Challenging current accounts of unilateral neglect

Challenging current accounts of unilateral neglect

I I, pp ,Vrurop,?rholoylo, Vol 32. No. 1431-1434, 1994 Copyright 1994 Elsewer Saence Ltd Prmted m Great Britain. All rights reserved 002%3932,‘94 $7...

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I I, pp

,Vrurop,?rholoylo, Vol 32. No. 1431-1434, 1994 Copyright 1994 Elsewer Saence Ltd Prmted m Great Britain. All rights reserved 002%3932,‘94 $7.CO+O.W

Pergamon

c

0028-3932(94)00070-O

NOTE CHALLENGING EDOARDO

CURRENT BISIACH,*t

ACCOUNTS

OF UNILATERAL

MARIA L. RUSCONIJ VALENTINO and GIUSEPPE VALLARC

NEGLECT

A. PERETTIQ:

tDipartimento di Psicologia Generale, Universita di Padova; fIstituto di Clinica Neurologica, Universita di Milano; #Casa di Cura Pederzoli, Peschiera del Garda; and EDipartimento di Psicologia, Universita di Roma, and Centro Ricerche Clinica S. Lucia, Roma, Italy (Receiwd

3 February

1994; accepted 29 April 1994)

Abstract-Two left-neglect patients were asked (i) to bisect a I5 cm line, (ii) to bisect the empty space between the endpoints ofa 15 cm virtual line, and (iii) to set the endpoints of a 15 cm virtual line, given its midpoint. With one patient, the subjective midpoint of the virtual line was found to be displaced leftwards with respect to the subjective midpoint of the real line, whereas with the other it was found to be displaced rightwards. However, in condition (iii) both patients significantly underestimated the distance from the centre of the rightmost point of the virtual line while relatively overestimating that from the centre to the left endpoint. This latter result challenges current accounts of unilateral neglect. Key Words:

unilateral

neglect; line bisection.

In their introduction to the Woodstock Neglect Meeting, Marshall and Halligan (unpublished) claimed that “the explanatory depth of current accounts of neglect is essentially zero”. This bold assertion might be resented as defeatist by some experts in the field (as it was by one of us at that time). Current accounts of neglect are claimed to explain, for example, the well-known phenomenon of misbisection of horizontal lines (towards the side of the brain lesion responsible for the disorder) as being due to factors such as: (a) ipsilesional deflection of local attention [lo]; (b) hampered disengagement of attention from ipsilesional cues (such as one of the endpoints of the line) [12]; (c) defective or abolished representation of the leftmost (or rightmost, according to the side of the lesion) sector of the line [4]; (d) unilateral directional hypokinesia for hand movements towards the side of space opposite to the lesion [9]. There are, however, facts that fully vindicate Marshall and Halligan’s scepticism. Marshall and Halligan’s [l l] finding that with very short lines misbisection may reverse from the typical into the opposite direction has been a repressed pain in the neck of neglect theorists. There are however further challenges. Indeed, it is far from clear what would be predicted by current accounts of neglect as regards the bisection of the empty space between two points. Even more enigmatic is-as least a priori-the outcome of a task in which patients were asked to set the endpoints of a virtual line of a given length, of which only the midpoint was marked by the examiner. We have recently collected surprising data from two patients. A.F. is a 65-year-old right-handed man with &year schooling who suffered from right-hemisphere stroke on 8 June 1993. CT scan had shown right fronto-temporal ischaemia. At the time of our observation, he still had severe left hemiplegia and hemianopia, but no apparent somatosensory disorders. Contralesional neglect was evident (50% omissions on Diller and Weinberg’s [7] cancellation task; 25 October 1993). Examined on Tegner and Levander’s [I43 mirror-reversed line cancellation task (16 November 1993), he showed the type of performance interpreted by those authors as being due to limb-hypokinetic neglect (leftside omissions on the tactual array, i.e. rightside omissions on the visual array). We gave him three versions of a line bisection task. He had first to set the midpoint of a horizontal black line, 150 mm long and 2 mm wide, located astride his trunk’s sagittal midplane at a comfortable reaching distance. Then he had to mark the midpoint between two dots corresponding to the endpoints of the line that had been shown him in the first step of the task. Finally, he had to set the endpoints of the (virtual) line on the basis of its midpoint, represented by a dot in the centre of the sheet of paper.

*Address

for correspondence:

Prof. Edoardo

Bisiach, 22070 Lurago 1431

Marinone

(Como),

Italy.

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NOTE

Figure 1 and Table 1 report the results obtained from three sessions with 9, 10 and 18 trials of each type, respectively. The subjective midpoint of the empty space between the endpoints of the virtual line was placed leftwards with respect to the subjective midpoint of the real line. When the endpoints of the virtual line had to be set according to the dot representing its centre, the rightmost one was placed nearer to the centre than the leftmost, so that both of them appeared relatively displaced leftwards. The patient marked first the rightmost point and then the leftmost, except for trial 8 in session 2 (10 November) and trials 3,6, and 14 in session 3 (16 November). Marking the leftmost point first did not make any difference: the mean distance of the subjective leftmost point of the virtual line from its objective midpoint was in this circumstance 108.25 mm (33.75); that of the rightmost 32.00 mm (26.87). AS. is an 80-year-old right-handed woman with g-year schooling who had a right middle c.a. ischaemia in 1990. Several aspects of her leftside neglect have been reported elsewhere 12, 3, 151. On Tegner and Levander’s [14] mirror-reversed cancellation task, she consistently showed “perceptual” neglect: rightside omissions on the tactunl display, i.e. leftside omssions on the tGsua/ display (see [2] for details). She still shows neglect phenomena in everyday life, though performing normally on several cancellation tasks [I, 7, 161. A.S. was given (18 January 1994) 15 trials on each conditions of the bisection task we had used with A.F. The results are shown in Fig. 2 and Table 2. Contrary to what we found with A.F., the empty space between the two endpoints of the virtual line was placed rightwards with respect to the subjective midpoint of the real line. However, when she had to set the endpoints of the virtual line with reference to the dot representing its centre, we found exactly the same type of behaviour as we had found in A.F. In this condition of the task, A.F. always marked the rightmost point first. As regards bisection of the empty space between two dots, the contrasting behaviour of our two patients is not very surprising: dissociations can even be found on the canonical line-bisection task, where increasing the length of the line may either cause significant (relative) increase or decrease of the bisection error (e.g. [4]). Dividing attention between two dots, rather than between the two endpoints of a line, might either enhance contralesional neglect because ofthe increased salience of the ipsilesional landmark, or improve (or even reverse) it by increasing the extent of purposeful contralesional exploration required for the detection of the leftside landmark [13]. A.F. and AS. might instantiate different resolutions of this tension.

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Fig. 1. A.F.‘s bisections; 25 October, 10 November and 16 November. Vertical bars show the subjective midpoint of the real line (first row), the subjective midpoint of the space between the two dots representing the endpoints of the virtual line (second row), and the subjective endpoints of the virtual line given its midpoint (third row), in the three sessions of the experiment.

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NOTE

Table 1. Patient

A.F. Mean scores (mm) recorded bisection experiment

(a)

(b)

in the

6)

Cd)

25 OCT M S.D.

f8.56 6.82

+

5.44

- 67.89 8.94

+ 35.44 14.42

10 NOV M S.D.

+9.90 5.76

-2.60 12.14

- 72.80 22.89

+ 56.60 15.38

16 NOV M S.D.

-0.56 5.07

- 16.06 11.37

- 106.83 15.20

+ 36.28 12.31

1.89

(a) Distance (mm) of the subjective from the objective midpoint of the line (positive and negative values correspond to rightward and leftward deviations, respectively). (b) Distance of the subjective from the objective midpoint of the empty space between the endpoints of the virtual line. (c) Distance of the subjective leftmost point of the virtual line from its objective midpoint. (d) Distance of the subjective rightmost point of the virtual line from its objective midpoint. The differences between scores (a) and (b) have been assessed by means of f-tests: t(25 October)=2.59, 16 d.f., PcO.02; t(10 November)=2.94, 18 d.f., P
Fig. 2. AX’s bisections.

Table 2. Patient

M S.D.

(Legend as in Fig. 1).

A.S. Mean scores (mm) recorded bisection experiment

+3.40 4.00

f8.07 3.06

- 72.20 5.12

in the

+59.53 10.49

(at(d) as in Table 1. The difference between scores (a) and (b) has been assessed by means of a r-test: t=3.59, 28 d.f., P
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NOTE

As for the third condition of the task, the results are self-eloquent. They can hardly, if at all, be explained on the basis of the above-mentioned putative factors of unilateral neglect (ad): the leftward displacement of the subjective right endpoint of the virtual line and the disproportion of the distances of the two subjective endpoints from the mark representing the midpoint of the virtual line-a mimicry of what is typically found in canonical line-bisection tasks!defy any simple interpretation of neglect behaviour in terms of ipsilesional twist of attention, inability to disengage attention from stimuli located on the ipsilesional side of space, inability to mentally represent the contralesional side of egocentric space, or inability to initiate and carry out motor activity towards that side. The kind of ad hoc readjustment by which current accounts of neglect might try to accommodate these results is far from obvious. Any attempt at framing our results in a new theory of spatial cognition would be premature and outside the scope of this note. We shall only incidentally remark on the family resemblance between these results and the behaviour of a former patient, A.R., on a task testing auditory function in unilateral neglect (Bisiach and Vallar, unpublished). A.R., a left neglect patient, had first been given near-threshold dichotic tones the two components ofwhich had been matched for intensity so that the resulting acoustic image was perceived as being located at the vertex of his head. Paradoxically, increasing the intensity of left-ear tone impaired overt detection of stimuli (a finding that could be explained as being due to shift of the perceived acoustic image towards the neglected side of space). However, on some such trials, the patient remarked that he could perceive the tone, but it was “very far away”! Altogether, these findings suggest that at least some of the phenomena known under the rubric of “unilateral neglect” are due to a marked distortion of the representational medium caused by the brain lesion [S, 6, 81, rather than to its contralesional “cognitive cut” or to a primary attentional inaccessibility of its contralesional side. The simple method we have described may apply to further investigation, part of which is under way with larger groups of patients, including A.F. and AS., whose preliminary records are reported in this Note mainly because of the heuristic value they are likely to hold. Acknowledgements-We thank John C. Marshall and preparation of the manuscript. This work was supported

Peter W. Halligan for discussion and advice in the by CNR and MURST grants to the first author.

REFERENCES 1. Albert, M. L. A simple test of visual neglect. Neurology 23, 658-664, 1973. 2. Bisiach, E. Perception and action in space representation: Evidence from unilateral neglect. In Internationul Perspectives on Psychological Science, Vol. 2: The State of the Art, G. d’Ydewalle,‘P. Eelen and P. Bertelson (Editors), pp. 51-66. Lawrence Erlbaum, Hove, 1994. M., Poncet, M. and Rusconi, M. L. Unilateral neglect in route description. 3. Bisiach, E., Brouchon, Neuropsycholoyia 31, 1255-1262, 1993. 4. Bisiach, E., Bulgarelli, C., Sterzi, R. and Vallar, G. Line bisection and cognitive plasticity of unilateral neglect of space. Brain Cognit. 2, 32-38, 1983. L., Sterzi, R. and Vallar, G. Disorders of perceived auditory lateralization after lesions 5. Bisiach, E., Cornacchia, of the right hemisphere. Brain 107, 37-52, 1984. 6. Bisiach, E. and Vallar, G. Hemineglect in humans. In Handbook of‘Neuropsychology, Vol. 1, F. Boiler and J. Grarman (Editors), pp. 195-222. Elsevier, Amsterdam, 1988. in rehabilitation: The evolution of a rational remediation I. Diller, L. and Weinberg, J. Hemi-inattention program. In Hemi-Inattention and Hemisphere Specialization, E. A. Weinstein and R. P. Friedland (Editors), pp. 62-82. Raven, New York, 1977. 8. Halligan, P. W. and Marshall, J. C. Spatial compression in visual neglect: A case study. Cortex 27,623-629, 1991. 9. Heilman, K. M., Bowers, D., Coslett, H. B., Whelan, H. and Watson, R. T. Directional hypokinesia. Nruroloy) 35, 855-859, 1985. M. Mechanisms of unilateral neglect. In Neurophysiologicul and NeuropsychologicaI Aspecrs of 10. Kinsbourne, Spatial Neglect, M. Jeannerod (Editor), pp. 69-86. North Holland, Amsterdam, 1987. of line bisection in a case of visual 11. Marshall, J. C. and Halligan, P. W. When right goes left: An investigation neglect. Cortex 25, 503-515, 1989. 12. Posner, M. I., Walker, J. A., Friedrich, F. J. and Rafal, R. D. Effects of parietal injury on covert orienting of attention. J. Neurosci. 4, 1863-1874, 1984. 13. Riddoch, M. J. and Humphreys, G. W. The effect of cueing on unilateral neglect. Neuropsychologiu 21,589 599, 1983. 14. Tegnkr, R. and Levander, M. Through a looking glass. A new technique to demonstrate directional hypokinesia in unilateral neglect. Brain 114, 1943-1951, 1991. information in unilateral neglect. Effects 15. Vallar, G., Rusconi, M. L. and Bisiach, E. Awareness ofcontralesional of cueing, tracing and vestibular stimulation. In Attention and Perfbrmance XV, M. Moscovitch and C. Umilti (Editors). MIT Press, Cambridge (MA), in press. 16. Weintraub, S. and Mesulam, M.-M. Mental state assessment of young and elderly adults in behavioral neurology. In Principles of Behaoioral Neurology, M.-M. Mesulam (Editor), pp. 71 123. Davis, Philadelphia, 1985.