NOTE EVIDENCE FOR AN INDEPENDENT STIMULUSCENTERED SPATIAL REFERENCE FRAME FROM A CASE OF VISUAL HEMINEGLECT* Martin Arguin and Daniel N. Bub (Montreal Neurological Institute) INTRODUCTION The computational literature suggests that several different reference frames relative to which the location of objects is specified may be required for proper visual function (Feldman, 1985; Marr, 1982; Marr and Nishihara, 1978; Monk, 1985). Most conceptualizations will concur with the following description: A viewer-centered spatial representation is one that defines the location of objects relative to the subject himself, and which therefore changes with every movement of the observer. In contrast, an environmentcentered representation specifies the location of objects relative to one another - e.g. x is above y - and thus is not affected by movements of the observer. Finally, an objectcentered representation is a volumetric internal model of an object and is independent of its location relative to either the viewer or the other stimuli in the environment. The study of patients with visual hemineglect appears as quite appropriate to investigate the levels of spatial representation which are used by human vision. In general, patients with visual hemineglect behave as if the contralesional part of the stimulation does not exist, in that they fail to attend to it (De Renzi, 1982; Freidland and Weinstein, 1977; Hecaen and Angelergues; 1963; Heilman, 1985; Kinsbourne, 1987; Roy, ReuterLorenz, Roy et al., 1987). This syndrome has been attributed alternatively to either a defective attention system preventing the orientation of attention to the part of a spatial representation that corresponds to contralesional space (Heilman, 1985; Kinsbourne, 1970; 1987; Mesulam, 1983; Morrow and Ratcliff, 1988; Riddoch and Humphreys, 1987; Roy et al., 1987) or to a damaged spatial representation (Bisiach and Berti, 1987; Bisiach, Capitani, Luzzatti et al., 1981; Ogden, 1985). At present, these two views appear equally viable since disorders of attentional or representational mechanisms are both plausible causes for the failure to attend to contralesional items. Whichever the case may be, experiments with neglect cases may be profitable in the study of spatial representations since these appear to be implicated, directly or indirectly, in the occurrence of neglect symptoms. In previous reports, authors have been able to dissociate the effects of the target location within subject-centered and environment-centered reference frames by having the subjects view the displays that were presented with their head either upright or tilted to one side (Calvanio, Petrone and Levine, 1987; Farah, Brunn, Wong et al., 1990; Utdavas, 1987; U.davas, Del Pesce and Provinciali, 1989). These experiments have shown that neglect may affect the processing of items in the contralesional parts of both viewercentered and environment-centered spatial reference frames. Also, Caramazza and Hillis (1990a; 1990b) reported a neglect dyslexic patient in which only a word-centered spatial reference frame - analogous to an object-centered representation - was neglected. These demonstrations that neglect may affect the processing of locations within a particular re- *The experiment reported in this paper was presented at the Tennet II conference in May 1991 in Montreal, Canada. Cortex, (1993) 29, 349-357 350 M. Arguin and D.N. Bub ference frame when tested in isolation is evidence that corresponding representations are being used by the human visual system. Moreover, they also indicate that many levels of spatial representation may be affected in visual hemineglect - either in isolation of in various combinations in any particular subject - and, by extension, that the allocation of visual attention across space in normal individuals may be performed on all of the spatial reference frames mentioned here. One question that needs further clarification concerns the specification of the reference frame(s) relative to which the spatial coordinates of objects within the environment are computed. As indicated above, an environment-centered representation is assumed to define the location of objects relative to one another. But certainly, not all visible objects may serve at the same time as reference points to localize all the others. More probably, within a particular spatial representation, there is, at any given moment, a single reference relative to which other objects are localized. As far as an environment-centered representation is concerned, two candidates, which are not mutually exclusive, may be considered. One is that observers use features of their surroundings which may be considered stable (e.g. the walls in a room) as the reference frame relative to which other objects are localized. Such a reference may be important for representing a stable environment which is not affected by the movements of the observer. This is the type of environmentcentered reference frame that has been isolated in the study of neglect patients by having the subjects tilt their head on one side (Calvanio et al., 1987; Farah et al., 1990; Liidavas, 1987; Liidavas et al., 1989). Another candidate for an environment-centered representation, which is distinct from the previous one, is that the reference frame may be task-dependent, in that it is based not on stable landmarks in the surroundings but rather on the spatial extent covered by the stimulation which is relevant to the task to be performed at a given point in time. In such a representation, which may be referred to as stimulus-centered, the location of an item is defined as a function of its position within the area occupied by the stimulus ensemble which is relevant to the subject's task. Take for example a task in which subjects are required to process a pair of stimuli aligned horizontally. In this case, the stimulus-relative location of, for instance, the left item is invariant wherever the pair of stimuli is presented relative to the observer or to stable environmental landmarks. We wish to emphasize that the concept of a stimulus-centered spatial representation discussed here is separate from that of an object-centered description, which depicts the spatial relations between the parts of a single object. Thus, it is assumed that a stimulus-centered reference frame represents the relative locations of spatially distinct stimuli and that it refers exclusively to visible surfaces rather than to a truly volumetric representation of the environment (i.e. in Marr's (1982) terms, the 3D sketch). The notion of a stimulus-centered spatial representation has been the subject of theoretical discussions before (Caramazza and Hillis, 1990b) and the construct has been used by Riddoch, Humphreys, Cleton et al. (1990) to account for the performance of a neglect dyslexia patient they studied. However, no systematic attempt to provide independent evidence for this type of spatial representation has yet been reported. The aim of the experiment presented here is to conduct a test of the hypothesis that a stimulus-centered spatial representation may be affected by visual hemineglect, and by extension, that it contributes to normal human vision. To this end, a patient with visual hemineglect was examined with the aid of a visual filtering paradigm which required her to name a target letter presented within a horizontal array of constant configuration. Distractors were filled circles. It was assumed that this task provided a direct measure of the allocation of visual attention across space 1, in that the less attention was allocated to the location at which the target was presented, the more time it would require to respond to it. Five neurologically intact controls were also tested. 1 The use of the concept of attention allocation is intended to remain neutral as to the hypothesized nature of the primary impairment that may underlie neglect symptoms. As mentioned. this question is presently a matter of debate, with some authors suggesting that neglect results from defective attentional mechanisms while others hold the position that it is due to a faulty representation of space. Hemineglect and object location frame 351 a) Viewer-relative position X X X X ®X b) Stimulus-relative position Extreme left Left of center Right of center Extreme right • • • • • • X X X X X X • • • • • • X Fig. I - (a) Set of possible locations (X) occupied by the target relative to the central fixation point (F). (b) Set of possible locations occupied by the target within the stimulus array. All these within-array locations were tested at each possible target location relative to the fixation point. The location of the target was varied according to two orthogonal factors (Figure 1). One was the position occupied by the target within the stimulus array (stimulus-relative location). The other was the location occupied by the target relative to stable landmarks in the environment (e.g. the edge of the screen), and also relative to the subject's body and point of ocular fixation - i.e. subjects always sat upright and straight in front of the display screen and the location at which the fixation point was displayed on the screen was kept constant throughout the experiment. For convenience, this latter factor will be called viewer-relative target location. It should be kept in mind however that the location of the target relative to the observer and to stable landmarks in the environment were confounded within this factor. To dissociate these two effects would have required to test the patient while lying on her side, which was not possible within the physical constraints of the testing situation. What is of primary concern here however is that the stimulus-relative factor be truly independent of any other variable which may affect the definition of the location of the target. This independence was achieved here by testing each level of the stimulus-relative location factor across all levels of the viewer-centered factor. MATERIALS AND METHOD Subjects The patient tested (B.A.) was a 79 year-old right-handed woman. She showed EEG evidence for a right parietal lesion, and brain-damage was of vascular origin. She showed normal visual fields on confrontation and a' strong left visual neglect. The latter was clearly apparent in a search task requiring the selection of multiple occurrences of a target (a bell shape) presented on a sheet of paper along with other depicted objects (Gauthier, Dehaut and Joanette, 1989). Neglect was also apparent in visual search tasks (longer RTs for contralesional stimuli) and B.A. showed a disorder of disengagement of visuo-spatial attention similar to that reported by Posner, Walker, Friedrich et al. (1987). Finally, evidence for left neglect was also apparent in daily life. In particular, she fre- 352 M. Arguin and D.N. Bub quently bumped into objects and doorframes that were located to her left and often ignored persons approaching her from the left. Five right-handed neurologically intact subjects were used as controls. Apparatus and Stimuli The experiment was run on a Macintosh Plus microcomputer and response times were recorded to the nearest millisecond. A microphone, linked to the computer, was used as a voice-key to register the verbal response that was required on each trial. Target stimuli were the consonants B, C, J, K, P, T, V, and Z. On each trial, a single target letter was randomly chosen from this set. Letters were 6.2 mm high and 4.1 mm wide. With the target, three distractors were presented. There were filled circles of 4.1 mm in diameter. Preceding the stimulus array, a fixation dot (4.1 mm in diameter) was presented at the center of the display screen for a duration of 1.5 sec. Subjects were instructed to keep their eyes fixated on this point as long as it was visible, but that after the onset of the search array they could freely move their eyes. All stimuli were white and shown on a black background. The search stimuli were always displayed as a horizontal array of four equidistant items. The distance separating consecutive items in the array was of I em. The location of the target relative to the central fixation point (viewer-relative location) was varied independently of the location of the target within the stimulus array (stimulus-relative location). Thus, the target could be presented in any of the eight locations illustrated in Figure Ia. Each of these potential target locations was separated from the other by a distance of I em. Moreover, for each of the possible target locations relative to the fixation point, the target location within the stimulus array could be any of the four illustrated in Figure I b. The stimuli remained visible until the subject responded. Procedure The task required subjects to name the target letter as rapidly as possible while avoiding errors. Two factors were involved in this experiment. Those were the location of the target relative to the fixation point (eight levels; viewer-relative location) and the location of the target within the four-item array (four levels; stimulus-relative location). These two factors were orthogonal in that each level of one factor was tested equally often across all the levels of the other. The main dependent variable was response time (RT). For each subject, the experiment was run in seven separate blocks of 64 trials each. One or two blocks were run in each testing session for B.A. while each control subject was run in a single session of seven blocks. An equal number of trials of .each condition was distributed randomly in each block. Subjects were seated at approximately 30 em from the display screen and always viewed the diplays with their heads upright. Some of the trials were eliminated due to failure of the subject's verbal response to trigger the microphone. This happened on 1.6% of the trials for B.A. and on 2.0% of the trials for the normal controls. These were not considered in the data analyses. RESULTS Figure 2 shows the mean correct RTs observed in the control subjects (Figure 2a) and in B.A. (Figure 2b) in each of the conditions of the present experiment. Only a single error was made by B.A. in the entire experiment while control subjects made an overall average of 0.27% errors. None of the analyses performed on error rates showed any significant effect. A two factor analysis of variance for repeated measures was performed on the correct RTs seen in the normal controls. This analysis showed only a main effect of the viewerrelative target location (F=5.0; d.f.=7, 28; p