Search patterns using the line bisection test for neglect Manho Kim, MD; Jeffrey M. Anderson, MS; and Kenneth M. Heilman, MD Article abstract-BackgroundIObjectiue: Neglect has been attributed to sensory-attentional, motor-intentional, and representational disorders. Although patients with neglect may have defective visual exploration, the nature of this exploration deficit has not been entirely elucidated. The purpose of this study is to learn how, compared with control subjects, a patient with neglect performs visual exploration. Methods: The line bisection test is commonly used to detect and evaluate the performance of patients with unilateral or hemispatial spatial neglect. We tested an experimental subject with left premotor-intentional neglect using a n infrared eye monitoring instrument. Thirteen right-handed healthy volunteers served as control subjects. From different starting ocular positions, we assessed the direction of eye movements when the subjects initially oriented to the line, scanned the line, and then attempted to look at the center of the line. ResuZts: Independent of starting ocular position, normal subjects most often initially orient to the left end of the line, scan rightward, then look leftward to the center. However, the eye movements in our experimental subject with neglect were directed to the right end of the line without any scanning or leftward eye movement back to the center of the line. Con,clusion: Our subject with neglect had defective line exploration that may be attributed to a directional ocular motor intentional deficit. NEUROLOGY 1997;49:936-940 The line bisection test is commonly used to detect and evaluate the performance of patients with uniTo correctly lateral or hemispatial spatial mark the center of the line, visual exploration of the line and visuospatial computational processes are needed. Patients with unilateral spatial neglect from right-hemisphere lesions incorrectly estimate the center of the line to the right of the true center, neglecting the left part of the line. Neglect has been attributed to sensory-attentional, motor-intentional, and representational disorders. Although patients with neglect may have defective visual exploration, the nature of this exploration deficit has not been entirely elucidated. Chedru and Leblanc3 and Chedru et al.4 recorded the eye movements of patients with left-sided spatial neglect and demonstrated that they had a failure to explore the left side of space. This failure to explore could not be accounted for by paralysis since these patients could look leftward on command. If patients do not fully explore the left side of a sheet, they may fail to cancel targets on the part of the sheet they have failed to explore. If patients fail to explore the left side of a line, they may never learn the full extent of the line, bisecting only the portion they have explored. Ishiai et al.5 also studied ocular search patterns of patients who had neglect when performing line bisection and compared patients with neglect with those with right or left visual field defects and no neglect as well as with normal controls. They found that the patients with a left hemianopia searched mostly leftward and patients with a right hemianopia searched mostly rightward. Ishiai et al. reported that in patients with neglect, the ocular search was limited t o rightward exploration. However, Ishiai et al. used the term “rightward or “leftward” to denote the portion of egocentric hemispace that was explored rather than direction of exploration. For example, quantitative analysis of rightward directional searches was determined by the eye position located in the right side of the line. To correctly bisect a line, subjects would need to explore both sides of the line and move their eyes in both directions. Visual exploration requires the coordinated function of several interconnected anatomic structures such as the prearcuate (dorsolateral) frontal lobe, superior colliculus, posterior parietal lobe, cingulate gyrus, and thalamus.6 Unlike Chedru et al.3 and Ishiai et al.6 who were interested in the area of visual search, we wanted to learn about the direction of exploration. Making a voluntary eye movement in one horizontal direction, independent of the eyes’ spatial position, requires activation of the contralateral hemisphere. Although rightward movements are controlled predominantly by the left hemisphere, leftward movements are controlled by the right hemisphere. Even in normal subjects, the means of searching a line are not entirely known. Therefore, as an initial step, we assessed search patterns in normal subjects. Estimating the center of the line requires visuospa- From the Department of Neurology, University of Florida College of Medicine, and the Neurology Service, Veterans Administration Medical Center. Gainesville, FL. Snpported by the Medical Research Service of the Department of Veterans Affairs. Received October 21, 1996. Accepted in final form May 5, 1997. Addrefis correspondence and reprint requests to Dr. Kenneth M. Heilman, Box 100236, University of Florida, Gainesville, FL 32610. 936 Copyright 0 1997 by the American Academy of Neurology Figure. Brain MRI of the experimental subject showing diffuse middle cerebral arterial territory infarction involving the frontotemporoparietal area. during line exploration when the subject looked from one end of the line to the other. If the subject scanned the line more than once, the last horizontal scan was assessed to determine final scanning direction. This final scan provides the best estimate of how long the subject perceived the line to be. The third stage was the direction and extent of eye movement when the subjects attempted to look to the center of the line. To assess the effect of initial eye position on line search patterns, we categorized the initial horizontal eye position into right, center, and left. We categorized the initial vertical eye position into upper, middle, and lower. Results. Normal control subjects. A total of 111 trials were analyzed. Although we tried to have nine trials for each subject (total 117 trials for 13 subjects), we had to delete six trials because they contained blink artifacts, which interfered with determining the direction of the eye movement. Line searching patterns of normal control subjects. None of our normal subjects showed repetitive eye scanning of the line. The direction of three stages (initial orientation, scanning, looking to the center of the line) of eye movements was sequentially linked, and two types of patterns were observed. One pattern was that of initial orientation to the left side of the line followed by rightward scanning through the whole line to the right end and then a final adjustment leftward back to the center of the line (we will call this scan pattern L-R). The other pattern was the opposite of the L-R pattern. In this R-L pattern, the 938 NEUROLOGY 49 October 1997 initial orientation is to the right end of the line with subsequent scanning to the left end and finally rightward back to the center of the line. Eleven of 13 subjects showed more frequent L-R scanning patterns. Six subjects showed L-R patterns in all their trials (loo%),and one subject showed eight L-R patterns out of nine trials (88.9%). Another subject showed seven L-R patterns out of eight trials (87.5%), and two subjects showed seven L-R patterns out of nine trials (77.8%).Lastly, one subject showed L-R patterns in five of nine trials. Two subjects showed primarily R-L patterns, with one showing R-L pattern on seven out of nine trials (77.8%)and the other eight out of nine (88.9%). Overall, there were more trials in which subjects scanned L-R (86 of 111 or 77.5%) than R-L (x2 = 59.99 [df = 121; p < 0.0001). In 28 of 37 trials when the normal subjects initiated their search from the right portion of the line, before bisecting the line, subjects moved their eyes to the left end of the line and scanned from the left to the right end. The initial eye position in the transverse plane (left, center, right) did not seem t o significantly influence the horizontal scan patterns. Twenty-nine of 36 trials (80.6%) from the center starting position, 28 of 37 trials (75.6%) from the right start, and 29 of 38 trials (76.3%)from the left start showed a L-R scanning pattern (x2 = 0.293 [df = 21; p > 0.5). Initial eye position in the coronal plane (upper, middle, lower) also showed no significant difference (upper 30137 tial computations. However, these computations are dependent on perceiving the entire line, including both ends. We posited that, before bisecting a line, normal subjects orient their eyes first to one end of the line, either to the left or to the right, a n d patients with neglect may initially orient in a different direction than do controls. The second stage in normal subjects m a y be the scanning of the entire line from one end t o the other. Patients with neglect m a y fail to scan the entire line. The third stage in normal subjects may be the final adjustment of the eyes to the center of the line based on the metric knowledge derived from exploration and spatial computations. The purpose of this study is to learn how, w h e n compared with control subjects, a patient with neglect performs each of these three stages. Methods. Control subjects, Seven men and six women served as control subjects. The average age was 40.0 2 18.3 years, and all subjects were right handed as determined by a handedness questi0nnaire.I All subjects were without history of neurologic or psychiatric diseases, including head trauma and learning disabilities. Subjects were also not taking any medication that could influence eye movements. Informed consent was obtained. Experimental subject. A 58-year-old, right-handed man served as the experimental subject. He was brought to the emergency room because of the recent onset of left hemiparesis. He was hypertensive and had a history of myocardial infarction in 1995. In April 1996, his mother found him lying on the floor with decreased responsiveness. He had a headache several days before this event. He had no evidence of head trauma. His cardiac rhythm was regular, and he had no heart murmurs. Otherwise, his general physical examination was unremarkable. On elementary neurologic examination, he was alert and oriented to time, person, and place. He had reduced emotional expression. Although his overall verbal output seemed to be decreased, there were no deficits in verbal communication. He was hypokinetic and showed motor impersistence of eye closure. He did not have a clinical gaze paresis. Visual field examination by bedside confrontation testing was normal. He had a hemiparesis of the left upper and lower extremities with increased deep tendon reflex in the left biceps, triceps, and knee. He also had an extensor plantar response on the left. Touch and pain sensory perception seemed to be intact, but he showed allesthesia, reporting left-side stimuli as being on the right side.RHe had left-side extinction with double simultaneous tactile stimulation. On the line bisection test his mark deviated to the right side. He neglected left-sided targets during the cancellation test. We also tested the patient with line bisection tasks using a video apparatus that dissociates perceptual-attentional from premotor-intentional determinants of performance.9 Based on the results of this test the patient was categorized as having premotor-intentional neglect, indicating that persistent bias toward the right side of the stimulus is primarily related to a failure to move leftward. Echocardiogram and ECG were normal. Doppler scan revealed complete right internal carotid occlusion. MRI on May 17, 1996, revealed a right middle cerebral arterial territory infarction involving the frontotemporoparietal area (figure). Apparatus. We used a n infrared eye monitoring instrument (OPTISCAN, manufactured by Stoelting, Chicago, IL) with microprocessor image enhancement technology that achieves a resolution of better than 0.1" of visual angle (0.2 mm of eye movement) for eye position. This apparatus monitors and collects data 30 timeshec. Because external illumination and reflections may influence or interfere with the recordings of the eye movement, we enclosed the testing space with wooden panels (80 x 90 x 70 cm) that were painted flat black. During the testing procedure, the room lights were turned off. A 1 4 super VGA computer screen was placed 50 cm from the subject's eyes. This screen was used to present the stimuli. The brightness of the screen's background was reduced to the darkest level to remove any visible margins of the screen. Therefore, during the testing procedure subjects were able to only see the experimental stimuli. Experimental procedures. The experimental and control subjects sat on an unmovable chair with their chin and forehead fixed by a chin brace and a forehead rest. The midsagittal plane of the body was aligned with the midsagittal plane of the head. The center of the test line was aligned with the midsagittal plane of the subject's head and body. There were nine trials. In each of these trials, we presented the number 5 on the screen followed by a line (185 mm x 3 mm). The number 5 was presented at different locations on the screen. However, the lines were always presented at the same location on the screen. We presented the number 5 at different locations on the screen because we wanted the subjects to initiate their search from different portions of space. The number 5 was presented on the left side of the screen three times, on the right side of the screen three times, and in the middle of the screen three times. In the vertical dimension, for three trials, it was presented on the same transverse plane as the line but at the left or right end of the line or the middle of the line. On another three trials, the number 5 was presented 8 cm above the line and at the left or right end or middle of the line. Lastly, in three trials, the number 5 was presented 8 cm below the left or right end of the line or middle of the line. We instructed the subjects that there would be multiple trials in which the number 5 would appear on different parts of the screen. To initiate the trial, they were instructed to look a t this number. Subsequently, a line would be presented. When the line was presented, they were to look at the whole line, to both ends of the line, and then look a t the center of this line. Data collection and analysis. For each trial, data were collected from the time the subjects looked at the number 5 until they looked to the center of the line. After collection, the data were transferred to an EXCEL software program (Microsoft, Cambridge, MA) that graphically displays eye positions over time. If artifacts obscured these measurements, that trial was deleted. Each trial was divided into three stages, and we determined the direction and extent of eye movement at these three different stages. In the first stage we assessed to which side of the line the subject initially oriented. During the second stage, line scanning, we evaluated the eye scan October 1997 NEUROLOGY 49 937 R-L or 81.1%;middle 27/36 R-L or 75.0%; lower 29/38 L-R or 76.3%;xz = 0.43 [df = 121;p > 0.5). Therefore, independent of initial position, most subjects in most trials initially oriented to the left of the line and then scanned rightward. Following this rightward scan, they looked leftward to the center of the line. Experimental subject with neglect. Our subject with neglect performed differently than did the control subjects. In the three trials that started from the center position, the only eye movement performed by the experimental subject was a saccade to the right end of the line without any further movement. From the starting point on the left side of the line, he made a saccade to the right end of the line without any further eye movement. In the three trials that started on the right side of the line, we could not detect any meaningful directional eye movement in the transverse plane. However, he did demonstrate downward or upward gaze to reach to the right end of the line from the above or below starting position. Therefore, regardless of previous eye position, all of his eye movements were only directed to the right end of the line. We did not observe any leftward eye movement back to the center of the line. Discussion. Normal subjects typically make a n initial leftward eye movement to the end of the line, followed by rightward scan, after which they again move leftward to the center of the line. Although the basis of this scan pattern has not been entirely elucidated, several mechanisms have been proposed. Kinsbourne’O has emphasized the directional nature of spatial behavior. According to his model, in the horizontal or transverse plane, each hemisphere is responsible for directing attention toward the opposite side of space. In healthy right-handers, the left hemisphere’s rightward vector prevails over the right hemisphere’s leftward vector. Although Kinsbourne’s hypothesis can explain the rightward scanning patterns in our normal subjects, it cannot explain the initial orienting to the left side. Heilman and Van Den Abell” posited that the right hemisphere was dominant for attention, and Verfaellie et a1.12demonstrated that the right hemisphere is superior for mediating preparation for action or intention. Right-hemisphere attentional and intentional dominance may lead to a propensity for leftward orienting. Our control subjects are readers of European languages who read from left t o right. Therefore, the L-R scan patterns we detected in our subjects may be a learned response. The experimental subject’s scan patterns were different from those of the normal subjects. When the line was presented, he shifted his eyes only toward the right end of the line. When the initiation point was located at the right side of the line, he did not show any further movement except vertical movements toward the line from above or below the line. Unlike control subjects who, after reaching the right end of the line, move their eyes leftward to the tenter of the line, we did not observe any significant movement toward the center of the line. Our experimental task did not require more effort or prompting than standard line bisection tests. Because he had no language deficit and, as instructed, moved his eyes to look a t the numbers in different positions and then moved his gaze to the line, his performance cannot be attributed to poor compliance or uncooperativeness. There are several possible mechanisms that may account for this patient’s failure to scan or move leftward. One possibility is that a severe left-side gaze paresis (an ocular directional akinesia) prevented the patient from moving his eyes leftward. However, the observation that the patient could look to the number 5 in different positions, including the left position, is not consistent with the directional akinesia or gaze paresis postulates. A second possibility is that the patient not only had a propensity to orient to the right, but after orienting to the right he could not disengage his attention from the right end of the line.13 However, when he bisected lines using his hand, his mark was not at the right end of the line, suggesting that he could covertly move his attention more to the left than he moved his eyes. This observation is not only inconsistent with the attentional disengagement account of his ocular defect, but also suggests that his leftward ocular directional akinesia was worse than his inability to direct attention leftward. Attention may be controlled by either a “topdown” (e.g., in response to a command) or “bottomup” (e.g., orienting to a novel stimulus) system. These systems may be functionally dissociated. Perhaps the action-intentional systems can also be controlled by top-down (e.g., in response t o commands such as “look left”) and bottom-up (e.g., spontaneous exploration) systems, and our patient’s ocular directional akinesia was primarily in the actionintentional bottom-up system. When we evaluated the patient’s ocular explorations or scanning pattern, it appeared that the patient had a defect of leftward line exploration. From the initiation point at the right, the patient never moved leftward, and from the center portion of the line, the patient directly shifted his eye to the right end of the line without further exploration leftward. From the initiation point on the left part of the line, the patient still directly reached the right end of the line without looking back to the left. The failure of this bottom-up directional-intentional system may be related to inability to activate the gaze systems that mediate leftward movement (e.g., activation failure), an inability to reduce or inhibit the activation of the systems that mediate rightward gaze (e.g., an intentional disengagement failure), o r a combination of activator and disengagement failures. Neglect is a heterogeneous syndrome with a variety of behavioral features induced by different mechanisms. The abnormal search pattern we have observed for this patient may be different from those of other patients, depending on their type of neglect. If we classify the neglect phenomenon into sensoryattentional and premotor-intentional, our experiOctober 1997 NEUROLOGY 49 939 mental subject would be categorized as having the premotor-intentional type of neglect. We have posited that visual line exploration is more related to the internally (top-down) generated ocular motor mechanism rather than external (bottom-up) stimulus-triggered behavior. Therefore, the defect of line exploration that our experimental subject exhibited may be attributed to an ocular motor intentional deficit. Patients with neglect from primarily sensoryattentional or representational disorders may perform differently. Therefore, future studies will have to be directed at investigating ocular exploration in these subjects. Acknowledgments We are grateful to Barbara Haws for technical support and thank Gregory Crucian and Anna Barrett for their contributions. References 1. Heilman KM. Neglect and related disorders. In: Heilman KM, Valenstein E, eds. Clinical neuropsychology. New York: Oxford University Press, 1979:268-307. 2. Schenkenberg T, Bradford DC, Ajax ET. Line bisection and unilateral visual neglect in patients with neurologic impairment. 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Heilman Neurology 1997;49;936-940 DOI 10.1212/WNL.49.4.936 This information is current as of October 1, 1997 Updated Information & Services including high resolution figures, can be found at: http://www.neurology.org/content/49/4/936.full.html References This article cites 12 articles, 3 of which you can access for free at: http://www.neurology.org/content/49/4/936.full.html##ref-list-1 Citations This article has been cited by 1 HighWire-hosted articles: http://www.neurology.org/content/49/4/936.full.html##otherarticle s Permissions & Licensing Information about reproducing this article in parts (figures,tables) or in its entirety can be found online at: http://www.neurology.org/misc/about.xhtml#permissions Reprints Information about ordering reprints can be found online: http://www.neurology.org/misc/addir.xhtml#reprintsus Neurology ® is the official journal of the American Academy of Neurology. Published continuously since 1951, it is now a weekly with 48 issues per year. 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