LEFT VISUQ-SPA TIAL NEGLECT: A MEANINGLESS ENTITY? Peter W. Halligan and John C. Marshall (Neuropsychology Unit, University Department of Clinical Neurology, The Radcliffe Infirmary, Oxford, and Rivermead Rehabilitation Centre, Oxford)
It is generally accepted that the spectrum of disorders described by the clinicallabel "the neglect syndrome" can all dissociate from each other. If the condition constitutes failure "to report, respond, or orient to novel or meaningful stimuli presented to the side opposite a brain lesion" (Heilman, Watson and Valenstein, 1985), then patients may show this behaviour in one situation but not another (Weinstein and Friedland, 1977). Dissociations may occur between one modality and another (visual, auditory, or tactile) or between one space and another (personal, peripersonal, or extrapersonal). Likewise, motor neglect (the underuse of a non-paretic limb) can dissociate from perceptual neglect (in any modality). Barbieri and De Renzi (1989) hence conclude their discussion of the area as follows: " ... the gamut of deficits covered by the concept of neglect do not constitute a unitary, coherent syndrome, which can be traced back to the disruption of a supramodal supervisor, controlling the deployment of attention to contralateral space." To the best of our knowledge, this conclusion is not contentious (Mesulam, 1981; Halsband, Gruhn and Ettlinger, 1985; Rizzolatti, Gentilucci and Matelli, 1985; Bisiach, Perani and Vallar, 1986; Halligan and Marshall, 1991). The radical claim we make in the current paper is that the more restricted 'syndrome' of left vi suo-spatial neglect (in peripersonal space) is likewise not an empirically well-founded or theoretically-coherent entity. The logical structure of our demonstration is as follows: We take two types of quantifiable test that have been regarded as sensitive measures of 'left visuo-spatial neglect': a cancellation test and a (horizontal) line bisection test (Heilman, Watson and Valenstein, 1985). We then show in four patients that the outcome of these tests can be consistent at three levels of performance after right brain damage: within normal limits on both tests; moderate impairment on both tests; and severe impairment on both tests. Next we show a classic double-dissociation (Shallice, 1988) between the two tests. We report one patient who is reliably unimpaired on cancellation but severely impaired on line bisection; and we demonstrate another patient who is severely impaired on cancellation but reliably unimpaired on.line bisection. A supplementary investigation then raises some issues about further dissociations in performance when drawing/copying tasks are introduced. Cortex, (1992) 28, 525-535
P. W. Halligan and J.C. Marshall MATERIAL AND METHOD
Subjects All six patients were right-handed adults who had sustained unilateral right hemisphere cerebro-vascular accidents, confirmed by CT. Their biographical and neurological particulars are shown in Table I.
Stimuli and Procedure The six patients undertook two tasks during one 20 minute testing session (with very short breaks determined by the subjects themselves). The tasks were Star cancellation from the Behavioural Inattention Test (Halligan, Cockburn and Wilson, 1991) and Line bisection as described in Manning, Halligan and Marshall (1990). The cancellation test comprises 56 small stars (the targets) pseudo-randomly interspersed with distractors (large stars, letters and words). The overall dimensions of the test are A4 (298 x 208 mm). The task is simply to cancel (that is, cross out) all the small stars seen. The two central stars are crossed out by the examiner whilst illustrating the nature of the test to the patient. The stimulus sheet, presented on the desk top, is centred on the sagittal midplane of the patient's head and trunk. The patient then attempts to cross out all the small stars with a fine pen held in the right hand. No time limit is imposed; the trial is terminated when the patients state that they have completed the task to their satisfaction. For scoring purposes the test is divided into six columns (Marshall and Halligan, 1989), where the columns contain (from left to right) 8, 8, 11, 11, 8, and 8 targets. Normal control subjects (N = 50: mean age 58.2 years, range 22 to 82) make a maximum of two omissions on the test (Halligan, Cockburn and Wilson, 1991). In the bisection test, patients are presented with a total of 100 horizontal lines. There are ten line lengths that range from 18 mm to 180 mm in steps of 18 mm. Each black line (1 mm wide) is drawn on a separate sheet of white A4 paper (298 mm x 208 mm). The stimuli are presented in pseudorandom order such that all ten lengths are transected once before the next interation of the stimulus subset. Each sheet was positioned on the desk top so that the objective midpoint of each line lay in the sagittal midplane of the patient's trunk. Patients were instructed to mark the midpoint of each line with a fine pen held in the (preferred) right hand. They were told that corrections were disallowed. Head and eye movements were in no way restricted, but moving the stimulus sheet was not permitted. Normal control subjects (N = 50) in the age range 20 to 97 have never been observed to bisect the longest line (180 mm) with a mean rightwards displacement (over 10 trials) that is greater than + 4.3 mm or a mean leftwards displacement greater than - 9.4 mm (Manning, Halligan and Marshall, 1990, and unpublished observations). When the linear regression of transection displacement on line length is calculated, the extremes of the distribution in normal controls (N = 50) are - 0.2 mm + (0.036 x line length), with 73070 of the variance captured, and + 1.12 mm - (0.051 x line length), with 93% of the variance captured. TABLE I
The Patient Sample Patient
NS FD PP HD WS
70 57 60 56 64
Internal capsule + mUltiple small infarcts Fronto-temporo-parietal Fronto-parietal Temporo-parietal Temporo-parietal Temporo-parietal
+ + + + +
3 months 5 months 20 months 6 months 3 months
F M M
+ + +
Left visuo-spatial neglect TABLE II
Number of Omissions for Each of the Six Columns of the Star Cancellation Test (left to right) Column Patient IK
NS FD PP HD WS
0 1 2 S S 1
0 1 3 S S 0
0 0 0 11 S 0
0 0 0 7 2 0
0 0 1 2 0 0
0 0 0 0 0 0
Mean Transection Displacements (and standard deviations) at 10 Line Lengths Patient
IS0mm 162mm 144mm 126mm IOSmm 90mm 72mm 54mm 36mm ISmm
+ 2.0 (4.1) +3.3 (3.7) + 2.9 (3.1) +0.7 (2.9) +0.6 (2.6) -0.5 (1.6) - 1.5 (Ll) - 2.2 (1.4) -1.3 (0.7) -1.0 (0.5)
+ 3.S (5.S) +2.5 (3.7) + 1.9 (5.3) +0.7 (5.3) + 1.9 (2.1) +3.6(2.7) +2.2 (2.3) +0.7 (1.6) + 0.5 (1.4) -0.3 (0.5)
+ 12.6 (3.7) + 9.6 (3.4) + 6.S (2.3) + 5.6 (2.5) + 5.2 (3.0) + 4.9 (3.9) + 0.4 (2.9) - 1.0 (2.3) - 1.7 (1.7) - 1.6 (1.2)
+20.6 ( 7.S) + IS.S (12.2) +22.2 ( 9.9) + 16.9 ( S.6) + 13.9 ( 9.9) + 12.4 (10.2) - 4.S (10.6) - 5.3 ( 9.0) - 1.5 ( 5.S) - 2.6 ( Ll)
-6.5 (5.4) - 5.3 (5.9) -2.5 (3.6) -5.7(3.5) - 3.3 (2.2) - 2.6 (3.9) - 5.S (2.1) - 2.9 (1.4) - 2.6 (1.9) -Ll (O.S)
+ 32.S (12.3) + 19.2 ( 9.7) + 17.5 ( 9.4) + 15.5 ( S.I) +15.1 (5.9) + 9.1 ( 7.1) + 7.3 ( S.O) + 4.3 ( 7.2) - 0.4 ( 2.7) - 1.4(1.4)
The results of the cancellation task are shown in Table II. It can be observed that three patients (lK, NS, and WS) fall within normal limits on this task (zero omissions, two omissions, and one omission, respectively). The remaining patients (FD, PP, and HD) show 'left visuospatial neglect', albeit of differing severities. The results of the line bisection task are shown in Table III. When the linear regressions of transection displacement on line length are calculated, three patients (IK, NS, and HD) fall within normal limits: IK: -2.78 mm + (0.031 x line length) (78%) NS: +0.06 mm+(O.017 x line length) (480/0) HD: -1.63 mm - (0.022 x line length) (44%) Three patients (FD, WS, and PP) are outside normal limits, albeit again to varying extents: FD: - 6.65 + (0.088 x line length) (95%) WS: -6.15+(O.182xline length) (93%) PP: -9.40+ (0.187 x line length) (82%)
P. W. Halligan and J.C. Marshall
The critical patients are HD and WS, who show a classic double dissociation between performance on the two tasks. Is this pattern reliable? Both patients were retested on star cancellation approximately two weeks after the previous data were collected. The results (number of omissions per column) are: Columns 1
Both patients have improved a little on star cancellation but the difference between them remains. During the same retesting session, HD and WS were given the 10 longest lines (180 mm) of the previously administered set to bisect. HD's transection accuracy was - 2.75 mm (SD 3.5), well within normal limits. WS's mean was + 56.4 mm (SD 14.0). Again, the difference between the two patients is stable.
Supplementary Investigation Can we be sure that neither IK nor NS show neglect? In early studies of the condition (before cancellation and bisection tests became standard tools), drawing and copying tasks were the preferred mode of investigation (Critchley, 1953). IK, tested at the same time as the experimental data were collected, showed no impairment on either copying geometrical figures or spontaneous representational drawing. NS, by contrast, showed striking and reliable leftsided omissions on free drawing (but not copying). Two examples of NS's attempts to draw a map of the United Kingdom are shown in Figure 1. Of the remaining patients, PP showed left omissions on both drawing and copying (consistent with her impaired performance on cancellation and bisection). The less severely impaired patient FD made no errors on copying, but produced a 'classic' neglect clockface with all the left side numbers missing. WS showed no impairment on either drawing or copying; HD showed left sided omissions on both tasks. DISCUSSION
The overall pattern of the current data would seem to leave the theorist on the horns of a dilemma. If we had only tested patients FD and PP (who are, no doubt, more 'representative' of 'left neglect' than HD and WS), no problem would arise. One would simply conclude that when right hemisphere damage does provoke left neglect, the severity thereof will vary from patient to patient. The performance of IK, however, shows that right hemisphere damage per se does not necessarily give rise to left neglect on these tests, or indeed on drawing and copying tasks. (Although no-one has ever assumed that right hemisphere damage per se always results in gross neglect, referees on some of our previous papers have suggested that right hemisphere lesions will invariably provoke an
Left visuo-spatial neglect
o Fig. 1 - Two attempts by NS to draw (from memory) a map of the United Kingdom.
abnormal shift to the right on line bisection. Patient WD, reported in Halligan, Manning and Marshall, 1990, shows that this is not so, as does HD, reported here). But what of HD and WS? HD is grossly impaired on cancellation, but falls within normal limits on bisection. Furthermore, the lateral bias of his transection displacements is in the wrong direction for a patient with 'left neglect'. WS, by contrast, is grossly impaired on bisection, but shows no cancellation deficit. Left sided omissions on cancellation tasks are a traditional indicant of hemispatial neglect and our particular star cancellation test has proved better than other measures in demonstrating the gross presence of the condition (Halligan, Marshall and Wade, 1989). Likewise, line bisection is always regarded as an excellent indicant of hemispatial neglect (Black, Vu, Martin et aI., 1990). The question thus arises as to whether either HD or WS (or neither, or both) have left visuo-spatial neglect? One could, of course, stipulate the answer by fiat. Both have left neglect because each shows the typical pattern of performance on (at least) one traditional test. Alternatively, neither shows neglect because both fail to show the typical pattern on (at least) one test. But to legislate a diagnostic category is to abdicate responsibility for attempting to understand what now appears to be a set of disorders. We accordingly propose that the term 'left visuo-spatial neglect' should be regarded as no more than a descriptive shorthand (Newcombe and Marshall,
P. W. Halligan and J.e. Marshall
1988) for all visual disorders whatsoever in which.there is a reliable impairment that is more pronounced in left than right space. But we insist that the clinical diagnosis of left visual neglect has no theoretical status; it does not refer to a 'natural kind' in any information-processing model of visuo-spatial perception. It is not an impairment of any known discrete, encapsulated psychological process. Group studies (Ogden, 1985, for example) have often defined the inclusion criterion for membership of the hemineglect group as neglect on anyone of N tests. Our investigation suggests that when this ploy is adopted, the resultant 'group' will manifest a heterogenous set of distinct behavioural impairments. The standard arguments against employing the mean performance of such 'groups' as the data-base in further experimental and theoretical inquiry will thus apply (Caramazza and McCloskey, 1988). Our proposal is actually quite modest if one bears in mind the meaning of a term such as 'aphasia'. There is no such entity as aphasia (although there are patients who manifest acquired disorders of language). The language-faculty is a highly complex system that can break down in a wide variety of distinct ways (Marshall, 1982). The expression 'aphasia' is a (useful) clinical shorthand for any (or all) of those disorders. By parity of argument, there is no such entity as left vi suo-spatial neglect (although there are patients who manifest different perceptual, or attentional, or representational problems with left space). But it would be unwise to assume that the spatial faculty is any less complex than the language faculty, and hence any less liable to show qualitatively distinct forms of impairment in response to damage. What is initially required, then, is a task-analysis of the varieties of hemispatial disorder. There has been a tendency to assume that the traditional tests used to assess left neglect are so simple that detailed task-analysis is unnecessary. By contrast, we have argued that performance on line bisection may be primarily a measure of the Weber fraction: if patients had an increased Weber fraction and approached from the right side the point at which the two segments of a line appeared equal in magnitude, then the observed linear regressions of transection displacement on line length would, of necessity, result (Wolfe, 1923; Marshall and Halligan, 1990). On this interpretation, patients who 'bisect' lines significantly to the right of true centre do not 'neglect' a portion of the left. Rather, they judge that two unequal magnitudes are the same, just as do normal subjects albeit with lesser inequalities. The requirements of cancellation tasks have only recently been investigated in any detail. A theoretical contrast between over·attention to the right side of a display and under-attention to the left side has been postulated (Mark, Kooistra and Heilman, 1988; see also De Renzi, Gentilini, Faglioni et aI., 1989; Ladavas, Petronio and Umilta, 1990). Other aspects of visual search with respect to cancellation have been investigated by Weintraub and Mesulam (1988), Rapcsak, Verfaellie, Fleet et al. (1989), and Kaplan, Verfaellie, Meadows et al. (1991). The manifestation of neglect on representational drawing tasks requires an explanation both of why patients omit 'obvious' left sided details and why they fail to notice that they have done so. The notion of 'completion' is often in-
Left visuo-spatial neglect
voked (Poppelreuter, 1917; Warrington, 1962), but .may be more descriptive than explanatory. In some patients, omissions in copying decrease dramatically when visual feedback is minimized (McGlinchey-Berroth, Milberg, Verfaellie et aI., 1992). Previous demonstrations of dissociated performance in peripersonal (visual) space have involved the contrast between language tasks (neglect dyslexia) and non-verbal stimuli (Costello and Warrington, 1987; Cubelli, Nichelli, Bonito et aI., 1991), although a recent paper by Binder, Lazar, Tatemichi et aI. (1992) suggests caution in the interpretation of these results. Our demonstration here is the first reported double dissociation we are aware of where (a) modality (visual), distance (peripersonal), response mode (manual), and general task character (non-verbal) are held constant; (b) performance is reliable; and (c) no argument about differential task-sensitivity is feasible: the double-dissociation is 'classic' (Shallice, 1988). Given these constraints we see no escape from the conclusion that left (peripersonal) vi suo-spatial neglect is a meaningless entity. The term is also, we believe, pernicious in that it encourages the belief that "neglect" (even when prefaced by "perceptual", "attentional", "representational", or "hypokinetic") is an explanatory construct rather than a crude description of the behaviours that stand in need of explication (Gianutsos and Matheson, 1987). If the expression is not too well entrenched to be changed, we suggest that a more neutral term such as "dyschiria", proposed by Zingerle (1913) and supported by Bisiach and Berti (1987), is preferable. But just as 'aphasia' is really 'the aphasias', so 'the dyschirias' may better enable us to appreciate the magnitude of the task that awaits: the description and explanation of spatial cognition and its disorders (De Renzi, 1982). ENVOI
We are, however, concerned that the thrust of our paper may be misinterpreted, and will accordingly conclude with a position-statement that is (we hope) unambiguous. We draw upon two sets of referees' comments that we found especially valuable. As Gainotti, D'Erme and Bartolomeo (1991) write, the standard (and uncontroversial) description of "hemi-neglect" states that it is "a multicomponent syndrome". Like many other traditional syndromes, it can be shown to fractionate. As a referee reminds us "the double dis sociability of 'neglect' phenomena is no longer a novelty." We agree, but the point of our arguments is not solely to add to the ever-growing documentation of those dissociations (e.g. Fujii, Fukatsu, Kimura at aI., 1991). Rather, we conjecture the possibility that the symptoms that are regarded as 'components' of left neglect have nothing in common other than the fact that, by definition, there is a differential involvement of 'left' space (in some of the many senses of 'left'). If we are correct, it would seem that there is little to be gained (and much to be lost) by thinking of neglect as a 'syndrome' or 'entity'. The explanation of a neglect 'syndrome' must (at minimum) show how a set of symptoms is caused by impairment to one component of the normal system. The
P. W. Halligan and J.e. Marshall
double dissociations we report suggest that no such single impairment can account for what were always regarded as the core symptoms of left visuo-spatial neglect in peripersonal space. It is for this reason that we subtitled our paper "A meaningless entity?" and it is for this same reason that we resist a referee's proposal that we moderate our (implied) hyperbole to: "An entity in search of definition." No: our claim is that there is no such entity (and hence that there never will be a theoretically-valid definition thereof). We can (for the moment) only compromise on: "A set of entities in search of explanations." Our critic does, however, provide a suggestion on which we are (very) close to agreement. Namely: "What is needed is an endeavour to tease out the abilities required by the performances that dissociate and to identify their contribution to neglect." Here we would only change the last word ("neglect"), replacing it with "the impairments." Another referee claims that our "scepticism as regards a 'natural kind' underlying such disorders, however, neglects the desirability of efforts to find basic principles of space representation." But we agree (with both referees) not merely on the desirability but rather the necessity of finding such "principles" (in the plural, note). Indeed, we have placed great emphasis upon one such principle (Weber's law) in our previous analyses of task-performance on line bisection (Marshall and Halligan, 1990); in the current paper we likewise emphasized the importance of the principle of visual completion with respect to other 'neglect' tasks (drawing and copying). Again, then, our conjecture is simply that no one principle will explain (or even describe) all the impairments that have gone under the label of 'neglect' . The referee who takes issue with our "scepticism" suggests that another basic principle (unspecified) may underlie "the coherent effect that vestibular stimulation is likely to have on phenomena such as various kinds of neglect, anosognosia, and somatoparaphrenia" (Cappo, Sterzi, Vallar et aI., 1987; Vallar, Sterzi, Bottini et aI., 1990; Bisiach, Rusconi and Vallar, 1991; Geminiani and Bottini, 1992). We too find these results intriguing and would venture that they reflect an overall increase in the general activation level of the right hemisphere (as proposed by Cappa, Sterzi, Vallar et aI., 1987). We are compelled to stress, however, that in Cappa, Sterzi, Vallar et aI. (1987), vestibular stimulation produced a transitory remission of neglect but not anosognosia in two patients; likewise, in Vallar, Sterzi, Bottini et aI. (1990), vestibular stimulation transiently abolished neglect but not anosognosia in one patient. These results do not therefore provide compelling evidence that neglect and anosognosia are deeply related. Be that as it may, the observation that neglect and anosognosia may sometimes be conjointly ameliorated by the same 'treatment' is a far cry from establishing a theoretical link between t4e dissociated phenomena that we report here. One would not, after all, claim that two distinct diseases were merely two manifestations of the same disease just because they could both be effectively treated by (for example) penicillin; that both diseases were caused by bacteria does not show that they were caused by the same bacterium. Is there, then, any link between the manifestations of so-called 'left neglect'? The only unifying hypothesis we are aware of is the conjecture by Kins-
Left visuo-spatial neglect
bourne (1970) that right hemisphere damage exerts maximal disruption upon the 'attentional balance' of the hemispheres by disinhibiting the natural tendency of the undamaged left hemisphere to attend strongly to the right (see also Pardo, Fox and Raichle, 1991). But, as we emphasized in our introduction, the entire range and pattern of dissociations in 'neglect' is totally inconsistent with the idea that all these deficits "can be traced back to the disruption of a supramodal supervisor, controlling the deployment of attention to contralateral space" (Barbieri and De Renzi, 1989). It is possible that the imbalance postulated by Kinsbourne (1970) is a necessary factor for the appearance of any manifestation that has been called 'unilateral neglect' but it cannot be a sufficient one. Our position therefore remains that left visuo-spatial neglect is a meaningless entity.
Six patients with unilateral right hemisphere damage are reported. Each patient performed two tasks that are traditionally regarded as diagnostic for left (peripersonai) visuospatial neglect: target cancellation and horizontal line bisection. Two patients were unimpaired on both tasks, and two were impaired on both. The two remaining patients showed a classic (and reliable) double-dissociation between the tasks. One of the patients who scored within normal limits on both cancellation and bisection showed left sided omissions on representational drawing. We argue that these results question the validity of any unitary concept of unilateral visuo-spatial neglect in peripersonal space.
Acknowledgements. This work was supported by the Medical Research Council and the Chest, Heart, and Stroke Association. We are also grateful to Dr. A.J. Marcel, who recently asked us "What does line bisection have to do with neglect?". Two anonymous referees forced us to clarify our theoretical position: we thank them sincerely.
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John C. Marshall, University Department of Clinical Neurology, The Radcliffe Infirmary, Woodstock Road, Oxford OX2 6HE, UK.