if during a normal letter cancellation task, subjects were required to generate random numbers, then this task would increase neglect because of its presumed load on the limited capacity “central executive” (Baddeley , 1986).
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EXPERIMENT I-METHOD
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Subjects
The subjects included ten patients suffering from unilateral left visual field neglect, five men and five women, all of whom were in-patients at the Santa Lucia Rehabilitation Hospital in Rome. All had suffered right hemisphere cerebral infarctions with accompanying left hemiplegia, and the mean number of weeks postinfarct was 15.9 (sd 6.3). Their mean age was 73.5 (sd 6.5) and the mean number of years of education was 4.9 (sd 3.0). Eight of the ten patients had been CT scanned, with the following results: 1 . Vast right fronto-parieto-temporal infarct, also in subcortical areas. 2. Poorly defined infarct in area of right sylvian fissure. 3. Right frontoparietal infarct with subcortical involvement. 4. Right temporal infarct. 5. Small right frontal infarct. 6. Large infarct in area of right sylvian fissure. 7. Infarct in posterior branch of internal capsule and on horn of caudate nucleus. 8 . Right fronto-parieto-temporal region. All showed significant left neglect on at least two of the following tests: letter cancellation (‘h’) (version by Diller et al., 1974), Albert’s line cancellation test (Albert, 1973) and a sentence reading test used at the Clinica S Lucia, but not published. The mean percentage errors on Albert’s test of line cancellation was 20.5% (sd 22.5%). Four of the subjects showed a left homonymous hemianopia, one a lower left quandrantanopia, and five showed no visual field defects. Visual field defects were all assessed using a Goldmann perimeter. Apparatus
A standard letter cancellation task (Diller, Ben-Yishay , Gerstman, Goodkin, Gordon, and Weinberg, 1974) was used, consisting of six lines of 52 letters each with the letter “H” appearing 52 times to the left of center and 52 times to the right. Procedure
The sheet of paper was laid on a desk in front of the patient at a distance of approximately 30 centimeters, and he or she was instructed to put a line through each H seen on the sheet, starting on the left, and without missing any. The same test was given three times in one session, in each of three conditions. The first was in the normal way without any additional instructions. The second required the subject to do the task while counting normally from one upwards. The third was to ask the subject to generate random numbers while doing the task, that is to give numbers between 1 and 9 without counting and without any pattern. The order of presentation of the two conditions was random. The total number of correct responses for left versus right were counted for each presentation and the mean left versus right scores obtained for the two separate conditions. The random number generation procedure required each patient to attempt to generate unconnected strings of numbers between 0 and 9. Because of the tendency of patients to match cancellation of letters with giving a number, and because of long pauses in both tasks caused presumably by the demands of dual tasks, the experimenter instructed the patient to say a number at the rate determined by the taps, which was one per second. If patients started to give obviously nonrandom strings of numbers, the experimenter reminded them to give unconnected numbers.
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standard
with normal counting
S
nc
20
with random counting
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10
0
sc
FIGURE 1 Index of neglect on letter cancellation in standard versus normal counting versus random number generation conditions.
An index of neglect was then calculated for each patient on each of the two tests, according to the method of Rapcsak et al. (1989), namely, percentage of responses expected on the left (i.e., 50%) minus the percentage actually observed. This index leads to a maximum neglect score of 50, and a minimum one of zero.
RESULTS An ANOVA showed no statistically significant main effect for condition (F = 1.38; p = .28). However, individual t-tests showed a statistically significant difference in the predicted direction between the standard condition and the random counting conditions ( t = -1.84; p = .049; one tailed). Figure 1 illustrates the results.
CONCLUSIONS FROM EXPERIMENT 1. These results provide only weak support for the hypothesis proposed, though it does suggest the need for further study along these lines. Letter cancellation is, however, a complex task involving psychomotor coordination and general attentional capacities which may make any effects of attentional load on lateralized omissions less easy to detect. Thus, a second experiment minimizing the general attentional and motor aspects of the previous task was devised.
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EXPERIMENT 2-INTRODUCTION The basic task in the second experiment consisted of a simple computerized numberreading/stimulus-detection exercise which only required the subject to press a button when a stimulus was seen, either in the left or in the right visual field. Hence, the attentional demands of the basic task were reduced, as were the visual search and psychomotor elements, as compared to the basic task of the previous experiment.
METHOD
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Subjects
The subjects included four patients suffering from unilateral left visual field neglect (two men and two women) and four control patients (two men and two women) with right hemisphere lesions and left hemiplagia who had no signs of unilateral left visual neglect. All were in-patients at the Santa Lucia Rehabilitation Hospital in Rome. All subjects had suffered right hemisphere cerebral infarctions with accompanying left hemiplegia. The four neglect patients had the following characteristics. Patient M 66 year-old man, right-handed, 13 weeks postinfarct, left homonymous hemianopia, left hemiplegia, nine years of formal education, with following CT scan report: “area of profound hypodensity in right Sylvian area, margins badly defined, with oedema and compression of the ventricle.” This patient made 14 errors on Albert’s test-all on the left-and cancelled only the rightmost five of 104 stimuli on a simple letter cancellation task. Patient B 67 year-old woman, right-handed, I 1 weeks postinfarct, left hemiplegia, six years of formal education, with following CT scan report: “area of hypodensity in right anterior medial temporal region with light perilesional oedema. ” This patient made no errors on Albert’s test, but omitted 57 letters on a letter cancellation test, all towards the left. Patient T 80 year-old right-handed woman, seven weeks postinfarct, left hemiplegia, six years of formal education. No CT scan carried out. This patient made four errors, all left, on Albert’s test, and omitted 64 letters, again all left, from the letter cancellation test. Patient I 68 year-old left-handed male, fifteen weeks postinfarct, left hemiplegia, eight years of formal education. No CT scan available. Fifteen errors on Albert’s test, all left, and 86 on letter cancellation, 79 on left.
The control patients were as follows. Patient F 73 year-old right-handed male, thirteen weeks postinfarct, left hemiplegia, six years of formal education. No CT scan available. No errors on Albert’s or letter cancellation tests. Patient N 64 year-old right-handed woman, eight weeks postinfarct, three years of formal education, no CT scan available, left hemiplegia. No errors on Albert’s or letter cancellation tests.
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Patient G 76 year-old right-handed woman, twelve weeks postinfarct, three years of formal education, no CT scan available, left hemiplegia. No errors on Albert's or letter cancellation tests. Patient D 59 year-old male, sixteen weeks postinfarct. Five years of formal education, left hemiplegia, CT reported "profound area of hypodensity in right temporofrontal area." No errors on Albert's or letter cancellation tests.
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Procedure
All subjects were given the letter cancellation ('h') (version by Diller et al., 1974), as well as Albert's line cancellation test (Albert, 1973). Subjects were seated in front of an Apple Macintosh 2E microcomputer, their eyes at a distance of 35 centimeters from the screen. They were asked to fixate a point marked at the center of the screen, which was adjusted to the subject's eye level. A chin rest was used to aid fixation. The experiment was prepared using the PsychLab software. Fixation was checked by the experimenter with the aid of a mirror. In the basic task, random numbers between 0 and 9 were presented randomly to the left and right 2.3" eccentric to the fixation point. This was within the intact visual fields of all hemianopic subjects. Numbers subtended a vertical angle of .80" and a horizontal angle of .46". Numbers were presented for three seconds or until the subject pressed the space bar on the keyboard. There was an interval of three seconds between presentations. There were twenty left and twenty right presentations for each of the two experimental conditions, and the left-right trials were randomized within each condition. In addition, ten "catch" trials were randomly presented within each group of 40 trials. These consisted of central presentation of an asterisk, .46" visual angle by .46". Patients were told not to respond to these, and any responses were recorded. In all cases in whom just one round was given, the standard (no counting) condition was given first. This was to minimize the stress of the procedure for patients, and also because any resulting practice effect would go against the direction predicted by the hypothesis, thus lessening the chances of a falsely positive result. In cases in whom the experiment was repeated, the backward counting condition was always given first in the second round. In some patients, depending on their tolerance of the procedure, two rounds of the 50 trials (including catch trials) were given. Reaction times less than 100 milliseconds were omitted from the analysis. Nonresponses were given the default value of 300 ms. In the basic task, the subject simply had to press the space bar on the keyboard as soon as a number was detected to the left or right. The computer recorded the response latency. Prior to the experiment, a practice round of ten left, ten right, and five catch trials was given. In some cases this was repeated if comprehension had been poor. The second condition consisted of the same task of responding to a stimulus as soon as it appeared, by pressing the space bar, but this time subjects were told that they had to count backward from 100 by threes, namely 100, 97, 94 etc. Errors were
'
'PsychLab software developed by Daniel Bub and Teren Gum of the Montreal Neurological Institute, Canada.
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not corrected unless the subject reverted to normal backward counting, in which case he or she was prompted to resume backward counting by threes. Several patients could not carry out this task and were excluded from the study. The number of correct responses in each trial was recorded. Responses were judged to be correct if they were three less than the previous one, even though the previous one may have been wrong with respect to its predecessor. Twenty left, twenty right, and ten catch trials with backward counting were given as a practice prior to the backward counting condition.
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RESULTS The backward counting task produced lengthening in both left and right latencies, and, therefore, the ratio of backward counting to normal performance latencies were calculated separately for left and right responses. Paired t-tests were then performed comparing the ratios of backward to normal latencies in the left versus right sides. The hypothesis under test was that there would be significantly greater ratios for left responses as compared with the right responses, and therefore one-tailed tests of significance were used. There was a significantly greater ratio on the left compared to the right for this subject. The mean ratio of left backward to left normal scores was 3.4 (sd 2.0), while the equivalent ratio for the right latencies was 1.6 (sd 1.2). This difference was statistically significant ( t = 4.3; p < .OOOl). This patient only made four errors of a total of 62 responses during backward counting, and made no catch trial errors.
Patient M
There was a significantly greater ratio on the left compared to the right for this subject. The mean ratio of left backward to left normal scores was 2.9 (sd 1.3), while the equivalent ratio for the right latencies was 2.2 (sd 1.3). This difference was statistically significant ( t = - 1.8; p = .04). This patient made twelve errors of a total of 50 responses during backward counting, and made no catch trial errors.
Patient B
There was no statistically significant difference in the two ratios (left ratio = 2.1 (sd 1.5); right ratio = 2.3 (sd = 1.9); t = -.42; p = .34). This patient made ten errors out of a total of 60 responses during backward counting, and made one catch trial error.
Patient T
There was no statistically significant difference in the two ratios (left ratio 2.2 (sd 1.2); right ratio = 2.3 (sd 1.5); t = -.73; p = .24). This patient made twelve errors out of a total of 61 responses during backward counting, and made one catch trial error.
Patient I =
Control Patients Patient F There was no statistically significant difference in the two ratios (left ratio = 1.8 (sd 1.2); right ratio = 2.4 (sd 1.9); t = -1.12; p = .14). This patient made five errors out of a total of 42 responses during backward counting, and made no catch trial errors.
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TABLE 1 Means and Standard Deviations of Latencies of Response to Lateralized Stimuli in Experiment 2 (All Values in Milliseconds)
Subject
Normal Left
Normal Right
m neglect b neglect
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t
neglect i neglect f control n control g control d control
Backcount Left
Backcount Right
2659 (753) 1759 (821) 1930 (948) 2023 (986) 1029 (749) 1769 (490) 2032 (841) 1357 (992)
1057 (840) 1265 (6 17) 1592 (976) 1592 (1048) 1245 (933) 1751 (515) 2214 (856) 1388 (976)
Patient N There was no statistically significant difference in the two ratios (left ratio = 2.4 (sd 1.0); right ratio = 2.5 (sd 1.0); t = -.36; p = .36). This patient made fourteen errors out of a total of 60 responses during backward counting, and made no catch trial errors. Patient G There was no statistically significant difference in the two ratios (left ratio = 1.3 (sd 1.83); right ratio = 1.7 (sd 2.9); t = -1.0; p = .16). This patient made eighteen errors out of a total of 67 responses during backward counting, and made no catch trial errors. Patient D There was no statistically significant difference in the two ratios (left ratio = 1.1 (sd .79); right ratio = 1.27 (sd = .85); t = -.53; p = .3). This patient made twelve errors out of a total of 58 responses during backward counting, and made no catch trial errors. Performance on the actual backward counting task was similar in both groups, and, indeed, between individual subjects. With the total number of trials given controlled for, (i.e., where only one round given the backward count total and error scores was doubled), the mean number of correct numbers given during the backward condition trials was 60.7 for the experimentals and 54.5 for the controls. The mean error responses given were 12.5 for the experimentals and 11.O for the controls. Catch trial responses were at very low levels for both groups. Table 1 shows the means and standard deviations of laltency of response for the eight subjects, by side and by experimental condition. Figures 2 and 3 show graphs of the responses of neglect patients M and B.
CONCLUSIONS FROM EXPERIMENT 2 The experimental hypothesis is supported by this study only in the case of two of the neglect patients. The two remaining neglect patients showed no tendency for
A'ITENTIONAL LOAD AND VISUAL NEGLECT
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Case 'M'
3000
2658
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2000
1000 0 l e f t right FIGURE 2 'M'.
*
l e f t right
Effect of backward counting task on speed of detection of left versus right stimuli: Case
their neglect to worsen when engaged in an attentionally demanding secondary task. None of the right brain-damaged control patients showed any such tendency. In the two patients who showed the hypothesized effect, engaging them in a nonvisual secondary task while carrying out a visual scanning test was significantly to
Case 'B'
2000 1
1758
1 01 l e f t right FIGURE 3 'B'.
*
l e f t right
Effect of backward counting task o n speed of detection of left versus right stimuli: Case
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I. ROBERTSON AND R. FRASCA
lengthen left reaction times with respect to right reaction times compared to performance under normal conditions. A group of right brain-damaged controls showed no such selectively lateralized effect of the secondary task on visual task performance, even though reaction times generally were increased during dual tasking. The secondary task was performed with reasonable accuracy in all cases, and there was no significant difference between the two groups on performance on this. This was no doubt in part due to the fact that several neglect patients were excluded who could not do either the counting task alone, or the counting task in conjunction with the visual scanning task. The generalizability of these results cannot, therefore, extent to the population of neglect patients unable to perform this combination of tasks.
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GENERAL CONCLUSIONS There is converging evidence to support the existence of a nonlateralized attentional deficit associated with unilateral left visual neglect. The two studies reported give some support to this view, though the second study suggests that there may be only some neglect patients who show such an association. One obvious objection to the above experiments is that the results are not specific to neglect. It could be argued that any impaired cognitive function would deteriorate under increased attentional load. While this is probably true for many conditions, the finding has special relevance for unilateral neglect, because of the demonstrated association between seventy of neglect on the one hand, and nonlateralized serial attentional problems on the other (Robertson, 1989, 1990; Rapscak et al., 1989; Lecours et al., 1987). The relevance of this phenomenon in neglect lies in a hypothesized special vulnerability of neglect patients to deteriorating performance in the face of additional attentional load. If this is true, then it might provide an explanation as to why neglect is such a major prognostic factor for poor motor, and other, recovery (see, for example, Denes, Semenza, Stoppa, and Lis, 1982). In other words, it is the nonlaterialized attentional deficit, as much as the lateralized attentional deficit, which is implicated in the poor recovery. By this argument, most patients who suffer from neglect in the early stages following CVA recover spontaneously by learning compensatory scanning habits which rapidly become automatic. The minority who do not recover (and who thereafter show poor rates of recovery, cf., for instance, Robertson, Gray, Pentland and Waite, 1990) may show poor automatization of compensatory scanning because of an associated limitation in dual tasking. In other words, a limited capacity for organizing attention to multiple tasks makes it very difficult for these people ever to render automatic these habits of compensation in the context of everyday activities such as reading, transferring from wheelchairs, etc. What could the origins of this possible association between neglect and attentional effort be? There are at least four possible explanations. 1. The relationship may be correlational, with both the attentional loss and the neglect being associated with severity of brain damage. If this were the case, then one would predict that the correlation would disappear when lesion size is partialled out. 2. The mechanisms involved in selective attention may be closely related to those underlying unilateral neglect. This is the hypothesis of Rapscak et al. (1989).
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3. Diaschisis may cause poor function in subcortical (e.g., thalamic) regions resulting from cortical (e.g., inferior pariental) damage, with associated loss of function on nonlateralized attentional capacity.
In relation to this last point, Deuel (1987) showed the mechanism of diaschisis operating in monkeys following cortical ablation which resulted in subcortical hypoperfusion, and Perani, Vallar, Cappa, Messa and Fazio (1987) found considerable hypoperfusion of cortical areas following subcortical strokes in humans, using SPECT. Hence, different neuropsychological mechanisms subserved by different structures may covary in the degree of deficit they manifest because of the effects of diaschisis. 4. A fourth explanation is suggested by the theoretical model of attention proposed by Posner and Peterson (1990). Posner, Inhoff, Freidrich and Cohen (1987) found that subjects with right parietal lesions showed significant decrements in performance in reaction time tasks in which no warning was given as compared to ones in which a warning signal was given. Their performance on warned reaction time tasks was comparable to that of left parietally-damaged subjects, though the latter did not show the same dramatic deterioration in performance in the absence of a warning stimulus. This suggests, as has been suggested by other authors, that the right cerebral hemisphere has some special responsibility for vigilance or alerting, the latter being one of the attentional systems proposed by Posner and Peterson. Another of their attentional systems is for orientation, which they propose to be bilaterally represented, probably in the parietal cortex. Posner and his colleagues (Posner et al., 1984) have already shown that parietally-damaged patients have difficulty in disengaging their attention from stimuli presented ipsilesionally, and have suggested this to be a basic mechanism for the lateralized problems in visual neglect. Thus, Posner and Peterson’s theory would predict a two-factor model of deficits following right parietal lesions: a lateralized deficit caused by disruption of the orientation mechanism of attention, and a vigilance-alerting deficit caused by disruption of a right hemisphere vigilance circuit. It is this combination of deficits which would explain the greater severity and prevalence of left over right visual neglect. Hence, the close relationship between lateralized and nonlateralized attentional problems presented above is explained, according to Posner and Peterson, in terms of the damage of two functionally separate but anatomically neighboring attentional systems. It should be possible to find subjects with damage to one type of attention but not the other, so the findings of the second study above, in which only two of four subjects showed the phenomenon, should not be surprising. Given, however, that subjects with visual neglect commonly have large cerebral lesions spreading into more than one lobe, then a large proportion of patients with neglect should show both types of attentional disorder. This fourth and last hypothesis is proposed as the strongest contender to explain the results presented above.
REFERENCES Albert, M . L. (1973). A simple test of visual neglect. Neurology, 23. 658-665. Baddeley, A . D. (1986). Working memory. Oxford: Oxford University Press. Crick, F. (1984). Functions of the thalamic reticular complex: the searchlight hypothesis. Proceedings of the National Academy of Science. USA, 81,4586-4590. Denes, G., Semenza, C . , Stoppa, E. & Lis, A . (1982). Unilateral spatial neglect and recovery from hemiplagia. A follow-up study. Bruin, 105, 543-552.
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Deuel, R. (1987). Diaschisis following frontal and panetal lesions in monkeys. In M. Jeannerod (ed.) Neurophysiological and Neuropsychologicul Aspects of Neglect. North Holland, Elsevier. Diller, L., Ben-Yishay, Y., Gerstman, L., Goodkin, R.,Gordon, W. & Weinberg, J. (1974). Studies in Cognition and Rehabilitation in Hemiplegia. Rehabilitation Monograph No. 50. New York, New York University Medical Center. Heilman, K. M. & Van Den Abell, T. (1980). Right hemisphere dominance for attention: the mechanism underlying hemisphere asymmetries of inattention (neglect). Neurology, 30. 327-330. Julesz, B. (1981). Textons, the elements of texture perception, and their interactions. Nature, 290, 9197. Lecours, A. R., Mehler, F., Parente, M. A. et al. (1987). Illiteracy and brain damage: 11. Manifestations of unilateral neglect in testing “auditory comprehension” with iconographic materials. Bruin and Cognition, 6. 243-265. Mark, V. W., Kooistra, C. A. & Heilman, K. M. (1988). Hemispatial neglect affected by non-neglected stimuli. Neurology, 38, 1207-121 1. Perani, D., Vallar, G., Cappa, S., Messa, C. & Fazio, F. (1987). Aphasia and neglect after subcortical stroke. Brain, I I O , 1211-1229. Posner, M. I. & Peterson, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25-42. Posner, M. I., Inhoff, A,, Friedrich, F. J. & Cohen, A. (1987). Isolating attentional systems: A cognitive-anatomical analysis. Psychobiology, 15, 107- 121. Rapcsack, S. Z . , Verfaellie, M., Fleet, S. & Heilman, K. M. (1989). Selective attention in hemispatial neglect. Arch. Neurol., 46, 172-178. Robertson, I. (1 989). Anomolies in the lateralisation omissions in unilateral left neglect: implications for an attentional theory of neglect. Neuropsychologia, 27, 157-165. Robertson, I. (1990). Digit span and visual neglect: a puzzling relationship. Neuropsychologiu, 28, 2 17222. Robertson, I., Gray, J., Pentland, B. & Waite, L. (1990). Microcomputer-based rehabilitation of unilateral left visual neglect: a randomised controlled trial. Archives of Physical Medicine and Rehabilitation, 71. 663-668. von Monakow, C. (1914). Die Lokalisation irn Grosshirn und der Abbau der Funktion durch Kortikale Herde. Wiesbaden: J. F. Bergmann. Weintraub, S. & Mesulam, M. (1987). Right cerebral dominance in spatial attention. Further evidence based on ipsilateral neglect. Archives of Neurology, 44, 621-625.
ISSN: 0020-7454 (Print) 1543-5245 (Online) Journal homepage: http://www.tandfonline.com/loi/ines20
Attentional Load and Visual Neglect Ian Robertson & Rita Frasca To cite this article: Ian Robertson & Rita Frasca (1991) Attentional Load and Visual Neglect, International Journal of Neuroscience, 62:1-2, 45-56, DOI: 10.3109/00207459108999756 To link to this article: http://dx.doi.org/10.3109/00207459108999756
Published online: 07 Jul 2009.
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0 1992 Gordon and Breach Science Publishers S.A.
Intern. J . Neuroscience, 1992, Vol. 62, pp. 45-56 Reprints available directly from the publisher Photocopying permitted by license only
Printed in the United States of America
ATTENTIONAL LOAD AND VISUAL NEGLECT IAN ROBERTSON Medical Research Council Applied Psychology Unit, 15 Chaucer Road, Cambridge, U . K .
RITA FRASCA
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Centro Richerche, Clinica S Lucia, Roma, Italy. (Received April 26, 1991)
Ten subjects suffering from left unilateral neglect carried out a letter cancellation task under normal conditions, while counting forward, and when generating random numbers, respectively. The index of neglect increased with each of these conditions, though only the normal-random difference was statistically significant. In a second study, four left unilateral neglect subjects and four right brain-damaged controls carried out a simple reaction time task, with stimuli appearing randomly to the left and right, with and without the simultaneous performance of a secondary task (counting backward in threes from 100). The discrepancy between left versus right latencies increased significantly in the secondary task condition for two patients in the neglect group but not for the other two. None of the control group showed this effect. Theoretical implications of these findings for understanding neglect are discussed. Keywords: Attention, neglect, vision.
The question of nonlateralized attentional difficulties in unilateral left visual neglect has been raised by a number of different authors. Rapcsak, Verfaellie, Fleet and Heilman (1989) showed that in a cancellation task, increasing the complexity of the task increased the degree of neglect. They argued that neglect may be a function of a selective attentional process. Mark, Kooistra and Heilman (1988) reported that subjects carrying out a cancellation task showed less left neglect when they cancelled lines by erasure than when they cancelled them by the more normal method of stroking through them with a pencil. This suggested a role for attentional processes on the nonneglected side in the neglect process. Lecours, Mehler, Parente et al. (1987) studied brain-damaged illiterates and found that left brain-damaged patients who explored both sides of space when tested with simple linguistic stimuli tended to restrict visual search to the left side of space when syntactically more complex sentences were used. Right brain-damaged patients were unaffected by sentence complexity in their visual search. This research was supported by the Medical Research Council of Great Britain in the form of a travelling fellowship to the first author. The second author was supported by the Research Committee of the Clinica S Lucia, Rome, Italy. We would like to thank Professor Pizzamiglio, University of Rome, for his help and support in carrying out this research, and also the Clinica S Lucia, Rome, for providing us with the facilities and support for carrying out the research. Many thanks also to all our colleagues at the Centro Ricerche at Clinica S Lucia. Thanks are also due to Professors Daniel Bub and Teren Gum of the Montreal Neurological Institute for allowing us to use their PsychLab software in the preparation of the experiment in Study 2, as well as to Professor Yves Joanette of the Centre de Recherche du Centre hospitalier CGte des Neiges, Montreal, who was also instrumental in allowing us access to the software. 45
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Weintraub and Mesulam ( 1 987) analyzed cancellation scores and found that right brain-damaged patients not only made more left-sided omissions than controls and left brain-damaged patients, but also made more right-sided omissions than either of these groups. Robertson (1989) also proposed a nonlateralized attentional deficit in unilateral left visual neglect, and predicted that one result of this would be a significant increase in right-sided omissions as compared with controls when left neglect patients were cued to the left during the presentation of rapid single of double stimuli. This prediction was substantiated, with left cueing resulting in the equalizing of left versus right errors among the left neglect patients. In a second paper, Robertson (1990) found that degree of neglect was highly correlated with the disparity between forward and backward digit span, which is often taken as an index of capacity for serial information processing. Other indices of possible mental deterioration such as verbal memory or perseveration were uncorrelated with degree of neglect, and the digit span-neglect relationship remained even when the effects of visuo-spatial efficiency were partialled out. This latter finding argues against the view that poor ability to represent the digits spatially in backward span underlies both the span performance and the neglect. Other studies also provide indirect evidence that nonlateralized attentional load affects lateralized neglect. Karnath ( 1988) presented unilateral and bilateral stimuli tachistoscopally to three patients with right brain damage. The degree of extinction of information on the left in bilateral conditions could be reduced by reducing the degree of information analysis required to be done by the subject in the right visual field. Karnath postulates three components underlying neglect and extention-two affecting covert orienting and lateralized attentional shifts, and the other “affecting the directionally nonspecific processing of information by sequential analysis. ” Volpe, Ledoux and Gazzaniga (1979) have shown the presence of pre-attentive processing of stimuli of which there was no awareness in the extinguished field of brain-damaged patients, and more recently Marshall and Halligan (1988) have demonstrated this process more dramatically in a single neglect patient. Pillon (198 1 ) has also shown how decreasing the complexity of the Rey complex figure reduces the amount of neglect shown for the left half of the figure, even though the retinal size of the total shape to be copied remained the same. The theoretical explanations for these diverse findings vary widely: What is in common to them all is the notion that more than just attention to one side of space is impaired in neglect. Hence, the hypothesis tested in this paper is that increasing the nonvisual serial processing demands on neglect patients while they are engaged in a letter-cancellation task should increase the degree of lateralized attentional loss. The first experiment was based on the assumption that if neglect is caused by deficits in a perceptual process which depends upon a limited capacity serial attentional system, then engaging that system with a demanding secondary task while the subject is carrying out a visual task sensitive to neglect should increase the degree of unilateral neglect observed. More specifically, it was predicted that, if during a normal letter cancellation task, subjects were required to generate random numbers, then this task would increase neglect because of its presumed load on the limited capacity “central executive” (Baddeley , 1986).
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EXPERIMENT I-METHOD
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Subjects
The subjects included ten patients suffering from unilateral left visual field neglect, five men and five women, all of whom were in-patients at the Santa Lucia Rehabilitation Hospital in Rome. All had suffered right hemisphere cerebral infarctions with accompanying left hemiplegia, and the mean number of weeks postinfarct was 15.9 (sd 6.3). Their mean age was 73.5 (sd 6.5) and the mean number of years of education was 4.9 (sd 3.0). Eight of the ten patients had been CT scanned, with the following results: 1 . Vast right fronto-parieto-temporal infarct, also in subcortical areas. 2. Poorly defined infarct in area of right sylvian fissure. 3. Right frontoparietal infarct with subcortical involvement. 4. Right temporal infarct. 5. Small right frontal infarct. 6. Large infarct in area of right sylvian fissure. 7. Infarct in posterior branch of internal capsule and on horn of caudate nucleus. 8 . Right fronto-parieto-temporal region. All showed significant left neglect on at least two of the following tests: letter cancellation (‘h’) (version by Diller et al., 1974), Albert’s line cancellation test (Albert, 1973) and a sentence reading test used at the Clinica S Lucia, but not published. The mean percentage errors on Albert’s test of line cancellation was 20.5% (sd 22.5%). Four of the subjects showed a left homonymous hemianopia, one a lower left quandrantanopia, and five showed no visual field defects. Visual field defects were all assessed using a Goldmann perimeter. Apparatus
A standard letter cancellation task (Diller, Ben-Yishay , Gerstman, Goodkin, Gordon, and Weinberg, 1974) was used, consisting of six lines of 52 letters each with the letter “H” appearing 52 times to the left of center and 52 times to the right. Procedure
The sheet of paper was laid on a desk in front of the patient at a distance of approximately 30 centimeters, and he or she was instructed to put a line through each H seen on the sheet, starting on the left, and without missing any. The same test was given three times in one session, in each of three conditions. The first was in the normal way without any additional instructions. The second required the subject to do the task while counting normally from one upwards. The third was to ask the subject to generate random numbers while doing the task, that is to give numbers between 1 and 9 without counting and without any pattern. The order of presentation of the two conditions was random. The total number of correct responses for left versus right were counted for each presentation and the mean left versus right scores obtained for the two separate conditions. The random number generation procedure required each patient to attempt to generate unconnected strings of numbers between 0 and 9. Because of the tendency of patients to match cancellation of letters with giving a number, and because of long pauses in both tasks caused presumably by the demands of dual tasks, the experimenter instructed the patient to say a number at the rate determined by the taps, which was one per second. If patients started to give obviously nonrandom strings of numbers, the experimenter reminded them to give unconnected numbers.
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standard
with normal counting
S
nc
20
with random counting
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10
0
sc
FIGURE 1 Index of neglect on letter cancellation in standard versus normal counting versus random number generation conditions.
An index of neglect was then calculated for each patient on each of the two tests, according to the method of Rapcsak et al. (1989), namely, percentage of responses expected on the left (i.e., 50%) minus the percentage actually observed. This index leads to a maximum neglect score of 50, and a minimum one of zero.
RESULTS An ANOVA showed no statistically significant main effect for condition (F = 1.38; p = .28). However, individual t-tests showed a statistically significant difference in the predicted direction between the standard condition and the random counting conditions ( t = -1.84; p = .049; one tailed). Figure 1 illustrates the results.
CONCLUSIONS FROM EXPERIMENT 1. These results provide only weak support for the hypothesis proposed, though it does suggest the need for further study along these lines. Letter cancellation is, however, a complex task involving psychomotor coordination and general attentional capacities which may make any effects of attentional load on lateralized omissions less easy to detect. Thus, a second experiment minimizing the general attentional and motor aspects of the previous task was devised.
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EXPERIMENT 2-INTRODUCTION The basic task in the second experiment consisted of a simple computerized numberreading/stimulus-detection exercise which only required the subject to press a button when a stimulus was seen, either in the left or in the right visual field. Hence, the attentional demands of the basic task were reduced, as were the visual search and psychomotor elements, as compared to the basic task of the previous experiment.
METHOD
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Subjects
The subjects included four patients suffering from unilateral left visual field neglect (two men and two women) and four control patients (two men and two women) with right hemisphere lesions and left hemiplagia who had no signs of unilateral left visual neglect. All were in-patients at the Santa Lucia Rehabilitation Hospital in Rome. All subjects had suffered right hemisphere cerebral infarctions with accompanying left hemiplegia. The four neglect patients had the following characteristics. Patient M 66 year-old man, right-handed, 13 weeks postinfarct, left homonymous hemianopia, left hemiplegia, nine years of formal education, with following CT scan report: “area of profound hypodensity in right Sylvian area, margins badly defined, with oedema and compression of the ventricle.” This patient made 14 errors on Albert’s test-all on the left-and cancelled only the rightmost five of 104 stimuli on a simple letter cancellation task. Patient B 67 year-old woman, right-handed, I 1 weeks postinfarct, left hemiplegia, six years of formal education, with following CT scan report: “area of hypodensity in right anterior medial temporal region with light perilesional oedema. ” This patient made no errors on Albert’s test, but omitted 57 letters on a letter cancellation test, all towards the left. Patient T 80 year-old right-handed woman, seven weeks postinfarct, left hemiplegia, six years of formal education. No CT scan carried out. This patient made four errors, all left, on Albert’s test, and omitted 64 letters, again all left, from the letter cancellation test. Patient I 68 year-old left-handed male, fifteen weeks postinfarct, left hemiplegia, eight years of formal education. No CT scan available. Fifteen errors on Albert’s test, all left, and 86 on letter cancellation, 79 on left.
The control patients were as follows. Patient F 73 year-old right-handed male, thirteen weeks postinfarct, left hemiplegia, six years of formal education. No CT scan available. No errors on Albert’s or letter cancellation tests. Patient N 64 year-old right-handed woman, eight weeks postinfarct, three years of formal education, no CT scan available, left hemiplegia. No errors on Albert’s or letter cancellation tests.
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Patient G 76 year-old right-handed woman, twelve weeks postinfarct, three years of formal education, no CT scan available, left hemiplegia. No errors on Albert's or letter cancellation tests. Patient D 59 year-old male, sixteen weeks postinfarct. Five years of formal education, left hemiplegia, CT reported "profound area of hypodensity in right temporofrontal area." No errors on Albert's or letter cancellation tests.
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Procedure
All subjects were given the letter cancellation ('h') (version by Diller et al., 1974), as well as Albert's line cancellation test (Albert, 1973). Subjects were seated in front of an Apple Macintosh 2E microcomputer, their eyes at a distance of 35 centimeters from the screen. They were asked to fixate a point marked at the center of the screen, which was adjusted to the subject's eye level. A chin rest was used to aid fixation. The experiment was prepared using the PsychLab software. Fixation was checked by the experimenter with the aid of a mirror. In the basic task, random numbers between 0 and 9 were presented randomly to the left and right 2.3" eccentric to the fixation point. This was within the intact visual fields of all hemianopic subjects. Numbers subtended a vertical angle of .80" and a horizontal angle of .46". Numbers were presented for three seconds or until the subject pressed the space bar on the keyboard. There was an interval of three seconds between presentations. There were twenty left and twenty right presentations for each of the two experimental conditions, and the left-right trials were randomized within each condition. In addition, ten "catch" trials were randomly presented within each group of 40 trials. These consisted of central presentation of an asterisk, .46" visual angle by .46". Patients were told not to respond to these, and any responses were recorded. In all cases in whom just one round was given, the standard (no counting) condition was given first. This was to minimize the stress of the procedure for patients, and also because any resulting practice effect would go against the direction predicted by the hypothesis, thus lessening the chances of a falsely positive result. In cases in whom the experiment was repeated, the backward counting condition was always given first in the second round. In some patients, depending on their tolerance of the procedure, two rounds of the 50 trials (including catch trials) were given. Reaction times less than 100 milliseconds were omitted from the analysis. Nonresponses were given the default value of 300 ms. In the basic task, the subject simply had to press the space bar on the keyboard as soon as a number was detected to the left or right. The computer recorded the response latency. Prior to the experiment, a practice round of ten left, ten right, and five catch trials was given. In some cases this was repeated if comprehension had been poor. The second condition consisted of the same task of responding to a stimulus as soon as it appeared, by pressing the space bar, but this time subjects were told that they had to count backward from 100 by threes, namely 100, 97, 94 etc. Errors were
'
'PsychLab software developed by Daniel Bub and Teren Gum of the Montreal Neurological Institute, Canada.
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not corrected unless the subject reverted to normal backward counting, in which case he or she was prompted to resume backward counting by threes. Several patients could not carry out this task and were excluded from the study. The number of correct responses in each trial was recorded. Responses were judged to be correct if they were three less than the previous one, even though the previous one may have been wrong with respect to its predecessor. Twenty left, twenty right, and ten catch trials with backward counting were given as a practice prior to the backward counting condition.
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RESULTS The backward counting task produced lengthening in both left and right latencies, and, therefore, the ratio of backward counting to normal performance latencies were calculated separately for left and right responses. Paired t-tests were then performed comparing the ratios of backward to normal latencies in the left versus right sides. The hypothesis under test was that there would be significantly greater ratios for left responses as compared with the right responses, and therefore one-tailed tests of significance were used. There was a significantly greater ratio on the left compared to the right for this subject. The mean ratio of left backward to left normal scores was 3.4 (sd 2.0), while the equivalent ratio for the right latencies was 1.6 (sd 1.2). This difference was statistically significant ( t = 4.3; p < .OOOl). This patient only made four errors of a total of 62 responses during backward counting, and made no catch trial errors.
Patient M
There was a significantly greater ratio on the left compared to the right for this subject. The mean ratio of left backward to left normal scores was 2.9 (sd 1.3), while the equivalent ratio for the right latencies was 2.2 (sd 1.3). This difference was statistically significant ( t = - 1.8; p = .04). This patient made twelve errors of a total of 50 responses during backward counting, and made no catch trial errors.
Patient B
There was no statistically significant difference in the two ratios (left ratio = 2.1 (sd 1.5); right ratio = 2.3 (sd = 1.9); t = -.42; p = .34). This patient made ten errors out of a total of 60 responses during backward counting, and made one catch trial error.
Patient T
There was no statistically significant difference in the two ratios (left ratio 2.2 (sd 1.2); right ratio = 2.3 (sd 1.5); t = -.73; p = .24). This patient made twelve errors out of a total of 61 responses during backward counting, and made one catch trial error.
Patient I =
Control Patients Patient F There was no statistically significant difference in the two ratios (left ratio = 1.8 (sd 1.2); right ratio = 2.4 (sd 1.9); t = -1.12; p = .14). This patient made five errors out of a total of 42 responses during backward counting, and made no catch trial errors.
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TABLE 1 Means and Standard Deviations of Latencies of Response to Lateralized Stimuli in Experiment 2 (All Values in Milliseconds)
Subject
Normal Left
Normal Right
m neglect b neglect
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t
neglect i neglect f control n control g control d control
Backcount Left
Backcount Right
2659 (753) 1759 (821) 1930 (948) 2023 (986) 1029 (749) 1769 (490) 2032 (841) 1357 (992)
1057 (840) 1265 (6 17) 1592 (976) 1592 (1048) 1245 (933) 1751 (515) 2214 (856) 1388 (976)
Patient N There was no statistically significant difference in the two ratios (left ratio = 2.4 (sd 1.0); right ratio = 2.5 (sd 1.0); t = -.36; p = .36). This patient made fourteen errors out of a total of 60 responses during backward counting, and made no catch trial errors. Patient G There was no statistically significant difference in the two ratios (left ratio = 1.3 (sd 1.83); right ratio = 1.7 (sd 2.9); t = -1.0; p = .16). This patient made eighteen errors out of a total of 67 responses during backward counting, and made no catch trial errors. Patient D There was no statistically significant difference in the two ratios (left ratio = 1.1 (sd .79); right ratio = 1.27 (sd = .85); t = -.53; p = .3). This patient made twelve errors out of a total of 58 responses during backward counting, and made no catch trial errors. Performance on the actual backward counting task was similar in both groups, and, indeed, between individual subjects. With the total number of trials given controlled for, (i.e., where only one round given the backward count total and error scores was doubled), the mean number of correct numbers given during the backward condition trials was 60.7 for the experimentals and 54.5 for the controls. The mean error responses given were 12.5 for the experimentals and 11.O for the controls. Catch trial responses were at very low levels for both groups. Table 1 shows the means and standard deviations of laltency of response for the eight subjects, by side and by experimental condition. Figures 2 and 3 show graphs of the responses of neglect patients M and B.
CONCLUSIONS FROM EXPERIMENT 2 The experimental hypothesis is supported by this study only in the case of two of the neglect patients. The two remaining neglect patients showed no tendency for
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Case 'M'
3000
2658
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2000
1000 0 l e f t right FIGURE 2 'M'.
*
l e f t right
Effect of backward counting task on speed of detection of left versus right stimuli: Case
their neglect to worsen when engaged in an attentionally demanding secondary task. None of the right brain-damaged control patients showed any such tendency. In the two patients who showed the hypothesized effect, engaging them in a nonvisual secondary task while carrying out a visual scanning test was significantly to
Case 'B'
2000 1
1758
1 01 l e f t right FIGURE 3 'B'.
*
l e f t right
Effect of backward counting task o n speed of detection of left versus right stimuli: Case
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I. ROBERTSON AND R. FRASCA
lengthen left reaction times with respect to right reaction times compared to performance under normal conditions. A group of right brain-damaged controls showed no such selectively lateralized effect of the secondary task on visual task performance, even though reaction times generally were increased during dual tasking. The secondary task was performed with reasonable accuracy in all cases, and there was no significant difference between the two groups on performance on this. This was no doubt in part due to the fact that several neglect patients were excluded who could not do either the counting task alone, or the counting task in conjunction with the visual scanning task. The generalizability of these results cannot, therefore, extent to the population of neglect patients unable to perform this combination of tasks.
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GENERAL CONCLUSIONS There is converging evidence to support the existence of a nonlateralized attentional deficit associated with unilateral left visual neglect. The two studies reported give some support to this view, though the second study suggests that there may be only some neglect patients who show such an association. One obvious objection to the above experiments is that the results are not specific to neglect. It could be argued that any impaired cognitive function would deteriorate under increased attentional load. While this is probably true for many conditions, the finding has special relevance for unilateral neglect, because of the demonstrated association between seventy of neglect on the one hand, and nonlateralized serial attentional problems on the other (Robertson, 1989, 1990; Rapscak et al., 1989; Lecours et al., 1987). The relevance of this phenomenon in neglect lies in a hypothesized special vulnerability of neglect patients to deteriorating performance in the face of additional attentional load. If this is true, then it might provide an explanation as to why neglect is such a major prognostic factor for poor motor, and other, recovery (see, for example, Denes, Semenza, Stoppa, and Lis, 1982). In other words, it is the nonlaterialized attentional deficit, as much as the lateralized attentional deficit, which is implicated in the poor recovery. By this argument, most patients who suffer from neglect in the early stages following CVA recover spontaneously by learning compensatory scanning habits which rapidly become automatic. The minority who do not recover (and who thereafter show poor rates of recovery, cf., for instance, Robertson, Gray, Pentland and Waite, 1990) may show poor automatization of compensatory scanning because of an associated limitation in dual tasking. In other words, a limited capacity for organizing attention to multiple tasks makes it very difficult for these people ever to render automatic these habits of compensation in the context of everyday activities such as reading, transferring from wheelchairs, etc. What could the origins of this possible association between neglect and attentional effort be? There are at least four possible explanations. 1. The relationship may be correlational, with both the attentional loss and the neglect being associated with severity of brain damage. If this were the case, then one would predict that the correlation would disappear when lesion size is partialled out. 2. The mechanisms involved in selective attention may be closely related to those underlying unilateral neglect. This is the hypothesis of Rapscak et al. (1989).
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3. Diaschisis may cause poor function in subcortical (e.g., thalamic) regions resulting from cortical (e.g., inferior pariental) damage, with associated loss of function on nonlateralized attentional capacity.
In relation to this last point, Deuel (1987) showed the mechanism of diaschisis operating in monkeys following cortical ablation which resulted in subcortical hypoperfusion, and Perani, Vallar, Cappa, Messa and Fazio (1987) found considerable hypoperfusion of cortical areas following subcortical strokes in humans, using SPECT. Hence, different neuropsychological mechanisms subserved by different structures may covary in the degree of deficit they manifest because of the effects of diaschisis. 4. A fourth explanation is suggested by the theoretical model of attention proposed by Posner and Peterson (1990). Posner, Inhoff, Freidrich and Cohen (1987) found that subjects with right parietal lesions showed significant decrements in performance in reaction time tasks in which no warning was given as compared to ones in which a warning signal was given. Their performance on warned reaction time tasks was comparable to that of left parietally-damaged subjects, though the latter did not show the same dramatic deterioration in performance in the absence of a warning stimulus. This suggests, as has been suggested by other authors, that the right cerebral hemisphere has some special responsibility for vigilance or alerting, the latter being one of the attentional systems proposed by Posner and Peterson. Another of their attentional systems is for orientation, which they propose to be bilaterally represented, probably in the parietal cortex. Posner and his colleagues (Posner et al., 1984) have already shown that parietally-damaged patients have difficulty in disengaging their attention from stimuli presented ipsilesionally, and have suggested this to be a basic mechanism for the lateralized problems in visual neglect. Thus, Posner and Peterson’s theory would predict a two-factor model of deficits following right parietal lesions: a lateralized deficit caused by disruption of the orientation mechanism of attention, and a vigilance-alerting deficit caused by disruption of a right hemisphere vigilance circuit. It is this combination of deficits which would explain the greater severity and prevalence of left over right visual neglect. Hence, the close relationship between lateralized and nonlateralized attentional problems presented above is explained, according to Posner and Peterson, in terms of the damage of two functionally separate but anatomically neighboring attentional systems. It should be possible to find subjects with damage to one type of attention but not the other, so the findings of the second study above, in which only two of four subjects showed the phenomenon, should not be surprising. Given, however, that subjects with visual neglect commonly have large cerebral lesions spreading into more than one lobe, then a large proportion of patients with neglect should show both types of attentional disorder. This fourth and last hypothesis is proposed as the strongest contender to explain the results presented above.
REFERENCES Albert, M . L. (1973). A simple test of visual neglect. Neurology, 23. 658-665. Baddeley, A . D. (1986). Working memory. Oxford: Oxford University Press. Crick, F. (1984). Functions of the thalamic reticular complex: the searchlight hypothesis. Proceedings of the National Academy of Science. USA, 81,4586-4590. Denes, G., Semenza, C . , Stoppa, E. & Lis, A . (1982). Unilateral spatial neglect and recovery from hemiplagia. A follow-up study. Bruin, 105, 543-552.
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Deuel, R. (1987). Diaschisis following frontal and panetal lesions in monkeys. In M. Jeannerod (ed.) Neurophysiological and Neuropsychologicul Aspects of Neglect. North Holland, Elsevier. Diller, L., Ben-Yishay, Y., Gerstman, L., Goodkin, R.,Gordon, W. & Weinberg, J. (1974). Studies in Cognition and Rehabilitation in Hemiplegia. Rehabilitation Monograph No. 50. New York, New York University Medical Center. Heilman, K. M. & Van Den Abell, T. (1980). Right hemisphere dominance for attention: the mechanism underlying hemisphere asymmetries of inattention (neglect). Neurology, 30. 327-330. Julesz, B. (1981). Textons, the elements of texture perception, and their interactions. Nature, 290, 9197. Lecours, A. R., Mehler, F., Parente, M. A. et al. (1987). Illiteracy and brain damage: 11. Manifestations of unilateral neglect in testing “auditory comprehension” with iconographic materials. Bruin and Cognition, 6. 243-265. Mark, V. W., Kooistra, C. A. & Heilman, K. M. (1988). Hemispatial neglect affected by non-neglected stimuli. Neurology, 38, 1207-121 1. Perani, D., Vallar, G., Cappa, S., Messa, C. & Fazio, F. (1987). Aphasia and neglect after subcortical stroke. Brain, I I O , 1211-1229. Posner, M. I. & Peterson, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25-42. Posner, M. I., Inhoff, A,, Friedrich, F. J. & Cohen, A. (1987). Isolating attentional systems: A cognitive-anatomical analysis. Psychobiology, 15, 107- 121. Rapcsack, S. Z . , Verfaellie, M., Fleet, S. & Heilman, K. M. (1989). Selective attention in hemispatial neglect. Arch. Neurol., 46, 172-178. Robertson, I. (1 989). Anomolies in the lateralisation omissions in unilateral left neglect: implications for an attentional theory of neglect. Neuropsychologia, 27, 157-165. Robertson, I. (1990). Digit span and visual neglect: a puzzling relationship. Neuropsychologiu, 28, 2 17222. Robertson, I., Gray, J., Pentland, B. & Waite, L. (1990). Microcomputer-based rehabilitation of unilateral left visual neglect: a randomised controlled trial. Archives of Physical Medicine and Rehabilitation, 71. 663-668. von Monakow, C. (1914). Die Lokalisation irn Grosshirn und der Abbau der Funktion durch Kortikale Herde. Wiesbaden: J. F. Bergmann. Weintraub, S. & Mesulam, M. (1987). Right cerebral dominance in spatial attention. Further evidence based on ipsilateral neglect. Archives of Neurology, 44, 621-625.
