Brain, Vol. 125, No. 9, 2012-2022,
September 2002
© 2002 Guarantors of Brain
Spatial neglect in near and far space investigated by repetitive transcranial magnetic stimulation
0 Department of Experimental Psychology, University of Oxford, Oxford, UK
Correspondence to: Otto Bjoertomt, Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD, UK E-mail: otto.bjoertomt{at}psy.ox.ac.uk
Received February 27, 2002. Revised April 10, 2001. Accepted April 13, 2002.
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Localized repetitive transcranial magnetic stimulation was used to disrupt visuospatial perception in the near and far space of six healthy volunteer subjects. In addition to the baseline condition, they were stimulated over the right posterior parietal cortex, the right or left dorsal occipital cortex or the right ventral occipital cortex, during the brief presentation of a transected horizontal line. Subjects had to indicate whether the part of the line to the left or right of the transection appeared longer. The stimulus display was back-projected on a screen at a viewing distance of either 50 or 150 cm (‘near’ and ‘far’ space, respectively). Reaction times and choices were measured. In a forced-choice paradigm, subjects showed ‘pseudoneglect’, the natural tendency of neurologically intact subjects to perceive the left side of a centrally transected line as slightly longer than the right. These errors occurred more for lines in near space than for lines in far space. Magnetic stimulation of the right posterior parietal cortex or the right ventral occipital lobe selectively induced a significant shift to the right in the perceived midpoint for near- and far-space lines, respectively. The results reproduced in normal subjects the dissociation between neglect in near and far space that has been described in patients with different right-hemisphere lesions. This dissociation supports the contention that there is a dorsal/near space–ventral/far space segregation of processing in the visual system which reflects the behavioural goals of the two putative visual streams.
Keywords: visual neglect; parietal cortex; near and far space; TMS
Abbreviations: fMRI = functional magnetic resonance imaging; PPC = posterior parietal cortex; rCBF = regional cerebral blood flow; RT = reaction time; rTMS = repetitive TMS, TMS = transcranial magnetic stimulation
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Introduction |
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Hemineglect is the failure to perceive/or to attend normally to one side of space. It occurs in tactile (Aglioti et al., 1999
), auditory (Bellmann et al., 2001) and visual modalities (Vallar, 1998). The commonest type of hemineglect is unilateral visual spatial neglect, characteristically associated with damage to the lateral frontal premotor area and the posterior and inferior lateral parietal areas of the right hemisphere (Vallar, 1998; but see Karnath et al, 2001, who reported that damage to the superior temporal gyrus is the principal cause of spatial neglect). In particular, it has been argued that the posterior parietal cortex (PPC) is important for unilateral visuospatial neglect (Leibovitch et al., 1998; Vallar, 1998), although damage to the inferior parietal cortex may also affect visuomotor action towards the contralesional side (Husain et al., 2000). Patients with damage to these areas often fail to register the contralesional side of their bilateral visual field. This is exemplified in failures to draw contralesional sides of objects, to eat food from the contralesional visual side of the plate and prominent failure to orient towards or represent novel stimuli in the neglected hemifield (Bisiach, 1993; Rafal, 1994). This does not necessarily mean that the neglected stimuli are not initially encoded but rather that encoded stimuli fail to influence the brain processes underlying verbal and non-verbal behaviour (Rafal, 1994). Under some conditions, however, covert perception of events in the neglected field has been shown to influence perceptual choices (Marshall and Halligan, 1988).
A task frequently used to measure visuospatial neglect in patients is line bisection (Best, 1919; Sato et al., 1983; Marshall and Halligan, 1989; Pizzamiglio et al., 2000). In this task, the subject is presented with a horizontal line and has to bisect it, i.e. show where the midpoint lies. In addition to abnormally low scores on tests of visuospatial processing such as the cancellation task (Poppelreuter, 1917; Bisiach et al., 1979) and the overlapping figures test (Poppelreuter, 1917; Gainotti et al., 1989), damage to the parietal cortex may also result in abnormal performance by individuals on line-bisection tasks. Most of these patients suffer from a right parietal lesion and commonly bisect the line to the right of its veridical midpoint. Furthermore, if the bisection task requires a manual response towards contralesional space, both perceptual and motor neglect may occur (Bisiach, 1993). Hence, when testing for visuospatial unilateral neglect, whether in brain-damaged patients or during transcranial magnetic stimulation (TMS) in healthy subjects, as in the present study, the tasks employed should not rely on manual responses in a way that allows a confound between perceptual and motor neglect. Normal viewing habits also need to be taken into account. For example, when healthy subjects are tested on line bisection tasks they show a slight but significant tendency to overestimate the length of the left side of the line relative to the right side. This ‘pseudoneglect’ (Bisiach et al., 1976; Bowers and Heilman, 1980), which is opposite to the right parietal neglect most commonly investigated in patients, is sensitive to viewing distance, being larger for peripersonal space than for extrapersonal space (McCourt and Garlinghouse, 2000).
The difference in pseudoneglect found for peri- and extrapersonal stimuli (McCourt and Garlinghouse, 2000) prompts the question of whether natural lesions may selectively affect spatial representation of stimuli in either near or far space. Halligan and Marshall (1991) reported a series of tests on a patient who suffered from an infarction of the right dorsolateral parietal cortex and who showed prominent left neglect mostly for near-space but not far-space stimuli. This was found in bisection tasks that required various types of manual responses. The opposite pattern occurred in the responses of a patient with a right hemisphere haematoma, who showed left neglect on line bisection tasks for stimuli in far space but not in near space (Halligan and Marshall, 1991). A double dissociation thus exists between near and far visuospatial processing or representation in these two patients. Comparing these two cases suggests the PPC as a candidate for near-space processing, with far space represented more in the inferior temporal cortex (Halligan and Marshall, 1991). This initial localization of processes underlying the perception of near and far space concurs with earlier suggestions that the occipitoparietal and occipitotemporal pathways encode near and far space, respectively (Heilman et al., 1990; Mennemeier et al., 1992). These suggestions are buttressed by functional MRI (fMRI) studies that found the right parietal lobe to be activated in healthy humans during line-bisection tasks in near space (Fink et al., 2000, 2001). Further dissociation between the processing of near- and far-space displays was also seen in a brain activation study which employed a line-bisection task. Weiss et al. (2000) used PET to monitor regional cerebral blood flow (rCBF) in 12 healthy human subjects during line-bisection tasks. The rCBF increased in the left intraparietal sulcus and the right medial temporal cortex for bisection of lines in near and far space, respectively. These intrahemispheric locations concur with those in patients with distance-specific unilateral neglect (Halligan and Marshall, 1991; Vuilleumier et al., 1998; Weiss et al., 2000). Furthermore, there was a double dissociation within the occipital lobe. Blood flow increased in the subjects’ left dorsal occipital lobe when perceiving near-space stimuli, whereas it increased bilaterally in the ventral occipital lobe for far-space stimuli. Collectively, the results support the notion of a dichotomy between the far space/ventral stream and the near space/dorsal stream. This spatiotopic anisotropy may reflect the importance of the parietal lobe for reaching and grasping in near space and the relatively greater role of more ventral regions in the perception of far space, although the specializations are, of course, not absolute. There are several examples of the importance of this distinction, the most general example being the dichotomy of ‘where’ and ‘how’ or perception and action (Goodale and Milner, 1992; Milner and Goodale, 1993): what is to be done with a seen stimulus influences how it is analysed in various regions or streams of the cortex (e.g. Janssen et al., 2000), and what can be done depends on distance from the viewer. The distance from an observer to stimuli processed by the ventral occipital lobe is, on average, greater than the distance of stimuli processed by the dorsal occipitoparietal region (Previc, 1990).
Repetitive TMS has been used to impair perception briefly in contralateral space and thus may be used to investigate spatiovisual processing (Pascal-Leone et al., 1994; Walsh et al., 1999; Hilgetag et al., 2001; Rushworth et al., 2001). For example, Oliveri et al. (2000) applied TMS to the contralesional hemisphere of 30 brain-damaged patients who exhibited unilateral tactile extinction. They found that, by interrupting the processing in patients’ undamaged hemisphere, the incidence of patients’ extinction of contralesional tactile stimuli could be reduced. This result can be interpreted within the theoretical framework of Kinsbourne (1977), who posited that the two cortical hemispheres compete to direct responses towards each contralateral space. By impairing processing in the undamaged hemisphere, the disordered activation of the damaged hemisphere becomes less inhibited by the intact hemisphere, resulting in less extinction of contralesional stimuli. Contralateral neglect, as opposed to extinction, has also been modelled in healthy subjects. Fierro et al. (2000) applied repetitive TMS (rTMS) to the right dorsolateral posterior parietal lobe and reduced the usual pseudoneglect exhibited by neurologically intact subjects. Thus, it has been shown that rTMS of cortical sites can selectively interrupt the perception of contralateral space.
The aim of the present study was to investigate distance-specific processes in human visuospatial perception. The first part of the study was designed to replicate the spatiotopic effects seen in normal subjects’ judgements of horizontal symmetry by presenting transected lines in near and far space. On the basis of the results of McCourt and Garlinghouse (2000), it was expected that the pseudoneglect for horizontal lines would be less pronounced in far space than in near space. In the second part of our study, rTMS over the PPC was used to investigate its role in the perception of near and far space. A decrease in normal subjects’ pseudoneglect, similar to that seen in Fierro et al. (2000), was expected during TMS over the parietal lobe. Finally, we tested whether TMS of the occipital lobe could produce ipsilateral shifts in the perceived midpoint of lines, and whether these effects also depend on viewing distance, as suggested by the functional neuroimaging study of Weiss et al. (2000).
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Methods |
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Subjects
Six healthy subjects, aged 21–26 years, participated (four female and two male, all right-handed). All bar one (O.B.) were naive to the purpose of the experiment. Subjects gave their signed informed consent to participation in the experiment. The study was approved by the Oxford Research Ethics Committee (OXREC). The exclusion criteria used in the selection of subjects conformed to current guidelines for rTMS research (Wassermann, 1998
). The subjects were informed that they could end the experiment at any moment if the stimulation was found to be uncomfortable. All participating subjects had normal or corrected-to-normal vision.
Stimuli and materials
The stimulus in each test consisted of a black, horizontal transected or bisected line on a light green background. The lines used in the tests were of various lengths. The computer-generated stimulus line was back-projected on a 2.2 x 1.9 m translucent screen facing the subject. Except for the light from the data projector, the room was darkened, with the mean luminance of the screen kept constant across conditions at 32.9 cd/m2 (< ±5%). Irrespective of distance, the black horizontal transected lines used in the tests had a mean length of 38° of visual angle within the range 36–40°, and they were of five different lengths (Fig. 1). A short, dark vertical line (2.2° long) transected the horizontal lines. All lines were 0.1° thick. In the tests, the horizontal line was always presented such that the transection mark was at the sagittal midline of the subject and the horizontal line was at eye level. When the line was asymmetrical about the transection, the elongated line segment was 1° longer than the shorter line segment. Before the presentation of the stimulus, the fixation cue, a symmetrical cross, was displayed at the centre of the screen (where the line would be transected) for 1000 ms. The subject was asked to fixate this point. A mask was displayed (55° x 41°) 200 ms after stimulus onset. The mask consisted of a thick horizontal line (thicker than the horizontal line of the stimulus) and a vertical line (with the same width as the transection mark). The mask was symmetrical around the sagittal midline, covered the entire area of the previously displayed stimulus and extended to the edges of the projected screen. The mask was displayed until the subject responded.
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In the TMS conditions, a Magstim Super Rapid stimulator (Magstim, Whitland, UK) was used. A figure-of-eight coil with a diameter of 50 or 70 mm (see Procedure) was used to deliver the TMS at 65% of maximal stimulator output (the average inductance of the 70 mm coil was
90% of that of the 50 mm coil; personal communication, Magstim Company, 2002). A single intensity was used for all subjects irrespective of any variation in motor or phosphene thresholds. As we have shown elsewhere (Stewart et al., 2001), motor thresholds and phosphene thresholds only have value for the sites at which they were obtained and cannot be assumed to be generalizable measures of cortical excitability. The level used was suprathreshold for phosphene and motor thresholds for all subjects.
Stimulation sites
The four sites used for TMS were: (i) the right posterior parietal cortex; (ii) the right dorsal occipital lobe; (iii) the right vertical occipital lobe; and (iv) the left dorsal occipital lobe. The right parietal site (PPC) was identified by using the hunting procedure described in Ashbridge et al. (1997). The subjects had to find a target line among non-target lines, targets being distinguished from non-targets by a combination of colour and orientation, e.g. a red slash among green slashes and backslashes of both colours. The PPC site was defined behaviourally when the TMS produced a marked (>10%) increase in mean latency for correct target-present responses in an ABAB design (Barlow and Hersen, 1984; Cozby, 1993) in a block of 10 trials. In four subjects, the site was located 9 cm dorsal and 5 cm lateral to the inion on the right side of the scalp (Fig. 2). In the other two it was 9 cm dorsal and 6 cm lateral to the inion. MRI scans co-registered with scalp coordinates show that this site overlies the inferior PPC (Rushworth et al., 2001; Walsh and Pascal-Leone, 2002).
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The localization of the three stimulation sites in the occipital cortex was based on the brain coordinates given by Weiss et al. (2000
). The reported activation foci were located near the left upper V3 for near-space stimuli and, bilaterally, near the lower portions of V3 for far-space stimuli (Weiss et al., 2000; Campana et al., 2002). These standard coordinates (Talairach and Tournoux, 1988) were used in conjunction with a Polaris infrared positioning system (Northern Digital, Waterloo, Canada) and the Brainsight Frameless software package (Rogue Research, Montreal, Canada). The coordinates were co-registered with their overlying scalp positions, using structural MRI data of two of the subjects. The scalp positions were calculated as distances along and orthogonal to the inion–nasion midline. The coordinates of the stimulation sites were adjusted for each individual subject according to their relative scalp size. For an inion–nasion distance of 35 cm, the dorsal site was 4.70 cm dorsal and 1.75 cm lateral (to the left) of the inion. The corresponding coordinates for the ventral occipital cortical site were 1.5 cm dorsal and 2.25 cm lateral to the inion (to the right).
The third site used for TMS was the right dorsal occipital cortex. This site was not found to be activated by Weiss et al. (2000) and was included here as a control site for possible non-specific effects (e.g. noise and tactile sensation) of TMS. The posterio-anterior and mediolateral coordinates for this site were the mirror image for the left dorsal occipital lobe.
Although Weiss et al. (2000) found several occipital functional activation foci during line bisection in far space, only one of the sites was needed to test a dorsal/ventral–near/far hypothesis. The right, rather than the left, ventral occipital site was chosen in order to allow the anatomical ‘far-space’ candidate to be in the same hemisphere as the parietal ‘near-space’ site interrupted by rTMS by Fierro et al., 2000.
Procedure
The subject was seated 50 or 150 cm from the screen. The subject rested the head on a chin-rest and held a computer mouse in the right hand, which was used to make the response. The stimulus in each test was a single line presented on the screen. All subjects used the right index and middle finger to make their response to the stimulus. In half the blocks the subject was required to press the left or right mouse button according to whether the left or right side of the line appeared longer, and in the remaining half of the blocks to press the mouse button corresponding to the shorter side of the line. The subject was given written instructions to respond as accurately and quickly as possible.
In order to minimize the effect of individual biases, the six subjects were informed that each side of the line was elongated in 50% of the trials. They were therefore unaware of the presentation of an exactly bisected line in 25% of the trials. Several precautions were taken against idiosyncratic response strategies that might have confounded the results. Each transected line was displayed so that the end-point of the shorter side of one line was at the same location as the end-point of the longer side of another line or a bisected line. Thus, the bisected lines were the longest and the shortest lines presented in the study. This manipulation was intended to minimize the use of only one unilateral end-point as a reference for the relative lengths of the two sides (see caption of Fig. 1).
There were two blocks of 64 trials in each condition within a session. The subjects were tested during two sessions (three sessions for two of the subjects). Each stimulus—one of eight types of line (two bisected, three left-elongated and three right-elongated)—was presented an equal number of times (i.e. eight times per block). All conditions were counterbalanced, employing a Latin square design in order to prevent systematic order effects of conditions and to equalize the numbers of times the subjects were required to report the shorter and longer line segments. Furthermore, the stimuli were presented in a random order within each block. In all baseline trials, sham rTMS was provided over the midline of the occipital cortex with the lateral edge of the figure-of-eight coil held perpendicular to the scalp. This form of sham stimulation does not produce measurable evoked potentials or rCBF changes when applied over the motor cortex (George et al., 1997; Loo et al., 2000). Neither phosphenes nor scalp sensations were reported by subjects during these baseline trials.
In the TMS conditions, the magnetic stimulation was applied at stimulus onset and lasted for 500 ms, i.e. throughout the 200 ms stimulus presentation and the first 300 ms of the mask presentation. Responses with a reaction time (RT) <500 ms did not end the rTMS.
In all conditions the coil used for TMS was the same, except during TMS of the ventral occipital lobe, when a smaller figure-of-eight coil was used (50 mm instead of 70 mm). This minimized unwanted stimulation of the neck muscles, which can occur when applying rTMS over this region with larger coils.
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Results |
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Pseudoneglect in normal subjects
For each subject, the average RT for each condition was calculated, excluding short outliers faster than 150 ms and long outliers slower than 1000 ms after stimulus onset (Ratcliff, 1993). Mean RTs for near space and far space were 406.3 (SD 146.9) ms and 424.5 (139.6) ms, respectively. Generally, RTs to right-elongated and bisected lines were longer than RTs to left-elongated lines: 447.6 and 455.3 versus 392.1 ms in near space and 438.5 and 438.4 versus 404.3 ms in far space (Table 1).
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For bisected lines, the left side was chosen as longer in 66.5% of the trials for near space and 56.1% of the trials for far space (Fig. 3). Since the subjects’ choices and RTs reported here were used as baselines for the TMS conditions, the effects of the independent variables for all conditions were analysed together for a more conservative estimate of the significance levels. A three-way ANOVA (analysis of variance) of distance (near and far), stimulation condition (baseline and four stimulation sites) and line type (left-elongated, right-elongated and bisected) revealed a main effect of viewing distance on subjects’ choices [F(1,5) = 35.68, P = 0.002], as well as an overall interaction between viewing distance, stimulation condition and line type [F(8,40) = 2.74, P = 0.016]. Paired t-tests (one-tailed) with multistage Bonferroni correction for multiple comparisons revealed a significant decrease in pseudoneglect with viewing distance for bisected lines (P < 0.05) and right-elongated lines (P < 0.01) but not for left-elongated lines (P > 0.05).
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TMS of posterior parietal cortex
The two dependent variables were the percentage choices of the longer side of the stimuli and the RTs. The effects on the subjects’ responses were analysed for each type of line by comparing RT means and percentage choices with the respective baselines for the same viewing distance. Three-way ANOVA revealed an overall significant effect of the TMS on subjects’ choices, but not for RTs. Paired t-tests (two-tailed) corrected for multiple comparisons with baseline for all conditions (Dunnett’s test) revealed a significant rightward shift in the perceived midpoint of bisected lines during TMS of PPC (P < 0.05), and also a significant leftward shift for the left-elongated lines (P < 0.05). These effects were only present for near-space stimuli. No significant changes in the subjects’ responses were found for the far-space condition (Fig. 4). Non-significant decreases in subjects’ RTs were found for bisected and right-elongated lines (P > 0.05) and there was a non-significant increase in RTs for left-elongated lines during TMS of the right PPC (P > 0.05) (for subjects’ RTs during TMS of PPC see Table 1).
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Occipital near–far dissociation
The dependent variables were the percentage of subjects’ choices of the longer side of the line and the subjects’ RTs. There was a main effect of TMS on subjects’ choices for different line types, revealed by three-way ANOVA. There were no significant effects on the RTs. Paired t-tests (two-tailed) were used to test for significant differences between baseline and each TMS condition. The results were corrected for multiple comparisons (Dunnett’s test). Only TMS of the right ventral occipital lobe produced a significant effect for bisected lines in far space (P < 0.001): subjects tended to perceive the right side as longer in this condition (Fig. 5B). TMS of neither the left dorsal occipital cortex (Fig. 5B) nor the control site (right dorsal occipital cortex) (Fig. 5C) produced any significant shift in the subjects’ choices (for RTs during TMS of PPC see Table 1).
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Task control: detection of line segments
The effect of TMS on the ability to detect the line stimuli was tested in a separate experiment to ensure that effects on line judgements were not a simple consequence of detection deficits. Five subjects had to detect the presence of a line segment (occurring 50% of the time on each side of the fixation cue), corresponding to the line elongation (1°) of the transected lines employed in the main study. These were presented in the same positions as the elongated parts of the transected lines (middle and lower lines in Fig. 1). For each stimulation condition used in the main study, there were 12 trials. Three subjects were tested for far-space stimuli and two subjects were tested for near-space stimuli. Materials, stimuli and procedures were otherwise the same as in the bisection conditions.
ANOVA of stimulation condition (baseline and four stimulation sites) and position of line segment (left or right side), did not reveal any significant effects of TMS on subjects’ choices (P > 0.05).
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Discussion |
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We found a dissociation between the cortical processing of visuospatial stimuli in near and far space in healthy subjects. Without TMS, subjects exhibited less pseudoneglect for far- than for near-space stimuli (see Results, Pseudoneglect in normal subjects). By using TMS to disrupt different stages of the cortical processing of visuospatial stimuli, an illusory spatial compression was induced selectively for line targets in either peri- or extrapersonal space. Recent studies have found a decrease in pseudoneglect for extrapersonal space compared with peripersonal space (Barrett et al., 1999
; McCourt and Garlinghouse, 2000) and the results from our first experiment are consistent with these findings. Several experiments suggest that the pseudoneglect is not an artefact of low-level visual processes such as covert scanning or visual memory, but instead reflects asymmetry in the allocation of attention at higher levels of visuospatial processing (McCourt and Jewell, 1999). Thus, the spatiotopic TMS-induced modulation of pseudoneglect found here suggests that attention to near and far space is mediated, at least in part, by separate processes. Further evidence for dissociation between the visuospatial perception of near and far space was seen in the shift of the apparent centre of the line in near space when stimulating the right inferior PPC. When stimulating the right parietal lobe, the left side of bisected lines was more often perceived to be shorter than the right (compared with baseline responding), but only for stimuli in near peripersonal space. Hence, these findings replicate and extend those reported by Fierro et al. (2000), who reduced healthy subjects’ pseudoneglect for bisected lines in near space by applying TMS over the right PPC. Right PPC stimulation also produced an unexpected left shift in the perceived midpoint of left-elongated lines in near space. There are two possible explanations of this, one theoretical and one methodological. Methodologically, it is not uncommon for the short-term disruption induced by TMS to differ from the effects of brain damage, probably because the damaged brain makes attempts to compensate, and this adjustment conceals defects that may have been present initially (Walsh et al., 1998; Hilgetag et al., 2001). This may also be the case here. It is notable that the shift is in near space, where the predicted right shift for bisected lines occurs. Theoretically, then, the right PPC may be important in the general organization of near space. A prediction that follows is that some patients with right parietal damage may have similar changes in near space perception for a short time following the brain insult before the brain readjusts. We propose to investigate this in future experiments. The results presented here also concur with neuropsychological studies of some patients with spatiotopic-dependent neglect, in which right parietal lesions produce left visuospatial neglect that is greater for near- than for far-space stimuli (Halligan and Marshall, 1991; Vuilleumier et al., 1998). However, when Cowey et al. (1999) investigated 13 brain-damaged patients with visuospatial hemineglect, all five of the patients who displayed distance-dependent neglect showed a gradual increase in their neglect with increasing viewing distance. There was no satisfactory explanation for this difference in terms of the lesion analysis. Their results also question the notion of a discrete boundary between peri- and extrapersonal space in cortical processing. An interesting extension of the current TMS study would be a parametric study of the interruption of healthy humans’ visuospatial perception as a function of the viewing distance. Furthermore, the recent evidence of Karnath et al. (2001), who reported that the right superior temporal gyrus better fits neuropsychological data as the crucial area for pure visuospatial neglect, could be evaluated by applying rTMS to these parietal or temporal areas during tests of spatial neglect. We are currently investigating this possibility.
Magnetic stimulation of the right ventral occipital cortex, but not the left or right dorsal occipital cortex, caused an ipsilateral shift in the perceived midpoint of bisected horizontal lines, i.e. the left side looked shorter, compared with the right side, than in the baseline condition. This effect was seen for lines in far space but not in near space. This echoes the findings by Weiss et al. (2000) who, using functional neuroimaging, found activation centres in the ventral occipital lobe in subjects judging stimuli in far, but not near, space. In the present study, we found that TMS applied over one of these centres, revealed by fMRI, disrupted the perception of contralateral visual stimuli in far space more than in near space. The apparent shortening of the contralateral line segment, compared with the ipsilateral segment, suggests a compression of space similar to that seen in patients with unilateral neglect (Milner and Harvey, 1995). However, we did not observe the interruption of near-space processing that has been suggested for the left dorsal occipital lobe, a site also identified by Weiss et al. (2000), suggesting that this site is not critical for near-space tasks of the kind used here.
The possibility that the TMS may have disrupted an initial detection stage rather than later processing of the contralateral line segment was tested in a control experiment, which showed no effect of the TMS on the subjects’ performance in any of the stimulation conditions used here. It could be argued that the results were from vertical shifts in the line of sight, as independent shifts in pseudoneglect were demonstrated when bisected lines were projected to the upper and the lower visual field (McCourt and Garlinghouse, 2000). Thus, if TMS produced a consistent vertical directional shift in the visual axis, there could be shifts in the perceived midpoint depending on whether the line was in the upper or lower visual field. Previous research, however, has shown that TMS over the occipital or parietal cortex does not elicit eye movements (Day et al., 1989; Wessel and Kompf, 1991; Priori et al., 1993). Furthermore, eye-tracking on one of the subjects did not reveal vertical shifts in fixation that could be consistently associated with any of the TMS conditions. Hence, the effects of TMS reported here are not attributable to either failure to register a contralateral line segment or to TMS-induced shifts in gaze.
The cortical mechanisms disrupted during TMS of the ventral occipital lobe may be considered with reference to several other studies. Higher perceptual areas in the parietal and temporal lobes provide feedback signals, it has been argued, that may gate the information flow of lower visual (or other sensory) areas (Desimone, 1998; Kastner et al., 1998). Martinez et al. (1999) found increased brain activity in the striate and extrastriate cortex when subjects were asked to attend to stimuli in the contralateral visual field. The foci of increased activation included ventral occipital lobe sites such as VP and V4v, both with stereotaxic coordinates (Talairach and Tournoux, 1988) close to the activation foci for far-space processing found by PET (Weiss et al., 2000). The combined fMRI and evoked potential recordings of the subjects revealed a late activation component in the right ventral occipital cortex (near V4v) 104–136 ms after stimulus onset in trials in which the subjects were asked to attend to the stimulus. The effects reported here of TMS over the ventral occipital lobe may be due to a disruption of this relatively late and possibly top-down enhancement of stimuli that have behavioural significance.
Several theoretical frameworks have been proposed to account for unilateral neglect in patients with parietal lesions. Milner and Goodale (1993) and many others argue that the ventral and dorsal streams encode mainly for recognition and action, respectively. The results reported here support such a dissociation: TMS of the PPC (dorsal stream component) altered judgements regarding near-space stimuli, while TMS of the ventral occipital cortex (part of the ventral stream) affected judgement of far-space stimuli. Recognition, on the other hand, is important in both near and far space, though it is perhaps more important in far space because there it is unsupported by touch. The findings of Weiss et al. (2000) point to the relative importance of far-space encoding in the ventral rather than the dorsal occipital cortex. Interestingly, in our study, the dissociation found between the processes was evident even though the task was purely perceptual, with the same visuomotor demands for both viewing distances.
In line with the majority of the cases of unilateral neglect, as well the findings of Fierro et al. (2000), our results suggest that the interference by TMS in processes in the right hemisphere was more influential in disrupting spatial judgements than similar interruption in the left hemisphere. It has been argued that space-encoding neurones in the right hemisphere are more bilaterally sensitive than those in the left hemisphere (Heilman and Van Den Abell, 1980). It is possible, then, that interruption of the more extensive higher-level spatiotopic representation of the right hemisphere produces greater unilateral neglect, owing to the relatively small ipsilateral visual representation in the left hemisphere (Heilman and Van Den Abell, 1980; Pouget and Driver, 2000).
The results presented here support a functional dissociation between near- and far-space processing in the cerebral cortex. This has implications for the interpretation of experiments on the neural basis of visual perception and cognition, which predominantly employ near-space stimuli on computer screens. In studies of neuropsychological patients, in brain-imaging investigations of near- and far-space processing and in the experiments reported in this paper, the emphasis has been on segregating function according to brain regions and behavioural goals. However, none of these studies addresses the temporal dynamics of near- and far-space processing, or potential interactions between them. Given the emerging consensus on the neurological division between near and far space, we propose to extend the current work to address the temporal characteristics of these behavioural domains by employing single-pulse TMS at specific times after the onset of the transected lines.
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Acknowledgements |
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The authors wish to thank Professor John Marshall for discussions of this project and for providing a preprint of Weiss et al. (2000
), Dr Amanda Ellison for help with the experiment and Professor Brian Rogers for the use of the large screen. Otto Bjoertomt was supported by a studentship from the Wellcome Trust, Alan Cowey was supported by a Medical Research Council grant and Vincent Walsh was supported by the Royal Society and the Dr Hadwen Trust.
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