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Evaluating visual bias and effect of proprioceptive feedback in unilateral neglect
Journal of Clinical Neuroscience 17 (2010) 1148–1152
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Evaluating visual bias and effect of proprioceptive feedback in unilateral neglect Yu Chiba a,b,c,*, Ken Nishihara b, Nobuhiko Haga a a
Department of Rehabilitation Medicine, The University of Tokyo Hospital, 7-3-1 Hongo, Bunkyo, Tokyo 113-0033, Japan Division of Rehabilitation Medicine, National Center of Neurology and Psychiatry, Tokyo, Japan c Division of Rehabilitation Medicine, Tsukuba University Hospital, Ibaraki, Japan b
a r t i c l e
i n f o
Article history: Received 24 August 2009 Accepted 7 February 2010
Keywords: Line-bisection task Proprioceptive sensation Unilateral neglect Visual neglect
a b s t r a c t We propose modified versions of the line-bisection task for assessing visual bias and effect of proprioceptive feedback in unilateral neglect; that is, the verbal line-bisection (VLB) task and the VLB plus pointing task. The VLB task requires only a verbal response to assess pure visual bias. Conversely, the VLB plus pointing task requires both a verbal response and pointing to assess visual and proprioceptive bias. Ten patients with unilateral neglect were administered these tasks on a computer using presentation software. Eight participants showed obvious rightward deviation in the VLB task, and were thus classified as patients with visual neglect. Four participants showed significantly greater deviation in the VLB plus pointing task than in the VLB task, and were thus classified as patients with proprioceptive bias. Visual bias and effect of proprioceptive feedback in unilateral neglect were successfully assessed by these tasks. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Patients with unilateral neglect (neglect) fail to report, respond to, or orient towards stimuli located on their contralesional side. This condition is more common after a right hemisphere lesion than after a left hemisphere lesion. Patients with left neglect may have trouble grooming the left side of their bodies, fail to eat from the left side of a tray, and respond poorly to people standing on their left side. On examination, these patients tend to mark a subjective midpoint of a horizontal line to the ipsilesional side of its true center and fail to draw the contralesional side of a figure. The causes of neglect are unclear, although some hypotheses have been proposed. Heilman et al. demonstrated that patients with neglect were significantly slower than control patients to initiate and complete movements towards the contralesional hemispace and hypothesized that neglect is a deficit in the ability to move towards the contralesional hemispace.1 This theory is supported by studies that demonstrate abnormal behaviour toward the contralesional side in patients with neglect (for review see Heilman).2 Mattingley et al. used the term ‘‘directional hypometria” to refer to direction-specific impairments of spatial exploration or movement amplitude, ‘‘directional hypokinesia” to denote slowing in the initiation of contralesionally directed movements, and ‘‘directional bradykinesia” to denote slowing in the execution of movements.3 An emerging hypothesis suggests that neglect is a heterogeneous phenomenon that can be classified into at least
* Corresponding author. Tel.: +81 3 5800 8795; fax: +81 3 5684 2094. E-mail address: [email protected] (Y. Chiba). 0967-5868/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2010.02.017
two types: motor-intentional and perceptual-attentional (non-motor) (for reviews see Buxbaum et al.4 and Ghacibeh et al.5). Several theories have been proposed to explain perceptualattentional neglect. Kinsbourne proposed the activation-orienting hypothesis, claiming that neglect occurs when a unilateral lesion provokes an imbalance in the direction of spontaneous attentional orientation.6 This hypothesis has been supported by multiple research groups. Posner et al. found that patients with right parietal lesions were impaired in their ability to disengage attention from a right cue in order to reorient towards the left space.7 De Renzi et al. found that, in patients with left neglect, attention is magnetically attracted by stimuli presented to the right side.8 Ladavas et al. found that patients with left neglect were faster to respond to targets on their right than to those in the relative left position.9 In contrast to these attentional explanations of spatial neglect, other researchers have proposed that neglect is a supramodal deficit rather than an input-related deficit. For example, Bisiach et al. found that patients with neglect showed symptoms even in imagined perspectives, and proposed the representational hypothesis, which states that neglect is due to a disordered internal representation that is not input-related.10 They also proposed the space anisometry hypothesis, which may account for the behavioural phenomena associated with neglect; according to this hypothesis, the representational medium appears abnormally anisometric along the horizontal dimension to patients with neglect.11 In other words, the medium in representation appears progressively compressed toward the ipsilesional space and relaxed toward the contralesional space logarithmically. Milner suggested that patients with left hemineglect might perceive leftward-located spatial extents as shrunken relative to those
Y. Chiba et al. / Journal of Clinical Neuroscience 17 (2010) 1148–1152
located on the right, and that the gradient of this distortion might be greater within the left hemispace than within the right.12 This suggests that the subjective space of patients with neglect is distorted and their entire space is misrepresented. Typically, neglect has been assessed by pencil-and-paper description tests, such as the line-bisection task, the line-cancellation task and the figure-copying task (for example, Wilson et al.).13 However, these tests cannot assess the severity of each type of bias involved in neglect (that is, visual, proprioceptive and motorintentional), because during the tests the participant must use both sensory and motor functions, and must perceive both visual and proprioceptive inputs, simultaneously. Thus, a method for assessing neglect in terms of specific modalities is required to select a suitable rehabilitation program for patients with each type of neglect. To assess only visual bias of neglect, some researchers have employed passive line-bisection tasks in which hand movement is not required;14–16 these methods have their own merits and demerits as follows. In some methods a bisector or a bisecting point is moved horizontally along a line by the experimenter, while the participant verbally indicates when the bisector arrives at the subjective midpoint of the line.14,16 In these methods, however, the bisector may act as a cue, and the error might represent the effect of cuing as well as the severity of visual bias. Milner et al. proposed the landmark task in which the participant verbally indicated which side of a pre-bisected line was longer by saying ‘‘right” or ‘‘left”.17 The nature of this test, however, is binary rather than quantitative. In addition, the results from this task are not directly comparable to results from the conventional line-bisection task, because the tasks measure different variables (the proportion of certain answers [%] versus deviational length [mm]). To assess proprioceptive neglect, some research groups have employed a pointing task that requires participants to point straight ahead with one hand while blindfolded (for review see Chokron et al.).18 When patients with right-brain damage and left neglect have been asked to perform this test, some authors have reported patients who demonstrate an ipsilateral shift in the position toward which they point. The straight-ahead pointing task, however, requires free hand movement and, therefore, may account for the motor aspect of neglect in its results even though the task does not require exploratory movement. In addition, the straight-ahead pointing task may be less accurate for patients who have postural instability, which is frequently observed in patients with brain damage. Several passive line-bisection tasks provide proprioceptive feedback to the participant. Na et al. proposed a character linebisection task in which a horizontally aligned character string was presented; the participant was required to identify the character nearest to the center of the string and circle it.19 Chiba et al. proposed the exactly bisected line-selection task, in which multi-
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ple horizontal lines, bisected in various proportions, were presented at the same time on a test paper. Participants first chose which line was the most equally bisected and then indicated it by pointing to the bisector on that line.20 In these tasks, the bisector and the character circled were selected before the patients moved their hands. Therefore, the coordinate of the bisector chosen by the patient represented the perceived midpoint and the deviational error was considered to represent sensory-attentional, rather than motor-intentional, bias of neglect. These tests assessed a combination of visual and proprioceptive bias rather than a single modality. To assess visual neglect quantitatively, without using directional stimuli, the verbal line-bisection (VLB) task was proposed.21 In this test, a long line with written characters (similar to the lowest of the three lines shown in Fig. 1) was presented; the participant identified the subjective midpoint of the line and read the character nearest to that point. However, presenting a line with written characters may cause problems. First, the characters may help participants to estimate the location of the midpoint; although participants are instructed to estimate the midpoint of the line rather than that of the character string, they may refer to the character string subconsciously. Second, presentation of the characters themselves might induce directional spatial bias because literal stimuli, which activate the uninjured left hemisphere, may increase the rightward bias associated with left-sided spatial neglect.6,22 A major aim of the present study was to propose an improved version of the VLB task that would assess visual bias of neglect more accurately. In this version, stimuli are presented on a computer rather than paper, and presentation of the characters is controlled through the use of presentation software, which allows the character string to emerge on the line only after the participant has identified the subjective midpoint of the line. Another major aim was to propose a method for assessing proprioceptive bias in neglect. We designed a variant of the VLB task, called the VLB plus pointing task. This test is performed in the same way as the VLB task until the patient reads the character and then points to it, thereby receiving proprioceptive feedback. The VLB plus pointing task is similar to the character line-bisection task and the exactly bisected line-selection task, in that it requires both visual and proprioceptive sensation; it differs in that it uses the same stimuli as the VLB task, so that the results obtained from the tasks are directly comparable. In the present study, the VLB task and the VLB plus pointing task were performed by patients with unilateral neglect. By comparing the results of these tasks, we were able to confirm the existence of proprioceptive bias. An additional aim of this study was to test whether the mechanism of neglect is supramodal or modality-specific, an issue that is currently contested (for review see Bisiach et al.).23 If neglect is a disorder of lower cognitive processes, involving either pathways of the visual modality or those of the proprioceptive
Fig. 1. A representation of the computer screen showing the fade-in function of the presentation software: the white character string emerges slowly onto the solid black line to prevent participants from making sudden eye movements.
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modality, it will probably occur in a modality-specific manner. If, conversely, neglect is a disorder of higher cognitive processes on the representational level, the results of comparable tests should tend to be similar. This issue remains unresolved because many studies use assessment methods requiring free hand movement or compare results obtained from assessment tasks using different stimuli. Because the VLB and the VLB plus pointing tasks were performed using the same stimuli, we were able to directly compare the results obtained. 2. Materials and methods 2.1. Participants Ten right-handed patients with neglect (six males and four females) with a mean age of 70 years (range = 55–85 years) were included in the study. All participants had right-hemisphere lesions due to cerebrovascular events and provided written informed consent before testing. MRI was performed on the patients who were able to undergo the procedure, and CT scans were performed on all others. The lesions were traced using the templates of Damasio et al.24 The presence of visual field defects was assessed by a confrontation method. Table 1 shows the clinical data for participants. The presence and severity of neglect was assessed by administering the following tasks: (i) a line-bisection task using a 204 mm line; (ii) a line-cancellation task with 40 line segments; and (iii) a drawing task involved a picture of a daisy with nine petals and two leaves. The presence of neglect, as assessed through the first task, was defined according to the criteria of Fukatsu et al. (threshold is 5% of the length of the line),25 and the presence of neglect, as assessed through the second task, was defined according to the criteria of Wilson et al. (more than three lines omitted).13 The severity of neglect was rated as mild, moderate, or severe according to the criteria of Levine et al.26 The presence and severity of neglect as assessed through the drawing task was rated according to the criteria of Ishiai et al.27 Participants were defined as having neglect when they met at least one of these three sets of criteria and when they showed clinical behaviour typical of neglect: (i) orienting towards the right side when addressed from the front or the left; (ii) spontaneous deviation of the head and eyes towards the right; and (iii) ignoring people or objects located on the left.28 2.2. Apparatus Images were presented to the participants on a laptop computer (eMachines M5307 or Acer Aspire 5920 [Xizhi, Taipei, Taiwan])
equipped with a 39-cm (15.4 inch) liquid-crystal display and running the Windows operating system (Microsoft; Redmond, WA, USA). The resolution was set at 800 1280 pixels. PowerPoint software (Microsoft) was used to present the images. The computer was controlled by the experimenter with a trackball or a mouse. 2.3. Experimental conditions Each participant was tested individually while seated. The computer was placed on a table in front of the participant and its center was aligned approximately with the participant’s sagittal axis. The viewing distance was approximately 45 cm. At the beginning of each trial, the participant’s right hand was placed on the table immediately beside the computer or on the right armrest of the chair. Each participant performed 12 consecutive trials of the VLB task, followed by the same number of trials of the VLB plus pointing task. 2.4. Stimuli used in the VLB and the VLB plus pointing tasks A 300 mm 7 mm horizontal black line was presented on the display. The character string that was later presented on the line consisted of 43 different ‘‘kana”, or Japanese language characters (white, 18 point font size). The distance between characters was 7 mm. The order in which the characters were presented on the line was different in each trial. 2.5. Procedure 2.5.1. Procedure common to the VLB and VLB plus pointing tasks First, the solid black line was presented, and the participant identified his or her subjective midpoint of the line. The examiner then used the animation function of the PowerPoint software to present the character string on the line, and the participant read the character nearest to the midpoint. 2.5.2. Procedure unique to the VLB task After the participant read the character, the examiner indicated it using the cursor (a white arrow, the default in Windows software) and asked the participant to confirm that the character indicated was the character they had read. 2.5.3. Procedure unique to the VLB plus pointing task After the participant read the character, he or she was asked to point to the character with their right index finger, thus receiving proprioceptive feedback, and to confirm that the character indicated was the character they had read.
Table 1 Clinical details and test results for each participant indicating the presence and severity of unilateral neglect Partic. No.
Age (yrs)
Gender
Lesion locations
VFD
Etiology
Line cancelln.
Line bisection
Copying a daisyà
1 2 3 4 5 6 7 8 9 10
55 73 67 58 72 70 85 75 73 68
M M M F M F F M F M
D DFrPTO DFrPT D FrPTO DFrP DFr DFrPT PT DFrPT
H H H
B I B+I I I B I I I B+I
+++ + +++ +
+++ ++ +++
+++ ++ ++
+ +
++
+ + ++
++ + +
Mean
70
H
H H
+ + + ++
B = bleeding, cancelln. = cancellation, D = deep central, F = female, Fr = frontal lobe, H = hemianopia, I = infarction, M = male, O = occipital lobe, P = parietal lobe, Partic. = participant, T = temporal lobe, VFD = visual field defect, yrs = years, = none, + = mild, ++ = moderate, +++ = severe. The severity was rated according to the criteria of Levine et al.26 à The severity was rated according to the criteria of Ishiai et al.27
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2.6. Analysis In the first trial of the VLB plus pointing task, no feedback was perceived. Therefore, the results of the first trial were excluded. The results of the remaining 11 trials for both tasks were analyzed. The distance between the true center of the line and the center of the character chosen was accepted as the deviational error in both tasks. A rightward deviation was designated as a positive value and a leftward one as a negative value. The presence and severity of neglect as assessed by these two tasks was evaluated and rated according to the criteria of Fukatsu et al. and Levine et al., respectively.25,26 Neglect was classified as severe (if the mean deviation was >90 mm from the true center of the line), moderate (>50 mm but <90 mm), mild (>15 mm but <50 mm), or not present (<15 mm). 3. Results Fig. 2 shows the VLB and VLB plus pointing test score results. Table 2 shows the participants’ classifications and the mean deviations of the subjective midpoints in both tasks for each participant and for the participant group as a whole. In the VLB task, participants selected and read a character without moving their hand. Therefore, the location of the character represented the visually
perceived midpoint, and the deviational error was considered to represent the visual bias of neglect. Seven participants (1–3, 5, 6, 8 and 9) showed rightward deviation greater than the threshold value and thus were classified as having visual neglect. In the VLB plus pointing task, participants were required to perceive a stimulus visually and also to perform a visually guided pointing movement toward the stimulus. Four participants (3, 6, 7 and 9) exhibited greater deviation in the VLB plus pointing task than in the VLB task which could be attributed to the bias caused by this pointing movement. We considered that this bias does not primarily represent intentional bias of neglect, because each visually guided pointing movement was aimed at a character that the participants themselves had identified; this helps avoid the problems associated with free hand movements to non-indicated points, as in the ordinary line-bisection, gap-bisection,29 and open-loop reaching tasks,30 which may cause hypo/hypermetric error. Fig. 3 shows the mean deviation of each trial time for the four patients who exhibited greater deviation in the VLB plus pointing task than in the VLB task. This deviation increased gradually in an alternating succession of trials in the VLB plus pointing task. We interpreted this to mean that the proprioceptive feedback generated in each trial affected the participant’s performance in the next trial, so that the increase in deviation, which was observed in the VLB plus pointing task but not in the VLB task, was caused by proprioceptive bias. Accordingly, these four participants were classified as having proprioceptive bias. The mean deviations exhibited by each patient in the two tasks were compared using a dependent Student’s t-test. Four participants (3, 6, 7 and 9) showed significantly greater rightward mean deviation in the VLB plus pointing task than in the VLB task. Two participants (5 and 10) showed significantly greater rightward mean deviation in the VLB task than in the VLB plus pointing task. Four participants (1, 2, 4 and 8) showed no significant difference in mean deviation between the two tasks (Table 2). As a group, the patients exhibited no significant difference in mean deviation between the two tasks, according to a paired Student’s t-test. 4. Discussion
Fig. 2. A bar graph showing results of the verbal line-bisection (VLB) and the VLB plus pointing task for 10 participants (P1–P10) with unilateral neglect. The mean deviations in both tasks are shown separately for some individual participants (Fig. 3).
Of our 10 participants, eight showed rightward deviation greater than the threshold value in the VLB task, and nine showed rightward deviation greater than the threshold value in the VLB plus pointing task. Thus, both tasks were considered successful in detecting the perceptual-attentional bias of neglect. Comparison of the results of the tasks varied for each participant. Participants 1, 2, 5, and 10 were classified as having visual neglect but no proprioceptive bias. Participant 7 was classified as having proprioceptive bias but no visual neglect. These results
Table 2 Verbal line bisection (VLB) and VLB plus pointing test results for each participant with unilateral neglect Partic. No.
Test score VLB (mm)
Severity
VLB plus pointing (mm)
Severity
1 2 3 4 5 6 7 8 9 10
97.4 (±24.5) 59.8 (±9.6) 57.3 (±13.3) 7.0 (±4.2) 49.6 (±11.7) 35.0 (±4.2) 0.6 (±5.5) 33.1 (±7.3) 17.2 (±9.1) 76.4 (±15.9)
+++ ++ ++
112.6 (±20.6) 66.8 (±11.7) 103.7 (±14.6) 12.1 (±8.5) 31.8 (±9.1) 50.2 (±13.3) 18.5 (±11.3) 35.6 (±5.5) 38.2 (±12.8) 49.6 (±11.7)
+++ ++ +++
Mean
43.2 (±30.9)
+ + + + ++
51.9 (± 33.6)
+ ++ + + + +
VLB vs. VLB plus pointing
Visual neglect present
Proprio. bias present
NS NS p< NS p< p< p< NS p< p<
Yes Yes Yes No Yes Yes No Yes Yes Yes
No No Yes No No Yes Yes No Yes No
0.001 0.01 0.005 0.001 0.005 0.001
NS
VLB = verbal line bisection, NS = not significant, Partic. = participant, Proprio. = proprioceptive,
= none, + = mild, ++ = moderate, +++ = severe.
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References
Fig. 3. The mean deviations of each trial time in the four patients who exhibited greater deviation in the verbal-line bisection (VLB) plus pointing task showing that the deviation increases gradually in the VLB plus pointing task.
indicate that neglect occurs in a modality-specific manner, supporting the attentional theory of neglect. At a minimum, these results show that supramodal disorder is not the only cause of perceptual-attentional neglect. Conversely, participants 3, 6, and 9 were classified as having both visual neglect and proprioceptive bias. These results support the theory that neglect occurs through a supramodal mechanism. Overall, the results of this study can be used to support both the supramodal theory and the modality-specific theory; the possibility remains that perceptual-attentional neglect is a heterogeneous phenomenon. From a clinical viewpoint, specific assessments for each type of neglect may be crucial. Some studies suggest that different subtypes of neglect may respond differently to various treatments (for reviews see Bowen et al.,31 Chokron et al.,32 and Pierce et al.).33 For patients with supramodal neglect, therapy that affects the organization of higher-level spatial representation may be more effective than modality-specific therapy. Cognitive exercise in a specific modality may improve neglect in that modality. Ladavas et al. attempted treatment limited to the visual modality for patients with neglect, and observed improvement specifically in the visual modality of neglect.34 Conversely, proprioceptive therapy such as neck muscle vibration and trunk rotation may be more effective for patients with proprioceptive neglect.35,36 However, few reports demonstrate the long-term efficacy of such facilitative techniques in cognitive rehabilitation. It is also possible that strengthening exercise of perceptual functions in a less severely damaged modality may compensate for residual neglect in another modality.
5. Conclusion The results of this study indicate the impact of proprioceptive feedback on performance in assessments of unilateral neglect and suggest that omissions and deviational errors that have been interpreted as motor-intentional or tactile neglect in previous studies may actually have been, at least in part, proprioceptive bias. To clarify this issue we must develop an assessment method that will allow us to dissociate proprioceptive bias from motor and tactile bias in neglect; we are investigating this possibility.
1. Heilman KM, Valenstein E. Mechanisms underlying hemispatial neglect. Ann Neurol 1979;5:166–70. 2. Heilman KM. Intentional neglect. Front Biosci 2004;9:694–705. 3. Mattingley JB, Bradshaw JL, Phillips JG. Impairments of movement initiation and execution in unilateral neglect: directional hypokinesia and bradykinesia. Brain 1992;115:1849–74. 4. Buxbaum LJ, Ferraro MK, Veramonti T, et al. Hemispatial neglect: subtypes, neuroanatomy, and disability. Neurology 2004;62:749–56. 5. Ghacibeh GA, Shenker JI, Winter KH, et al. Dissociation of neglect subtypes with transcranial magnetic stimulation. Neurology 2007;69:1122–7. 6. Kinsbourne M. A model for the mechanism of unilateral neglect of space. Trans Am Neurol Assoc 1970;95:143. 7. Posner MI, Walker JA, Friedrich FJ, et al. Effects of parietal injury on covert orienting of attention. J Neurosci 1984;4:1863–74. 8. De Renzi E, Gentilini M, Faglioni P, et al. Attentional shift towards the rightmost stimuli in patients with left visual neglect. Cortex 1989;25:231–7. 9. Ladavas E, Umilta C, Ziani P, et al. The role of right side objects in left side neglect: a dissociation between perceptual and directional motor neglect. Neuropsychologia 1993;31:761–73. 10. Bisiach E, Luzzatti C. Unilateral neglect of representational space. Cortex 1978;14:129–33. 11. Bisiach E, Neppi-Modona M, Genero R, et al. Anisometry of space representation in unilateral neglect: empirical test of a former hypothesis. Conscious Cogn 1999;8:577–84. 12. Milner AD. Animal models for the syndrome of spatial neglect. In: Jeannerod M, editor. Neurophysiological and neuropsychological aspects of spatial neglect. Amsterdam: Elsevier; 1987. p. 259–88. 13. Wilson B, Cockburn J, Halligan P. Behavioural inattention test. Titchfield: Thames Valley Test Company; 1987. 14. Chiba Y, Yamaguchi A, Eto F. Assessment of sensory neglect: a study using moving images. Neuropsychol Rehabil 2006;16:641–52. 15. Chiba Y, Nishihara K, Yamaguchi A, et al. Midpoint fixation task: quantitative assessment of visual neglect. J Clin Neurosci 2008;15:647–9. 16. Reuter-Lorenz PA, Posner MI. Components of neglect from right-hemisphere damage: an analysis of line bisection. Neuropsychologia 1990;28:327–33. 17. Milner AD, Harvey M, Roberts RC, et al. Line bisection errors in visual neglect: misguided action or size distortion? Neuropsychologia 1993;31:39–49. 18. Chokron S, Colliot P, Atzeni T, et al. Active versus passive proprioceptive straight-ahead pointing in normal subjects. Brain Cogn 2004;55:290–4. 19. Na DL, Adair JC, Choi SH, et al. Ipsilesional versus contralesional neglect depends on attentional demands. Cortex 2000;36:455–67. 20. Chiba Y, Haga N. Analysing non-motor bias in unilateral neglect with a new variant of the line bisection task. Brain Inj 2008;22:952–9. 21. Chiba Y, Yamaguchi A, Eto F. A simple method to dissociate sensory-attentional and motor-intentional biases in unilateral visual neglect. Brain Cogn 2005;58:269–73. 22. Heilman KM, Watson RT. Changes in the symptoms of neglect induced by changing task strategy. Arch Neurol 1978;35:47–9. 23. Bisiach E, McIntosh RD, Dijkerman HC, et al. Visual and tactile length matching in spatial neglect. Cortex 2004;40:651–8. 24. Damasio H, Damasio AR. Lesion analysis in neuropsychology. New York: Oxford University Press; 1989. 25. Fukatsu R, Fujii T, Kimura I, et al. Effects of hand and spatial conditions on visual line bisection. Tohoku J Exp Med 1990;161:329–33. 26. Levine DN, Warach JD, Benowitz L, et al. Left spatial neglect: effects of lesion size and premorbid brain atrophy on severity and recovery following right cerebral infarction. Neurology 1986;36:362–6. 27. Ishiai S, Furukawa T, Tsukagoshi H. Visuospatial processes of line bisection and the mechanisms underlying unilateral spatial neglect. Brain 1989;112:1485–502. 28. Karnath HO, Himmelbach M, Rorden C. The subcortical anatomy of human spatial neglect: putamen, caudate nucleus and pulvinar. Brain 2002;125:350–60. 29. Goodale MA, Milner AD, Jakobson LS, et al. Kinematic analysis of limb movements in neuropsychological research: subtle deficits and recovery of function. Can J Psychol 1990;44:180–95. 30. Harvey M, Milner AD, Roberts RC. Spatial bias in visually-guided reaching and bisection following right cerebral stroke. Cortex 1994;30:343–50. 31. Bowen A, Lincoln NB. Cognitive rehabilitation for spatial neglect following stroke. Cochrane Database Syst Rev 2007;18:CD003586. 32. Chokron S, Dupierrix E, Tabert M, et al. Experimental remission of unilateral spatial neglect. Neuropsychologia 2007;45:3127–48. 33. Pierce SR, Buxbaum LJ. Treatments of unilateral neglect: a review. Arch Phys Med Rehabil 2002;83:256–68. 34. Ladavas E, Menghini G, Umilta C. A rehabilitation study of hemispatial neglect. 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Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Evaluating visual bias and effect of proprioceptive feedback in unilateral neglect Yu Chiba a,b,c,*, Ken Nishihara b, Nobuhiko Haga a a
Department of Rehabilitation Medicine, The University of Tokyo Hospital, 7-3-1 Hongo, Bunkyo, Tokyo 113-0033, Japan Division of Rehabilitation Medicine, National Center of Neurology and Psychiatry, Tokyo, Japan c Division of Rehabilitation Medicine, Tsukuba University Hospital, Ibaraki, Japan b
a r t i c l e
i n f o
Article history: Received 24 August 2009 Accepted 7 February 2010
Keywords: Line-bisection task Proprioceptive sensation Unilateral neglect Visual neglect
a b s t r a c t We propose modified versions of the line-bisection task for assessing visual bias and effect of proprioceptive feedback in unilateral neglect; that is, the verbal line-bisection (VLB) task and the VLB plus pointing task. The VLB task requires only a verbal response to assess pure visual bias. Conversely, the VLB plus pointing task requires both a verbal response and pointing to assess visual and proprioceptive bias. Ten patients with unilateral neglect were administered these tasks on a computer using presentation software. Eight participants showed obvious rightward deviation in the VLB task, and were thus classified as patients with visual neglect. Four participants showed significantly greater deviation in the VLB plus pointing task than in the VLB task, and were thus classified as patients with proprioceptive bias. Visual bias and effect of proprioceptive feedback in unilateral neglect were successfully assessed by these tasks. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Patients with unilateral neglect (neglect) fail to report, respond to, or orient towards stimuli located on their contralesional side. This condition is more common after a right hemisphere lesion than after a left hemisphere lesion. Patients with left neglect may have trouble grooming the left side of their bodies, fail to eat from the left side of a tray, and respond poorly to people standing on their left side. On examination, these patients tend to mark a subjective midpoint of a horizontal line to the ipsilesional side of its true center and fail to draw the contralesional side of a figure. The causes of neglect are unclear, although some hypotheses have been proposed. Heilman et al. demonstrated that patients with neglect were significantly slower than control patients to initiate and complete movements towards the contralesional hemispace and hypothesized that neglect is a deficit in the ability to move towards the contralesional hemispace.1 This theory is supported by studies that demonstrate abnormal behaviour toward the contralesional side in patients with neglect (for review see Heilman).2 Mattingley et al. used the term ‘‘directional hypometria” to refer to direction-specific impairments of spatial exploration or movement amplitude, ‘‘directional hypokinesia” to denote slowing in the initiation of contralesionally directed movements, and ‘‘directional bradykinesia” to denote slowing in the execution of movements.3 An emerging hypothesis suggests that neglect is a heterogeneous phenomenon that can be classified into at least
* Corresponding author. Tel.: +81 3 5800 8795; fax: +81 3 5684 2094. E-mail address: [email protected] (Y. Chiba). 0967-5868/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2010.02.017
two types: motor-intentional and perceptual-attentional (non-motor) (for reviews see Buxbaum et al.4 and Ghacibeh et al.5). Several theories have been proposed to explain perceptualattentional neglect. Kinsbourne proposed the activation-orienting hypothesis, claiming that neglect occurs when a unilateral lesion provokes an imbalance in the direction of spontaneous attentional orientation.6 This hypothesis has been supported by multiple research groups. Posner et al. found that patients with right parietal lesions were impaired in their ability to disengage attention from a right cue in order to reorient towards the left space.7 De Renzi et al. found that, in patients with left neglect, attention is magnetically attracted by stimuli presented to the right side.8 Ladavas et al. found that patients with left neglect were faster to respond to targets on their right than to those in the relative left position.9 In contrast to these attentional explanations of spatial neglect, other researchers have proposed that neglect is a supramodal deficit rather than an input-related deficit. For example, Bisiach et al. found that patients with neglect showed symptoms even in imagined perspectives, and proposed the representational hypothesis, which states that neglect is due to a disordered internal representation that is not input-related.10 They also proposed the space anisometry hypothesis, which may account for the behavioural phenomena associated with neglect; according to this hypothesis, the representational medium appears abnormally anisometric along the horizontal dimension to patients with neglect.11 In other words, the medium in representation appears progressively compressed toward the ipsilesional space and relaxed toward the contralesional space logarithmically. Milner suggested that patients with left hemineglect might perceive leftward-located spatial extents as shrunken relative to those
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located on the right, and that the gradient of this distortion might be greater within the left hemispace than within the right.12 This suggests that the subjective space of patients with neglect is distorted and their entire space is misrepresented. Typically, neglect has been assessed by pencil-and-paper description tests, such as the line-bisection task, the line-cancellation task and the figure-copying task (for example, Wilson et al.).13 However, these tests cannot assess the severity of each type of bias involved in neglect (that is, visual, proprioceptive and motorintentional), because during the tests the participant must use both sensory and motor functions, and must perceive both visual and proprioceptive inputs, simultaneously. Thus, a method for assessing neglect in terms of specific modalities is required to select a suitable rehabilitation program for patients with each type of neglect. To assess only visual bias of neglect, some researchers have employed passive line-bisection tasks in which hand movement is not required;14–16 these methods have their own merits and demerits as follows. In some methods a bisector or a bisecting point is moved horizontally along a line by the experimenter, while the participant verbally indicates when the bisector arrives at the subjective midpoint of the line.14,16 In these methods, however, the bisector may act as a cue, and the error might represent the effect of cuing as well as the severity of visual bias. Milner et al. proposed the landmark task in which the participant verbally indicated which side of a pre-bisected line was longer by saying ‘‘right” or ‘‘left”.17 The nature of this test, however, is binary rather than quantitative. In addition, the results from this task are not directly comparable to results from the conventional line-bisection task, because the tasks measure different variables (the proportion of certain answers [%] versus deviational length [mm]). To assess proprioceptive neglect, some research groups have employed a pointing task that requires participants to point straight ahead with one hand while blindfolded (for review see Chokron et al.).18 When patients with right-brain damage and left neglect have been asked to perform this test, some authors have reported patients who demonstrate an ipsilateral shift in the position toward which they point. The straight-ahead pointing task, however, requires free hand movement and, therefore, may account for the motor aspect of neglect in its results even though the task does not require exploratory movement. In addition, the straight-ahead pointing task may be less accurate for patients who have postural instability, which is frequently observed in patients with brain damage. Several passive line-bisection tasks provide proprioceptive feedback to the participant. Na et al. proposed a character linebisection task in which a horizontally aligned character string was presented; the participant was required to identify the character nearest to the center of the string and circle it.19 Chiba et al. proposed the exactly bisected line-selection task, in which multi-
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ple horizontal lines, bisected in various proportions, were presented at the same time on a test paper. Participants first chose which line was the most equally bisected and then indicated it by pointing to the bisector on that line.20 In these tasks, the bisector and the character circled were selected before the patients moved their hands. Therefore, the coordinate of the bisector chosen by the patient represented the perceived midpoint and the deviational error was considered to represent sensory-attentional, rather than motor-intentional, bias of neglect. These tests assessed a combination of visual and proprioceptive bias rather than a single modality. To assess visual neglect quantitatively, without using directional stimuli, the verbal line-bisection (VLB) task was proposed.21 In this test, a long line with written characters (similar to the lowest of the three lines shown in Fig. 1) was presented; the participant identified the subjective midpoint of the line and read the character nearest to that point. However, presenting a line with written characters may cause problems. First, the characters may help participants to estimate the location of the midpoint; although participants are instructed to estimate the midpoint of the line rather than that of the character string, they may refer to the character string subconsciously. Second, presentation of the characters themselves might induce directional spatial bias because literal stimuli, which activate the uninjured left hemisphere, may increase the rightward bias associated with left-sided spatial neglect.6,22 A major aim of the present study was to propose an improved version of the VLB task that would assess visual bias of neglect more accurately. In this version, stimuli are presented on a computer rather than paper, and presentation of the characters is controlled through the use of presentation software, which allows the character string to emerge on the line only after the participant has identified the subjective midpoint of the line. Another major aim was to propose a method for assessing proprioceptive bias in neglect. We designed a variant of the VLB task, called the VLB plus pointing task. This test is performed in the same way as the VLB task until the patient reads the character and then points to it, thereby receiving proprioceptive feedback. The VLB plus pointing task is similar to the character line-bisection task and the exactly bisected line-selection task, in that it requires both visual and proprioceptive sensation; it differs in that it uses the same stimuli as the VLB task, so that the results obtained from the tasks are directly comparable. In the present study, the VLB task and the VLB plus pointing task were performed by patients with unilateral neglect. By comparing the results of these tasks, we were able to confirm the existence of proprioceptive bias. An additional aim of this study was to test whether the mechanism of neglect is supramodal or modality-specific, an issue that is currently contested (for review see Bisiach et al.).23 If neglect is a disorder of lower cognitive processes, involving either pathways of the visual modality or those of the proprioceptive
Fig. 1. A representation of the computer screen showing the fade-in function of the presentation software: the white character string emerges slowly onto the solid black line to prevent participants from making sudden eye movements.
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modality, it will probably occur in a modality-specific manner. If, conversely, neglect is a disorder of higher cognitive processes on the representational level, the results of comparable tests should tend to be similar. This issue remains unresolved because many studies use assessment methods requiring free hand movement or compare results obtained from assessment tasks using different stimuli. Because the VLB and the VLB plus pointing tasks were performed using the same stimuli, we were able to directly compare the results obtained. 2. Materials and methods 2.1. Participants Ten right-handed patients with neglect (six males and four females) with a mean age of 70 years (range = 55–85 years) were included in the study. All participants had right-hemisphere lesions due to cerebrovascular events and provided written informed consent before testing. MRI was performed on the patients who were able to undergo the procedure, and CT scans were performed on all others. The lesions were traced using the templates of Damasio et al.24 The presence of visual field defects was assessed by a confrontation method. Table 1 shows the clinical data for participants. The presence and severity of neglect was assessed by administering the following tasks: (i) a line-bisection task using a 204 mm line; (ii) a line-cancellation task with 40 line segments; and (iii) a drawing task involved a picture of a daisy with nine petals and two leaves. The presence of neglect, as assessed through the first task, was defined according to the criteria of Fukatsu et al. (threshold is 5% of the length of the line),25 and the presence of neglect, as assessed through the second task, was defined according to the criteria of Wilson et al. (more than three lines omitted).13 The severity of neglect was rated as mild, moderate, or severe according to the criteria of Levine et al.26 The presence and severity of neglect as assessed through the drawing task was rated according to the criteria of Ishiai et al.27 Participants were defined as having neglect when they met at least one of these three sets of criteria and when they showed clinical behaviour typical of neglect: (i) orienting towards the right side when addressed from the front or the left; (ii) spontaneous deviation of the head and eyes towards the right; and (iii) ignoring people or objects located on the left.28 2.2. Apparatus Images were presented to the participants on a laptop computer (eMachines M5307 or Acer Aspire 5920 [Xizhi, Taipei, Taiwan])
equipped with a 39-cm (15.4 inch) liquid-crystal display and running the Windows operating system (Microsoft; Redmond, WA, USA). The resolution was set at 800 1280 pixels. PowerPoint software (Microsoft) was used to present the images. The computer was controlled by the experimenter with a trackball or a mouse. 2.3. Experimental conditions Each participant was tested individually while seated. The computer was placed on a table in front of the participant and its center was aligned approximately with the participant’s sagittal axis. The viewing distance was approximately 45 cm. At the beginning of each trial, the participant’s right hand was placed on the table immediately beside the computer or on the right armrest of the chair. Each participant performed 12 consecutive trials of the VLB task, followed by the same number of trials of the VLB plus pointing task. 2.4. Stimuli used in the VLB and the VLB plus pointing tasks A 300 mm 7 mm horizontal black line was presented on the display. The character string that was later presented on the line consisted of 43 different ‘‘kana”, or Japanese language characters (white, 18 point font size). The distance between characters was 7 mm. The order in which the characters were presented on the line was different in each trial. 2.5. Procedure 2.5.1. Procedure common to the VLB and VLB plus pointing tasks First, the solid black line was presented, and the participant identified his or her subjective midpoint of the line. The examiner then used the animation function of the PowerPoint software to present the character string on the line, and the participant read the character nearest to the midpoint. 2.5.2. Procedure unique to the VLB task After the participant read the character, the examiner indicated it using the cursor (a white arrow, the default in Windows software) and asked the participant to confirm that the character indicated was the character they had read. 2.5.3. Procedure unique to the VLB plus pointing task After the participant read the character, he or she was asked to point to the character with their right index finger, thus receiving proprioceptive feedback, and to confirm that the character indicated was the character they had read.
Table 1 Clinical details and test results for each participant indicating the presence and severity of unilateral neglect Partic. No.
Age (yrs)
Gender
Lesion locations
VFD
Etiology
Line cancelln.
Line bisection
Copying a daisyà
1 2 3 4 5 6 7 8 9 10
55 73 67 58 72 70 85 75 73 68
M M M F M F F M F M
D DFrPTO DFrPT D FrPTO DFrP DFr DFrPT PT DFrPT
H H H
B I B+I I I B I I I B+I
+++ + +++ +
+++ ++ +++
+++ ++ ++
+ +
++
+ + ++
++ + +
Mean
70
H
H H
+ + + ++
B = bleeding, cancelln. = cancellation, D = deep central, F = female, Fr = frontal lobe, H = hemianopia, I = infarction, M = male, O = occipital lobe, P = parietal lobe, Partic. = participant, T = temporal lobe, VFD = visual field defect, yrs = years, = none, + = mild, ++ = moderate, +++ = severe. The severity was rated according to the criteria of Levine et al.26 à The severity was rated according to the criteria of Ishiai et al.27
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2.6. Analysis In the first trial of the VLB plus pointing task, no feedback was perceived. Therefore, the results of the first trial were excluded. The results of the remaining 11 trials for both tasks were analyzed. The distance between the true center of the line and the center of the character chosen was accepted as the deviational error in both tasks. A rightward deviation was designated as a positive value and a leftward one as a negative value. The presence and severity of neglect as assessed by these two tasks was evaluated and rated according to the criteria of Fukatsu et al. and Levine et al., respectively.25,26 Neglect was classified as severe (if the mean deviation was >90 mm from the true center of the line), moderate (>50 mm but <90 mm), mild (>15 mm but <50 mm), or not present (<15 mm). 3. Results Fig. 2 shows the VLB and VLB plus pointing test score results. Table 2 shows the participants’ classifications and the mean deviations of the subjective midpoints in both tasks for each participant and for the participant group as a whole. In the VLB task, participants selected and read a character without moving their hand. Therefore, the location of the character represented the visually
perceived midpoint, and the deviational error was considered to represent the visual bias of neglect. Seven participants (1–3, 5, 6, 8 and 9) showed rightward deviation greater than the threshold value and thus were classified as having visual neglect. In the VLB plus pointing task, participants were required to perceive a stimulus visually and also to perform a visually guided pointing movement toward the stimulus. Four participants (3, 6, 7 and 9) exhibited greater deviation in the VLB plus pointing task than in the VLB task which could be attributed to the bias caused by this pointing movement. We considered that this bias does not primarily represent intentional bias of neglect, because each visually guided pointing movement was aimed at a character that the participants themselves had identified; this helps avoid the problems associated with free hand movements to non-indicated points, as in the ordinary line-bisection, gap-bisection,29 and open-loop reaching tasks,30 which may cause hypo/hypermetric error. Fig. 3 shows the mean deviation of each trial time for the four patients who exhibited greater deviation in the VLB plus pointing task than in the VLB task. This deviation increased gradually in an alternating succession of trials in the VLB plus pointing task. We interpreted this to mean that the proprioceptive feedback generated in each trial affected the participant’s performance in the next trial, so that the increase in deviation, which was observed in the VLB plus pointing task but not in the VLB task, was caused by proprioceptive bias. Accordingly, these four participants were classified as having proprioceptive bias. The mean deviations exhibited by each patient in the two tasks were compared using a dependent Student’s t-test. Four participants (3, 6, 7 and 9) showed significantly greater rightward mean deviation in the VLB plus pointing task than in the VLB task. Two participants (5 and 10) showed significantly greater rightward mean deviation in the VLB task than in the VLB plus pointing task. Four participants (1, 2, 4 and 8) showed no significant difference in mean deviation between the two tasks (Table 2). As a group, the patients exhibited no significant difference in mean deviation between the two tasks, according to a paired Student’s t-test. 4. Discussion
Fig. 2. A bar graph showing results of the verbal line-bisection (VLB) and the VLB plus pointing task for 10 participants (P1–P10) with unilateral neglect. The mean deviations in both tasks are shown separately for some individual participants (Fig. 3).
Of our 10 participants, eight showed rightward deviation greater than the threshold value in the VLB task, and nine showed rightward deviation greater than the threshold value in the VLB plus pointing task. Thus, both tasks were considered successful in detecting the perceptual-attentional bias of neglect. Comparison of the results of the tasks varied for each participant. Participants 1, 2, 5, and 10 were classified as having visual neglect but no proprioceptive bias. Participant 7 was classified as having proprioceptive bias but no visual neglect. These results
Table 2 Verbal line bisection (VLB) and VLB plus pointing test results for each participant with unilateral neglect Partic. No.
Test score VLB (mm)
Severity
VLB plus pointing (mm)
Severity
1 2 3 4 5 6 7 8 9 10
97.4 (±24.5) 59.8 (±9.6) 57.3 (±13.3) 7.0 (±4.2) 49.6 (±11.7) 35.0 (±4.2) 0.6 (±5.5) 33.1 (±7.3) 17.2 (±9.1) 76.4 (±15.9)
+++ ++ ++
112.6 (±20.6) 66.8 (±11.7) 103.7 (±14.6) 12.1 (±8.5) 31.8 (±9.1) 50.2 (±13.3) 18.5 (±11.3) 35.6 (±5.5) 38.2 (±12.8) 49.6 (±11.7)
+++ ++ +++
Mean
43.2 (±30.9)
+ + + + ++
51.9 (± 33.6)
+ ++ + + + +
VLB vs. VLB plus pointing
Visual neglect present
Proprio. bias present
NS NS p< NS p< p< p< NS p< p<
Yes Yes Yes No Yes Yes No Yes Yes Yes
No No Yes No No Yes Yes No Yes No
0.001 0.01 0.005 0.001 0.005 0.001
NS
VLB = verbal line bisection, NS = not significant, Partic. = participant, Proprio. = proprioceptive,
= none, + = mild, ++ = moderate, +++ = severe.
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References
Fig. 3. The mean deviations of each trial time in the four patients who exhibited greater deviation in the verbal-line bisection (VLB) plus pointing task showing that the deviation increases gradually in the VLB plus pointing task.
indicate that neglect occurs in a modality-specific manner, supporting the attentional theory of neglect. At a minimum, these results show that supramodal disorder is not the only cause of perceptual-attentional neglect. Conversely, participants 3, 6, and 9 were classified as having both visual neglect and proprioceptive bias. These results support the theory that neglect occurs through a supramodal mechanism. Overall, the results of this study can be used to support both the supramodal theory and the modality-specific theory; the possibility remains that perceptual-attentional neglect is a heterogeneous phenomenon. From a clinical viewpoint, specific assessments for each type of neglect may be crucial. Some studies suggest that different subtypes of neglect may respond differently to various treatments (for reviews see Bowen et al.,31 Chokron et al.,32 and Pierce et al.).33 For patients with supramodal neglect, therapy that affects the organization of higher-level spatial representation may be more effective than modality-specific therapy. Cognitive exercise in a specific modality may improve neglect in that modality. Ladavas et al. attempted treatment limited to the visual modality for patients with neglect, and observed improvement specifically in the visual modality of neglect.34 Conversely, proprioceptive therapy such as neck muscle vibration and trunk rotation may be more effective for patients with proprioceptive neglect.35,36 However, few reports demonstrate the long-term efficacy of such facilitative techniques in cognitive rehabilitation. It is also possible that strengthening exercise of perceptual functions in a less severely damaged modality may compensate for residual neglect in another modality.
5. Conclusion The results of this study indicate the impact of proprioceptive feedback on performance in assessments of unilateral neglect and suggest that omissions and deviational errors that have been interpreted as motor-intentional or tactile neglect in previous studies may actually have been, at least in part, proprioceptive bias. To clarify this issue we must develop an assessment method that will allow us to dissociate proprioceptive bias from motor and tactile bias in neglect; we are investigating this possibility.
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