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Repetita iuvant: Object-centered neglect with non-verbal visual stimuli induced by repetition
cortex 45 (2009) 863–869
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Research report
Repetita iuvant: Object-centered neglect with non-verbal visual stimuli induced by repetition Silvia Savazzia,*, Francesca Mancinia,b, Gianluigi Veronesib and Lucio Posteraroc a
Department of Neurological and Vision Sciences, University of Verona, and National Institute of Neuroscience, Italy Rehabilitation Unit, Zevio, Verona, Italy c Rehabilitation Unit, Bozzolo, Mantova, Italy b
article info
abstract
Article history:
Neglect can be ego-centered or object-centered depending on the reference frames for
Received 12 May 2008
‘‘left’’ and ‘‘right’’, of either the body or an object. It has been suggested that object-
Reviewed 25 August 2008
centered neglect is not a general phenomenon but is limited to words because only they
Revised 16 September 2008
have a true canonical representation. Here, we examined whether object-centered neglect
Accepted 6 November 2008
could be observed for non-verbal material by creating, after repeated exposure, a canonical
Action editor Giuseppe Vallar
representation of a nonsense figure. Fourteen neglect patients repeatedly bisected a series
Published online 14 November 2009
of asymmetrical nonsense drawings containing two different shapes at their right and left end-points (canonical trials). In the critical trials, which were the last three in the series,
Keywords:
the position of the two shapes was mirror-reversed. Afterwards, neglect patients were
Frames of reference
asked to draw the stimulus, which provided a further measure of whether a canonical
Object-centered neglect
representation of the object has been built by the patients. All the patients made rightward
Object-based neglect
errors with the canonical stimuli. With mirror-reversed stimuli, the bisection errors were reversed to the contralesional side in one patient, returned to zero in one patient and significantly decreased in three patients. In addition, 10 patients reliably drew the canonical stimulus at the end of the series of trials, providing an indication that they built up a canonical representation of the stimulus. The present data provide evidence that object-centered neglect is a phenomenon that is not limited to words. The nature of a stimulus, verbal or non-verbal, is not critical for observing object-centered neglect. What is critical is the way in which material is represented by the patients. ª 2008 Elsevier Srl. All rights reserved.
1.
Introduction
Unilateral neglect is typically defined as a disorder in which patients fail to perceive, orient or respond to stimuli in the contralesional hemispace. Although the spatial nature of neglect is without doubt, the representation of ‘‘left’’ and
‘‘right’’ can relate not only to space, but also to objects. Indeed, it is well known that neglect can be ego-centered (where ‘‘left’’ and ‘‘right’’ are represented with respect to the observer) and allocentric (with respect to an object in space). Beginning with Gainotti and colleagues’ (Gainotti et al., 1972) paper, a growing number of studies have reported
* Corresponding author. Department of Neurological and Vision Sciences, Section of Physiology, University of Verona, Strada le Grazie, 8, 37134 Verona, Italy. E-mail address: [email protected] (S. Savazzi). 0010-9452/$ – see front matter ª 2008 Elsevier Srl. All rights reserved. doi:10.1016/j.cortex.2008.11.006
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examples of allocentric neglect. In contrast to the great amount of evidence in favor of this allocentric neglect, however, ‘‘object-centered neglect’’ remains an ambiguous concept at least for non-verbal stimuli (Mozer, 2002, page 178). This ambiguity is increased by the fact that object-based and object-centered neglect are often used in literature as synonymous even though they reflect the involvement of different frames of reference in defining ‘‘left’’ and ‘‘right’’. According to Walker’s interpretation (Walker, 1995; see also Umilta`, 2001), object-based neglect corresponds to a stimuluscentered neglect derived from an ego-centered coordinate frame. In the clever experiment by Driver and Halligan (1991), for instance, the neglect patient PP was asked to judge if two elongated nonsense shapes were the same or different. In the critical condition the two shapes were both rotated 45 clockwise, so that differences located on the left of the object’s principal axis fell into the right of the patient’s frame of reference. Patient PP missed differences on the left side of the shape’s principal axis even when these differences fell on the right side of egocentric space. These results demonstrate an axis-based neglect of details located to the left side of the shape’s principal axis. Nevertheless, this effect does not imply the presence of an established abstract canonical representation of the shape. The tilted stimuli may be mentally realigned to vertical position so that the neglect is really for leftsided material in viewer-centered coordinates, rather than a seemingly object-centered neglect (Buxbaum et al., 1996). In this case although the patient is still neglecting characteristics of an object, that neglect is based on an egocentric coordinate system not on a coordinate system linked to a canonical representation of the object. Object-centered neglect, on the other hand, indicates an abstract, viewer-independent, representation of the intrinsic ‘‘left’’ and ‘‘right’’ parts of such an object. Thus, to demonstrate object-centered neglect, the object must have a canonical representation that contains a left and right, an attribute that has been considered peculiar to letters and words. A clear and convincing example of an object-centered deficit is the well known case of NG (Caramazza and Hillis, 1990a, 1990b), a left brain-damaged woman with right neglect dyslexia which made neglect errors on the final segments of words, irrespectively of the topographic arrangement of letters (and, thus, viewer-independent). What is required to distinguish object-based and objectcentered neglect is the presence (object-centered) or absence (object-based) of a canonical representation of such an object (where here ‘‘object’’ refers both to words and non-verbal visual stimuli). What remains to be settled instead is which intrinsic properties make a certain type of configuration a ‘‘canonical representation’’. First of all the ‘‘canonical handedness’’ of an object may be a crucial feature in object-centered neglect. Second, the intrinsic asymmetry of such an object is a necessary characteristic for the appearance of this phenomenon (Behrmann and Moscovitch, 1994). In contrast to words, which have an intrinsic handedness, common objects do not have a canonical orientation. Hence for objects, the concepts of ‘‘right’’ and ‘‘left’’ have necessarily to be referred to the viewpoint of the observer. Whereas asymmetric letters (e.g., J/K/R) may not be transformed to their mirror image to the detriment of identity, common objects as well as symmetrical letters (e.g.,
I/W) can have their left and right sides transposed while their identity is still maintained. In such cases, the object’s coordinates are determined solely from the viewer perspective. With regards to this issue, Cubelli and Speri (2001) pointed out that no study with non-verbal material has been able to find evidence of a pure object-centered neglect (see Savazzi et al., 2004 for an exception), but rather have just demonstrated varieties of object-based neglect (or relative egocentric neglect, see Driver and Pouget, 2000). Consequently, it has been suggested (Driver and Pouget, 2000; Mozer, 2002) that object-centered neglect can only be shown with words because they are the only type of visual object that truly has a canonical representation. What seems to be overlooked in this argument, however, is that asymmetrical letters and non-palindrome words have a true canonical representation only because it is derived from the knowledge of a particular written language. In this regard, words do not have a priori distinctive quality that provides for this higher level of representation. Rather, the ‘‘handedness’’ of such items arises from repeated exposure and familiarization of their visual properties (i.e., a particular orientation) that are stable in time. Following this logic, it should be possible to establish a canonical representation after repeated exposure for any kind of material, including non-verbal material, and test whether object-centered neglect can be observed for non-verbal stimuli. As an initial exploration of this idea, Savazzi et al. (2004) asked twenty-four neglect patients to repeatedly bisect a horizontally-aligned 20 cm caricature of a basset hound in a series of 15 trials presented with the head always aligned in a particular position (to the right in a first experiment and to the left in a second experiment). The stimulus was always shown in this particular orientation so as to create a ‘‘canonical’’ representation. At the end of the series of trials patients had to bisect the same, left-right reversed, caricature of the basset hound (i.e., with the head in the opposite position with respect to the stimulus’ vertical axis). With canonical stimuli, neglect patients made errors towards the ipsilesional side (as is typically observed in neglect). When the mirror-reversed version of the basset hound was presented, however, the bisection error reversed from ipsi- to contralesional side in 6 patients and significantly decreased in 4 patients. We interpreted these results as demonstrating object-centered neglect for a newly established canonical representation of a nonverbal object through repeated exposure. However, these results could remain somewhat inconclusive because of a possible alternative interpretation. It is possible that the patient came to expect to see a particular part of the stimulus, which would be that portion of the basset hound that was positioned to the right in the ‘‘canonical’’ stimuli he or she viewed (e.g., the head or the tail depending on the particular condition to which the patient was assigned). If this were the case, the ‘‘novelty’’ of the last, mirror-reversed, trial might induce the patient to search more of visual space for the portion of the basset hound he or she was used to seeing. Since this portion of the basset hound was now located to the left, their search may have drawn their attention leftward reducing the observed neglect. The main goal of the present experiment is to strongly control for this ‘‘novelty effect’’ so that it can be ruled out as
cortex 45 (2009) 863–869
an explanation for our previous results. To do this, in the present experiment 14 neglect patients underwent a task very similar to the one used in our previous experiment, with two important modifications. Firstly, the stimuli to be repeatedly bisected were asymmetrical nonsense drawings as a whole, that is a line where at the right and left end-points a square and a circle were placed (see Fig. 1). We used a nonsense drawing instead of the basset hound in order to reduce the probability that the rightward stimulus could become more familiar, because nonsense drawings are less salient than the head or the tail of the basset hound. Secondly and more importantly, at the end the series of trials, that is after the first critical (mirror-reversed) stimulus, we added two additional mirror-reversed trials. The decision to add two (and not more or less) mirror-reversed trials was taken in order to use an ‘‘ideal’’ number of trials to both exclude the novelty effect as an explanation and to maintain the newly established canonical representation as stable as possible among sessions. We reasoned that only one trial was not enough to adequately substantiate our prediction (no evidence of the ‘‘novelty effect’’) and that more than two trials could weaken the canonical representation. Thus, a total of three trials seem to be a good balance between to have the minimum number of trials to control for the novelty effect and that of not to induce a reduction of the strength of the canonical representation. If the patient’s response is being driven by the ‘‘novelty effect’’, one would predict that neglect errors would become progressively more rightwards from the first to the third mirror-reversed stimulus. This pattern would be expected because the novelty of such an item in reversed orientation would have dissipated over trials, inducing an attentional reorienting towards the right. On the other hand, if the bisection errors remain stable in the three mirror-reversed trials, we would be able to confirm the existence of a true objectcentered neglect even with non-verbal stimuli. If this prediction will be confirmed, it would mean that words have no peculiar qualities that create a higher level canonical representation. Rather, repeated exposure of a particular orientation of a stimulus can establish a high level, viewerindependent, canonical representation even with non-verbal material.
2.
Experiment
2.1.
Methods
2.1.1.
Subjects
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Data were collected from 14 right brain-damaged patients with contralesional neglect and 5 right brain-damaged patients without neglect, who gave informed consent to participate in the experiment. All of them were right-handed. Patients N 3, Nþ 3, Nþ 8 and Nþ 14 suffered from hemianopia as assessed by means of a kinetic Goldmann perimetry. The experiment was performed according to the Declaration of Helsinki. Contralesional visual neglect was assessed by means of the following tasks: (a) Albert cancellation task. Patients were presented with a modified version (Driver and Halligan, 1991) of Albert’s (Albert, 1973) cancellation task composed of 50 short black segments (2 cm long and .5 mm thick) printed on an A4 sheet of paper placed in front of the subject at reading distance. The segments, distributed in ten columns and five rows, were randomly oriented and grouped by proximity in two sub-arrays, each composed of 25 lines, separated by an empty gap, vertically oriented and 4 cm wide. The patients’ task was to cross out all lines with no limitation of time. The number of uncrossed lines homogeneously distributed in an area confined to the left sub-array or comprising the right sub-array was recorded (see NeppiModona et al., 2002 on page 1922 for details). (b) Letter Hs cancellation task (Diller and Weinberg, 1977). Patients were presented with 6 rows of letters (104 Hs and 208 distracting letters) distributed in 52 columns, printed on an A3 sheet of white paper, and asked to cross out all the Hs. The number of omitted Hs to the left was recorded. (c) Line bisection task (Schenkenberg et al., 1980). Patients were required to bisect a series of five 20 cm long and 2 mm thick black horizontal lines. Errors were measured with approximation to the nearest mm. Positive values indicate a rightward error and negative values a leftward error. The mean bisection error was recorded in each subject. Neglect was defined according to the following criteria: 5 or more omissions in the Albert task and/ or 5 or more omissions to the left in the Diller task and/or
Fig. 1 – Stimuli used in the bisection task. A: canonical stimulus and B: mirror-reversed stimulus for half of the patients. The position of the two shapes at each end-point of the line was counterbalanced among patients.
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a mean rightward bisection error equal to or exceeding 10 mm. Demographic and clinical data are reported in Table 1.
2.1.2.
Stimuli and procedure
Patients had to bisect 20 cm long lines printed in black and centered, both horizontally and vertically, on a sheet of A4 white paper. At the end-points of the line a square and a circle were positioned. In 18 trials, the stimulus was horizontally oriented with one shape (e.g., the square) on the right side and a different shape (e.g., the circle) on the left side (‘‘canonical’’ stimulus). The last 3 of these trials were critical for testing our hypotheses. On these trials the two shapes were placed at the opposite end-point from their original position (‘‘mirrorreversed’’ stimulus). In two trials (6th, 12th) the stimulus was vertically oriented. Vertical stimuli were given in order to have an additional means to prevent mere surprise or novelty on the presentation of the horizontal mirror-reversed trials, and were not considered in the analysis of the results (see Savazzi et al., 2004 for a similar approach). The position of the two shapes was counterbalanced among patients so that what was the ‘‘canonical’’ stimulus for half of the patients was the ‘‘mirror-reversed’’ stimuli for the other half (Fig. 1). Each series of trials was repeated 5 times, each time on different days, for a total of 100 stimuli to bisect (90 horizontally oriented – 75 canonical and 15 mirrorreversed and 10 vertically oriented). In addition, after each series of 20 trials, patients were requested to draw the stimulus previously bisected without any instruction on the orientation in which it should be drawn (i.e., canonical or mirror-reversed). Neglect patients typically started drawing the right half of the figure and, occasionally, did not complete the left part. In order to obtain a reliable measure, neglect patients were requested to draw the entire figure, if not spontaneously done. This task provided us with a way to measure whether the individual had indeed created
a ‘‘canonical’’ representation of the object. If the patient drew the stimulus in its canonical orientation, despite from the fact that the last three times it was viewed in a mirror-oriented position, we can infer that indeed he or she created a canonical representation of the stimulus, which is a prerequisite to demonstrate object-centered neglect.
2.2.
Results
Table 2 shows mean bisection errors (mm) made by individual patients on horizontal ‘‘canonical’’ and critical (mirrorreversed) trials, averaged across the 5 repetitions of the series of 20 trials (15 in the ‘‘canonical’’ and 3 in the mirror-reversed with the 2 vertical presentations not analyzed). Positive and negative values refer to rightward and leftward errors, respectively.
2.2.1.
Bisection error
N patients showed a comparable [T(4) ¼ .426, p ¼ .692] mean bisection error of .28 mm with canonical stimuli and of .38 mm with mirror-reversed stimuli, indicating no difference between the two stimulus configurations, as expected. This result indicates that an effect with neglect patients cannot be due to an unspecific difference between the two configurations. Nþ patients made a mean bisection error of .75 mm upwards with vertical stimuli, not significantly different from zero on a one sample t-test [T(27) ¼ .353, p ¼ .727]. A separate analysis on bisection errors with respect to the two configurations (canonical vs mirror-reversed) showed no reliable difference on deviation of the bisection error. This null effect could be due to the fact that the vertical stimuli were intermingled among horizontal stimuli and that the canonical representation may not be strong enough to produce an effect on vertical trials. A group analysis on the bisection errors with the canonical and the critical conditions showed that in Nþ patients the mean rightward bisection error with the critical stimuli
Table 1 – Demographic and clinical data Patient Nþ 1 Nþ 2 Nþ 3 Nþ 4 Nþ 5 Nþ 6 Nþ 7 Nþ 8 Nþ 9 Nþ 10 Nþ 11 Nþ 12 Nþ 13 Nþ 14 N 1 N 2 N 3 N 4 N 5
Sex
Age
Education
Lesion site (CT)
Length of illness (months)
MMSE
Albert
Diller
Line Bisection (mm)
F M M M M F M M F M F F M F M F F M M
74 74 74 59 61 62 70 72 75 76 73 75 63 85 70 66 71 64 67
3 11 5 11 8 5 8 9 5 5 5 3 9 2 3 5 3 9 5
P TP TO T FTP T FTP TPO FTP bg P TP FP ci-O ci-TP P TO T TP
2 2 1 11 2 5 2 3 4 6 1 2 3 1 2 3 5 2 1
24 27 30 29 27 28 25 24 24 27 24 27 26 29 28 27 29 30 29
28 0 27 11 1 0 41 39 25 15 39 25 5 29 0 0 0 0 0
85 67 29 51 45 59 97 / 83 90 85 72 85 / 0 0 1 0 2
29.4 13 60.8 36.8 12.6 16.6 40.4 68 6.8 25.4 25.8 25.6 20.2 45 1.7 .8 1.1 1.3 .8
F ¼ frontal; T ¼ temporal; P ¼ parietal; O ¼ occipital; bg ¼ basal ganglia; ci ¼ capsula interna.
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Table 2 – Mean bisection errors in mm (SD) for canonical and critical stimuli as a function of individual patients Patient
Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ N N N N N
1 2 3 4 5 6 7 8 9 10 11 12 13 14 1 2 3 4 5
Canonical Stimuli (N ¼ 75)
Critical stimuli (N ¼ 15)
Number of canonical stimuli (N ¼ 5) drawn
31 (11.48) 18.23 (7.08) 25.23 (8.54) 32.57 (9.23) 10.74 (4.53) 15.16 (4.56) 34.43 (14.93) 26.69 (15.35) 7.56 (6.41) 20.29 (6.11) 45.88 (15.45) 22.56 (13.24) 85.69 (3.05) 35.04 (12.33) 2.2 (3.45) 1.2 (2.7) -1 (1.1) -2.6 (3.4) 1.6 (2.5)
32.27 (8.38) 17.4 (10.03) 24.47 (7.76) 30.94 (8.20) .27 (3.73) 17.4 (5.90) 15.27 (13.66) 13.54 (24.41) -4.8 (7.55) 20.94 (11.34) 42.27 (13.04) 19.27 (20.36) 83.14 (12.74) 25.47 (9.34) 1.9 (2.16) 1.7 (2.9) -.7 (1.8) -3.2 (3.8) 2.2 (2.8)
2 5 2 1 4 4 5 4 5 4 5 5 1 4 2 3 4 5 4
Bold indicates patients with a significant decrement or reversal of the bisection error on the critical trials. Bold italics indicate a significant number of times the patient drew the canonical stimulus at the end of the series of trials.
(24.12 mm) was smaller [T(13) ¼ 3.002, p < .05] than that with the canonical stimuli (29.36 mm). To further substantiate the source of this difference, that is to find which patients showed an object-centered neglect, we performed single subject analyses. For each Nþ patient, the difference between errors with canonical and reversed stimuli was tested by means of a mixed ANOVA (using a Type II Sum of Squares method for the computation of within subjects variability to take into account the different numerosity of canonical and reversed stimuli they had to bisect) with Condition (canonical vs mirrorreversed stimuli) as a between-subject factor and Session (1 to 5) as a within-subject factor. Significant results were found in five neglect patients: Nþ 5, Nþ 7, Nþ 8, Nþ 9 and Nþ 14. In patient Nþ 5 the bisection error markedly reduced in the critical trial [F(1,16) ¼ 121.454; p < .001], showing no rightward (.27 mm) error. Patient Nþ 9 showed a significant reversal in the direction of the bisection error [F(1,16) ¼ 51.92; p < .001]. In the remaining three patients the rightward bisection error was markedly reduced with the mirror-reversed stimulus: slight for patient Nþ 14 [F(1,16) ¼ 14.067; p < .005] but very strong for patient Nþ 7 [F(1,16) ¼ 27.032; p < .001] and patient Nþ 8 [F(1,16) ¼ 7.869; p < .05]. These results indicate that words are not the only material for which object-centered neglect can be demonstrated; even nonsense objects can produce a higherorder, viewer-independent, canonical representation after repeated exposure of the same orientation of such an object, and neglect of the left-side of such canonical representations can occur.
2.2.2.
Novelty effect
To examine the possibility that our results with neglect patients were driven by a ‘‘novelty effect’’, the bisection errors
with the three mirror-reversed stimuli (Table 3) were entered in a one-way between-subject ANOVA for each Nþ patient. The prediction if a ‘‘novelty effect’’ is occurring would be to find a progressive worsening of the rightward bisection error from the first to the third mirror-reversed stimulus. Contrary to this prediction in none of the Nþ patients were the bisection errors reliably different (all Fs < 1) among the three mirror-reversed stimuli, ruling out the ‘‘novelty effect’’ hypothesis as an explanation for the observed pattern of results. A possible cause for this negative effect could be the low statistical power of the analyses since there were only 5 cases per cell. To control for this possibility, we performed a group analysis on the bisection errors with the three mirrorreversed trials which allow us to increase the statistical power due to a bigger numerosity of the sample. This new analysis showed the same result as the single subjects analyses, that is no difference in the line bisection error among the three critical trials [F(2,39) ¼ .006, p ¼ .994].
2.2.3.
Drawing task
As a test to ensure that indeed a canonical representation had been created, the proportion of canonical stimuli drawn at the end of the series of trials (Table 2, rightmost column) were entered in a 1-tailed binomial analysis. Three of the five N patients revealed a reliable effect of drawing the stimuli in the canonical orientations: Patients N 3 and N 5 drew 4 canonical stimuli, p < .01; whereas patients N 4 drew 5 canonical stimuli, p < .001. More importantly, all the Nþ patients showing objectcentered effects in the bisection task also showed the same effect in the drawing task: that is, they consistently drew the canonical version of the stimulus (patients Nþ 5, Nþ 8 and Nþ 14 drew 4 canonical stimuli, p < .01; whereas patients Nþ7 and Nþ 9 drew 5 canonical stimuli, p < .001). Moreover, five of the remaining 9 Nþ patients with no object-centered effects in the bisection task, revealed a reliable effect of drawing the stimuli in the canonical orientations. Patients Nþ 6 and Nþ 10 drew 4 canonical stimuli ( p < .01), whereas patients Nþ 2, Nþ 11 and Nþ 12 drew 5 canonical stimuli ( p < .001). These results indicate that, independently from the fact that the last three
Table 3 – Mean bisection errors in mm (SD) the three critical stimuli as a function of individual patients Patient
Critical Stimuli
Nþ 1 Nþ 2 Nþ 3 Nþ 4 Nþ 5 Nþ 6 Nþ 7 Nþ 8 Nþ 9 Nþ 10 Nþ 11 Nþ 12 Nþ 13 Nþ 14
1
2
3
31.4 (8.91) 15.8 (7.05) 23.8 (8.23) 33 (9) .6 (5.13) 18.4 (6.80) 21 (11.11) 12.4 (23.94) -5 (7.91) 20.4 (10.06) 45.6 (14.93) 12.4 (33.40) 84 (7.65) 26.4 (7.89)
30.2 (6.65) 17 (14.92) 25.6 (7.54) 28.6 (9.29) 0 (4.30) 14.8 (7.43) 14.6 (9.53) 16.8 (13.55) -4.8 (6.69) 24 (14.71) 42.2 (10.94) 18.2 (8.81) 79.4 (21.72) 24.4 (10.64)
35.2 (10.26) 19.4 (8.47) 24 (9.17) 31.2 (7.46) .2 (1.92) 19 (2.74) 10.2 (19.11) 11.4 (36.15) -4.6 (9.61) 18.4 (10.60) 39 (15) 27.2 (10.89) 86 (3.08) 25.6 (11.28)
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stimuli bisected were mirror-reversed, when asked to draw a stimulus, the strongest and more accessible configuration is the canonical representation, strongly indicating that a nonsense object can have access to such a high-level representation.
3.
Discussion
The present study confirms and adds further evidence to previous data by Savazzi et al. (2004) showing that objectcentered neglect is not limited to words. In the present experiment 14 neglect patients and 5 brain-damaged patients without neglect repeatedly bisected a nonsense drawing with two different shapes placed at the right and left end-points, making an error towards the ipsilesional side. When presented with a mirror-reversed version of the stimulus, a subset of neglect patients showed either a reduction or reversal of the bisection error. In addition, the majority of patients with and without neglect in the study, when requested to drew the stimulus, reliably draw the canonical stimulus in the series indicating that this stimulus was represented in a high-level canonical form. Importantly, our result also rules out an alternative explanation for the demonstration of object-centered neglect, namely that the reversal was induced by a ‘‘novelty effect’’. Such an explanation would have predicted a progressive worsening of the bisection errors from the first to the third mirror-reversed stimulus. Such a change would occur because the novelty of the item in reversed orientation would have dissipated over trials. In contrast to such a prediction, no difference in bisection was found across these three trials. The variability in the pattern of response across patients deserves some consideration. Five out of 14 (35.7%) neglect patients of our sample showed a reversal or a reduction of the bisection error from ipsi- to contralesional space in the critical stimulus presentation condition (all of them also showing a significant effect in the drawing task, indicating that they had created a canonical representation of the item). Five other neglect patients (35.7%) showed evidence of having created a canonical representation of the object in the drawing task and the remaining 4 (28.6%) did not. What can account for these differences? Since 4 neglect patients did not show evidence of creating a canonical representation of the object, it would obviously be impossible to demonstrate objectcentered neglect in these individuals. This could be due to the fact that for such neglect patients, the number of repetitions of the canonical stimulus was not enough to create a stable canonical representation. Another explanation could be that these patients might have a strong egocentric neglect preventing them to access an object-centered representational level. To disentangle these two possibilities, further studies could try and find whether by adding more presentations of the canonical stimulus (thus increasing the strength of the canonical representation), the percentage of patients showing object-centered neglect would increase or not. Of the remaining neglect patients who did show evidence of creating an object-centered representation, only half showed evidence of object-centered neglect in bisecting the drawings. We can speculate that for those patients who did
not show evidence of object-centered neglect, the canonical representation of the object was less strong than for those neglect patients who did show object-centered neglect. Unlike words, which patients have been familiarized with over a long period of time, the short familiarization time used in the present study did not allow for the creation of as strong a canonical representation. Another possibility could be that the drawing task and the bisection task have a different sensitivity to detect object-centered neglect. Indeed, it is well known that neglect can dissociate among tests. As an example, in the present paper patients Nþ 2, Nþ 5 and Nþ 6 are below the selection criteria with respect to the Albert task but very above the selection criteria with respect to the Diller and the bisection tasks. Thus, it could be possible that the bisection task have a lower sensitivity than the drawing task to reveal a high level, object-centered, representation of the material proposed. Further investigation will be needed to explore these possibilities. The results of the present experiment, in addition, aid in considering what the requisite conditions are for demonstrating object-centered neglect. We have ascertained that the nature of the material, verbal or non-verbal, is irrelevant as we have observed object-centered neglect with nonsense visual stimuli. What seems to be critical, however, is the following. (1) The stimulus used must have a canonical representation. In order to look for object-centered neglect, stimulus must be asymmetric so that a canonical representation that has a ‘‘handedness’’ exists (this is true also for neurologically intact subjects; see Drain and Reuter-Lorenz, 1997). Importantly, this higher level of representation can be both a long time established characteristic of the item, as occurs for words (Caramazza and Hillis, 1990a, 1990b), or a quality of the objects which can be newly acquired in a relatively short time interval as shown by Savazzi et al. (2004) and by the present experiment. (2) The use of a task that cannot be solved by the mental rotation or alignment of the stimulus to an ego-centered reference frame of reference. As pointed out before, if a rotational strategy is engaged, the object-centered nature of neglect with intrinsically (canonically) defined left and right parts is only apparent, instead reflecting just an object-based neglect (Buxbaum et al., 1996; Driver and Halligan, 1991; Maguire et al., 2002). This could occur not only when a stimulus does not have a canonical representation, as in the experiment by Driver and Halligan (1991), but, surprisingly, even with words. This was demonstrated by Savazzi’s (Savazzi, 2003) single case study with a right-handed woman with left neglect dyslexia. In this experiment, the patient MC was asked to read words in different orientations: (1) canonical; (2) 90 clockwise rotation; (3) 180 clockwise rotation, (4) 90 counterclockwise rotation; (5) horizontal mirror-reversal; (6) vertical, with letters in canonical orientation but aligned from top to bottom. MC made ego-centered errors with words rotated through 180 (condition 3), and object-based errors with words horizontally mirror-reversed (condition 5). On the basis of this and other 4 control experiments, the author interpreted the relation between the two types of neglect dyslexia and the two orientations of words
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claiming that the 180 and mirror-reversed conditions implied two different strategies in order to solve the task. Unlike for words rotated 180 , patient MC was unable to read mirror-reversed words without using a mental rotation strategy. So, this pattern of results reflects the involvement of an object-based representation and, thus, in an ego-centered coordinates frame. Rather, in the present experiment and in our previous one (Savazzi et al., 2004), the rotational strategy is weakly relevant to the task: the patient may solve the task regardless of the orientation of the drawing (nonsense objects or the basset hound) used. So, it is unlikely that such a strategy is engaged. In conclusion, the main finding of the present paper is that object-centered neglect can be found for any type of material for which a canonical representation can be built over time, regardless of whether that material is verbal or non-verbal. Future research should take into account that, regardless of the material used, verbal or not, the previously highlighted constraints are required to ascertain that a certain pattern of results is evidence of an object-centered neglect and not just a type of object-based neglect.
Acknowledgements This research was supported by a MIUR grant to SS. We are in debt to Marie T. Banich for her insightful comments on an earlier version of the manuscript.
references
Albert ML. A simple test of visual neglect. Neurology, 23: 658–664, 1973. Behrmann M and Moscovitch M. Object-centered neglect in patients with unilateral neglect: effects of left-right coordinates of objects. Journal of Cognitive Neuroscience, 6: 1–16, 1994. Buxbaum LJ, Coslett HB, Montgomery MW, and Farah MJ. Mental rotation may underlie apparent object-based neglect. Neuropsychologia, 34: 113–126, 1996.
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Caramazza A and Hillis AE. Levels of representation, co-ordinate frames, and unilateral neglect. Cognitive Neuropsychology, 7: 391–445, 1990a. Caramazza A and Hillis AE. Spatial representation of words in the brain implied by studies of a unilateral neglect patient. Nature, 346: 267–269, 1990b. Cubelli R and Speri V. Naming rotated pictures and the riddle of object-centered neglect. Cortex, 37: 159–174, 2001. Diller L and Weinberg J. Heminattention in Rehabilitation. In Weinstein AE and Friedland RP (Eds), Eminattention and Hemisphere Specialization. New York: Raven, 1977. Drain M and Reuter-Lorenz PA. Object-centered neglect for letters: do informational asymmetries play a role? Neuropsychologia, 35: 445–456, 1997. Driver J and Halligan PW. Can visual neglect operate in objectcentered co-ordinates? Cognitive Neuropsychology, 8: 475–496, 1991. Driver J and Pouget A. Object-centered visual neglect, or relative egocentric neglect? Journal of Cognitive Neuroscience, 12: 542– 545, 2000. Gainotti G, Messerli P, and Tissot R. Qualitative analysis of unilateral spatial neglect in relation to laterality of cerebral lesions. Journal of Neurology, Neurosurgery and Psychiatry, 35: 545–550, 1972. Maguire AM, Bates TC, Boycott N, and Corballis MC. Effect of asymmetry on visual attention. Brain and Cognition, 48: 457– 462, 2002. Mozer M. Frames of reference in unilateral neglect and visual perception: a computational perspective. Psychological Review, 109: 156–185, 2002. Neppi-Modona M, Savazzi S, Ricci R, Genero R, Berruti G, and Pepi R. Unilateral neglect and perceptual parsing: a largegroup study. Neuropsychologia, 40: 1918–1929, 2002. Savazzi S. Object-based versus object-centered neglect in reading words. Neurocase, 9: 203–212, 2003. Savazzi S, Neppi-Modona M, Zettin M, Gindri P, and Posteraro L. Object-centered neglect for non-verbal visual stimuli. Cognitive Brain Research, 18: 232–239, 2004. Schenkenberg T, Bradford DC, and Ajax ET. Line bisection and unilateral visual neglect in patients with neurologic impairment. Neurology, 30: 509–517, 1980. Umilta` C. Mechanisms of attention. In Rapp B (Ed), Handbook of Cognitive Neuropsychology. Philadelphia: Psychology Press, 2001. Walker R. Spatial and object-based neglect. Neurocase, 1: 371–383, 1995.
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Research report
Repetita iuvant: Object-centered neglect with non-verbal visual stimuli induced by repetition Silvia Savazzia,*, Francesca Mancinia,b, Gianluigi Veronesib and Lucio Posteraroc a
Department of Neurological and Vision Sciences, University of Verona, and National Institute of Neuroscience, Italy Rehabilitation Unit, Zevio, Verona, Italy c Rehabilitation Unit, Bozzolo, Mantova, Italy b
article info
abstract
Article history:
Neglect can be ego-centered or object-centered depending on the reference frames for
Received 12 May 2008
‘‘left’’ and ‘‘right’’, of either the body or an object. It has been suggested that object-
Reviewed 25 August 2008
centered neglect is not a general phenomenon but is limited to words because only they
Revised 16 September 2008
have a true canonical representation. Here, we examined whether object-centered neglect
Accepted 6 November 2008
could be observed for non-verbal material by creating, after repeated exposure, a canonical
Action editor Giuseppe Vallar
representation of a nonsense figure. Fourteen neglect patients repeatedly bisected a series
Published online 14 November 2009
of asymmetrical nonsense drawings containing two different shapes at their right and left end-points (canonical trials). In the critical trials, which were the last three in the series,
Keywords:
the position of the two shapes was mirror-reversed. Afterwards, neglect patients were
Frames of reference
asked to draw the stimulus, which provided a further measure of whether a canonical
Object-centered neglect
representation of the object has been built by the patients. All the patients made rightward
Object-based neglect
errors with the canonical stimuli. With mirror-reversed stimuli, the bisection errors were reversed to the contralesional side in one patient, returned to zero in one patient and significantly decreased in three patients. In addition, 10 patients reliably drew the canonical stimulus at the end of the series of trials, providing an indication that they built up a canonical representation of the stimulus. The present data provide evidence that object-centered neglect is a phenomenon that is not limited to words. The nature of a stimulus, verbal or non-verbal, is not critical for observing object-centered neglect. What is critical is the way in which material is represented by the patients. ª 2008 Elsevier Srl. All rights reserved.
1.
Introduction
Unilateral neglect is typically defined as a disorder in which patients fail to perceive, orient or respond to stimuli in the contralesional hemispace. Although the spatial nature of neglect is without doubt, the representation of ‘‘left’’ and
‘‘right’’ can relate not only to space, but also to objects. Indeed, it is well known that neglect can be ego-centered (where ‘‘left’’ and ‘‘right’’ are represented with respect to the observer) and allocentric (with respect to an object in space). Beginning with Gainotti and colleagues’ (Gainotti et al., 1972) paper, a growing number of studies have reported
* Corresponding author. Department of Neurological and Vision Sciences, Section of Physiology, University of Verona, Strada le Grazie, 8, 37134 Verona, Italy. E-mail address: [email protected] (S. Savazzi). 0010-9452/$ – see front matter ª 2008 Elsevier Srl. All rights reserved. doi:10.1016/j.cortex.2008.11.006
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examples of allocentric neglect. In contrast to the great amount of evidence in favor of this allocentric neglect, however, ‘‘object-centered neglect’’ remains an ambiguous concept at least for non-verbal stimuli (Mozer, 2002, page 178). This ambiguity is increased by the fact that object-based and object-centered neglect are often used in literature as synonymous even though they reflect the involvement of different frames of reference in defining ‘‘left’’ and ‘‘right’’. According to Walker’s interpretation (Walker, 1995; see also Umilta`, 2001), object-based neglect corresponds to a stimuluscentered neglect derived from an ego-centered coordinate frame. In the clever experiment by Driver and Halligan (1991), for instance, the neglect patient PP was asked to judge if two elongated nonsense shapes were the same or different. In the critical condition the two shapes were both rotated 45 clockwise, so that differences located on the left of the object’s principal axis fell into the right of the patient’s frame of reference. Patient PP missed differences on the left side of the shape’s principal axis even when these differences fell on the right side of egocentric space. These results demonstrate an axis-based neglect of details located to the left side of the shape’s principal axis. Nevertheless, this effect does not imply the presence of an established abstract canonical representation of the shape. The tilted stimuli may be mentally realigned to vertical position so that the neglect is really for leftsided material in viewer-centered coordinates, rather than a seemingly object-centered neglect (Buxbaum et al., 1996). In this case although the patient is still neglecting characteristics of an object, that neglect is based on an egocentric coordinate system not on a coordinate system linked to a canonical representation of the object. Object-centered neglect, on the other hand, indicates an abstract, viewer-independent, representation of the intrinsic ‘‘left’’ and ‘‘right’’ parts of such an object. Thus, to demonstrate object-centered neglect, the object must have a canonical representation that contains a left and right, an attribute that has been considered peculiar to letters and words. A clear and convincing example of an object-centered deficit is the well known case of NG (Caramazza and Hillis, 1990a, 1990b), a left brain-damaged woman with right neglect dyslexia which made neglect errors on the final segments of words, irrespectively of the topographic arrangement of letters (and, thus, viewer-independent). What is required to distinguish object-based and objectcentered neglect is the presence (object-centered) or absence (object-based) of a canonical representation of such an object (where here ‘‘object’’ refers both to words and non-verbal visual stimuli). What remains to be settled instead is which intrinsic properties make a certain type of configuration a ‘‘canonical representation’’. First of all the ‘‘canonical handedness’’ of an object may be a crucial feature in object-centered neglect. Second, the intrinsic asymmetry of such an object is a necessary characteristic for the appearance of this phenomenon (Behrmann and Moscovitch, 1994). In contrast to words, which have an intrinsic handedness, common objects do not have a canonical orientation. Hence for objects, the concepts of ‘‘right’’ and ‘‘left’’ have necessarily to be referred to the viewpoint of the observer. Whereas asymmetric letters (e.g., J/K/R) may not be transformed to their mirror image to the detriment of identity, common objects as well as symmetrical letters (e.g.,
I/W) can have their left and right sides transposed while their identity is still maintained. In such cases, the object’s coordinates are determined solely from the viewer perspective. With regards to this issue, Cubelli and Speri (2001) pointed out that no study with non-verbal material has been able to find evidence of a pure object-centered neglect (see Savazzi et al., 2004 for an exception), but rather have just demonstrated varieties of object-based neglect (or relative egocentric neglect, see Driver and Pouget, 2000). Consequently, it has been suggested (Driver and Pouget, 2000; Mozer, 2002) that object-centered neglect can only be shown with words because they are the only type of visual object that truly has a canonical representation. What seems to be overlooked in this argument, however, is that asymmetrical letters and non-palindrome words have a true canonical representation only because it is derived from the knowledge of a particular written language. In this regard, words do not have a priori distinctive quality that provides for this higher level of representation. Rather, the ‘‘handedness’’ of such items arises from repeated exposure and familiarization of their visual properties (i.e., a particular orientation) that are stable in time. Following this logic, it should be possible to establish a canonical representation after repeated exposure for any kind of material, including non-verbal material, and test whether object-centered neglect can be observed for non-verbal stimuli. As an initial exploration of this idea, Savazzi et al. (2004) asked twenty-four neglect patients to repeatedly bisect a horizontally-aligned 20 cm caricature of a basset hound in a series of 15 trials presented with the head always aligned in a particular position (to the right in a first experiment and to the left in a second experiment). The stimulus was always shown in this particular orientation so as to create a ‘‘canonical’’ representation. At the end of the series of trials patients had to bisect the same, left-right reversed, caricature of the basset hound (i.e., with the head in the opposite position with respect to the stimulus’ vertical axis). With canonical stimuli, neglect patients made errors towards the ipsilesional side (as is typically observed in neglect). When the mirror-reversed version of the basset hound was presented, however, the bisection error reversed from ipsi- to contralesional side in 6 patients and significantly decreased in 4 patients. We interpreted these results as demonstrating object-centered neglect for a newly established canonical representation of a nonverbal object through repeated exposure. However, these results could remain somewhat inconclusive because of a possible alternative interpretation. It is possible that the patient came to expect to see a particular part of the stimulus, which would be that portion of the basset hound that was positioned to the right in the ‘‘canonical’’ stimuli he or she viewed (e.g., the head or the tail depending on the particular condition to which the patient was assigned). If this were the case, the ‘‘novelty’’ of the last, mirror-reversed, trial might induce the patient to search more of visual space for the portion of the basset hound he or she was used to seeing. Since this portion of the basset hound was now located to the left, their search may have drawn their attention leftward reducing the observed neglect. The main goal of the present experiment is to strongly control for this ‘‘novelty effect’’ so that it can be ruled out as
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an explanation for our previous results. To do this, in the present experiment 14 neglect patients underwent a task very similar to the one used in our previous experiment, with two important modifications. Firstly, the stimuli to be repeatedly bisected were asymmetrical nonsense drawings as a whole, that is a line where at the right and left end-points a square and a circle were placed (see Fig. 1). We used a nonsense drawing instead of the basset hound in order to reduce the probability that the rightward stimulus could become more familiar, because nonsense drawings are less salient than the head or the tail of the basset hound. Secondly and more importantly, at the end the series of trials, that is after the first critical (mirror-reversed) stimulus, we added two additional mirror-reversed trials. The decision to add two (and not more or less) mirror-reversed trials was taken in order to use an ‘‘ideal’’ number of trials to both exclude the novelty effect as an explanation and to maintain the newly established canonical representation as stable as possible among sessions. We reasoned that only one trial was not enough to adequately substantiate our prediction (no evidence of the ‘‘novelty effect’’) and that more than two trials could weaken the canonical representation. Thus, a total of three trials seem to be a good balance between to have the minimum number of trials to control for the novelty effect and that of not to induce a reduction of the strength of the canonical representation. If the patient’s response is being driven by the ‘‘novelty effect’’, one would predict that neglect errors would become progressively more rightwards from the first to the third mirror-reversed stimulus. This pattern would be expected because the novelty of such an item in reversed orientation would have dissipated over trials, inducing an attentional reorienting towards the right. On the other hand, if the bisection errors remain stable in the three mirror-reversed trials, we would be able to confirm the existence of a true objectcentered neglect even with non-verbal stimuli. If this prediction will be confirmed, it would mean that words have no peculiar qualities that create a higher level canonical representation. Rather, repeated exposure of a particular orientation of a stimulus can establish a high level, viewerindependent, canonical representation even with non-verbal material.
2.
Experiment
2.1.
Methods
2.1.1.
Subjects
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Data were collected from 14 right brain-damaged patients with contralesional neglect and 5 right brain-damaged patients without neglect, who gave informed consent to participate in the experiment. All of them were right-handed. Patients N 3, Nþ 3, Nþ 8 and Nþ 14 suffered from hemianopia as assessed by means of a kinetic Goldmann perimetry. The experiment was performed according to the Declaration of Helsinki. Contralesional visual neglect was assessed by means of the following tasks: (a) Albert cancellation task. Patients were presented with a modified version (Driver and Halligan, 1991) of Albert’s (Albert, 1973) cancellation task composed of 50 short black segments (2 cm long and .5 mm thick) printed on an A4 sheet of paper placed in front of the subject at reading distance. The segments, distributed in ten columns and five rows, were randomly oriented and grouped by proximity in two sub-arrays, each composed of 25 lines, separated by an empty gap, vertically oriented and 4 cm wide. The patients’ task was to cross out all lines with no limitation of time. The number of uncrossed lines homogeneously distributed in an area confined to the left sub-array or comprising the right sub-array was recorded (see NeppiModona et al., 2002 on page 1922 for details). (b) Letter Hs cancellation task (Diller and Weinberg, 1977). Patients were presented with 6 rows of letters (104 Hs and 208 distracting letters) distributed in 52 columns, printed on an A3 sheet of white paper, and asked to cross out all the Hs. The number of omitted Hs to the left was recorded. (c) Line bisection task (Schenkenberg et al., 1980). Patients were required to bisect a series of five 20 cm long and 2 mm thick black horizontal lines. Errors were measured with approximation to the nearest mm. Positive values indicate a rightward error and negative values a leftward error. The mean bisection error was recorded in each subject. Neglect was defined according to the following criteria: 5 or more omissions in the Albert task and/ or 5 or more omissions to the left in the Diller task and/or
Fig. 1 – Stimuli used in the bisection task. A: canonical stimulus and B: mirror-reversed stimulus for half of the patients. The position of the two shapes at each end-point of the line was counterbalanced among patients.
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a mean rightward bisection error equal to or exceeding 10 mm. Demographic and clinical data are reported in Table 1.
2.1.2.
Stimuli and procedure
Patients had to bisect 20 cm long lines printed in black and centered, both horizontally and vertically, on a sheet of A4 white paper. At the end-points of the line a square and a circle were positioned. In 18 trials, the stimulus was horizontally oriented with one shape (e.g., the square) on the right side and a different shape (e.g., the circle) on the left side (‘‘canonical’’ stimulus). The last 3 of these trials were critical for testing our hypotheses. On these trials the two shapes were placed at the opposite end-point from their original position (‘‘mirrorreversed’’ stimulus). In two trials (6th, 12th) the stimulus was vertically oriented. Vertical stimuli were given in order to have an additional means to prevent mere surprise or novelty on the presentation of the horizontal mirror-reversed trials, and were not considered in the analysis of the results (see Savazzi et al., 2004 for a similar approach). The position of the two shapes was counterbalanced among patients so that what was the ‘‘canonical’’ stimulus for half of the patients was the ‘‘mirror-reversed’’ stimuli for the other half (Fig. 1). Each series of trials was repeated 5 times, each time on different days, for a total of 100 stimuli to bisect (90 horizontally oriented – 75 canonical and 15 mirrorreversed and 10 vertically oriented). In addition, after each series of 20 trials, patients were requested to draw the stimulus previously bisected without any instruction on the orientation in which it should be drawn (i.e., canonical or mirror-reversed). Neglect patients typically started drawing the right half of the figure and, occasionally, did not complete the left part. In order to obtain a reliable measure, neglect patients were requested to draw the entire figure, if not spontaneously done. This task provided us with a way to measure whether the individual had indeed created
a ‘‘canonical’’ representation of the object. If the patient drew the stimulus in its canonical orientation, despite from the fact that the last three times it was viewed in a mirror-oriented position, we can infer that indeed he or she created a canonical representation of the stimulus, which is a prerequisite to demonstrate object-centered neglect.
2.2.
Results
Table 2 shows mean bisection errors (mm) made by individual patients on horizontal ‘‘canonical’’ and critical (mirrorreversed) trials, averaged across the 5 repetitions of the series of 20 trials (15 in the ‘‘canonical’’ and 3 in the mirror-reversed with the 2 vertical presentations not analyzed). Positive and negative values refer to rightward and leftward errors, respectively.
2.2.1.
Bisection error
N patients showed a comparable [T(4) ¼ .426, p ¼ .692] mean bisection error of .28 mm with canonical stimuli and of .38 mm with mirror-reversed stimuli, indicating no difference between the two stimulus configurations, as expected. This result indicates that an effect with neglect patients cannot be due to an unspecific difference between the two configurations. Nþ patients made a mean bisection error of .75 mm upwards with vertical stimuli, not significantly different from zero on a one sample t-test [T(27) ¼ .353, p ¼ .727]. A separate analysis on bisection errors with respect to the two configurations (canonical vs mirror-reversed) showed no reliable difference on deviation of the bisection error. This null effect could be due to the fact that the vertical stimuli were intermingled among horizontal stimuli and that the canonical representation may not be strong enough to produce an effect on vertical trials. A group analysis on the bisection errors with the canonical and the critical conditions showed that in Nþ patients the mean rightward bisection error with the critical stimuli
Table 1 – Demographic and clinical data Patient Nþ 1 Nþ 2 Nþ 3 Nþ 4 Nþ 5 Nþ 6 Nþ 7 Nþ 8 Nþ 9 Nþ 10 Nþ 11 Nþ 12 Nþ 13 Nþ 14 N 1 N 2 N 3 N 4 N 5
Sex
Age
Education
Lesion site (CT)
Length of illness (months)
MMSE
Albert
Diller
Line Bisection (mm)
F M M M M F M M F M F F M F M F F M M
74 74 74 59 61 62 70 72 75 76 73 75 63 85 70 66 71 64 67
3 11 5 11 8 5 8 9 5 5 5 3 9 2 3 5 3 9 5
P TP TO T FTP T FTP TPO FTP bg P TP FP ci-O ci-TP P TO T TP
2 2 1 11 2 5 2 3 4 6 1 2 3 1 2 3 5 2 1
24 27 30 29 27 28 25 24 24 27 24 27 26 29 28 27 29 30 29
28 0 27 11 1 0 41 39 25 15 39 25 5 29 0 0 0 0 0
85 67 29 51 45 59 97 / 83 90 85 72 85 / 0 0 1 0 2
29.4 13 60.8 36.8 12.6 16.6 40.4 68 6.8 25.4 25.8 25.6 20.2 45 1.7 .8 1.1 1.3 .8
F ¼ frontal; T ¼ temporal; P ¼ parietal; O ¼ occipital; bg ¼ basal ganglia; ci ¼ capsula interna.
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Table 2 – Mean bisection errors in mm (SD) for canonical and critical stimuli as a function of individual patients Patient
Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ Nþ N N N N N
1 2 3 4 5 6 7 8 9 10 11 12 13 14 1 2 3 4 5
Canonical Stimuli (N ¼ 75)
Critical stimuli (N ¼ 15)
Number of canonical stimuli (N ¼ 5) drawn
31 (11.48) 18.23 (7.08) 25.23 (8.54) 32.57 (9.23) 10.74 (4.53) 15.16 (4.56) 34.43 (14.93) 26.69 (15.35) 7.56 (6.41) 20.29 (6.11) 45.88 (15.45) 22.56 (13.24) 85.69 (3.05) 35.04 (12.33) 2.2 (3.45) 1.2 (2.7) -1 (1.1) -2.6 (3.4) 1.6 (2.5)
32.27 (8.38) 17.4 (10.03) 24.47 (7.76) 30.94 (8.20) .27 (3.73) 17.4 (5.90) 15.27 (13.66) 13.54 (24.41) -4.8 (7.55) 20.94 (11.34) 42.27 (13.04) 19.27 (20.36) 83.14 (12.74) 25.47 (9.34) 1.9 (2.16) 1.7 (2.9) -.7 (1.8) -3.2 (3.8) 2.2 (2.8)
2 5 2 1 4 4 5 4 5 4 5 5 1 4 2 3 4 5 4
Bold indicates patients with a significant decrement or reversal of the bisection error on the critical trials. Bold italics indicate a significant number of times the patient drew the canonical stimulus at the end of the series of trials.
(24.12 mm) was smaller [T(13) ¼ 3.002, p < .05] than that with the canonical stimuli (29.36 mm). To further substantiate the source of this difference, that is to find which patients showed an object-centered neglect, we performed single subject analyses. For each Nþ patient, the difference between errors with canonical and reversed stimuli was tested by means of a mixed ANOVA (using a Type II Sum of Squares method for the computation of within subjects variability to take into account the different numerosity of canonical and reversed stimuli they had to bisect) with Condition (canonical vs mirrorreversed stimuli) as a between-subject factor and Session (1 to 5) as a within-subject factor. Significant results were found in five neglect patients: Nþ 5, Nþ 7, Nþ 8, Nþ 9 and Nþ 14. In patient Nþ 5 the bisection error markedly reduced in the critical trial [F(1,16) ¼ 121.454; p < .001], showing no rightward (.27 mm) error. Patient Nþ 9 showed a significant reversal in the direction of the bisection error [F(1,16) ¼ 51.92; p < .001]. In the remaining three patients the rightward bisection error was markedly reduced with the mirror-reversed stimulus: slight for patient Nþ 14 [F(1,16) ¼ 14.067; p < .005] but very strong for patient Nþ 7 [F(1,16) ¼ 27.032; p < .001] and patient Nþ 8 [F(1,16) ¼ 7.869; p < .05]. These results indicate that words are not the only material for which object-centered neglect can be demonstrated; even nonsense objects can produce a higherorder, viewer-independent, canonical representation after repeated exposure of the same orientation of such an object, and neglect of the left-side of such canonical representations can occur.
2.2.2.
Novelty effect
To examine the possibility that our results with neglect patients were driven by a ‘‘novelty effect’’, the bisection errors
with the three mirror-reversed stimuli (Table 3) were entered in a one-way between-subject ANOVA for each Nþ patient. The prediction if a ‘‘novelty effect’’ is occurring would be to find a progressive worsening of the rightward bisection error from the first to the third mirror-reversed stimulus. Contrary to this prediction in none of the Nþ patients were the bisection errors reliably different (all Fs < 1) among the three mirror-reversed stimuli, ruling out the ‘‘novelty effect’’ hypothesis as an explanation for the observed pattern of results. A possible cause for this negative effect could be the low statistical power of the analyses since there were only 5 cases per cell. To control for this possibility, we performed a group analysis on the bisection errors with the three mirrorreversed trials which allow us to increase the statistical power due to a bigger numerosity of the sample. This new analysis showed the same result as the single subjects analyses, that is no difference in the line bisection error among the three critical trials [F(2,39) ¼ .006, p ¼ .994].
2.2.3.
Drawing task
As a test to ensure that indeed a canonical representation had been created, the proportion of canonical stimuli drawn at the end of the series of trials (Table 2, rightmost column) were entered in a 1-tailed binomial analysis. Three of the five N patients revealed a reliable effect of drawing the stimuli in the canonical orientations: Patients N 3 and N 5 drew 4 canonical stimuli, p < .01; whereas patients N 4 drew 5 canonical stimuli, p < .001. More importantly, all the Nþ patients showing objectcentered effects in the bisection task also showed the same effect in the drawing task: that is, they consistently drew the canonical version of the stimulus (patients Nþ 5, Nþ 8 and Nþ 14 drew 4 canonical stimuli, p < .01; whereas patients Nþ7 and Nþ 9 drew 5 canonical stimuli, p < .001). Moreover, five of the remaining 9 Nþ patients with no object-centered effects in the bisection task, revealed a reliable effect of drawing the stimuli in the canonical orientations. Patients Nþ 6 and Nþ 10 drew 4 canonical stimuli ( p < .01), whereas patients Nþ 2, Nþ 11 and Nþ 12 drew 5 canonical stimuli ( p < .001). These results indicate that, independently from the fact that the last three
Table 3 – Mean bisection errors in mm (SD) the three critical stimuli as a function of individual patients Patient
Critical Stimuli
Nþ 1 Nþ 2 Nþ 3 Nþ 4 Nþ 5 Nþ 6 Nþ 7 Nþ 8 Nþ 9 Nþ 10 Nþ 11 Nþ 12 Nþ 13 Nþ 14
1
2
3
31.4 (8.91) 15.8 (7.05) 23.8 (8.23) 33 (9) .6 (5.13) 18.4 (6.80) 21 (11.11) 12.4 (23.94) -5 (7.91) 20.4 (10.06) 45.6 (14.93) 12.4 (33.40) 84 (7.65) 26.4 (7.89)
30.2 (6.65) 17 (14.92) 25.6 (7.54) 28.6 (9.29) 0 (4.30) 14.8 (7.43) 14.6 (9.53) 16.8 (13.55) -4.8 (6.69) 24 (14.71) 42.2 (10.94) 18.2 (8.81) 79.4 (21.72) 24.4 (10.64)
35.2 (10.26) 19.4 (8.47) 24 (9.17) 31.2 (7.46) .2 (1.92) 19 (2.74) 10.2 (19.11) 11.4 (36.15) -4.6 (9.61) 18.4 (10.60) 39 (15) 27.2 (10.89) 86 (3.08) 25.6 (11.28)
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stimuli bisected were mirror-reversed, when asked to draw a stimulus, the strongest and more accessible configuration is the canonical representation, strongly indicating that a nonsense object can have access to such a high-level representation.
3.
Discussion
The present study confirms and adds further evidence to previous data by Savazzi et al. (2004) showing that objectcentered neglect is not limited to words. In the present experiment 14 neglect patients and 5 brain-damaged patients without neglect repeatedly bisected a nonsense drawing with two different shapes placed at the right and left end-points, making an error towards the ipsilesional side. When presented with a mirror-reversed version of the stimulus, a subset of neglect patients showed either a reduction or reversal of the bisection error. In addition, the majority of patients with and without neglect in the study, when requested to drew the stimulus, reliably draw the canonical stimulus in the series indicating that this stimulus was represented in a high-level canonical form. Importantly, our result also rules out an alternative explanation for the demonstration of object-centered neglect, namely that the reversal was induced by a ‘‘novelty effect’’. Such an explanation would have predicted a progressive worsening of the bisection errors from the first to the third mirror-reversed stimulus. Such a change would occur because the novelty of the item in reversed orientation would have dissipated over trials. In contrast to such a prediction, no difference in bisection was found across these three trials. The variability in the pattern of response across patients deserves some consideration. Five out of 14 (35.7%) neglect patients of our sample showed a reversal or a reduction of the bisection error from ipsi- to contralesional space in the critical stimulus presentation condition (all of them also showing a significant effect in the drawing task, indicating that they had created a canonical representation of the item). Five other neglect patients (35.7%) showed evidence of having created a canonical representation of the object in the drawing task and the remaining 4 (28.6%) did not. What can account for these differences? Since 4 neglect patients did not show evidence of creating a canonical representation of the object, it would obviously be impossible to demonstrate objectcentered neglect in these individuals. This could be due to the fact that for such neglect patients, the number of repetitions of the canonical stimulus was not enough to create a stable canonical representation. Another explanation could be that these patients might have a strong egocentric neglect preventing them to access an object-centered representational level. To disentangle these two possibilities, further studies could try and find whether by adding more presentations of the canonical stimulus (thus increasing the strength of the canonical representation), the percentage of patients showing object-centered neglect would increase or not. Of the remaining neglect patients who did show evidence of creating an object-centered representation, only half showed evidence of object-centered neglect in bisecting the drawings. We can speculate that for those patients who did
not show evidence of object-centered neglect, the canonical representation of the object was less strong than for those neglect patients who did show object-centered neglect. Unlike words, which patients have been familiarized with over a long period of time, the short familiarization time used in the present study did not allow for the creation of as strong a canonical representation. Another possibility could be that the drawing task and the bisection task have a different sensitivity to detect object-centered neglect. Indeed, it is well known that neglect can dissociate among tests. As an example, in the present paper patients Nþ 2, Nþ 5 and Nþ 6 are below the selection criteria with respect to the Albert task but very above the selection criteria with respect to the Diller and the bisection tasks. Thus, it could be possible that the bisection task have a lower sensitivity than the drawing task to reveal a high level, object-centered, representation of the material proposed. Further investigation will be needed to explore these possibilities. The results of the present experiment, in addition, aid in considering what the requisite conditions are for demonstrating object-centered neglect. We have ascertained that the nature of the material, verbal or non-verbal, is irrelevant as we have observed object-centered neglect with nonsense visual stimuli. What seems to be critical, however, is the following. (1) The stimulus used must have a canonical representation. In order to look for object-centered neglect, stimulus must be asymmetric so that a canonical representation that has a ‘‘handedness’’ exists (this is true also for neurologically intact subjects; see Drain and Reuter-Lorenz, 1997). Importantly, this higher level of representation can be both a long time established characteristic of the item, as occurs for words (Caramazza and Hillis, 1990a, 1990b), or a quality of the objects which can be newly acquired in a relatively short time interval as shown by Savazzi et al. (2004) and by the present experiment. (2) The use of a task that cannot be solved by the mental rotation or alignment of the stimulus to an ego-centered reference frame of reference. As pointed out before, if a rotational strategy is engaged, the object-centered nature of neglect with intrinsically (canonically) defined left and right parts is only apparent, instead reflecting just an object-based neglect (Buxbaum et al., 1996; Driver and Halligan, 1991; Maguire et al., 2002). This could occur not only when a stimulus does not have a canonical representation, as in the experiment by Driver and Halligan (1991), but, surprisingly, even with words. This was demonstrated by Savazzi’s (Savazzi, 2003) single case study with a right-handed woman with left neglect dyslexia. In this experiment, the patient MC was asked to read words in different orientations: (1) canonical; (2) 90 clockwise rotation; (3) 180 clockwise rotation, (4) 90 counterclockwise rotation; (5) horizontal mirror-reversal; (6) vertical, with letters in canonical orientation but aligned from top to bottom. MC made ego-centered errors with words rotated through 180 (condition 3), and object-based errors with words horizontally mirror-reversed (condition 5). On the basis of this and other 4 control experiments, the author interpreted the relation between the two types of neglect dyslexia and the two orientations of words
cortex 45 (2009) 863–869
claiming that the 180 and mirror-reversed conditions implied two different strategies in order to solve the task. Unlike for words rotated 180 , patient MC was unable to read mirror-reversed words without using a mental rotation strategy. So, this pattern of results reflects the involvement of an object-based representation and, thus, in an ego-centered coordinates frame. Rather, in the present experiment and in our previous one (Savazzi et al., 2004), the rotational strategy is weakly relevant to the task: the patient may solve the task regardless of the orientation of the drawing (nonsense objects or the basset hound) used. So, it is unlikely that such a strategy is engaged. In conclusion, the main finding of the present paper is that object-centered neglect can be found for any type of material for which a canonical representation can be built over time, regardless of whether that material is verbal or non-verbal. Future research should take into account that, regardless of the material used, verbal or not, the previously highlighted constraints are required to ascertain that a certain pattern of results is evidence of an object-centered neglect and not just a type of object-based neglect.
Acknowledgements This research was supported by a MIUR grant to SS. We are in debt to Marie T. Banich for her insightful comments on an earlier version of the manuscript.
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