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Vertical bias in neglect: A question of time?
Neuropsychologia 49 (2011) 2369–2374
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Vertical bias in neglect: A question of time? Dario Cazzoli, Thomas Nyffeler, Christian W. Hess, René M. Müri ∗ Perception and Eye Movement Laboratory, Department of Neurology, Department of Clinical Research, Bern University Hospital Inselspital, and University of Bern, Freiburgstrasse 10, 3010 Bern, Switzerland
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Article history: Received 14 December 2010 Received in revised form 7 April 2011 Accepted 11 April 2011 Available online 16 April 2011 Keywords: Human Hemispatial neglect Altitudinal neglect Visual attention Visual search Eye movements
a b s t r a c t Neglect is defined as the failure to attend and to orient to the contralesional side of space. A horizontal bias towards the right visual field is a classical finding in patients who suffered from a right-hemispheric stroke. The vertical dimension of spatial attention orienting has only sparsely been investigated so far. The aim of this study was to investigate the specificity of this vertical bias by means of a search task, which taps a more pronounced top-down attentional component. Eye movements and behavioural search performance were measured in thirteen patients with left-sided neglect after right hemispheric stroke and in thirteen age-matched controls. Concerning behavioural performance, patients found significantly less targets than healthy controls in both the upper and lower left quadrant. However, when targets were located in the lower left quadrant, patients needed more visual fixations (and therefore longer search time) to find them, suggesting a time-dependent vertical bias. © 2011 Elsevier Ltd. All rights reserved.
1. Introduction Neglect is a common and disabling neurological syndrome, generally associated with right hemispheric strokes in the territory of the middle cerebral artery (e.g., Parton, Malhotra, & Husain, 2004). Patients suffering from neglect fail to orient, react, and act upon the contralesional side of space. In the acute phase, neglect patients may behave as if the contralesional side of the world would not exist anymore. Besides the typical horizontal bias in favour of the ipsilesional side of space, a vertical bias has also been described in neglect patients. A vertical neglect component was described after bilateral cortical lesions (Adair, Williamson, Jacobs, & Heilman, 1995; Mennemeier, Wertman, & Heilman, 1992; Rapcsak, Cimino, & Heilman, 1988; Shelton, Bowers, & Heilman, 1990). Vertical neglect was also occasionally described after unilateral cortical lesions. For instance, when asked to cancel lines in the Albert’s Barrage test, neglect patients often omitted more targets in the left, lower quadrant (Halligan & Marshall, 1989; Pitzalis, Spinelli, & Zoccolotti, 1997). A vertical neglect component was also found for the imagined space in a mental number line bisection task. When asked to bisect vertically oriented mental number lines (i.e., the floor numbers in a building), neglect patients showed a shift towards the superior part of the lines (Cappelletti, Freeman, & Cipolotti, 2007). Finally, a more pronounced impairment in the automatic, covert
∗ Corresponding author. Tel.: +41 0 31 632 30 83; fax: +41 0 31 632 97 70. E-mail address: [email protected] (R. M. Müri). 0028-3932/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2011.04.010
attentional orienting in the left, lower quadrant was found when neglect patients were asked to respond to briefly flashed visual stimuli (Làdavas, Carletti, & Gori, 1994). Eye movement recordings have been shown to provide reliable information on the allocation of visual attention in space. At least in situations where the eyes are free to move (often referred to as overt attentional orienting), eye movements and visual attention seem to move together across the visual space. For instance, subjects cannot produce eye movements towards a spatial location and attend to another one at the same time (Hoffman & Subramaniam, 1995). Moreover, neural networks controlling visual attention and eye movements have been consistently shown to be overlapping (e.g., Corbetta et al., 1998; Haan, Morgan, & Rorden, 2008; Ignashchenkova, Dicke, Haarmeier, & Thier, 2004; Nobre, Gitelman, Dias, & Mesulam, 2000). Indeed, eye movements during visual exploration show typical patterns in neglect patients, reflecting their impairment to direct attention towards the contralesional space. This includes an ipsilesional bias of early attentional orienting, a lack of exploratory eye movements towards the contralesional space, a shift of the visual fixation distribution towards the ipsilesional space, recursive refixations (i.e., repeated fixations to the same regions), and an impairment of saccadic metrics (e.g., Malhotra, Coulthard, & Husain, 2006; Mort & Kennard, 2003; Niemeier & Karnath, 2000; Pflugshaupt et al., 2004; Sprenger, Kömpf, & Heide, 2002). Furthermore, the abovementioned attentional bias along the vertical spatial dimension was also detectable by means of eye movement recordings. In a recent study, a more pronounced reduction of visual fixations was found in the lower part of the left screen half during free
0 0 2
1.5 1.07 1.92 n/a 1.6 1.22 1.80* 0.89 .97 1.90* 0 1 0 n/a 0 0 0 0 0 0 4.9** 4.08** 4.01** n/a 5.26** 4.49** 4.79** 3.04** 4.59** 3.86**
Mean RT left [s]d
Omitted targets right
Mean RT right [s]d
visual exploration of naturalistic pictures (Müri, Cazzoli, Nyffeler, & Pflugshaupt, 2009). Hence, during free visual exploration – without specific instructions and with a marked bottom-up (or stimulusdriven) component – neglect patients showed both a horizontal and a vertical bias in their visual exploration. Up to now, it is not clear whether a vertical bias is also present in tasks with a more pronounced top-down (or concept-driven) component, such as in a search task. Thus, the present study aimed to assess behavioural performance and eye movement patterns in neglect patients on both vertical and horizontal spatial planes during a visual search task with naturalistic scenes.
1.18 1.14 3.68**
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2.66* 2.7* 7.8**
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0.9 1 1 3.4 1.8 2.1 2.4 1.6 3.9 1.9 Ischemia Ischemia Ischemia Haemorrhage Ischemia Ischemia Ischemia Ischemia Haemorrhage Ischemia 48 61 59 56 57 58 48 45 63 43 m w w m w m w m m m
n/a = not available. a Lesion location (areas involved): BG = basal ganglia; front = frontal cortex; ins = insula; op = operculum; par = parietal cortex; temp = temporal cortex; th = thalamus. b Time between the insult and the experiment, in months. c Drawing performance was scored as: 0 = intact; 1 = distorted left side; 2 = flagrant omissions on the left side. d PVT, mean reaction time: *borderline performance; **impaired performance (based on percent ranges, cut-off value of 15, according to Heaton, Miller, Taylor, & Grant, 2004).
1 1 0 n/a 7 5 3 0 12 2 No Yes Yes Yes No Yes Yes Yes Yes Yes 0 1 1 2 2 0 1 1 2 2 7.44 9.98 5.12 16.38 18.04 3.46 22.55 n/a n/a 20.1 3 5 3 5 4 1 8 2 10 n/a Paresis Plegia Paresis Paresis Paresis Paresis Paresis Plegia Paresis Plegia
2 0 9 n/a n/a No 2 0 2 4 5 8 Paresis Paresis Paresis 0.7 1.3 2.1 Ischemia Ischemia Ischemia
BG; ins BG; par; front BG; ins; op; temp; th; par op; ins; par; BG ins; par; temp; op front; ins temp; par temp; op; par ins; op; temp; BG BG; temp; par BG; ins; op; front par; temp ins; op; front; temp
Left omissions Bells Test Time postb Lesiona
54 74 47
The 32 stimuli were pseudo-randomly assigned to four blocks of eight images each. Each block started with an explanatory display in which the four target objects were centrally presented on an exemplary background photograph (not used elsewhere in the experiment). Subjects were instructed to search for one of the four possible targets and, once found, to click on it with the mouse cursor. Stimuli were presented until mouse click or until the subjects declared that they could not find the target. In the latter case, the experimenter tagged the trial as failed and manually started the next one. Prior to each stimulus, a central fixation point was presented during 1 s, ensuring a common starting point for all subjects. The compliance to this
m m m
2.4. Procedure
Aetiology
Stimuli were displayed in a dimly lit room on a cathode ray tube computer display (Samsung SyncMaster 959NF) with an active size of 36 × 27 cm, a resolution of 800 × 600 pixels, 24 bit colour depth, and a refresh rate of 85 Hz. Eye position was recorded with an infrared video-based eye-tracking system (EyeLinkTM , Sensomotoric Instruments GmbH, Teltow, Germany). The system is equipped with a camera recording screen position to compensate for head movements. For this reason, only a chin rest was used to secure a constant viewing distance of 70 cm. The eye-tracking system is characterised by a temporal resolution of 250 Hz, a spatial resolution of .01◦ according to the manufacturer, and a typical gaze position accuracy of .5–1◦ , depending on calibration precision. The system was periodically calibrated by means of a 3 × 3 grid calibration sequence. Eye movements were recorded and parsed into fixations and saccades online, and then transferred to an external computer for offline evaluation.
Table 1 Demographic and clinical data of the patients.
2.3. Apparatus
Age
Stimuli consisted of 32 full colour photographs of everyday scenes as background in which common, small search target objects were embedded. Each background photograph contained only one embedded target object. Eight categories of background photographs were presented (four pictures per category): fruits, edibles, naturalistic scenes, everyday objects, interior scenes, transportation means, transportation routes, and buildings. Four search target objects were used: a clock, a leaf, a pear, and a screw. In each visual field quadrant, four positions were defined for the presentation of the target object. Each position was tested by two objects, resulting in eight targets presented in each quadrant overall. Background photographs were presented in full screen size, with two small black bars on the upper and lower borders (1.5 cm in height, full screen in width), which allowed to avoid deformation of the original motifs. Background photographs subtended a viewing angle of about 29 × 19.5◦ . Embedded target objects were presented with a viewing angle of about 1.6 × 1.6◦ . Fig. 1 depicts an example of a stimulus.
Sex
2.2. Stimuli
Motor deficit
Relative bisection bias [%]
Drawing scorec
Left reading omissions
Thirteen patients with left-sided neglect after right hemispheric damage (aged between 43 and 74 years, mean = 54.85, SD = 8.65, all right-handed, 4 women) and thirteen healthy subjects (aged between 40 and 63 years, mean = 52.38, SD = 7.03, all right-handed, 5 women) participated in the study. There was no statistically significant difference in age between the two groups (Mann–Whitney U = 74.5, p = 0.622, exact sig., 2-tailed). All subjects were naïve with respect to the experimental hypotheses. Neglect diagnosis was based on clinical examination and neuropsychological tests, such as Bells Test (Gauthier, Dehaut, & Joanette, 1989), line bisection (Schenkenberg, Bradford, & Ajax, 1980), drawing and reading performance, and a subtask of the Vienna Test System (PVT, Dr G. Schuhfried GmbH, Mödling, Austria). All subjects had normal or corrected-to-normal visual acuity, no signs of strabismus, and normal colour vision as assessed by Ishihara’s test (Ishihara, 1999). In all patients, the central 30◦ of the visual field were intact as assessed by perimetry. Demographic and clinical data of the patients are shown in Table 1. All subjects gave written informed consent prior to the experiment. The study was conducted in compliance with the latest version of the Declaration of Helsinki and was approved by the ethical committee of the State of Bern.
n/a n/a 6.65
PVT
2.1. Subjects
Omitted targets left
2. Materials and methods
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Fig. 1. Example of a stimulus. The target object (a screw, marked by a white arrow) is embedded in the left, upper quadrant of the background photograph (category: transportation means). In the experiment, all stimuli were presented in full colour.
request was monitored online by the experimenter. The four blocks were separated by a short break of about 2 min, which also permitted the periodical recalibration of the eye-tracking system. Before the beginning of the experiment, subjects were given eight practice trials. The background pictures in the practice trials were not used elsewhere in the experiment. 2.5. Data analysis Performance in the search task was computed as the percentage of targets found during the experiment for each subject in the whole visual field and in the four visual field quadrants. Results of patients and healthy controls were compared by means of Mann–Whitney U tests (exact significance, 2-tailed). For the analysis over visual field quadrants, the ˛ error rate was corrected for multiple comparisons by means of the Bonferroni-procedure (˛/n, where n represents the number of comparisons). To evaluate search performance on the vertical dimension, a Laterality Index (LI) was computed for the upper and lower visual field quadrants. The LI was calculated according to the formula: percentage of targets found in the left quadrant/percentage of targets found in the right quadrant. Values greater than 1 indicate a better search performance in the left quadrant, whereas values lower than 1 indicate better search performance in the right quadrant. The LI was calculated for the time until response (no time limit). Moreover, in order to evaluate the temporal evolution during performance, the LI was computed for different time limits (6, 8, 10, 12, 14, 16, 18, and 20 s). The results of the LI underwent a repeated-measures analysis of variance (ANOVA) with within factors ‘search time limit’ (levels: 6, 8, 10, 12, 14, 16, 18, 20 s, and no limit) and ‘quadrants’ (levels: upper quadrants, lower quadrants). Fixations outside the photographs and saccades starting or ending outside the photographs were filtered out. Moreover, fixations shorter than 100 ms were excluded (Carpenter, 1988). The percentage of cumulative fixation duration over the four quadrants was computed for each trial and then averaged over all trials for each subject. The results of the parameter ‘percentage of cumulative fixation duration’ underwent a repeated-measures ANOVA with within factor ‘quadrant’ (levels: left upper, right upper, left lower, right lower) and between factor ‘group’ (levels: healthy controls, patients). The direction of the first saccade (towards the quadrants) was determined for each trial and then computed as percentage of the trials for each direction in each subject. The results of the parameter ‘first saccade direction’ underwent a repeatedmeasures ANOVA with within factor ‘direction’ (levels: left upper, right upper, left lower, right lower) and between factor ‘group’ (levels: healthy controls, patients). The number of fixations until target object detection was computed for each trial and then averaged over all trials for each subject. Only trials in which the target object was found were included in this analysis. The results of the parameter ‘number of fixations until target detection’ underwent a repeated-measures ANOVA with within factor ‘quadrant’ (levels: left upper, right upper, left lower, right lower), indicating in which quadrant the target was presented, and between factor ‘group’ (levels: healthy controls, patients). All subsequent post hoc analyses were assessed by Fisher’s least significant difference (LSD) tests.
3. Results 3.1. Performance in the search task Patients with neglect found significantly less objects (median = 91%, range = 72–100%) compared to healthy controls (median = 100%, range = 94–100%) (U = 31.0; p = 0.005). Analysis of the number of hits per quadrant revealed that patients found significantly less targets than healthy controls in both the upper left (patients: median = 88%, interquartile range [IQR] = 18.75%; controls: median = 100%, IQR = 0%) (U = 31.0; p = 0.003) and the lower left (patients: median = 88%, IQR = 12.5%; controls: median = 100%, IQR = 0%) (U = 39.0; p = 0.005) quadrant. However, there were no significant differences between healthy controls and patients in the number of hits in the upper right (patients: median = 88%, IQR = 18.75%; controls: median = 100%, IQR = 12.5%) (U = 57.5; n.s.) or in the lower right (patients: median = 100%, IQR = 12.5%; controls: median = 100%, IQR = 0%) (U = 45.5; n.s.) quadrant. The results of the LI in neglect patients for the upper and lower quadrants showed no significant effects of the factor “search time limit” (F(8,96) = 1.439; n.s.) or of the factor “quadrants” (F(1,12) = 3.217; n.s.). However, the interaction “search time limit × quadrants” was highly significant (F(8,96) = 3.921; p < 0.001). Subsequent post hoc tests revealed a significant reduction of search performance in the left inferior quadrant if the search time was limited to 6, 8, or 10 s. For times over 10 s, the LI of the lower and upper quadrants was not significantly different. The results are depicted in Fig. 2.
3.2. Percentage of cumulative fixation duration The repeated-measures ANOVA showed significant differences for the factor “quadrant” (F(3,72) = 13.002; p < 0.001) and for the interaction “quadrant × group” (F(3,72) = 24.902; p < 0.001). As assessed by subsequent post hoc tests, patients showed a significant reduction of the percentage of cumulative fixation duration in both the left upper and the left lower quadrant. The results are shown in Fig. 3.
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Fig. 2. Evolution over time of the Laterality Index (LI) for target hits in the upper and lower quadrants in neglect patients (left panel), asterisks represent significant post hoc tests (**p < 0.001; *p < 0.01). For comparison, the right panel depicts the evolution over time of the LI in healthy controls. Error bars indicate standard error of the mean (SEM).
Fig. 3. Mean percentage of cumulative fixation duration over the four quadrants in patients and controls. Controls show a symmetrical distribution of the percentage of cumulative fixation duration. Patients show a significant reduction of the percentage of the cumulative fixation duration in the left screen part for both the upper and lower quadrant (**p < 0.001). Error bars indicate standard error of the mean (SEM).
3.3. First saccade direction As revealed by the repeated-measures ANOVA, there were significant differences for the factor “direction” (F(3,72) = 12.395; p < 0.001) and for the interaction “direction × group” (F(3,72) = 33.419; p < 0.001). As assessed by subsequent post hoc tests, patients produced significantly more first saccades towards the right upper and the right lower quadrant than towards the left upper and the left lower quadrant. Controls showed the reverse pattern (Fig. 4). 3.4. Number of fixations until target detection Finally, the repeated-measures ANOVA on the number of fixations showed that patients needed more fixations than controls to find the target (F(1,24) = 6.684; p = 0.02; mean number of fixations until target detection ± SEM: Patients 15.9 ± 2.17; Controls: 8 ± 2.17). The factor “quadrant” was not significant (F(3,72) = 1.446; n.s.). However, the interaction “quadrant × group” was significant (F(3,72) = 6.149; p < 0.001). Post hoc testing revealed that patients needed significantly more fixations to find the target when it was
Fig. 4. Direction of the first saccade. The percentages of first saccades towards the right upper and lower quadrants were significantly increased in neglect patients. Controls showed the reversed pattern (**p < 0.001). Error bars indicate standard error of the mean (SEM).
located in the lower left quadrant. Furthermore, a significant difference between patients and controls was found for the left lower quadrant (see Fig. 5). 4. Discussion The aim of the present study was to investigate performance and oculomotor behaviour of neglect patients during a naturalistic search task. We were particularly interested in assessing the influence of the horizontal as well as of the vertical target localisation. In general, we found that neglect patients (1) displayed longer exploration times to find targets, and (2) found significantly less targets, especially when these were located in the left screen half, irrespective of their vertical localisation (upper or lower left visual quadrant). However, if the target was located in the left lower visual quadrant, patients needed more fixations (and therefore more time) to detect it, suggesting a time-dependent vertical bias. Concerning oculomotor parameters, patients showed typical findings described in the literature, such as an ipsilesional bias in the distribution of cumulative fixation duration during visual
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Fig. 5. Mean number of fixations until target detection depending on the quadrant in which the target was located. In patients, the number of fixations was significantly higher for targets in the left lower quadrant compared to the other quadrants (*p < 0.05; **p < 0.001). Error bars indicate standard error of the mean (SEM).
search (e.g., Behrmann, Watt, Black, & Barton, 1997; Heide & Kömpf, 1998) and in the early attentional orientation (Azouvi et al., 2002; Gainotti, D’Erme, & Bartolomeo, 1991; Mattingley, Bradshaw, Bradshaw, & Nettleton, 1994; Olk, Harvey, & Gilchrist, 2002; Pflugshaupt et al., 2004). These effects were observed for both the upper and lower left quadrants. With respect to the search performance in patients, the number of hits was not significantly different for targets located in the left upper or lower quadrant. However, to achieve the same search efficiency, patients had to produce significantly more fixations in the left lower quadrant. A vertical component of neglect has sparsely been described in the literature. In some patients, a vertical bias was found in classical paper–pencil line cancellation tasks (Halligan & Marshall, 1989; Pitzalis et al., 1997), during free visual exploration of pictures (Müri et al., 2009), or covert, automatic attentional orienting (Làdavas et al., 1994). A vertical neglect component was also found in the imagined space, as described in a mental number line bisection task (Cappelletti et al., 2007). However, an association between the horizontal and the vertical neglect components may not always be present. For instance, Cappelletti et al. (2007) reported that all tested neglect patients showed a horizontal neglect component, but three out of five also showed a vertical neglect component. To the best of our knowledge, a vertical neglect component in a search task has not yet been described in the literature. Since a vertical neglect component was also found in free visual exploration (Müri et al., 2009), the vertical bias seems not to be specific to tasks in which the bottom-up component is more prominent (such as in free visual exploration), but it is also observable in tasks with a pronounced top-down component (such as in the present search task). The vertical component is a challenge for explanatory models of neglect and has rarely been discussed. One may argue that the vertical component could be a consequence of the confounding effect of spatial distance dissociation of neglect symptoms. In paper–pencil tasks, the lower border of the sheet of paper is closer to the patient’s body (personal space), whereas the upper border is more displaced towards the peripersonal space. However, this hypothesis can obviously not account for the results of studies in which the upper and lower parts of the stimulus array were equidistantly located in the peripersonal space (e.g., when presented on a computer screen) (Làdavas et al., 1994; Müri et al., 2009) or for the results in the imagined space (Cappelletti et al., 2007).
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The lesion location may also play a role for the presence of a vertical neglect component. In analogy to the classical interhemispheric rivalry posited by Kinsbourne (1993), an intrahemispheric rivalry could also be postulated (Drain & ReuterLorenz, 1996). Assuming that the lower visual field is mainly represented in the dorsal occipito-parietal pathway and the upper visual field in the ventral occipito-temporal pathway (Previc, 1990), a selective lesion of one of the two pathways may result in a deficient inhibition of the other one. This would result in a relative hyperactivity of the intact pathway and thus in a vertical neglect component (Drain & Reuter-Lorenz, 1996). However, such an explanation does not seem very likely in the majority of neglect patients, since they typically show large lesions. Finally, compensatory mechanisms may explain why the vertical component of neglect is not constantly reported in the literature. In fact, it can be postulated that when neglect patients have enough time to solve a task, the vertical neglect component may not be detectable on the performance level. This is supported by our observation that patients presented a search deficit in the left lower quadrant only when the search time analysis was limited to the first seconds. However, this hypothesis does possibly not apply to all previous reports, e.g., when the search time in the paper–pencil cancellation tasks was not limited (Halligan & Marshall, 1989; Pitzalis et al., 1997). In conclusion, the present study shows that a vertical bias in neglect is also present in tasks with a more pronounced top-down component, such as visual search. This bias is accentuated when search time is restricted, possibly reflecting top-down compensatory mechanisms. Our results suggest that a vertical component in neglect may be more frequent than previously thought and should be considered to a greater extent in experimental and clinical investigations. Acknowledgement This work was supported by the Swiss National Science Foundation [Grant Nos. 320000-108146 and 3200B0-116074/1]. References Adair, J. C., Williamson, D. J., Jacobs, D. H., & Heilman, K. M. (1995). Neglect of radial and vertical space: Importance of the retinotopic reference frame. Journal of Neurology, Neurosurgery, and Psychiatry, 58, 724–728. Azouvi, P., Samuel, C., Louis-Dreyfus, A., Bernati, T., Bartolomeo, P., Beis, J.-M., et al. (2002). Sensitivity of clinical and behavioural tests of spatial neglect after right hemisphere stroke. Journal of Neurology, Neurosurgery, and Psychiatry, 73, 160–166. Behrmann, M., Watt, S., Black, S. E., & Barton, J. J. (1997). Impaired visual search in patients with unilateral neglect: An oculographic analysis. Neuropsychologia, 35, 1445–1458. Cappelletti, M., Freeman, E. D., & Cipolotti, L. (2007). The middle house or the middle floor: Bisecting horizontal and vertical mental number lines in neglect. Neuropsychologia, 45, 2989–3000. Carpenter, R. H. S. (1988). Movements of the eyes. London: Pion Ltd. Corbetta, M., Akbudak, E., Conturo, T. E., Snyder, A. Z., Ollinger, J. M., Drury, H. A., et al. (1998). A common network of functional areas for attention and eye movements. Neuron, 21, 761–773. De Haan, B., Morgan, P. S., & Rorden, C. (2008). Covert orienting of attention and overt eye movements activate identical brain regions. Brain Research, 1204, 102–111. Drain, M., & Reuter-Lorenz, P. A. (1996). Vertical orienting control: Evidence for attentional bias and “neglect” in the intact brain. Journal of Experimental Psychology: General, 125, 139–158. Gainotti, G., D’Erme, P., & Bartolomeo, P. (1991). Early orientation of attention toward the half space ipsilateral to the lesion in patients with unilateral brain damage. Journal of Neurology, Neurosurgery, and Psychiatry, 54, 1082–1089. Gauthier, L., Dehaut, F., & Joanette, Y. (1989). The Bells test: A quantitative and qualitative test for visual neglect. International Journal of Clinical Neuropsychology, 11, 49–54. Halligan, P. W., & Marshall, J. C. (1989). Is neglect (only) lateral? A quadrant analysis of line cancellation. Journal of Clinical and Experimental Neuropsychology, 11, 793–798. Heaton, R. K., Miller, S. W., Taylor, M. J., & Grant, I. (2004). Revised comprehensive norms for an expanded Halstead-Reitan Battery: Demographically adjusted neu-
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Vertical bias in neglect: A question of time? Dario Cazzoli, Thomas Nyffeler, Christian W. Hess, René M. Müri ∗ Perception and Eye Movement Laboratory, Department of Neurology, Department of Clinical Research, Bern University Hospital Inselspital, and University of Bern, Freiburgstrasse 10, 3010 Bern, Switzerland
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Article history: Received 14 December 2010 Received in revised form 7 April 2011 Accepted 11 April 2011 Available online 16 April 2011 Keywords: Human Hemispatial neglect Altitudinal neglect Visual attention Visual search Eye movements
a b s t r a c t Neglect is defined as the failure to attend and to orient to the contralesional side of space. A horizontal bias towards the right visual field is a classical finding in patients who suffered from a right-hemispheric stroke. The vertical dimension of spatial attention orienting has only sparsely been investigated so far. The aim of this study was to investigate the specificity of this vertical bias by means of a search task, which taps a more pronounced top-down attentional component. Eye movements and behavioural search performance were measured in thirteen patients with left-sided neglect after right hemispheric stroke and in thirteen age-matched controls. Concerning behavioural performance, patients found significantly less targets than healthy controls in both the upper and lower left quadrant. However, when targets were located in the lower left quadrant, patients needed more visual fixations (and therefore longer search time) to find them, suggesting a time-dependent vertical bias. © 2011 Elsevier Ltd. All rights reserved.
1. Introduction Neglect is a common and disabling neurological syndrome, generally associated with right hemispheric strokes in the territory of the middle cerebral artery (e.g., Parton, Malhotra, & Husain, 2004). Patients suffering from neglect fail to orient, react, and act upon the contralesional side of space. In the acute phase, neglect patients may behave as if the contralesional side of the world would not exist anymore. Besides the typical horizontal bias in favour of the ipsilesional side of space, a vertical bias has also been described in neglect patients. A vertical neglect component was described after bilateral cortical lesions (Adair, Williamson, Jacobs, & Heilman, 1995; Mennemeier, Wertman, & Heilman, 1992; Rapcsak, Cimino, & Heilman, 1988; Shelton, Bowers, & Heilman, 1990). Vertical neglect was also occasionally described after unilateral cortical lesions. For instance, when asked to cancel lines in the Albert’s Barrage test, neglect patients often omitted more targets in the left, lower quadrant (Halligan & Marshall, 1989; Pitzalis, Spinelli, & Zoccolotti, 1997). A vertical neglect component was also found for the imagined space in a mental number line bisection task. When asked to bisect vertically oriented mental number lines (i.e., the floor numbers in a building), neglect patients showed a shift towards the superior part of the lines (Cappelletti, Freeman, & Cipolotti, 2007). Finally, a more pronounced impairment in the automatic, covert
∗ Corresponding author. Tel.: +41 0 31 632 30 83; fax: +41 0 31 632 97 70. E-mail address: [email protected] (R. M. Müri). 0028-3932/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2011.04.010
attentional orienting in the left, lower quadrant was found when neglect patients were asked to respond to briefly flashed visual stimuli (Làdavas, Carletti, & Gori, 1994). Eye movement recordings have been shown to provide reliable information on the allocation of visual attention in space. At least in situations where the eyes are free to move (often referred to as overt attentional orienting), eye movements and visual attention seem to move together across the visual space. For instance, subjects cannot produce eye movements towards a spatial location and attend to another one at the same time (Hoffman & Subramaniam, 1995). Moreover, neural networks controlling visual attention and eye movements have been consistently shown to be overlapping (e.g., Corbetta et al., 1998; Haan, Morgan, & Rorden, 2008; Ignashchenkova, Dicke, Haarmeier, & Thier, 2004; Nobre, Gitelman, Dias, & Mesulam, 2000). Indeed, eye movements during visual exploration show typical patterns in neglect patients, reflecting their impairment to direct attention towards the contralesional space. This includes an ipsilesional bias of early attentional orienting, a lack of exploratory eye movements towards the contralesional space, a shift of the visual fixation distribution towards the ipsilesional space, recursive refixations (i.e., repeated fixations to the same regions), and an impairment of saccadic metrics (e.g., Malhotra, Coulthard, & Husain, 2006; Mort & Kennard, 2003; Niemeier & Karnath, 2000; Pflugshaupt et al., 2004; Sprenger, Kömpf, & Heide, 2002). Furthermore, the abovementioned attentional bias along the vertical spatial dimension was also detectable by means of eye movement recordings. In a recent study, a more pronounced reduction of visual fixations was found in the lower part of the left screen half during free
0 0 2
1.5 1.07 1.92 n/a 1.6 1.22 1.80* 0.89 .97 1.90* 0 1 0 n/a 0 0 0 0 0 0 4.9** 4.08** 4.01** n/a 5.26** 4.49** 4.79** 3.04** 4.59** 3.86**
Mean RT left [s]d
Omitted targets right
Mean RT right [s]d
visual exploration of naturalistic pictures (Müri, Cazzoli, Nyffeler, & Pflugshaupt, 2009). Hence, during free visual exploration – without specific instructions and with a marked bottom-up (or stimulusdriven) component – neglect patients showed both a horizontal and a vertical bias in their visual exploration. Up to now, it is not clear whether a vertical bias is also present in tasks with a more pronounced top-down (or concept-driven) component, such as in a search task. Thus, the present study aimed to assess behavioural performance and eye movement patterns in neglect patients on both vertical and horizontal spatial planes during a visual search task with naturalistic scenes.
1.18 1.14 3.68**
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2.66* 2.7* 7.8**
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0.9 1 1 3.4 1.8 2.1 2.4 1.6 3.9 1.9 Ischemia Ischemia Ischemia Haemorrhage Ischemia Ischemia Ischemia Ischemia Haemorrhage Ischemia 48 61 59 56 57 58 48 45 63 43 m w w m w m w m m m
n/a = not available. a Lesion location (areas involved): BG = basal ganglia; front = frontal cortex; ins = insula; op = operculum; par = parietal cortex; temp = temporal cortex; th = thalamus. b Time between the insult and the experiment, in months. c Drawing performance was scored as: 0 = intact; 1 = distorted left side; 2 = flagrant omissions on the left side. d PVT, mean reaction time: *borderline performance; **impaired performance (based on percent ranges, cut-off value of 15, according to Heaton, Miller, Taylor, & Grant, 2004).
1 1 0 n/a 7 5 3 0 12 2 No Yes Yes Yes No Yes Yes Yes Yes Yes 0 1 1 2 2 0 1 1 2 2 7.44 9.98 5.12 16.38 18.04 3.46 22.55 n/a n/a 20.1 3 5 3 5 4 1 8 2 10 n/a Paresis Plegia Paresis Paresis Paresis Paresis Paresis Plegia Paresis Plegia
2 0 9 n/a n/a No 2 0 2 4 5 8 Paresis Paresis Paresis 0.7 1.3 2.1 Ischemia Ischemia Ischemia
BG; ins BG; par; front BG; ins; op; temp; th; par op; ins; par; BG ins; par; temp; op front; ins temp; par temp; op; par ins; op; temp; BG BG; temp; par BG; ins; op; front par; temp ins; op; front; temp
Left omissions Bells Test Time postb Lesiona
54 74 47
The 32 stimuli were pseudo-randomly assigned to four blocks of eight images each. Each block started with an explanatory display in which the four target objects were centrally presented on an exemplary background photograph (not used elsewhere in the experiment). Subjects were instructed to search for one of the four possible targets and, once found, to click on it with the mouse cursor. Stimuli were presented until mouse click or until the subjects declared that they could not find the target. In the latter case, the experimenter tagged the trial as failed and manually started the next one. Prior to each stimulus, a central fixation point was presented during 1 s, ensuring a common starting point for all subjects. The compliance to this
m m m
2.4. Procedure
Aetiology
Stimuli were displayed in a dimly lit room on a cathode ray tube computer display (Samsung SyncMaster 959NF) with an active size of 36 × 27 cm, a resolution of 800 × 600 pixels, 24 bit colour depth, and a refresh rate of 85 Hz. Eye position was recorded with an infrared video-based eye-tracking system (EyeLinkTM , Sensomotoric Instruments GmbH, Teltow, Germany). The system is equipped with a camera recording screen position to compensate for head movements. For this reason, only a chin rest was used to secure a constant viewing distance of 70 cm. The eye-tracking system is characterised by a temporal resolution of 250 Hz, a spatial resolution of .01◦ according to the manufacturer, and a typical gaze position accuracy of .5–1◦ , depending on calibration precision. The system was periodically calibrated by means of a 3 × 3 grid calibration sequence. Eye movements were recorded and parsed into fixations and saccades online, and then transferred to an external computer for offline evaluation.
Table 1 Demographic and clinical data of the patients.
2.3. Apparatus
Age
Stimuli consisted of 32 full colour photographs of everyday scenes as background in which common, small search target objects were embedded. Each background photograph contained only one embedded target object. Eight categories of background photographs were presented (four pictures per category): fruits, edibles, naturalistic scenes, everyday objects, interior scenes, transportation means, transportation routes, and buildings. Four search target objects were used: a clock, a leaf, a pear, and a screw. In each visual field quadrant, four positions were defined for the presentation of the target object. Each position was tested by two objects, resulting in eight targets presented in each quadrant overall. Background photographs were presented in full screen size, with two small black bars on the upper and lower borders (1.5 cm in height, full screen in width), which allowed to avoid deformation of the original motifs. Background photographs subtended a viewing angle of about 29 × 19.5◦ . Embedded target objects were presented with a viewing angle of about 1.6 × 1.6◦ . Fig. 1 depicts an example of a stimulus.
Sex
2.2. Stimuli
Motor deficit
Relative bisection bias [%]
Drawing scorec
Left reading omissions
Thirteen patients with left-sided neglect after right hemispheric damage (aged between 43 and 74 years, mean = 54.85, SD = 8.65, all right-handed, 4 women) and thirteen healthy subjects (aged between 40 and 63 years, mean = 52.38, SD = 7.03, all right-handed, 5 women) participated in the study. There was no statistically significant difference in age between the two groups (Mann–Whitney U = 74.5, p = 0.622, exact sig., 2-tailed). All subjects were naïve with respect to the experimental hypotheses. Neglect diagnosis was based on clinical examination and neuropsychological tests, such as Bells Test (Gauthier, Dehaut, & Joanette, 1989), line bisection (Schenkenberg, Bradford, & Ajax, 1980), drawing and reading performance, and a subtask of the Vienna Test System (PVT, Dr G. Schuhfried GmbH, Mödling, Austria). All subjects had normal or corrected-to-normal visual acuity, no signs of strabismus, and normal colour vision as assessed by Ishihara’s test (Ishihara, 1999). In all patients, the central 30◦ of the visual field were intact as assessed by perimetry. Demographic and clinical data of the patients are shown in Table 1. All subjects gave written informed consent prior to the experiment. The study was conducted in compliance with the latest version of the Declaration of Helsinki and was approved by the ethical committee of the State of Bern.
n/a n/a 6.65
PVT
2.1. Subjects
Omitted targets left
2. Materials and methods
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Fig. 1. Example of a stimulus. The target object (a screw, marked by a white arrow) is embedded in the left, upper quadrant of the background photograph (category: transportation means). In the experiment, all stimuli were presented in full colour.
request was monitored online by the experimenter. The four blocks were separated by a short break of about 2 min, which also permitted the periodical recalibration of the eye-tracking system. Before the beginning of the experiment, subjects were given eight practice trials. The background pictures in the practice trials were not used elsewhere in the experiment. 2.5. Data analysis Performance in the search task was computed as the percentage of targets found during the experiment for each subject in the whole visual field and in the four visual field quadrants. Results of patients and healthy controls were compared by means of Mann–Whitney U tests (exact significance, 2-tailed). For the analysis over visual field quadrants, the ˛ error rate was corrected for multiple comparisons by means of the Bonferroni-procedure (˛/n, where n represents the number of comparisons). To evaluate search performance on the vertical dimension, a Laterality Index (LI) was computed for the upper and lower visual field quadrants. The LI was calculated according to the formula: percentage of targets found in the left quadrant/percentage of targets found in the right quadrant. Values greater than 1 indicate a better search performance in the left quadrant, whereas values lower than 1 indicate better search performance in the right quadrant. The LI was calculated for the time until response (no time limit). Moreover, in order to evaluate the temporal evolution during performance, the LI was computed for different time limits (6, 8, 10, 12, 14, 16, 18, and 20 s). The results of the LI underwent a repeated-measures analysis of variance (ANOVA) with within factors ‘search time limit’ (levels: 6, 8, 10, 12, 14, 16, 18, 20 s, and no limit) and ‘quadrants’ (levels: upper quadrants, lower quadrants). Fixations outside the photographs and saccades starting or ending outside the photographs were filtered out. Moreover, fixations shorter than 100 ms were excluded (Carpenter, 1988). The percentage of cumulative fixation duration over the four quadrants was computed for each trial and then averaged over all trials for each subject. The results of the parameter ‘percentage of cumulative fixation duration’ underwent a repeated-measures ANOVA with within factor ‘quadrant’ (levels: left upper, right upper, left lower, right lower) and between factor ‘group’ (levels: healthy controls, patients). The direction of the first saccade (towards the quadrants) was determined for each trial and then computed as percentage of the trials for each direction in each subject. The results of the parameter ‘first saccade direction’ underwent a repeatedmeasures ANOVA with within factor ‘direction’ (levels: left upper, right upper, left lower, right lower) and between factor ‘group’ (levels: healthy controls, patients). The number of fixations until target object detection was computed for each trial and then averaged over all trials for each subject. Only trials in which the target object was found were included in this analysis. The results of the parameter ‘number of fixations until target detection’ underwent a repeated-measures ANOVA with within factor ‘quadrant’ (levels: left upper, right upper, left lower, right lower), indicating in which quadrant the target was presented, and between factor ‘group’ (levels: healthy controls, patients). All subsequent post hoc analyses were assessed by Fisher’s least significant difference (LSD) tests.
3. Results 3.1. Performance in the search task Patients with neglect found significantly less objects (median = 91%, range = 72–100%) compared to healthy controls (median = 100%, range = 94–100%) (U = 31.0; p = 0.005). Analysis of the number of hits per quadrant revealed that patients found significantly less targets than healthy controls in both the upper left (patients: median = 88%, interquartile range [IQR] = 18.75%; controls: median = 100%, IQR = 0%) (U = 31.0; p = 0.003) and the lower left (patients: median = 88%, IQR = 12.5%; controls: median = 100%, IQR = 0%) (U = 39.0; p = 0.005) quadrant. However, there were no significant differences between healthy controls and patients in the number of hits in the upper right (patients: median = 88%, IQR = 18.75%; controls: median = 100%, IQR = 12.5%) (U = 57.5; n.s.) or in the lower right (patients: median = 100%, IQR = 12.5%; controls: median = 100%, IQR = 0%) (U = 45.5; n.s.) quadrant. The results of the LI in neglect patients for the upper and lower quadrants showed no significant effects of the factor “search time limit” (F(8,96) = 1.439; n.s.) or of the factor “quadrants” (F(1,12) = 3.217; n.s.). However, the interaction “search time limit × quadrants” was highly significant (F(8,96) = 3.921; p < 0.001). Subsequent post hoc tests revealed a significant reduction of search performance in the left inferior quadrant if the search time was limited to 6, 8, or 10 s. For times over 10 s, the LI of the lower and upper quadrants was not significantly different. The results are depicted in Fig. 2.
3.2. Percentage of cumulative fixation duration The repeated-measures ANOVA showed significant differences for the factor “quadrant” (F(3,72) = 13.002; p < 0.001) and for the interaction “quadrant × group” (F(3,72) = 24.902; p < 0.001). As assessed by subsequent post hoc tests, patients showed a significant reduction of the percentage of cumulative fixation duration in both the left upper and the left lower quadrant. The results are shown in Fig. 3.
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Fig. 2. Evolution over time of the Laterality Index (LI) for target hits in the upper and lower quadrants in neglect patients (left panel), asterisks represent significant post hoc tests (**p < 0.001; *p < 0.01). For comparison, the right panel depicts the evolution over time of the LI in healthy controls. Error bars indicate standard error of the mean (SEM).
Fig. 3. Mean percentage of cumulative fixation duration over the four quadrants in patients and controls. Controls show a symmetrical distribution of the percentage of cumulative fixation duration. Patients show a significant reduction of the percentage of the cumulative fixation duration in the left screen part for both the upper and lower quadrant (**p < 0.001). Error bars indicate standard error of the mean (SEM).
3.3. First saccade direction As revealed by the repeated-measures ANOVA, there were significant differences for the factor “direction” (F(3,72) = 12.395; p < 0.001) and for the interaction “direction × group” (F(3,72) = 33.419; p < 0.001). As assessed by subsequent post hoc tests, patients produced significantly more first saccades towards the right upper and the right lower quadrant than towards the left upper and the left lower quadrant. Controls showed the reverse pattern (Fig. 4). 3.4. Number of fixations until target detection Finally, the repeated-measures ANOVA on the number of fixations showed that patients needed more fixations than controls to find the target (F(1,24) = 6.684; p = 0.02; mean number of fixations until target detection ± SEM: Patients 15.9 ± 2.17; Controls: 8 ± 2.17). The factor “quadrant” was not significant (F(3,72) = 1.446; n.s.). However, the interaction “quadrant × group” was significant (F(3,72) = 6.149; p < 0.001). Post hoc testing revealed that patients needed significantly more fixations to find the target when it was
Fig. 4. Direction of the first saccade. The percentages of first saccades towards the right upper and lower quadrants were significantly increased in neglect patients. Controls showed the reversed pattern (**p < 0.001). Error bars indicate standard error of the mean (SEM).
located in the lower left quadrant. Furthermore, a significant difference between patients and controls was found for the left lower quadrant (see Fig. 5). 4. Discussion The aim of the present study was to investigate performance and oculomotor behaviour of neglect patients during a naturalistic search task. We were particularly interested in assessing the influence of the horizontal as well as of the vertical target localisation. In general, we found that neglect patients (1) displayed longer exploration times to find targets, and (2) found significantly less targets, especially when these were located in the left screen half, irrespective of their vertical localisation (upper or lower left visual quadrant). However, if the target was located in the left lower visual quadrant, patients needed more fixations (and therefore more time) to detect it, suggesting a time-dependent vertical bias. Concerning oculomotor parameters, patients showed typical findings described in the literature, such as an ipsilesional bias in the distribution of cumulative fixation duration during visual
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Fig. 5. Mean number of fixations until target detection depending on the quadrant in which the target was located. In patients, the number of fixations was significantly higher for targets in the left lower quadrant compared to the other quadrants (*p < 0.05; **p < 0.001). Error bars indicate standard error of the mean (SEM).
search (e.g., Behrmann, Watt, Black, & Barton, 1997; Heide & Kömpf, 1998) and in the early attentional orientation (Azouvi et al., 2002; Gainotti, D’Erme, & Bartolomeo, 1991; Mattingley, Bradshaw, Bradshaw, & Nettleton, 1994; Olk, Harvey, & Gilchrist, 2002; Pflugshaupt et al., 2004). These effects were observed for both the upper and lower left quadrants. With respect to the search performance in patients, the number of hits was not significantly different for targets located in the left upper or lower quadrant. However, to achieve the same search efficiency, patients had to produce significantly more fixations in the left lower quadrant. A vertical component of neglect has sparsely been described in the literature. In some patients, a vertical bias was found in classical paper–pencil line cancellation tasks (Halligan & Marshall, 1989; Pitzalis et al., 1997), during free visual exploration of pictures (Müri et al., 2009), or covert, automatic attentional orienting (Làdavas et al., 1994). A vertical neglect component was also found in the imagined space, as described in a mental number line bisection task (Cappelletti et al., 2007). However, an association between the horizontal and the vertical neglect components may not always be present. For instance, Cappelletti et al. (2007) reported that all tested neglect patients showed a horizontal neglect component, but three out of five also showed a vertical neglect component. To the best of our knowledge, a vertical neglect component in a search task has not yet been described in the literature. Since a vertical neglect component was also found in free visual exploration (Müri et al., 2009), the vertical bias seems not to be specific to tasks in which the bottom-up component is more prominent (such as in free visual exploration), but it is also observable in tasks with a pronounced top-down component (such as in the present search task). The vertical component is a challenge for explanatory models of neglect and has rarely been discussed. One may argue that the vertical component could be a consequence of the confounding effect of spatial distance dissociation of neglect symptoms. In paper–pencil tasks, the lower border of the sheet of paper is closer to the patient’s body (personal space), whereas the upper border is more displaced towards the peripersonal space. However, this hypothesis can obviously not account for the results of studies in which the upper and lower parts of the stimulus array were equidistantly located in the peripersonal space (e.g., when presented on a computer screen) (Làdavas et al., 1994; Müri et al., 2009) or for the results in the imagined space (Cappelletti et al., 2007).
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The lesion location may also play a role for the presence of a vertical neglect component. In analogy to the classical interhemispheric rivalry posited by Kinsbourne (1993), an intrahemispheric rivalry could also be postulated (Drain & ReuterLorenz, 1996). Assuming that the lower visual field is mainly represented in the dorsal occipito-parietal pathway and the upper visual field in the ventral occipito-temporal pathway (Previc, 1990), a selective lesion of one of the two pathways may result in a deficient inhibition of the other one. This would result in a relative hyperactivity of the intact pathway and thus in a vertical neglect component (Drain & Reuter-Lorenz, 1996). However, such an explanation does not seem very likely in the majority of neglect patients, since they typically show large lesions. Finally, compensatory mechanisms may explain why the vertical component of neglect is not constantly reported in the literature. In fact, it can be postulated that when neglect patients have enough time to solve a task, the vertical neglect component may not be detectable on the performance level. This is supported by our observation that patients presented a search deficit in the left lower quadrant only when the search time analysis was limited to the first seconds. However, this hypothesis does possibly not apply to all previous reports, e.g., when the search time in the paper–pencil cancellation tasks was not limited (Halligan & Marshall, 1989; Pitzalis et al., 1997). In conclusion, the present study shows that a vertical bias in neglect is also present in tasks with a more pronounced top-down component, such as visual search. This bias is accentuated when search time is restricted, possibly reflecting top-down compensatory mechanisms. Our results suggest that a vertical component in neglect may be more frequent than previously thought and should be considered to a greater extent in experimental and clinical investigations. Acknowledgement This work was supported by the Swiss National Science Foundation [Grant Nos. 320000-108146 and 3200B0-116074/1]. References Adair, J. C., Williamson, D. J., Jacobs, D. H., & Heilman, K. M. (1995). Neglect of radial and vertical space: Importance of the retinotopic reference frame. Journal of Neurology, Neurosurgery, and Psychiatry, 58, 724–728. Azouvi, P., Samuel, C., Louis-Dreyfus, A., Bernati, T., Bartolomeo, P., Beis, J.-M., et al. (2002). Sensitivity of clinical and behavioural tests of spatial neglect after right hemisphere stroke. Journal of Neurology, Neurosurgery, and Psychiatry, 73, 160–166. Behrmann, M., Watt, S., Black, S. E., & Barton, J. J. (1997). Impaired visual search in patients with unilateral neglect: An oculographic analysis. Neuropsychologia, 35, 1445–1458. Cappelletti, M., Freeman, E. D., & Cipolotti, L. (2007). The middle house or the middle floor: Bisecting horizontal and vertical mental number lines in neglect. Neuropsychologia, 45, 2989–3000. Carpenter, R. H. S. (1988). Movements of the eyes. London: Pion Ltd. Corbetta, M., Akbudak, E., Conturo, T. E., Snyder, A. Z., Ollinger, J. M., Drury, H. A., et al. (1998). A common network of functional areas for attention and eye movements. Neuron, 21, 761–773. De Haan, B., Morgan, P. S., & Rorden, C. (2008). Covert orienting of attention and overt eye movements activate identical brain regions. Brain Research, 1204, 102–111. Drain, M., & Reuter-Lorenz, P. A. (1996). Vertical orienting control: Evidence for attentional bias and “neglect” in the intact brain. Journal of Experimental Psychology: General, 125, 139–158. Gainotti, G., D’Erme, P., & Bartolomeo, P. (1991). Early orientation of attention toward the half space ipsilateral to the lesion in patients with unilateral brain damage. Journal of Neurology, Neurosurgery, and Psychiatry, 54, 1082–1089. Gauthier, L., Dehaut, F., & Joanette, Y. (1989). The Bells test: A quantitative and qualitative test for visual neglect. International Journal of Clinical Neuropsychology, 11, 49–54. Halligan, P. W., & Marshall, J. C. (1989). Is neglect (only) lateral? A quadrant analysis of line cancellation. Journal of Clinical and Experimental Neuropsychology, 11, 793–798. Heaton, R. K., Miller, S. W., Taylor, M. J., & Grant, I. (2004). Revised comprehensive norms for an expanded Halstead-Reitan Battery: Demographically adjusted neu-
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