Journal of Clinical and Experimental Neuropsychology, 2014 Vol. 36, No. 8, 787–793, http://dx.doi.org/10.1080/13803395.2014.940855

The influence of stimulus proximity on judgments of spatial relationships in patients with chronic unilateral right or left hemisphere stroke John B. Williamson1,2, Salsabil Haque1,2, Brandon Burtis1,2, Michal Harciarek1,3, Damon Lamb1,2, Eduardo Zilli1,2, and Kenneth M. Heilman1,2 1

Malcom Randall VAMC, Gainesville, FL, USA Department of Neurology, University of Florida College of Medicine, the Center for Neuropsychological Studies, Gainesville, FL, USA 3 Institute of Psychology, University of Gdańsk, Gdańsk, Poland 2

(Received 27 June 2013; accepted 27 June 2014) Objective: This was to learn how chronic right hemispheric damage (RHD) versus left hemispheric damage (LHD) may influence attentional biases in proximal and distal space. Background: Prior research has suggested that the left hemisphere primarily attends to proximal space and the right hemisphere to distal space. The purpose of this study was to contrast line bisection performed in proximal versus distal space in patients with chronic LHD versus RHD. Design/method: Participants were 32 LHD and 26 RHD patients who sustained a stroke a mean of 3.4 years prior to testing, along with 9 healthy controls. Subjects attempted to bisect 30 lines in proximal space and 30 lines in distal space. Results: Patients with both RHD and LHD had a greater contralesional bias in proximal than distal space (rightward bias for patients with LHD and leftward bias for patients with RHD). Compared to controls, patients with LHD were most different in proximal space, and patients with RHD were most different in distal space. Conclusions: Proximity appears to influence spatial judgments of patients with RHD and LHD in an opposing manner. Relatively, both patient groups bisect lines contralesionally in proximal space and ipsilesionally (relative to proximal) in distal space. Patients with RHD have the biggest difference between their proximal and distal judgments. The reason for these differences is unknown. However, these biases may be related to an attentional or action-intentional grasp or a learned compensation strategy, and proximity may increase the allocation of attention or intention and thereby enhance this grasp or use of this compensation strategy. Another contributing factor may be dominance of the left and right hemisphere for information presented in proximal and distal space, respectively. Keywords: Neglect; Laterality; Stroke; Chronic; Distance.

Many hemispheric functional asymmetries of the human brain have been described, including the processing of spatial information. Each hemisphere allocates attention to contralateral hemispace, but data have suggested that the right hemisphere is better able to allocate attention to ipsilateral hemispace than the left hemisphere

(Adair, Na, Schwartz, & Heilman, 2003; Barrett, Schwartz, Crucian, Kim, & Heilman, 2000; Bowers & Heilman, 1980; Heilman & van den Abell, 1980). There are multiple forms of attention, and there appear to be hemispheric asymmetries for several of these different forms. For example, studies have

Funded by Department of Veterans Affairs Merit Review, Clinical Science Research and Development [grant number 465], Approach-Avoidance Spatial Neglect, PI: Kenneth M. Heilman. Address correspondence to: John B. Williamson, Department of Neurology, University of Florida College of Medicine, HSC Box 100236, Gainesville, FL 32610-0236, USA (E-mail: [email protected]).

This work was authored as part of the Contributor’s official duties as an Employee of the United States Government and is therefore a work of the United States Government. In accordance with 17 U.S.C. 105, no copyright protection is available for such works under U.S. Law.

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suggested that focal attention (e.g., attending to the details of a scene or an object) may be predominantly a function of the left hemisphere, whereas global attention (e.g., attending to an entire scene or object) may be predominantly a function of the right hemisphere (Barrett, Beversdorf, Crucian, & Heilman, 1998; Kosslyn et al., 1989; Lamb, Robertson, & Knight, 1990; Mapstone et al., 2003; Robertson, Lamb, & Knight, 1988). In the current experiment, we investigate differences in hemispheric specialization for making spatial judgments in proximal-peripersonal space (within an arm’s reach) and distal-extrapersonal space (outside an arm’s reach). Although proximal space is represented in a multisensory fashion and relies on a widely distributed neuronal network (Magosso, Zavaglia, Serino, di Pellegrino, & Ursino, 2010), the processing of visual information from proximal space has been reported to be primarily mediated by the functional systems in the left hemisphere. In contrast, the processing of visual information from distalextrapersonal space may rely primarily on functional systems in the right hemisphere (Berberovic & Mattingley, 2003; Chewning, Adair, Heilman, & Heilman, 1998; Heilman, Chatterjee, & Doty, 1995; Jeerakathil & Kirk, 1994; Jeong, Drago, & Heilman, 2006; Weiss et al., 2000). These right–left hemispheric proximal–distal spatial asymmetries may also be interactive. Based on this interaction, when normal subjects attempt to bisect horizontal lines in proximal space, they should activate their left hemisphere more than the right and, thus, deviate toward the right. However, studies of healthy participants attempting to bisect proximal horizontal lines have shown that people in fact deviate towards the left side of the line, a phenomenon known as “pseudoneglect” (Bowers & Heilman, 1980; Bradshaw, Bradshaw, Nathan, Nettleton, & Wilson, 1986; McCourt, Garlinghouse, & ReuterLorenz, 2005). An alternative hypothesis that may account for this asymmetry is related to the concepts of focal and global attention. As the right hemisphere is dominant for global attention, and a line bisection task requires a judgment of the center of an object (a global task), activation of the right hemisphere may induce a leftward attention bias with leftward deviation. Since the right hemisphere appears also to be dominant in mediating distal attention, this leftward bias might be greater in distal than in proximal space. However, this leftward bias is no longer present when these subjects bisect lines in distal space (Varnava, McCarthy, & Beaumont, 2002). Whereas the results of these bisection studies in normal subjects appear to contradict the left hemisphere proximal, right hemisphere distal dichotomy, the subjects who show this left-sided bias on near bisections have learned to read

from left to right, and Varnava et al. (2002) suggest that this proximal leftward bias may be related to this learned scanning strategy, and, thus, pseudoneglect may represent a learned attentional bias. In the current experiment, we assessed the ability of people with a unilateral stroke of the right or left hemisphere as well as healthy controls to bisect lines in proximal and distal space. Since the right hemisphere appears to be dominant for attending to distal space, we posited that this attentional asymmetry may be additive with the lesion-induced inattention such that subjects with RHD, when compared to LHD participants, will demonstrate relatively decreased attention to stimuli or portions of stimuli presented in distal left space. In addition, it is also possible that since the left hemisphere appears to be dominant for attending in proximal space, patients with LHD, when compared to those with RHD, would have a greater inattention to stimuli or portions of stimuli presented in right proximal space. An alternative possibility is that the proximal versus distal placement of the stimuli would influence both the right and left hemisphere damaged participants in a similar manner. Since, in general, proximal stimuli may be more strongly attended than distal stimuli, injury to either the right or the left hemisphere may induce greater changes in a patient’s ability to allocate spatial attention, and thus asymmetrical changes in proximal space may be more robust than those in distal space, independent of the side of injury. Alternatively, since proximity may enhance attention, and this enhancement could obscure subtle alterations of attention, it is possible that the injured hemisphere will be relatively less attentive in distal than in proximal space. Therefore, when tested in distal versus proximal space, patients with hemispheric lesion reveal a greater ipsilesional bias. Finally, some patients with contralesional neglect subsequently develop ipsilateral or ipsilesional neglect and demonstrate a contralesional bias (Kim et al., 1999; Kwon & Heilman, 1991). Ipsilesional neglect has been posited to be induced by an attentional or intentional grasp (Kim et al., 1999), and, therefore, it is also possible that there may be greater ipsilesional neglect with proximal than with distal presentations as well as hemispheric asymmetries. The purpose of this study is to test these alternative hypotheses and predictions.

METHOD Participants Fifty-eight patients (after exclusions) with a chronic unilateral stroke were recruited from the

STROKE, LATERALITY, SPATIAL JUDGMENTS, AND STIMULUS PROXIMITY

North Florida region through the North Florida/ South Georgia VA Medical Center’s Brain Research and Rehabilitation Center (BRRC) Stroke Registry. Two subjects were excluded due to hemianopia at the time of the study evaluation. Two subjects were excluded due to the presence of bilateral hemisphere strokes. Two subjects were excluded due to developmental eye disorders, one for diplopia and the other due to developmental blindness in the left eye. One subject was excluded due to history of concussions with loss of consciousness (a former boxer). Finally, one subject was excluded due to an impairment in verbal comprehension as determined by failure of the Western Aphasia Battery sequential commands subtest. Of the remaining patients, 26 (18 male) had right hemisphere damage (RHD), and 32 (20 male) had left hemisphere damage (LHD) and were included in the study. Furthermore, 9 (4 male) neurologically and psychiatrically healthy controls were also recruited and assessed. Demographic and stroke data are presented in Table 1. Imaging and neurological information was collected as part of the BRRC registry process, and evaluation thereof was used to classify subjects into LHD or RHD groups. Neurological evaluation was completed by a BRRC neurologist who was not involved in the current study. Imaging data were collected from multiple sources and include both computed tomography (CT) and magnetic resonance imaging (MRI) scans. Most of these participants’ strokes were in the middle cerebral artery distribution (see Table 1). The inclusion criteria for the experimental participants were: (a) over the age of 21 years, English as their first language, and at least a 6th grade education; (b) a single, unilateral stroke of either

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the right or the left cerebral hemisphere; (c) since the goal was to assess participants with chronic strokes, only those subjects with strokes that occurred six or more months prior to the study were included, and there was no limit on number of years post stroke; (d) willingness of the participant and caregiver/family to perform this research and sign an informed consent approved by the University of Florida Institutional Review Board for the protection of human subjects; (e) corrected visual acuity of greater than 20/50 (assessed as part of the BRRC screening process, also verified by self-report at time of assessment); (f) ability to comprehend instructions as assessed by the Western Aphasia Battery. The exclusion criteria for the experimental participants were: (a) a history or evidence of other diseases that involve the central nervous system—for example, a clinical diagnosis of Alzheimer disease; (b) impaired verbal comprehension as determined by the Western Aphasia Battery (WAB) such that the patient was unable to understand the instructions for performing the research tasks; (c) chronic medical conditions that might be associated with a metabolic encephalopathy—for example, vital organ failure (i.e., uremia, hypoxia, hepatic failure, and severe cardiac failure); (d) treatment with psychotropic drugs other than antidepressants that might influence alertness, arousal, and activation, such as benzodiazepines, barbiturates, anticonvulsants, neuroleptics, amphetamines, and dopaminergic agents; (e) history of severe head trauma or a learning disability. Subjects also underwent detailed neurological testing, including examination of the cranial nerves and motor and sensory systems as well as reflexes. Subjects were administered a structured interview, sometimes with family member present, including

TABLE 1 Demographic and stroke information

Variables Age (years) Education (years) MMSE Handedness (% right) Arterial distribution (% MCA) Years since stroke Stroke volumea (cm3) Hypertension (%) Diabetes (%)

Healthy controls (n = 9)

Left hemisphere stroke (n = 32)

Right hemisphere stroke (n = 26)

58.88 ± 14.03 15.00 ± 2.87 28.33 ± 1.32 88 N/A N/A N/A 75 0

61.37 ± 11.57 14.19 ± 2.62 25.45 ± 4.65 94 74 3.78 ± 4.99 54.87 ± 98.79 74 20

61.73 ± 12.46 14.73 ± 2.64 27.54 ± 2.04 85 60 3.08 ± 2.77 51.22 ± 58.67 84 36

Note. MMSE = Mini-Mental State Examination; MCA = middle cerebral artery. Calculated from subsample with available imaging, n = 19 (right hemisphere damage, RHD), n = 24 (left hemisphere damage, LHD). a

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questions about: age, education, occupation, history of learning disability, prescription medications, hypertension and diabetes history, history of stroke occurrence, traumatic brain injury (TBI), other neurological conditions, alcohol use, tobacco use, illicit drug use, and psychiatric history. These were also surveyed in each subject’s medical record. Subjects completed a paper and pencil test of neglect (Mesulam’s symbol cancellation test) and a computerized touch screen test of neglect (a line bisection task requiring the subjects to touch the middle of each line). Mini-Mental Status Exam (MMSE) scores were also obtained, though these were confounded by language disturbances, and thus we used the WAB subtests as a complementary inclusion criterion. Annett’s inventory was used to assess for handedness (Briggs & Nebes, 1975). Only subjects who were capable of performing the experimental tests were included.

Apparatus and procedure All subjects performed the same procedure. Line bisection tasks were presented in proximal and distal space (as described below). Sixty trials were administered, with 30 in proximal space and 30 in distal space. Proximity was pseudorandomized and counterbalanced. The horizontal (intersection of the coronal and transverse planes) line stimuli were presented at eye level in both distal and proximal conditions. The proximal condition was presented on a display that was placed 30 cm from the patient. The presented lines were 24 cm long. In the distal condition the lines were presented at 167.75 cm from the patient. The lines were 134.2 cm long, matched to subtend the same visual angle (43.5°) as the lines presented in the proximal (peripersonal space) condition. The thickness of these lines were also matched for the subtended visual angle (i.e., 3.0 mm for proximal lines, 17.0 mm for distal lines). The lines were printed on paper and displayed on a display board. In both conditions, the patient used a laser pointer to indicate the location on the line that would divide these lines into two equal segments. Each patient’s performance on these line bisection tasks was recorded by a video camera, and the bisection marks and deviations from the actual midline were measured by an investigator who was unaware of the subject’s group classification. To score the bisections, the video was examined on a computer monitor (27” Apple Cinema Display). A ratio was calculated based on measurements of deviations of the line and the total measured line (using a ruler). A measurement of .50 indicates a perfect bisection. A

measurement below .50 indicates a leftward deviation and above .50 a rightward deviation. On the 30-cm line, each .01 deviation in the ratio is equivalent to a 3-mm shift. On the 134.2-cm line, each .01 deviation in the ratio is equivalent to a 13-mm shift. On the computer line bisection task, subjects were seated 30 cm from a touch screen computer monitor on which lines were presented and were instructed to touch the middle of each line. Fifty lines were presented of varying length with a random-noise screen interference screens presented between each trial. Scoring was similar to the above (.5 = middle, >.5 = rightward deviation, and

The influence of stimulus proximity on judgments of spatial relationships in patients with chronic unilateral right or left hemisphere stroke.

This was to learn how chronic right hemispheric damage (RHD) versus left hemispheric damage (LHD) may influence attentional biases in proximal and dis...
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