An investigation of the relationship between free-viewing perceptual asymmetries for vertical and horizontal stimuli

Cognitive Brain Research 19 (2004) 289 – 301 www.elsevier.com/locate/cogbrainres

Research report

An investigation of the relationship between free-viewing perceptual asymmetries for vertical and horizontal stimuli Michael E.R. Nicholls a,*, Jason B. Mattingley a, Nadja Berberovic a, Amanda Smith a, John L. Bradshaw b a

Department of Psychology, University of Melbourne, Swanston St., Parkville, VIC 3010, Australia b Department of Psychology, Monash University, Australia Accepted 3 December 2003

Abstract Two experiments examine the relationship between free-viewing vertical and horizontal perceptual biases. In Experiment 1, normal participants (n = 24) made forced-choice luminance judgments on two mirror-reversed luminance gradients (the ‘grayscales’ task). The stimuli were presented in vertical, horizontal and oblique ( F 45j) orientations. Leftward and upward biases were observed in the horizontal and vertical conditions, respectively. In the oblique conditions, leftward and upward biases combined to produce a strong shift of attention away from the lower/right space toward the upper/left. Regression analyses revealed that the oblique biases were the combined product of the vertical and horizontal biases. A lack of correlation between the vertical and horizontal biases, however, suggests they reflect the operation of independent cognitive/neural mechanisms. In Experiment 2, the same stimuli were given to right-hemisphere-lesioned patients with spatial neglect (n = 4). Rightward and upward biases were observed for horizontal and vertical stimuli, respectively. The biases combined to produce a strong shift of attention away from the lower/left space toward the upper/right. While our research demonstrates that vertical and horizontal attentional biases are additive, it also appears that they reflect the operation of independent cognitive/neural mechanisms. Potential applications of these findings to the remediation of spatial neglect are discussed. D 2004 Elsevier B.V. All rights reserved. Theme: Neural basis of behavior Topic: Cognition Keywords: Neglect; Left; Right; Pseudoneglect; Attention; Coordinate frames

1. Introduction For horizontally oriented visual stimuli, the majority of normal observers overestimate the leftward features of the stimulus relative to those on the right (for a review, see Ref. [26]). Thus, for tasks such as horizontal line bisection, participants transect lines slightly to the left of the true center (e.g. Refs. [7,51,57]). This leftward bias has been referred to as ‘pseudoneglect’ [5] because it mirrors the chronic rightward attentional bias and leftward neglect that occurs following right parietal damage [35]. Leftward biases have been observed for a number of judgments other than length, such as numerosity [31,46], luminance [46] and size [46]. These tasks appear to engage a similar, but not

* Corresponding author. Tel.: +61-3-83444299; fax: +61-3-9347-6618. E-mail address: [email protected] (M.E.R. Nicholls). 0926-6410/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.cogbrainres.2003.12.008

identical, set of cognitive and neural mechanisms to those engaged by the line bisection task [31,46]. A number of different mechanisms have been proposed to account for pseudoneglect. Manning et al. [32] suggested that the leftward bias was the result of asymmetrical scanning of the stimulus. Such biases could be related to the direction in which text is read (e.g. Refs. [10 –12], but cf. Ref. [45]). Asymmetrical scanning of a stimulus could also be a manifestation of asymmetries in the distribution of attention. Given that scanning paths are affected by the distribution of spatial attention [58], a leftward bias in attention could bring about a preponderance of left-to-right scans. Support for a role of attention in pseudoneglect comes from studies using cueing paradigms. By asking participants to report lateralized cues during a line bisection task, Milner et al. [44] demonstrated that bisection points moved towards the side where attention was directed. Similar results have been reported by a number of others (e.g.

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Ref. [21,43,54]). While there is some suggestion that these cueing effects are perceptual rather than attentional [22,34], Nicholls and Roberts [45] demonstrated that cueing effects persist when the cue is no longer physically present. Leftward attentional biases during line bisection could be generated by asymmetric hemispheric activation. This notion stems from Kinsbourne [29], who found that unilateral activation of a hemisphere (usually the left) generated an attentional bias to the contralateral hemispace. Thus, for tasks such as length estimation and luminance judgments, it is possible that the right hemisphere is activated more than the left, leading to a bias of attention to the left hemispace. While some support exists for an effect of unilateral activation [6,8,59,64], a number of researchers have reported no [47] or little [40] effect. As an alternative to activation accounts of the leftward bias, Nicholls and Roberts [45] argued that the attentional bias was driven by asymmetries in the neural mechanisms that control attention, which are independent of task-related activation. Heilman et al. [24] have suggested that the right hemisphere plays a dominant role in spatial attention; a proposal supported by unilateral lesion [35] and neuroimaging [13] research. Besides being dominant for spatial attention, Heilman et al. [23] suggested that the right hemisphere is responsible for the deployment of attention in the left and right hemispaces, whereas the left hemisphere only attends to the contralateral hemispace. Given that efferent and afferent connections to the hemispheres are primarily contralateral, it is possible that right hemisphere specialization for attention leads to a general bias of attention to the left hemispace. This bias may be particularly strong for stimuli that cross from left to right and thus require a contribution from the right hemisphere, which can simultaneously attend to both sides of the stimulus. In addition to the leftward biases found for horizontally stimuli, there also appears to be an upward bias for vertically aligned stimuli. Drain and Reuter-Lorenz [14] asked participants to judge the position of a break in vertical lines and found that bisections were shifted upwards from the true midpoint of the line. Upward biases for line bisection tasks have been reported by a number of others [6,39,63]. The magnitude of the upward bias relative to the leftward bias is the subject of some controversy. While some researchers have reported that the leftward bias is greater than the upward bias [6,39], others have reported the opposite [63]. Drain and Reuter-Lorenz [14] demonstrated that the upward bias is attentional in origin and have linked it to asymmetries in the relative activation of the dorsal and ventral visual pathways. In a review of the function and physiology of the upper and lower visual fields, Previc [52] suggested that the upper visual field has a stronger input into the ventral pathway and vice versa for the lower visual field. Bearing in mind that the ventral pathway is implicated in object recognition processes, Drain and Reuter-Lorenz proposed that the line bisection task, because it is object-based, activated the ventral stream, causing an upward attentional

bias. It can be seen that the model proposed by Drain and Reuter-Lorenz shares much in common with the hemispheric activation model put forward by Kinsbourne [29]. An alternative explanation for the upward bias has been proposed by Jeerakathil and Kirk [25]. They asked participants to bisect vertical, horizontal and radially oriented lines that had one end labeled ‘top’ and the other, ‘bottom’. By opposing or combining the retinotopic and labeled coordinates, they were able to gauge the relative importance of physiological mechanisms related to the upper/lower visual fields and internal object-centered representations. Jeerakathil and Kirk found that labeling affected the upward bias and suggested that the results reflected a general tendency to attend more to the upper features of an object. This bias was proposed to exist because the upper features of an object (for example, the face in relation to the body) generally contain more information than the lower features. It can be seen that, while horizontal and vertical perceptual biases share a number of features, they also have some unique characteristics. Bearing this in mind, the present study sought to gain an insight into the cognitive and neural bases for free-viewing perceptual asymmetries by comparing and contrasting the biases. A number of studies have investigated perceptual asymmetries for vertical, horizontal and radial lines for normal and spatial neglect populations within the one experiment (e.g. [1,19,20,27,28,50]). The present set of experiments was different because the vertical and horizontal biases were made to be concordant or discordant by rotating them around an axis parallel to the participant’s sagittal plane. Using this technique, two experiments examined the interdependence between horizontal and vertical biases in normal participants and in righthemisphere-lesioned patients with chronic attentional biases (spatial neglect).

2. Experiment 1 McCourt and Olafson [39] examined the relationship between vertical and horizontal pseudoneglect by presenting pre-transected lines in four orientations: (1) horizontal, (2) vertical, (3) + 45j oblique (relative to vertical) and (4) 45j oblique (relative to vertical). They predicted that, if performance for the oblique lines is the algebraic sum of the horizontal and vertical biases, the biases should be additive in the 45j oblique condition and should cancel each other in the + 45j oblique condition. The effect of response context was investigated by asking participants to respond either left/right or up/down in the oblique conditions. McCourt and Olafson found the expected leftward and upward biases for horizontal and vertical lines, respectively. For the 45j oblique lines, the bias depended upon decision type. When the decision was labeled as ‘up/down’, the leftward and upward biases were additive. An additive pattern was not observed, however, when discriminations were made within a ‘left/right’ context. For + 45j oblique

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lines, there was no evidence that leftward and upward biases cancelled one another for either decision context. Because vertical and horizontal biases were neither separable nor additive, McCourt and Olafson concluded that leftward and upward biases reflected the operation of independent attentional mechanisms that operated in one dimension only. The present study sought to re-examine the issue of the interdependence between biases in the vertical and horizontal planes. Perceptual biases were induced using the grayscales task [46]. This task (see Fig. 1) requires a judgment of relative luminance between two horizontal rectangles, which change from black on one side to white on the other [35]. The stimuli within each pair are arranged so that they are left/right mirror reversals of each other. Thus, one is dark on the left whereas the other is dark on the right. Despite being equiluminant overall, participants tend to select the stimulus that is dark on the left as being the darker of the pair [46,47,62]. This asymmetry is not restricted to judgments of darkness; it has also been found when participants are asked to select the lighter stimulus. In this case, judgments are biased toward the stimulus that is lighter on the left [46]. Hence, it would appear that the leftward features of the stimuli are more salient than those of the right. The grayscales task shares much in common with traditional line bisection tasks [45], and provides a very sensitive measure of attentional bias in unilateral lesion patients [36]. Like McCourt and Olafson [39], the present study presented stimuli in four orientations (horizontal, vertical, 45j oblique, and + 45j oblique). McCourt and Olafson manipulated the context in which discriminations were made for oblique lines. For half of the trials, participants indicated whether the transector was to the left or right of the midline. For the other half of trials, an upper/lower response was used. We believe this procedure may have militated against an additive pattern of results for the oblique lines. The use of one decision context (e.g. left/right) may have selectively inhibited the activation of the orthogonal attentional system (e.g. up/down). Potential conflicts between response context and the activation of both coordinate systems were circumvented in the present study by ensuring that the mapping of stimulus and response was compatible. To achieve this, a two-button panel was mounted below the display and was rotated between the different stimulus orientations so that the buttons mapped onto the stimuli. We predicted a leftward bias for horizontal stimuli and an upward bias for vertical stimuli. Some researchers (e.g. Ref.

Fig. 1. An example of the grayscales stimuli against a white background. In this case, the stimuli within the pair are equiluminant.

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[63]) have shown that the upward bias is stronger than the leftward bias, while others (e.g. Ref. [39]) have found the opposite. For + 45j oblique lines, we predicted that the upward and leftward biases would oppose one another, resulting in no overall bias. For 45j oblique lines, we expected an additive pattern whereby the bias would be equal to the algebraic sum of the leftward and upward biases. In addition to measures of response bias, reaction time (RT) was also measured. Research with horizontal grayscales [46] has demonstrated that leftward response biases are faster than rightward responses. In the present study, we predicted a pattern of RT asymmetries that corroborated the response bias data. To investigate the independence of the mechanisms that give rise to the biases, a series of regression analyses was conducted. The analysis allows us to establish the degree to which biases in the oblique conditions are dependent upon biases in the vertical and horizontal orientations. The direction of causality can be deduced by examining the correlation between the vertical and horizontal biases. If a single cognitive mechanism (i.e. an upper/left bias) gives rise to the vertical and horizontal biases, the vertical and horizontal biases should be correlated. Conversely, if independent vertical and horizontal biases give rise to the upper/left bias, one would predict no correlation between the primary biases.

3. Method 3.1. Participants Twenty-four (m = 5, f = 19) undergraduate students participated in the experiments as part of their course requirements. The modal age of participants was 18 years and all were right-handed, as determined by the Edinburgh Inventory [48]. Participants had normal, or corrected to normal, visual acuity in both eyes, and were naı¨ve in relation to the aims and expected outcomes of the study. 3.2. Apparatus Stimulus presentations were controlled with a PC interfaced with a digital input/output card with an on-board 1.0 ms timer (Blue Chip Technology, DCM-16). Stimuli were presented on a 280  210-mm (480  360 pixels) VGA monitor. The monitor was mounted in a rotating drum, which allowed it to be turned around an axis parallel to the participant’s sagittal plane. A degaussing wand was used to reset the monitor after it was rotated. Participants responded using a two-button response panel. The panel was mounted below the center of the monitor on a surface facing the participant. The response panel was mounted with Velcro so it could be realigned following stimulus rotation. A chin rest was used to stabilize participants’ heads. A video camera and monitor were used to ensure that participants kept their heads still throughout the experiment.

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3.3. Stimuli Each grayscales stimulus was defined by a thin black rectangle and displayed against a light gray background. Stimuli were viewed at a distance of 500 mm and presented at two different lengths: 132 and 154 mm. For each trial, two stimuli, which changed from black at one end to white at the other end, were presented simultaneously (see Fig. 1). The stimuli were arranged so that they were left – right mirror reversals of each other, i.e. if one stimulus was black on the left side, the other stimulus was black on the right side. The horizontal midline of each stimulus pair was aligned with the center of the screen, while the vertical midline of the upper and lower stimuli were placed 29 mm above and below the center of the screen, respectively. Each stimulus was 49 pixels (22 mm) high and was divided into 50 horizontal increments, with the size of each increment varying according to the length of the stimulus. Each stimulus changed in luminance from one end to the other by adjusting the ratio of white to black pixels within each increment. For example, at the white end of the stimulus, the first increment contained no black pixels, the second increment contained one black pixel per vertical line, the third increment two black pixels per line and so on, until the final increment contained no white pixels resulting in a completely black section. The vertical position of the pixels within each line was randomized to create the impression of a smooth change in brightness and make each stimulus within a pair appear slightly different. In previous versions of the grayscales task (e.g. Ref. [46]), the stimuli were equiluminant. In this version of the task, the relative luminance of the stimuli was adjusted so that one stimulus was slightly darker than the other. Changes in luminance were made by adding black pixels to one stimulus while adding white pixels to the other. The sites at which pixels were added within the stimuli was random, with the constraint that the site was opposite in polarity to the pixel being added. Changes in luminance were symmetrical between the stimuli. So, if the upper stimulus was darker by 20 pixels, the lower stimulus was lighter by 20 pixels: resulting in an overall luminance difference of 40 pixels. In the present study, the stimuli differed from one another by 200, 160 or 120 pixels. Pretests revealed that these levels of luminance difference yielded error levels around 40%. This level of error was chosen because it allowed a meaningful measure of accuracy to be gained while allowing sufficient errors for response biases to occur. Printable and computerized versions of the grayscales test are freely available at: http:// www.psych.unimelb.edu.au/research/laterality/greyscales. html. 3.4. Procedure The testing session lasted 50 min and was conducted in a quiet and well-lit room. A closed-circuit video camera was

focused on the participant’s face and monitored by the experimenter. The four stimulus orientations were run in separate blocks. In the horizontal condition, the monitor was left in its normal position, so that the longer axis of the screen was horizontal. The button panel was turned so that the buttons were arranged vertically. Participants pressed the upper button to indicate that the upper stimulus was darker and vice versa for the lower button. In the vertical condition, the screen was turned 90j clockwise so that the screen’s longer axis was vertical. The button panel was also turned 90j clockwise so that the buttons were arranged horizontally. To select the left or right stimuli as darker, participants pressed the left or right buttons, respectively. In the + 45j oblique condition, the monitor was rotated so that it was 45j clockwise from the vertical. The button panel was turned 45j clockwise from the vertical so that the buttons mapped onto the stimuli. In the 45j oblique conditions, the monitor and button-panel was turned 45j anticlockwise from the vertical. The order in which the blocks were run was balanced between participants. Each block contained 96 trials. The factors of length (132 or 154 mm), stimulus configuration (original or mirror-reversed), the stimulus that was overall darker and luminance difference were factorially balanced within the blocks. Each trial began with the presentation of the grayscales stimuli. Participants determined which stimulus within the pair was darker overall and pressed the button that mapped onto the stimulus to indicate their response. Half of the subjects used their left index finger to respond, while the other half used their right index finger. If participants failed to respond within 4000 ms, the trial was rejected and replaced later in the block with a trial of an identical configuration. Participants were encouraged to respond more quickly when trials were rejected. Following a response, the screen was cleared and a new trial was begun in 1500 ms. Before the experimental trials, participants were given 24 practice trials to familiarize them with the task. The luminance difference of these trials was set at a high level to facilitate learning.

4. Results 4.1. Error Percent error was calculated by summing trials where participants failed to detect correctly the darker stimulus. This sum was then converted to a percentage of the total number of trials. The error data were analyzed with a repeated measures analysis of variance (ANOVA) with luminance-difference (200, 160 or 120 pixels) and stimulus orientation (horizontal, vertical, + 45j oblique, 45j oblique) as within participants factors. Error rate rose progressively as luminance-difference declined (39.0%, 41.8% and 42.9%, respectively), resulting in a significant

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main effect of luminance-difference [ F(2,46) =6.7, p < 0.005]. There was no effect of stimulus orientation [ F(2,46) = 0.5, ns], and no interaction between the factors.

p < 0.05] conditions only. The ANOVA showed no significant effect of stimulus length [ F(1,23) = 0.1, ns] and no significant interaction between the factors.

4.2. Response bias

4.3. Reaction time

Responses were categorized according to the stimulus that was selected and the quadrant in which the stimulus was darker. Thus, for horizontal presentations, selection of the stimulus that was dark on the right was classified as a ‘right’ response. For + 45j oblique presentations, selection of the stimulus that was darker in the left-lower quadrant was scored as a ‘left-lower’ response. The number of responses made within each of the two alternatives for each of the stimulus orientations is shown in Table 1. A measure of response bias was calculated by subtracting the response numerator from the response denominator within each of the stimulus orientations. For example, for horizontal stimulus orientations, ‘left’ responses were subtracted from ‘right’ responses. This figure was then converted to a percentage of the total number of trials. Response bias scores therefore range from 100 to + 100. Scores approaching zero indicate no response bias. For horizontal, vertical and 45j oblique stimulus orientations, a negative score indicates a leftward and/or an upward bias. For + 45j oblique stimulus orientations, a negative score indicates a lower-left bias. The response bias data are shown in Table 1. Inspection of Table 1 reveals that response biases were negative for the horizontal, vertical and 45j oblique orientations, but not for + 45j oblique orientations. A series of t-tests revealed that response bias scores were significantly different from zero for the horizontal [t(23)= 3.2, p < 0.005], vertical [t(23) = 2.4, p < 0.05] and 45j oblique [t(23) = 4.3, p < 0.001] stimulus orientations, but not for + 45j oblique stimulus orientations [t(23) = 0.4, ns]. The response bias data were analyzed with a repeated measures ANOVA with stimulus orientation and length as within-participants factors. Stimulus orientation had a significant effect on response bias [ F(3,69) = 4.3, p < 0.005]. Post-hoc t-tests revealed significant differences between the + 45j oblique and 45j oblique [t(23) = 2.9, p < 0.01], + 45j oblique and horizontal [t(23) = 3.3, p < 0.005] and vertical and 45j oblique [t(23) = 2.6,

Mean reaction times (RT) were calculated within each of the conditions. The effect of outliers was controlled by the experimental procedure, which rejected and replaced trials with RTs greater than 4000 ms. In one condition, where a participant failed to make a response, the mean RT for the condition was substituted. The RT data (shown in Table 1) were analyzed with an ANOVA with stimulus orientation, length and response-type (left, right) as within participants factors. Reaction times were 16 ms faster for short compared to long stimuli, resulting in a significant effect of stimulus length [ F(1,23) = 4.4, p < 0.05]. There was a significant effect of response-type [ F(1,23) = 11.1, p < 0.005], but no effect of stimulus orientation [ F(3,69) = 0.6, ns]. The effect of response-type was influenced by stimulus orientation [ F(3,69) = 3.5, p < 0.05]. A series of post-hoc t-tests were conducted on the effect of response-type for each stimulus orientation (see Table 1). Consistent with the response bias results, the tests revealed that (1) left responses were faster than right responses in the horizontal condition, (2) upper responses were faster than lower responses in the vertical condition and (3) left-upper responses were faster than right-lower responses in the 45j oblique condition. There was no effect of response-type for + 45j oblique stimulus orientations. No other interactions in the ANOVA were statistically significant. 4.4. Regression analyses Regression analyses were conducted to examine the degree to which the bias in the + 45j and 45j oblique conditions was determined by an individual’s bias in the vertical and horizontal conditions. Table 2 shows the effect of entering the horizontal and vertical components separately and combined for each of the oblique conditions. For the + 45j condition, significant models emerged for the horizontal and vertical components separately and

Table 1 Response bias and reaction time data for the different stimulus orientations used in Experiment 1 Stimulus orientation

Response type

Number of responses

Horizontal

Left Right Upper Lower Lower/left Upper/right Upper/left Lower/right

61.0 35.0 58.0 38.0 46.4 49.6 64.9 31.1

Vertical + 45j oblique 45j oblique

Response bias (S.D.) 27.1 (8.6) 20.7 (8.8) 3.30 (9.0) 35.1 (8.1)

Reaction time (S.D.) 1127 (53.5) 1166 (56.2) 1115 (48.6) 1180 (44.1) 1191 (51.1) 1168 (49.6) 1123 (54.3) 1209 (53.8)

t-test of RT data t(23) = 2.1, p < 0.05 t(23) = 2.4, p < 0.05 t(23) = 0.7, ns t(23) = 3.7, p < 0.05

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Table 2 Regression analyses between the oblique orientations and the horizontal and vertical conditions Stimulus orientation

Enter

F

df

p

Adj. R2

+ 45j oblique

Horizontal Vertical Horizontal + Vertical Horizontal Vertical Horizontal + Vertical Vertical

5.4 8.0 9.2 3.0 34.4 27.8 0.1

(1,22) (1,22) (2,21) (1,22) (1,22) (2,21) (1,22)

< 0.05 < 0.01 < 0.005 < 0.1 < 0.001 < 0.001 ns

0.16 0.23 0.42 0.08 0.59 0.70 0.00

45j oblique

Horizontal

combined. The explanatory power (R2) of the models was maximized when the biases for the horizontal and vertical vectors were combined. For the 45j condition, significant models emerged for the vertical component and when the vertical and horizontal components were combined. An association between horizontal and 45j biases approached significance. The explanatory power (R2) of the models was maximized when the biases for the horizontal and vertical vectors were combined. Analysis of the biases for the horizontal and vertical conditions revealed no relationship between them.

5. Discussion Experiment 1 measured the degree of perceptual bias in luminance gradients as a function of their orientation with respect to the viewer. The average error rate (41.2%) fell within the targeted level of performance. Error levels were set at this relatively high rate to provide sufficient freedom for response biases to occur. One might argue that participants were operating at chance at these high levels of error. However, the fact that error rate rose as the difference in luminance between the stimuli declined militates against this proposition. Error rate was not affected by changes in stimulus orientation. Thus, any changes observed for response bias between stimulus orientations cannot be attributed to changes in threshold. As expected, a leftward response bias was observed for horizontal stimuli. On average, participants selected the stimulus that was dark on the left side 63% of the time. The leftward bias in the horizontal condition was accompanied by a significant 39 ms RT advantage for leftward responses. The leftward response bias and RT advantage observed in Experiment 1 is in line with the biases previously reported for the grayscales task [45 – 47,62]. For vertical stimuli, participants selected the stimulus that was darker at the top 60.4% of the time. This response bias was accompanied by a 65-ms RT advantage in favor of upward responses. While an upward bias has been reported previously for line bisection tasks [6,14,39,63], it has not been shown before for luminance discrimination, as measured by the grayscales task. Post-hoc tests revealed

that the magnitude of the upward and leftward biases did not differ. The lack of difference between the conditions reflects the current state of the literature surrounding this issue; with some studies reporting greater leftward biases [6,39] and others reporting greater upward biases [63]. The discrepancies in the relative magnitude of the biases could be related to the different tasks that are employed to generate free-viewing perceptual asymmetries, with some tasks being more sensitive than others. The discrepancy could also reflect the fact that upward and leftward biases involve the operation of autonomous cognitive/neural processes which are affected in different ways by the demands of a particular task (see below for further discussion of this point). There was no difference in the frequency of upper/ right and lower/left responses in the + 45j oblique condition, and no difference in RT between these two conditions. Thus, participants appear to devote equal amounts of attention between the upper/right and lower/ left hemispaces. The symmetry observed in this condition most likely reflects an opposition of leftward and upward biases. Thus, any bias toward the left side of the stimulus was attenuated because the left side was located in the lower visual field (and vice versa for biases toward the upper visual field). The fact that the biases opposed each other symmetrically adds further support to the proposition that leftward and upward biases are of a similar magnitude. A strong response bias (67.6%) towards upper/left responses was observed for the 45j oblique condition. This response bias was complemented by an RT advantage of 86 ms in favor of upper/left responses. Thus, there was a strong attentional bias towards the upper/left space and ‘neglect’ of the lower/right space. If this bias reflects the combined operation of upward and leftward biases, one would expect the 45j oblique bias to be greater than the constituent biases. In partial support of this proposition, the upper/left bias was significantly stronger than the upward bias, but not the leftward bias. Thus, the data provide mixed support for an additive effect for the 45j oblique condition. The weak additive effect may reflect a threshold beyond which perceptual biases do not readily exceed. The patterns of results observed for the + 45j and 45j oblique conditions both suggest an additive effect and support the proposition that upward and leftward biases operate within a single two-dimensional plane. The results contrast with McCourt and Olafson’s [39] conclusion that biases in the vertical and horizontal axes were controlled by ‘independent and largely one-dimensional mechanisms’ (p. 378). McCourt and Olafson may have failed to observe an additive effect because they framed responses within either an upper/lower or left/right decision context. Activation of an attentional system aligned to a single axis may have selectively discouraged the use of the orthogonal system. The present study avoided problems associated with response context by

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mapping the response panel onto the stimulus array for each of the stimulus orientation conditions. To determine the interdependence between the biases in the oblique conditions and horizontal and vertical biases, regression analyses were conducted. The combined effects of horizontal and vertical biases accounted for 42% and 70% of the variation in the + 45j oblique and 45j oblique conditions, respectively. In both cases, the predictive power obtained by combining the vertical and horizontal components was greater than the predictive power of either of the constituent biases alone. The relation between the oblique and vertical and horizontal biases can be interpreted in two ways. First, it is possible there is a single bias toward the upper/left space, which has vertical and horizontal vectors. That is, a bias toward the upper/left space would cause a leftward bias for horizontal stimuli and an upward bias for vertical stimuli. If the vertical and horizontal biases stem from a single cognitive/neural process, however, the vertical and horizontal biases should be related. Regression analysis demonstrated that this was not the case. An alternative explanation is that the vertical and horizontal biases reflect the operation of distinct cognitive/neural processes. These orthogonal biases operate in a vectorial fashion to produce a particularly strong attentional bias away from the lower/ right towards the upper/left space. The lack of correlation between the vertical and horizontal biases supports this latter proposition. In summary, it appears that the leftward and upward biases are the product of separate cognitive and/or neural mechanisms. Despite this, the leftward and upward biases combine in a vectorial fashion to produce a strong bias away from the lower/right space toward the upper/left space. 5.1. Experiment 2 The second experiment examined the interrelation between vertical and horizontal attentional biases in spatial neglect patients. Such patients fail to perceive or respond to sensory stimuli arising from the side of space opposite to their lesioned (typically right) hemisphere, particularly when the damage involves the posterior parietal cortex [35]. In addition to left neglect, altitudinal neglect has been observed in patients with posterior cortical damage. Rapc-

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sak et al. [53] found that a patient with bilateral parietal/ occipital infarctions consistently bisected rods above their true midpoint. Altitudinal neglect, whereby patients make bisections below the true center have also been observed for a patient with bilateral temporal lesions [60]. Drain and Reuter-Lorenz [14] argue that the critical difference between patients who neglect upper or lower space is related to the locus of the lesion. Lesions to occipito-parietal regions damage the dorsal visual system, which represents the lower visual field more strongly, and thus causes neglect in this region. In contrast, damage to occipitotemporal region affects the ventral stream, and is more likely to disrupt representations of the upper visual field. The right hemisphere appears to play a particularly important role in altitudinal neglect. Pitzalis et al. [49] required 100 patients with right parietal damage and neglect to cancel 21 lines distributed across a page. After dividing the page into four quadrants, Pitzalis et al. observed that most omissions were made in the lower-left quadrant of the page. Halligan and Marshall [18] have also observed that lower neglect was stronger in patients with right hemisphere damage than in those with left hemisphere damage. Marshall and Halligan [33] and Burnett-Stuart et al. [9] investigated the relation between horizontal and vertical attentional biases in patients with right hemisphere damage and left spatial neglect. Patients bisected lines that were oriented vertically (0j), horizontally (90j) and at six intermediate orientations (22.5j, 45j, 67.5j, 112.5j, 135j and 157.5j). The experiments produced a number of interesting findings. First, in all but one of the patients, the horizontal neglect was markedly stronger than the vertical neglect. Second, the oblique orientations produced biases that were intermediate in value between the vertical and horizontal biases. Thus, there was no sign of an additive effect between the vertical and horizontal biases. For patients neglecting the lower and left hemispaces, one might have predicted a particularly strong bias for the + 45j oblique orientation where rightward and upward biases combine. Conversely, for the 45j oblique condition, a weak bias would be predicted when the rightward and upward biases cancel each other. The experiments by Marshall et al. may have failed to observe an additive effect between the horizontal and vertical biases because the horizontal biases were so much stronger than the vertical biases. That is, strong leftward

Table 3 Personal details and clinical test performances for right hemisphere patients in Experiment 2 Patient

Sex

Age (years)

Tested (months post-stroke)

Albert’s lines

Star cancellation

Feature search

Conjunction search

1 2 3 4

F M M M

53 56 54 67

14 7 3 7

0 12.5 2.5 40

11 0 18 2

5 0 5 0

27 41 9 9

Scores for clinical tests represent the percentage of visual targets omitted.

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neglect may have swamped the weaker altitudinal bias. In the current study, we hoped to provide a more sensitive test of the additive model by applying the techniques used in Experiment 1 to a group of right-hemisphere-lesioned patients with left spatial neglect. In line with the data collected by Mattingley et al. [36], we predicted that patients would show a strong rightward bias for the grayscales task in the horizontal condition. Occipito-parietal damage to the right hemisphere was a common feature of all patients.

However, the damage was also diffused and sometimes extended to the temporal regions. As such, the patients do not provide an ideal means of testing the dorsal/ventral model of altitudinal neglect [14]. Nevertheless, given the preponderance of occipito-parietal (dorsal) damage, we expected that patients would tend to neglect the lower hemispace and therefore select the stimulus that was darker at the top. In line with the results of previous studies [9,33], altitudinal neglect was expected to be weaker than leftward

Fig. 2. Lesion reconstructions (shown in red) for right hemisphere patients tested in Experiment 2. For Patients 1 – 3, lesioned areas are superimposed on a magnetic resonance image (MRI) of a standard normal brain, based on computerised tomographic (CT) scans obtained for each individual. For Patient 4, the lesioned area is depicted on the patient’s own MRI scan. Numbers in red above each horizontal slice represent z-coordinates in Talairach space [61]. Lesions were reconstructed using MRIcro software [56].

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neglect. If the vertical and horizontal biases are additive, there should be a particularly strong right/upper bias in the + 45j oblique condition and little or no bias in the 45j oblique condition. Conversely, if the biases are not additive, there should be no difference in the bias between the oblique conditions.

6. Method 6.1. Participants Four patients with right hemisphere lesions were tested (see Table 3). All patients were right-handed, and all had full visual fields, as assessed by the clinical method of confrontation [55]. Spatial neglect was assessed using a battery of standard clinical tests, which included Albert’s line cancellation test [2], the star cancellation task from the Behavioral Inattention Test [65], and the feature- and conjunction-search tasks from the Balloons Test [15]. All these tests require the patient to search for and cancel visual targets scattered on a sheet of paper that has been centered at the body midline. As shown in Table 3, all four patients showed evidence of left neglect on at least one of the clinical measures. Patients 1 –3 had suffered a stroke involving the vascular territory of the right middle cerebral artery; Patient 4 suffered a stroke in the territory of the posterior cerebral artery. Reconstructions of their lesions are shown in Fig. 2. 6.2. Apparatus The grayscales stimuli were printed onto 40 sheets of white A4 paper and laminated. Stimulus identification and absolute orientation were marked on the back of the cards. The cards were held in a display device, which positioned the cards so that they faced directly toward the patient. The device allowed the topmost card to be removed from the pack to reveal the card underneath. Hence, each trial began with the removal of the previous stimulus. The display panel was mounted on an axle that operated parallel to the patient’s sagittal plane. The axle allowed the stimuli to be rotated between the four orientations (vertical, horizontal, + 45j oblique, 45j oblique). A chin rest was used to prevent patients from tilting their heads to match the orientation of the stimuli. 6.3. Stimuli

6.4. Procedure Patients were tested either in hospital or at their home. A total of 160 trials were given to each patient. Stimulus orientation was manipulated between four blocks of 40 trials. The four orientations (horizontal, vertical, + 45j oblique, 45j oblique) were achieved by rotating the display device. The order in which the orientations were presented was pseudo-randomly manipulated between patients. Within blocks, the factors of length and stimulus configuration (original or mirror-reversed) were balanced and presented in a random order. Before the experimental trials, the task was explained to the patients and they were given a few practice trials. Our previous research using the grayscales has shown that patients readily understand the nature of the task [35,36]. Patients made their response by pointing to the stimulus that they perceived as being darker overall. They were encouraged to take their time and inspect the stimuli thoroughly. Besides these points, the procedure was fundamentally the same as that described for Experiment 1.

7. Results 7.1. Response bias Response bias data were categorized using the procedure described for Experiment 1. Data from each patient are shown in Table 4. Inspection of Table 4 reveals that all patients showed a rightward bias for horizontal stimuli. Three of the four patients also showed an upward bias for vertical stimuli, while patient 2 showed no bias. For + 45j oblique orientations, all participants showed a strong rightupper bias. For 45j oblique orientations, there was a trend for a right-lower bias for all patients except patient 3, who showed a bias in the opposite direction. Average response biases were calculated using the procedure described for Experiment 1 (see Table 5). To test whether the bias was significant within each of the orientation conditions, a series of single-sample t-tests was conducted (see Table 5). Patients selected the stimulus that was dark on the right significantly more than the left in the horizontal condi-

Table 4 Number of responses made by neglect patients within each of the response categories and stimulus orientations Stimulus Horizontal

The grayscales were generated using the principles described in Experiment 1. The stimuli within a pair were 22 mm high and were either 105 or 126 mm long. The centers of the stimuli were separated by a vertical distance of 55 mm. Stimuli were viewed from a distance of approximately 500 mm. Like earlier versions of the grayscales task [46], the stimuli within a pair were equiluminant.

297

Vertical

+ 45j oblique

45j oblique

Response Left Right Upper Lower Leftlower

Rightupper

Leftupper

Rightlower

Patient 1 2 3 4

37 39 39 39

13 9 24 2

27 31 16 38

0 0 10 7

40 40 30 33

34 19 31 27

6 21 9 13

3 1 1 1

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Table 5 Response bias data across the different stimulus orientations for the neglect patients Stimulus orientation

Response type

Number of responses

Horizontal

Left Right Upper Lower Lower/left

4.3 35.7 27.7 12.3 1.5

Upper/right Upper/left

38.5 12.0

92.5 (5)

t(3) = 37, p < 0.001

Lower/right

28.0

40.0 (46)

t(3) = 1.7, ns

Vertical + 45j oblique 45j oblique

Response bias

t-test comparing bias with zero

78.7 (25)

t(3) = 6.2, p < 0.01

38.8 (32)

t(3) = 2.4, p < 0.1

tion. For vertical stimuli, there was a trend for a significant upward bias. There was a particularly strong right-upper bias for + 45j oblique orientations. In contrast, no response bias was observed for 45j oblique orientations.

8. Discussion Despite the small sample used in the present experiment, a clear pattern can be discerned in the data. For horizontal stimuli, participants selected the stimulus that was dark on the right 89% of the time, resulting in a significant rightward bias overall. This strong rightward bias is consistent with that reported previously for the grayscales task in right hemisphere patients [35,36] and appears to be greater in magnitude than the leftward bias shown by normal participants (63% in Experiment 1). For the vertical stimuli, three of the patients showed an upward bias, while the fourth showed no bias. On average, patients selected the stimulus that was dark on the top 69% of the time. Despite being slightly larger than the upward bias reported for normal participants in Experiment 1 (60%), the average bias only reached marginal significance ( p < 0.1). The reduced magnitude of the vertical bias relative to the horizontal bias is in line with that reported by other researchers [9,33]. The relatively weak vertical bias can be interpreted in two ways. First, it may reflect a pathological disturbance in the distribution of altitudinal attention like that reported by Rapcsak et al. [53]. The preponderance of patients with damage to right occipito-parietal region also provides some support for the notion that damage to the dorsal, but not ventral, pathways give rise to neglect of the lower hemispace [14]. A second possibility that cannot be dismissed, however, is that the relatively moderate altitudinal bias reflects a non-pathological asymmetry in attention—like that seen in normal participants. It is certainly true that the upward bias does not approach the chronic rightward bias seen in neglect. If this latter proposition were correct, it would suggest that the neural mechanisms that control vertical and horizontal attentional biases have

a separate locus. Thus, damage to one coordinate system will not necessarily affect the other. All four patients showed a right-upper bias for the + 45j oblique condition. On average, participants selected the stimulus that was dark in the upper/right quadrant 96% of the time. This bias was highly significant. The small number of patients precludes the possibility of inferential statistics to test for differences between the experimental conditions. However, inspection of the data reveals that the upper/right bias in the + 45j oblique condition was slightly stronger than the right bias in the horizontal condition and markedly stronger than the upward bias in the vertical condition. The fact that oblique bias was not the algebraic sum of the constituent biases most likely reflects the operation of a ceiling effect. Thus, the pattern provides some support for the hypothesis that the rightward and upward biases united to produce a stronger upper/right bias in the + 45j oblique condition. In the 45j oblique condition, three patients made more lower/right than upper/left responses. However, the lower/ right bias failed to reach statistical significance. The weak bias observed for the 45j oblique condition most likely reflects the opposition of rightward and upward biases. It is interesting to note, however, that the direction of the bias (albeit non-significant) was towards ‘right’ rather than ‘up’ responses. The direction of the bias is in line with the data collected in this study and by Marshall and Halligan [33] showing that rightward biases are stronger than upward biases in neglect. The data support the proposition that vertical and horizontal attentional biases operate within a single two-dimensional space. In this regard, the results are very similar to those reported in Experiment 1 and support the suggestion that normal pseudoneglect and clinical neglect share many features [26]. However, the additive pattern observed in the current study conflicts with the results reported by BurnettStuart et al. [9] and Marshall and Halligan [33]. It is possible that they failed to find an additive effect between vertical and horizontal biases because the horizontal bias (due to left neglect) was so much stronger than the vertical bias. It is also possible that response protocols may have affected the results. Marshall and Halligan [33] used a manual line bisection procedure, whereas the present study asked participants to make a forced-choice discrimination and point to the stimulus that was darker. The manual bisection procedure used by Mashall and Halligan may have emphasized the adoption of motor biases aligned to the vertical and horizontal dimensions. In contrast, the present procedure emphasized the perceptual aspects of neglect, which may have facilitated the production of biases not tied to the cardinal axes.

9. General discussion The leftward bias observed for the horizontal grayscales task in normal participants is in line with a growing body of

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research demonstrating that participants overestimate the leftward features of a stimulus (e.g. [12,31,37,38,40,51]). In accord with the clinical literature [34,35], patients with neglect showed a very strong bias in the opposite direction for the grayscales task. Both the neglect and normal participants showed an upward bias for the vertical version of the grayscales task (though this just failed to reach significance in the clinical group). While some researchers have reported an upward bias for normal participants (e.g. [39]), the bias is typically weak and many researchers only observe a trend (e.g. Ref. [6]). The fact that a significant upward bias was observed with normal participants supports the proposition that the grayscales is a particularly sensitive measure of freeviewing perceptual asymmetries [36]. The first experiment demonstrated that the vertical and horizontal biases cooperate with one another in the 45j condition to produce a strong perceptual bias toward the upper/left quadrant and ‘neglect’ of the lower/right quadrant. In the + 45j condition, leftward and upward biases counteracted each other, resulting in equal amounts of attention being devoted to the lower/left and upper/right quadrants. Fig. 3 illustrates the net effect of these biases, with a shift of responses away from the lower/right quadrant toward the upper/left. Regression analyses demonstrated that biases in the oblique orientations were determined by performance in the vertical and horizontal dimensions. Patients with neglect showed an analogous trend. In this case, however, attention was biased toward the upper/right quadrant, while the lower/left quadrant was the most neg-

Fig. 3. Graph representing the biases for the different orientations for normal and neglect populations. Scores reflect the average percentage of the two responses made within a particular orientation. Inspection of the graph reveals a moderate shift away from the lower/right quadrant towards the upper/left quadrant for normal participants. Neglect patients show a strong shift away from the lower/left quadrant towards the upper right.

299

lected (see Fig. 3). Thus, the vertical and horizontal biases evident in pseudoneglect and clinical neglect both appear to be additive and to operate within a single two-dimensional space. The similarity observed between pseudoneglect and clinical neglect supports the proposition that the two phenomena share many common features and are ‘‘twin manifestations of parameter changes in a unitary set of underlying hemispheric attentional asymmetries’’ (Ref. [38], p. 853). Shelton et al. [60] have reported that attention in neglect patients is distributed along three orthogonal axes (vertical, horizontal and radial). It remains to be determined whether the oblique biases observed in the present study extend to the third dimension of extrapersonal space located along the distal/proximal axis. A number of investigators have reported that visually presented radial lines are misbisected toward their distal end in normal participants [17,60]. Bearing this in mind, it could be predicted that a particularly strong perceptual asymmetry would be observed for a stimulus that was oriented at 45j in the x,y plane and which receded distally toward the upper/left end in the z axis. There are a number of reasons to suspect that the vertical and horizontal biases evident in this study are governed by relatively independent cognitive/neural mechanisms. First, analysis of the association between upward and leftward biases revealed no correlation between them. Second, while some similarities in the type of mechanism that leads to vertical and horizontal biases were noted in the introduction, the mechanisms themselves are invariably different. Thus, vertical and horizontal biases may both be the result of an attentional bias brought about by changes in activation. However, horizontal biases are brought about by asymmetries in activation between the hemispheres [29], whereas vertical biases may be the product of asymmetries in activation between the ventral and dorsal streams [14]. Similarly, explanations of why the asymmetries exist are quite different. Vertical biases in attention are often explained with reference to their ecological significance. Thus, we may pay more attention to the lower visual field because it is associated with peri-personal space [52] or the upper visual field because the top of an object contains more information [25]. No explanation of the ecological significance of a leftward bias has been put forward—presumably because left and right are defined in terms of the observer and are essentially arbitrary in the natural world [41]. Finally, it was noted that altitudinal biases were less affected in patients with spatial neglect than were horizontal biases. Indeed, the vertical biases shown by neglect patients were not markedly different to those shown by normal participants and could therefore be considered ‘non-pathological’. If horizontal biases, but not vertical biases, are affected in spatial neglect, it would suggest that the biases are the product of relatively independent neural mechanisms. While the present study demonstrates some independence between horizontal and vertical biases, it is unlikely

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that they operate in isolation, or that they do not intersect at some point in the brain. One candidate region in which interaction could occur is the lateral intraparietal (LIP) area. The LIP has been divided, based on myelo-architecture, into dorsal and ventral sub-divisions [4]. The ventral portion of the LIP is connected to the dorsal visual stream, whereas the dorsal portion is connected to the ventral stream [3]. Given that the LIP has access to information from both the upper and lower visual fields, it would be ideally suited to compare information between them. While receiving information predominantly from the contralateral visual field, the LIP also receives input extending 5j into the ipsilateral visual field [3]. Thus, it may also play a role in comparing the lateral features of stationary, horizontally aligned stimului. This is supported by a recent neuroimaging study. Fink et al. [16] measured brain activation using fMRI while normal participants judged whether pre-transected lines were correctly bisected. Maximum activation was observed in the right parietal cortex, particularly along the intraparietal sulcus. If the LIP is the point of interaction between horizontal and vertical attentional biases, it may explain the similarities between the phenomena and their additive effects. The results from this study could prove relevant to the clinical management of spatial neglect. We have demonstrated that leftward neglect can be ameliorated by opposing it with upward attentional biases. Thus, if ‘left’ can somehow be associated with ‘up’ in neglect patients, more normal levels of performance in the neglected field could be achieved. Jeerakathil and Kirk [25] have demonstrated that labeling is an important component of altitudinal attentional biases. Bearing this in mind, if neglect patients were to associate their left side with ‘up’, it could result in a significant reduction of their leftward neglect. Alternatively, it has been shown that tilting the head to the left or right can affect the distribution of spatial attention [30,42], presumably because the spread of attention is defined by gravitational and retinotopic coordinates. Tilting the head slightly to the left in neglect could, therefore, bring leftward stimuli within the over-attended upper visual field—leading to a reduction in left neglect. While both of the suggestions seem plausible, they remain to be tested.

Acknowledgements We would like to thank two reviewers for their helpful comments on an earlier version of this manuscript.

References [1] J.C. Adair, D.J. Williamson, D.H. Jacobs, D.L. Na, K.M. Heilman, Neglect of radial and vertical space: importance of the retinotopic reference frame, Journal of Neurology, Neurosurgery and Psychiatry 58 (1995) 724 – 728.

[2] M.L. Albert, A simple test of visual neglect, Neurology 23 (1973) 658 – 664. [3] S. Ben-Hamed, J.R. Duhamel, F. Bremmer, W. Graf, Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis, Experimental Brain Research 140 (2001) 127 – 144. [4] G.J. Blatt, R.A. Anderson, G.R. Stoner, Visual receptive field organisation and cortico-cortico connections of the intraparietal area (area LIP) in the macaque, Journal of Comparative Neurology 299 (1990) 421 – 445. [5] D. Bowers, K.M. Heilman, Pseudoneglect: effects of hemispace on a tactile line bisection task, Neuropsychologia 18 (1980) 491 – 498. [6] J.L. Bradshaw, N.C. Nettleton, G. Nathan, L. Wilson, Bisecting rods and lines: effects of horizontal and vertical posture on left-side underestimation by normal subjects, Neuropsychologia 23 (1985) 421 – 425. [7] J.L. Bradshaw, J.A. Bradshaw, G. Nathan, N.C. Nettleton, L.E. Wilson, Leftwards error in bisecting the gap between two points: stimulus quality and hand effects, Neuropsychologia 24 (1986) 849 – 855. [8] E.E. Brodie, L.E.L. Pettigrew, Is left always right? Directional deviations in visual line bisection as a function of hand and initial scanning direction, Neuropsychologia 34 (1996) 467 – 470. [9] G. Burnett-Stuart, P.W. Halligan, J.C. Marshall, A Newtonian model of perceptual distortion in visuospatial neglect, NeuroReport 2 (1991) 255 – 257. [10] S. Chokron, M. De Agostini, Reading habits and line bisection: a developmental approach, Cognitive Brain Research 3 (1995) 51 – 58. [11] S. Chokron, M. Imbert, Influence of reading habits on line bisection, Cognitive Brain Research 1 (1993) 219 – 222. [12] S. Chokron, J.M. Bernard, M. Imbert, Length representation in normal and neglect subjects with opposite reading habits studied through a line extension task, Cortex 33 (1997) 47 – 64. [13] M. Corbetta, F.M. Miezin, G.L. Shulman, S.E. Peterson, A PET study of visuospatial attention, Journal of Neuroscience 13 (1993) 1202 – 1226. [14] M. Drain, P.A. Reuter-Lorenz, Vertical orienting bias: evidence for attentional bias and ‘neglect’ in the intact brain, Journal of Experimental Psychology. General 125 (1996) 139 – 158. [15] J. Edgeworth, I. Robertson, T. McMillan, The Balloons Test, Thames Valley Test, UK, 1998. [16] G.R. Fink, J.C. Marshall, N.J. Shah, P.H. Weiss, P.W. Halligan, M. Grosse-Ruyken, K. Ziemons, K. Zilles, H.J. Freund, Line bisection judgements implicate right parietal cortex and cerebellum as assessed by fMRI, Neurology 54 (2000) 1324 – 1331. [17] D.S. Geldmacher, K.M. Heilman, Visual field influence on radial line bisection, Brain and Cognition 26 (1994) 65 – 72. [18] P.W. Halligan, J.C. Marshall, Is neglect (only) lateral? A quadrant analysis of line cancellation, Journal of Clinical and Experimental Neuropsychology 11 (1989) 793 – 798. [19] P.W. Halligan, J.C. Marshall, The bisection of horizontal and radial lines: a case study of normal controls and ten patients with left visuospatial neglect, International Journal of Neuroscience 70 (1993) 149 – 167. [20] P.W. Halligan, J.C. Marshall, Lateral and radial neglect as a function of spatial position: a case study, Neuropsychologia 33 (1995) 1697 – 1702. [21] M. Harvey, A.D. Milner, R.C. Roberts, Differential effects of line length on bisection judgements in hemispatial neglect, Cortex 31 (1995) 711 – 722. [22] M. Harvey, T.D. Pool, M.J. Roberson, B. Olk, Effects of visible and invisible cueing procedures on perceptual judgments in young and elderly subjects, Neuropsychologia 38 (2000) 22 – 31. [23] K.M. Heilman, R.T. Watson, E. Valenstein, Neglect and related disorders, in: K.M. Heilman, E. Valenstein (Eds.), Clinical Neuropsychology, 2nd ed., Oxford Univ. Press, New York, 1985, pp. 243 – 293. [24] K.M. Heilman, D. Bowers, E. Valenstein, R.T. Watson, Hemispace

M.E.R. Nicholls et al. / Cognitive Brain Research 19 (2004) 289–301

[25] [26]

[27]

[28] [29] [30]

[31]

[32]

[33]

[34]

[35]

[36]

[37]

[38]

[39]

[40]

[41] [42]

[43]

and hemispatial neglect, in: M. Jeannerod (Ed.), Neurophysiological and Neuropsychological Aspects of Spatial Neglect, Elsevier, Amsterdam, 1987, pp. 115 – 150. T.J. Jeerakathil, A. Kirk, A representational vertical bias, Neurology 44 (1994) 703 – 706. G. Jewell, M.E. McCourt, Pseudoneglect: a review and meta-analysis of performance factors in line bisection tasks, Neuropsychologia 38 (2000) 93 – 110. S. Kageyama, M. Imagase, M. Okubo, Y. Takayama, Neglect in three dimensions, American Journal of Occupational Therapy 48 (1994) 206 – 210. J.L. Kashmere, A. Kirk, The complex interaction of normal biases in line bisection, Neurology 49 (1997) 887 – 889. M. Kinsbourne, The cerebral basis of lateral asymmetries in attention, Acta Psychologica 33 (1970) 193 – 201. E. Ladavas, Is the hemispatial deficit produced by right parietal lobe damage associated with retinal or gravitational coordinates? Brain 110 (1987) 167 – 180. K.E. Luh, L.M. Rueckert, J. Levy, Perceptual asymmetries for free viewing of several types of chimeric stimuli, Brain and Cognition 16 (1991) 83 – 103. L. Manning, P.W. Halligan, J.C. Marshall, Individual variation in line bisection: a study of normal subjects with application to the interpretation of visual neglect, Neuropsychologia 28 (1990) 647 – 655. J.C. Marshall, P.W. Halligan, The psychophysics of visuo-spatial neglect: a new orientation, Medical Science Research 18 (1990) 429 – 430. J.B. Mattingley, J.M. Pierson, J.L. Bradshaw, J.G. Phillips, J.A. Bradshaw, To see or not to see: the effects of visible and invisible cues on line bisection judgments in unilateral neglect, Neuropsychologia 31 (1993) 1201 – 2115. J.B. Mattingley, J.L. Bradshaw, N.C. Nettleton, J.A. Bradshaw, Can task specific perceptual bias be distinguished from unilateral neglect? Neuropsychologia 32 (1994) 805 – 817. J.B. Mattingley, N. Berberovic, L. Corben, J.L. Bradshaw, M.E.R. Nicholls, The grayscales task: a perceptual measure of attentional bias following right hemisphere damage, Neuropsychologia 42 (2003) 387 – 394. M.E. McCourt, M. Garlinghouse, Asymmetries of visuospatial attention are modulated by viewing distance and visual field elevation: pseudoneglect in peripersonal and extrapersonal space, Cortex 36 (2000) 715 – 731. M.E. McCourt, G. Jewell, Visuospatial attention in line bisection: stimulus modulation of pseudoneglect, Neuropsychologia 37 (1999) 843 – 855. M.E. McCourt, C. Olafson, Cognitive and perceptual influences on visual line bisection: psychophysical and chronometric analyses of pseudoneglect, Neuropsychologia 35 (1997) 369 – 380. M.E. McCourt, P. Freeman, C. Tahmahkera-Stevens, M. Chaussee, The influence of unimanual response on pseudoneglect magnitude, Brain and Cognition 45 (2001) 52 – 63. I.C. McManus, Left Hand, Right Hand, Weidenfeld and Nicolson, London, 2002, 412 pp. M. Mennemeier, A. Chatterjee, K.M. Heilman, A comparison of the influences of body and environment centered reference frames in neglect, Brain 117 (1994) 1013 – 1021. M. Mennemeier, E. Vezey, A. Chatterjee, S.Z. Rapcsak, K.M. Heilman,

[44]

[45] [46]

[47]

[48] [49] [50]

[51]

[52]

[53] [54] [55] [56] [57]

[58]

[59]

[60] [61] [62]

[63] [64] [65]

301

Contributions of the left and right cerebral hemispheres to line bisection, Neuropsychologia 35 (1997) 703 – 715. A.D. Milner, M. Brechmann, L. Pagliarini, To halve or to halve not: an analysis of line bisection judgements in normal subjects, Neuropsychologia 30 (1992) 515 – 526. M.E.R. Nicholls, G.R. Roberts, Pseudoneglect: a scanning, pre-motor or attentional bias? Cortex 38 (2002) 113 – 136. M.E.R. Nicholls, J.L. Bradshaw, J.B. Mattingley, Free-viewing perceptual asymmetries for the judgement of shade, numerosity and size, Neuropsychologia 37 (1999) 307 – 314. M.E.R. Nicholls, J.L. Bradshaw, J.B. Mattingley, Unilateral hemispheric activation does not affect free-viewing perceptual asymmetries, Brain and Cognition 46 (2001) 219 – 223. R.C. Oldfield, The assessment of handedness: the Edinburgh inventory, Neuropsychologia 9 (1971) 97 – 133. S. Pitzalis, D. Spinelli, P. Zoccoltti, Vertical neglect: behavioral and electrophysiological data, Cortex 33 (1997) 679 – 688. S. Pitzalis, F. Di Russo, D. Spinelli, P. Zoccolotti, Influence of the radial and vertical dimensions on lateral neglect, Experimental Brain Research 136 (2001) 281 – 294. R.B. Post, K.J. Caufield, R.B. Welch, Contributions of object- and space-based mechanisms to line bisection errors, Neuropsychologia 39 (2001) 856 – 864. F.H. Previc, Functional specialization in the lower and upper visual fields in humans: its ecological origins and neurophysiological implications, Behavioral and Brain Sciences 13 (1991) 519 – 575. S.Z. Rapcsak, C.R. Cimino, K.M. Heilman, Altitudinal neglect, Neurology 38 (1988) 277 – 281. P.A. Reuter-Lorenz, M. Kinsbourne, M. Moscovitch, Hemispheric control of spatial attention, Brain and Cognition 12 (1990) 240 – 266. P.L. Rodnitzky, Van Allen’s Pictorial Manual of Neurologic Tests, 3rd ed., Year Book Medical Publishers, Chicago, 1988. C. Rorden, M. Brett, Stereotaxic display of brain lesions, Behavioural Neurology 12 (2001) 191 – 200. L. Rueckert, A. Deravanesian, D. Baboorian, A. Lacalamita, M. Repplinger, Pseudoneglect and the cross-over effect, Neuropsychologia 40 (2002) 162 – 173. A.F. Sanders, M. Donk, Visual search, in: O. Neumann, A.F. Sanders (Eds.), Handbook of Perception and Action, Attention, vol. 3, Academic Press, San Diego, CA, US, 1996, pp. 43 – 77. B.B. Schiff, C. Truchon, Effect of unilateral contraction of hand muscles on perceiver biases in the perception of chimeric and neutral faces, Neuropsychologia 31 (1993) 1351 – 1365. P.A. Shelton, D. Bowers, K.M. Heilman, Peripersonal and vertical neglect, Brain 113 (1990) 191 – 205. J. Talairach, P. Tournoux, Co-Planar Stereotaxic Atlas of the Human Brain, George Thieme, New York, 1988, 122 pp. M.L.M. Tant, J.B.M. Kuks, A.C. Kooijman, F.W. Cornelissen, W.H. Brouwer, Greyscales uncover similar attentional deficits in homonymous hemianopia and visual hemi-neglect, Neuropsychologia 40 (2002) 1474 – 1481. P. Van Vugt, I. Fransen, W. Creten, P. Paquier, Line bisection performances of 650 normal children, Neuropsychologia 38 (2000) 886 – 895. W. Vingiano, Pseudoneglect on a cancellation task, International Journal of Neuroscience 25 (2001) 245 – 254. B. Wilson, J. Cockburn, P.W. Halligan, Behavioural Inattention Test, Thames Valley Test, UK, 1987.