Grasping at sticks: pseudoneglect for perception but not action
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1 Exp Brain Res (2004) 157: DOI /s RESEARCH NOTES Laura E. Hughes. Tim C. Bates. Anne Aimola Davies Grasping at sticks: pseudoneglect for perception but not action Received: 4 November 2003 / Accepted: 27 April 2004 / Published online: 24 June 2004 # Springer-Verlag 2004 Abstract A current question in theories of visual cognition is whether distinct cognitive processes subserve perceptual judgments and perception for action. This paper examines bisection tasks which have previously been used to demonstrate a dissociation between perception and action in brain injured patients. Forty neurologically intact participants completed a standard line bisection task and a variant of this task rod bisection. A typical leftwards bias was observed for line bisection but when asked to locate the centre of wooden rods using perceptual judgments, a distinct rightwards bias was shown. By contrast, when participants were asked to pick the rods up by the centre, their judgments showed no bias. The results are in line with theories suggesting that perception and action are independent; however, alternative explanations are also considered. Keywords Action. Perception. Pseudoneglect. Visual illusion Introduction Whether conscious perceptual judgments and perception for action are dissociable is a current concern for theories of visual cognition (e.g. Milner and Goodale 1995; Pritchard et al. 1997; Robertson et al. 1995). Distinctions between types of perception have been discussed in several theories (e.g. Bridgeman et al. 1979; Goodale and Milner 1992; Ungerleider and Mishkin 1982) and attributed to the functions of the ventral and dorsal stream. Goodale and Milner (1992) proposed that a dissociation between perception and action arises due to the differential L. E. Hughes (*). T. C. Bates. A. Aimola Davies Macquarie Centre for Cognitive Science, Macquarie University, NSW 2109 Sydney, Australia lhughes@maccs.mq.edu.au A. Aimola Davies School of Psychology, The Australian National University, ACT 0200 Canberra, Australia processing of these two streams. They suggested the ventral stream primarily uses visual information for perceptual judgments, whereas the dorsal stream utilises information to visually guide actions. Their model is supported by evidence from neuropsychological studies of patients who had lesions to the dorsal stream, which resulted in impaired visually guided actions (optic ataxia), and lesions to the ventral stream, which impaired visual object perception (visual agnosia) (e.g. Goodale et al. 1994; Milner et al. 1991, 1999, 2001). In addition to patients with optic ataxia and visual agnosia, dissociations in patients with visual spatial neglect have also been studied. Adapted line bisection tasks have been used to assess the extent of neglect for perceptual judgments and visually guided actions. In standard line bisection tasks, neglect patients typically bisect the line to the right of centre, which is contrary to the performance of neurologically intact participants in both the extent of the error but also in the direction; neurologically intact participants tend to bisect lines to the left of centre (see Jewell and McCourt 2000 for a review). This bias has been attributed to hemispheric activation (Kinsbourne 1970a) and the theory suggests that the distribution of attention in space is biased towards the hemispace contralateral to the more activated hemisphere. Thus for neurologically intact participants, line bisection results in a leftward bias because it is principally a spatial task which recruits right hemisphere processing and the increased activation of the right hemisphere biases perception towards the left visual hemispace (e.g. Bowers and Heilman 1980; Reuter-Lorenz et al. 1990). For neglect patients their rightwards bias may be due to deficient right hemisphere processing which results in a more active left hemisphere, which drives attention rightwards (Kinsbourne 1970a, b). The line bisection task has been adapted by Robertson et al. (1995) and Edwards and Humphreys (1999) to include wooden rods as the stimuli. They measured the extent of neglect for bisecting a rod and when picking a rod up by the centre. Typically, when pointing to the centre, neglect was evident, resulting in a rightwards bias.
2 398 However, when picking the rod up by the centre, the patient s grasp was observed to be more accurate. This dissociation has been discussed in terms similar to those suggested by Goodale and Milner, namely that different neural areas could be responsible for pointing and grasping. Alternative interpretations have also been suggested. Robertson et al. (1995) proposed that the frame of reference may play a role in the dissociation. Manipulations of an object may be dependent on a frame of reference for grasping which is not used for perceptual judgments. Edwards and Humphreys (1999) also entertained this possibility but suggested it was unlikely because both pointing and grasping were influenced similarly by rod length and spatial location. However, whether this precludes the frame of reference as a plausible alternative was not explored experimentally. Dissociations between perception and action in neurologically intact participants have also been studied. Visual illusions are used to induce a perceptual bias which is suggested to be ineffective on visually guided actions. A variety of illusions have been employed, including the Judd illusion in which participants are asked to point to and grasp the centre of a rod flanked by aligned arrows (e.g. Ellis et al. 1999; Mon-Williams and Bull 2000; Post and Welch 1996), the Ebbinghaus illusion in which participants are asked to manually estimate the size of a central disc and then to grasp the same disc (Agliotti et al. 1995; Haffenden and Goodale 1998; Haffenden et al. 2001) and the Muller-Lyer Illusion in which participants indicate the length of a shaft and also grasp the shaft by its length (Gentilucci et al 1996; Otto-de Haart et al. 1999; Westwood et al. 2000; Wraga et al. 2000). These studies reported that participants were susceptible to the illusion when making perceptual judgments but their actions remained veridical. Explanations of the dissociation differ, however, and alternative suggestions to Goodale and Milner s hypothesis were proposed. The frame of reference has, again, been used to explain dissociations in neurologically intact participants. Gentilucci et al. (1996) suggest that the use of different frames of reference for perception and action may result in the apparent dissociation. In a series of studies using the Muller-Lyer illusion they observed that when actions were performed immediately with concurrent visual access to the hand and object, illusory effects were minimized, but perceptual judgments were strongly influenced. When performance relied more on memory, the illusory effect on action increased to concur with the perceptual judgment. This dissociation is suggested to arise due to encoding the object in an allocentric frame for perceptual judgments which encompasses the whole array, but during the visuomotor phase the coordinates of the target are transposed to an egocentric frame of reference which focuses on one part of the array and, during this phase, illusory influences are minimized. However, the dissociation has also been attributed to confounding variables. Several studies note that methodological artefacts could contribute to the dissociation. For example Mon-Williams and Bull (2000) observed that in grasping tasks the illusion can become occluded, which may account for the effect being minimized during visuo-motor action. Vishton et al. (1999) argued that studies using the Ebbinghaus illusion do not take into account several factors which may confound the results, for example the introduction of additional elements in the display may influence the grasp, and also the tactile feedback may provide learning support. Furthermore, perceptual judgments are subject to relative comparisons between several objects which causes the illusory effect; grasping, however, manipulates just one object and consequently the illusion is minimized or eliminated. Vishton et al. used the horizontal-vertical illusion to examine this last theory. In an initial experiment participants compared the relative length of the horizontal and vertical line and judged the vertical line to be longer. Their actions in grasping the vertical line, though, did not reflect this illusion. However, when perceptual judgments were absolute, not relative, the illusory perception disappeared, and when grasping required a relative judgment, then accuracy was again biased by the illusion. These methodological factors have proved problematic for studies using illusions to demonstrate the dissociation in neurologically intact participants. A task not subject to such influences may be the solution. The rod bisection task used with the neglect patients is an interesting candidate. Neurologically intact participants show pseudoneglect, a leftwards bias on standard tasks of line bisection, but the question remains: will pseudoneglect occur for rod bisection? In addition, how participants will perform when grasping the centre of a rod is also of interest. In light of Goodale and Milner s hypothesis, we may expect that, even if pseudoneglect is observed in rod bisection, grasping may not be subject to this effect. The present study aims to investigate these hypotheses. We used a paradigm similar to that of Edwards and Humphreys (1999) and adapted a line bisection task to include wooden rods as stimuli. This method should also avoid the artefacts which may have affected the results of previous illusion tasks. We predict that participants will show a leftwards bias in line bisection tasks and we also predict a directional bias in rod bisection tasks. The direction of the bias is unpredictable; however, we may expect (according to the activation hypothesis) that the bias will be towards the side contralateral to the activated hemisphere. Finally, with regard to visually guided actions, we expect no evidence of pseudoneglect for rod bisection when participants grasp the rod by the centre. Materials and methods Participants Forty first-year undergraduate students, 14 male (mean age 19.5 years; age range 19 22) and 26 female (mean age 19.5 years; age range 19 22) participated after providing informed consent and in return for course credit. The study was approved by the Human Research Ethics Committee and tests were conducted in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. All participants were right-handed, as
3 399 assessed by self-report from a seven-item questionnaire adapted from the Edinburgh Handedness inventory (Oldfield 1971). Extreme right-handedness was indicated by a maximum score of +100; the mean laterality score of the participants was +90, with a range of to Design A repeated-measures design comprising several bisection tasks was used to assess the degree of asymmetry in spatial attention. An initial line bisection task assessed a leftward bias, as previously reported, and three additional rod bisection tasks measured the degree of asymmetry when bisecting rods in three conditions: a non manual cued bisection condition in which the experimenter cues the subject to the left or the right side of the rod (the side cued first was counterbalanced); a manual bisection condition in which the subject points to the centre of each rod; and an action condition in which the subject grasps the rod by the centre. Five rod lengths were used to examine whether length would have an effect on bisection condition. The rod bisection tasks were presented in one of two orders: cued bisection task first followed by pointing and then grasping or, alternatively, in reversed order. Order was balanced across subjects. The order was not completely randomized so any effects of grasping on pointing, or pointing on grasping could be monitored. In each condition the position indicated as centre was measured; this measurement reflected the amount of error, in centimeters, from veridical centre. Apparatus and material The line bisection task was presented by a Visual Basic program run from a Toshiba notebook and viewed on a 40-cm (15 ) monitor. The lines were 12 cm in length and either thin (0.5 mm) or thick (1.5 cm) and presented in the centre of the screen, on the left (mid point of line shifted from centre of screen 12 cm left) and on the right (mid point of line shifted from centre of screen 12 cm right). The rod bisection tasks used five black rods (2 cm in circumference) of five lengths (25 45 cm in 5-cm increments). One side was covered with black Velcro and on another side a ruler was printed to facilitate accurate recording of response. Responses were made using a pointer: a ring made of Velcro which was worn on the index finger. On contact with the rod, the ring stuck to the Velcro and a small arrow affixed to the ring indicated the central point. Procedure All participants completed each task using their right, and dominant, hand. The line bisection task was presented first. Participants sat approximately 40 cm from the monitor and used the computer mouse to click on the centre of each line; the position of the mouse click was recorded. All participants then completed each of the rod bisection tasks. For the rod bisection tasks, participants sat opposite the experimenter at a 1 2 m table. Rods were presented in a random order and were placed directly in front of the subject, approximately at their midline, 20 cm from the edge of the table. The tasks were completed in a free-viewing untimed condition. In the cued condition the experimenter passed the pointer across the top of the rod starting from either the left or right side. The participants were instructed to say stop when they thought the pointer was in the centre; they were also allowed to adjust the position by verbally instructing the experimenter to move the pointer left or right. All five rods were presented with the same cue direction and then repeated from the opposite direction. In the pointing task participants were asked to use the pointer to point to the centre of the rod themselves. For the grasping task, participants were asked to use their forefinger (on which the pointer was worn) and thumb to pick the rod up by the centre so it would be evenly balanced in their hand using one smooth natural grasping movement. Measurements were taken immediately after each bisection. Results Line bisection A significant leftwards bias was observed in the line bisection task, which conforms to previous reports of a leftward bias for this task. For the lines presented in the centre of the screen a significant leftwards bias was evident (thin lines: mean error = 2.79 mm, SD=8.07, t (39) =2.2, p<0.05; thick lines: mean error = 5.05 mm, SD=10.68, t (39) =2.9, p<0.05) and significantly more participants bisected the line to the left of centre (thin lines: 67% of participants, χ 2 1=5.4, p<0.05; thick lines: 62% of participants, χ 2 1=4.3, p<0.05). Fig. 1 The percentage of participants making leftward and rightward errors in each of the bisection tasks. In the line bisection task a leftward bias is apparent, which conforms to previous reports of similar tasks. In the rod bisection tasks, however, a distinct rightward bias is notable, but not in the grasping task, in which no bias is evident
4 400 A bias was also evident when participants were required to bisect lines which were off centre. When the lines were presented on the left, a significant leftwards bias was present (thin lines: mean error = 4.83, SD=13.57, t (39) =2.2, p<0.05; thick lines: mean error = 6.86, SD=6.86, t (39) =6.3, p<0.05) but significantly more participants made leftward bisections for the thick lines only (thin lines: 50% of participants, χ 2 1=0.23, p>0.05; thick lines: 82% of participants, χ 2 1=19.6, p<0.05). When the lines were presented on the right a rightwards bias occurred but this bias was not significant (thin lines: mean error = 3.95, SD=15.02, t (39) =1.7, p<0.05; thick lines: mean error = 4.65, SD=19.3, t (39) =1.5, p<0.05); however, significantly more participants made right rather than left errors (thin lines: 72% of participants,χ 2 1=7.04, p<0.05; thick lines: 75% of participants, χ 2 1=8.8, p<0.05). Rod bisection An analysis of variance was performed on the errors made on each of the five rod lengths across the four different rod bisection tasks (Left Cue, Right Cue, Pointing and Grasping). There were no significant differences between the bisection errors across the five rod lengths (F (4,156) =2.57, p>0.05) but there was a significant difference between the errors made on the four bisection tasks (F (3,117) =10.9, p<0.01) No interaction between task and rod length was present (F (12,486) =1.5, p>0.05). The lack of interaction between task and rod length suggests that length did not differentially affect error on the bisection tasks. Similar results were found by Edwards and Humphreys (1999): patient MP also showed no interaction between bisection task (pointing or grasping) and rod length. The extent of pseudoneglect in the rod bisection tasks was assessed by analyzing the direction of errors, including analysis of the magnitude of errors and the frequency of leftward and rightward errors. Figure 1 displays the frequency data for the line and rod bisection tasks. In the Left Cued bisection task, the centre of the rod was perceived to be, on average, 0.34 cm (SD=0.37 cm) from veridical centre and this distance was revealed to be significantly different from 0 (t (39) =5.7, p<0.01), demonstrating a rightwards bias. In addition, rightward errors were observed significantly more frequently, with 69% of participants making rightward errors (χ 2 1=44.72, p<0.01). Similar results were observed in the Right Cued task. The perceived centre was judged to be a mean of 0.27 cm (SD=0.41 cm) from true centre, which was significantly different from 0 (t (39) =4.2, p<0.01), and again rightwards errors were significantly more frequent, with 64.5% of participants showing a rightward bias (χ 2 1=27.871, p<0.01). In the pointing task the perceived centre was judged to be a mean of 0.14 cm (SD=0.41 cm) from true centre, which was significantly different from 0 (t (39) =2.2, p<0.05), and the frequency of rightward errors was significant, with 58% of participants erring to the right (χ 2 1=14.370, p<0.01). The grasping task, however, showed no significant biases; the average error was 0.02 cm (SD=0.35 cm), which was not significant (t (39) =0.37, p>0.05). In addition, only 49% of participants erred rightward of true centre, thus demonstrating no significant bias (χ 2 1=0.433, p>0.05); participants were equally likely to make a leftwards or rightwards error. Sex differences No significant sex differences were observed between the extent of errors made on the tasks (F (1,38) =0.38, p>0.05). There was no significant interaction between sex and task (F (3,114) =1.18, p>0.05) and no significant interaction between rod length and sex (F (4,152) =0.36, p>0.05). Task order An analysis of variance was used to examine whether task order affected bisection. Typically studies examining the action/perception dissociation in patients or neurologically intact participants present the tasks in the order of perceptual judgments first followed by visually guided actions, so that the actions which are hypothesized to be more veridical do not influence the perceptual judgment in any way. In the present study no significant differences were observed between the bisections of participants asked to complete the grasping task first and participants asked to complete the cued bisection tasks first, implying that previous tasks had no influence on subsequent tasks. (Left Cue: F (1,39) =3.781, p>0.05; Right Cue: (F (1,39) =1.741, p>0.05; Pointing: F (1,39) =1.523, p>0.05; Grasping: F (1,39) =0.025, p>0.05). Discussion The results of the line bisection task replicated the finding of a leftward bias in neurologically intact participants, which has been frequently reported in many similar bisection studies (see Jewell and McCourt 2000 for a review). Manipulating the azimuthal position of the lines, to the left and right of centre, resulted in a centrifugal pattern of error, which is also consistent with previous reports (see McCourt et al. 2000). Overall, the results of the line bisection tasks demonstrate our subject pool is not atypical. In the cued and pointing rod bisection tasks an opposite bias to the line bisection task was obtained: we observed a rightward bias. The grasping task showed no pattern of bias in either a rightward or leftward direction, supporting our hypothesis. The rightward biased judgments in the pointing and cued tasks suggest that these tasks are relying on similar perceptual processes, whereas
5 401 the grasping task, which shows no bias, may rely on an alternative method of visual analysis. The rightward bias in the perceptual tasks was surprising, as the literature mostly reports leftward biases for bisection tasks. In a metaanalysis of 73 studies and 2,191 participants, Jewell and McCourt (2000) found an overall leftward bias for both visual and non-visual bisection tasks, although no studies included in the metaanalysis tested visual bisection of rods presented at a participant s midline. Hand use may affect bisection error (Brodie and Pettigrew 1996; Halligan et al. 1991; Hausmann et al. 2002). In the present study all participants used their right (and dominant) hand when required to bisect the stimuli, which could underlie the right bias in the pointing bisection task, but not the right bias which also occurred in the cued conditions. Scanning direction has also been implicated as another cause of bias direction. A study monitoring eye movements during a line bisection task reported that participants tended to look left first, which may explain the leftwards bias (Kim et al. 1997). Furthermore, scanning from right to left has been reported to induce a rightwards bias, and left-to-right scanning, a leftwards bias (Chokron et al. 1998). In our study, though, we found that both the left- and right-cued perceptual bisection tasks resulted in a rightwards bias. This suggests that a further factor may be influencing the direction of bias, in addition to hand used and scanning direction. The stimuli could be the critical factor. Rods were used, as opposed to lines which have been used in previous studies, and this may have contributed to the rightward bias observed. Few other studies have examined rod bisection, and those that have tend to investigate non-visual tactile bisection. These studies are similarly affected by variables such as hand used (Bradshaw et al. 1983; Brodie and Pettigrew 1995) and scanning direction (Baek et al. 2002) but the results are not consistent with each other. The leftwards bias in line bisection could be due to hemispheric activation (Bowers and Heilman 1980; Kinsbourne 1970a, b; Reuter-Lorenz et al. 1990), and, if this theory is applied to the present study, the rightwards bias could be explained by left hemisphere activation. So, why might rods activate the left hemisphere? A possible explanation could be that they are thought of as tools, since tool observation has been found to activate areas of the left premotor cortex (e.g. Chao and Martin 2000; Grafton et al. 1997), but this begs the question of why grasping then resulted in no perceptual bias. The lack of bias for grasping and the directional bias for the perceptual tasks could be predicted by Goodale and Milner s theory of ventral and dorsal processing. Perceptual tasks rely on ventral representations, which are suggested to be susceptible to perceptual distortions and visual illusions; thus, we would expect the pointing and cued bisection tasks to be subject to pseudoneglect (or a reverse pseudoneglect). The grasping task, which requires a visually guided action, should recruit the dorsal stream, which is hypothesized to be less influenced by illusions; thus, we would not expect any evidence of perceptual bias in this task. Although the results concur with the two stream theory, alternative explanations should also be considered. Frame of reference has been proposed to explain the dissociations observed in the visual illusion (Gentilucci et al. 1996) and in the patient studies (Robertson et al. 1995) and may also provide one explanation for the dissociation observed in the present study. In accordance with the proposal by Gentilucci et al. (1996), the rods could be encoded in an allocentric frame which is used for the perceptual judgment tasks and, during the grasping phase, the coordinates are transposed into an egocentric frame. However, this explanation is limited in explaining the biases of the present data. It is proposed that global and local processing requirements could encompass more of the results. Global and local processing explanations have frequently been applied to elucidate the performance of neglect patients; patients with visual spatial neglect can be aware of the whole structure and form of shapes (global processing) but are impaired when they then turn their attention to the individual parts comprising the whole (local processing) (Halligan and Marshall 1998; Marshall and Halligan 1995). These processing requirements may also provide an explanation for why pseudoneglect was not apparent in grasping and why there was an error bias in the perceptual bisection tasks. Perceptual bisection could utilize local processing because the task involves dividing the rod into two equal parts and attention may be focused on comparing the two halves rather than on one whole. Grasping may involve global processing because the task involves lifting the whole rod rather than dividing it. The neglect patients studied by Robertson et al. (1995) and Edwards and Humphreys (1999) may be impaired at rod bisection tasks because they are impaired at processing local stimuli in left hemispace and they may be able to grasp the rods more accurately because they employ global processing to do so. Global and local processing may also explain why the rightward bias occurred for the perceptual bisection tasks but not for grasping. Local processing is suggested to be a left hemisphere process and global a right hemisphere process (Fink et al. 1996; Robertson et al. 1990). According to the activation hypothesis, activation of the left hemisphere for tool use and for local processing may drive attention rightwards, resulting in a rightwards bias. No bias would occur in grasping, however, because global processing is utilized and, thus, the right hemisphere is activated, which focuses attention on both the left and right hemispaces. This appears plausible as a theory to explain dissociations in rod bisection observed in both patients and neurologically intact participants. If the dissociation between pointing and grasping is due to global and local processing, this does not rule out the possibility that the ventral and dorsal stream are also involved. It may be the
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