Effects of prismatic adaptation on judgements of spatial extent in peripersonal and extrapersonal space

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Abstract

Recent research has shown that visuomotor adaptation to a lateral displacement of the visual field induces significant perceptual aftereffects in normal observers, and in right hemisphere patients with spatial neglect [Neuroreport 11 (2000) 1899; Nature 395 (1998) 166]. These findings suggest that adaptive realignment following prism exposure induces a bias in visual space perception, even in tasks that require no visually guided motor response. Given recent neurophysiological and behavioural data suggesting independent visual representations for peripersonal and extrapersonal space, here we asked whether adaptive aftereffects extend beyond participants’ immediate reaching space to stimuli presented beyond arms’ reach (i.e. in extrapersonal space). Thirty-two participants underwent adaptive realignment to 10° left- or right-displacing wedge-prisms. Before and after adaptation participants performed a visual landmark task that required estimation of the midpoint of horizontal line stimuli. There was a significant rightward shift in visual midpoint judgements following adaptation to left-deviating prisms, which was evident in both peripersonal and extrapersonal space. Paradoxically, a significant rightward shift also occurred following adaptation to right-deviating prisms, but only in extrapersonal space. We suggest that the pattern of adaptive aftereffects observed reflects the different reference frames used by participants to perform spatial judgements in peripersonal and extrapersonal space. We also propose that an underlying hemispheric asymmetry in the processing of spatial errors during adaptation may contribute to the direction of aftereffects in both normal observers, and in patients with unilateral lesions.

Introduction

The effects of sensorimotor adaptation to optical-wedge prisms have been studied in humans for over 100 years [12], [32]; for review see [26]. In the standard experimental paradigm, normal observers exposed to a prism-induced displacement of the visual field adapt rapidly by adjusting their motor behaviour (e.g. manual pointing) to reduce errors. With practice there is gradual recalibration of visual and proprioceptive/kinaesthetic correspondences, so that motor errors are effectively eliminated [26]. That this adaptation reflects genuine spatial realignment, rather than a conscious strategy adopted by the subject, is supported by the presence of negative aftereffects following removal of the prisms [26], [30], [37], [39].

Although there have been many studies of the behavioural and cognitive effects of prismatic adaptation, the neural basis for these effects has remained uncertain. A recent human neuroimaging study by Clower et al. [1] found significant activity in the posterior parietal cortex contralateral to the reaching limb, during visually guided pointing under conditions of prismatic displacement. Unfortunately, since the direction of prismatic displacement (left versus right) was alternated after every four reaching movements, true adaptive realignment was not achieved. Nevertheless, the results of this pioneering study suggest that the human parietal cortex plays an important role in the detection and correction of spatial errors during manual actions.

More recently, in a series of elegant studies Rossetti and co-workers [29], [31], [34] have shown that spatial realignment following adaptation to a right-lateral shift of the visual field leads to profound and enduring improvements in patients with spatial neglect due to right hemisphere damage. For instance, Rossetti and co-workers [31] reported that a short (<10 min) period of adaptation to a 10° rightward displacement of the visual field significantly improved the performance of right hemisphere patients on a range of clinical tests for neglect, including line bisection, cancellation, copying, drawing, and reading. Importantly, there was no significant effect of adaptation to leftward displacing prisms, suggesting that the beneficial effects of rightward displacement are not attributable to general alerting from visuomotor activity. Subsequent research has also revealed significant improvements in such patients on measures of visual imagery and postural balance [29], [34]. These effects appear to last for at least 2 h following adaptation [31], and may even extend over several days [24], thus making prismatic adaptation a useful tool for rehabilitation.

These results in neglect patients prompted Colent et al. [2] to examine the effects of prismatic adaptation on visual perception in normals. They compared bisection errors made by normal participants in a standard, manual version of the horizontal line bisection test, and in a ‘landmark’ variant of the task [10]. Following a short period of visuomotor adaptation to 15° left-deviating prisms, normal participants showed a significant rightward deviation in the perceived midpoint of the pretransected lines, relative to a pre-adaptation baseline. Interestingly, this effect was not apparent for the manual version of the test, and did not occur following equivalent adaptation to right-deviating prisms. Thus, adaptation to left-deviating prisms induces rightward ‘pseudoneglect’ in normals1 [2], but has no effect on pathological neglect in right hemisphere patients. Conversely, adaptation to right-deviating prisms has no effect on bisection judgements in normals, but induces significant and long-lasting improvements in spatial neglect in patients [24], [31]. It therefore appears that the processes involved in visuomotor adaptation engage the two hemispheres differentially according to the direction of prism-induced displacement; and that these processes may be differentially susceptible to the effects of lateralised brain damage [31].

In the present study, we attempted to replicate the findings of Colent et al. [2], with several important extensions to their methodology. First, we asked whether the effects of prismatic adaptation on bisection judgements in the landmark task also extend to stimuli presented beyond participants’ immediate reaching space. There is considerable neurophysiological and behavioural evidence in monkey and man that the space within arms’ reach (i.e. ‘peripersonal space’) is represented by neural circuits that are functionally distinct from those devoted to the representation of space beyond arms’ reach (i.e. ‘extrapersonal space’ [7], [27], [28]; for a review see [25]). Moreover, it is known that visual neglect may occur predominantly in either peripersonal or extrapersonal space, depending presumably on the locus of damage [4], [9]. Peripersonal space is typically conceptualised as an ‘action space’, for which visual representations are encoded in body- or limb-centred co-ordinates [25]. In contrast, extrapersonal space is more important for object recognition and visual search, and is probably represented in allocentric or gravitational co-ordinates [25].

Given the results of Colent et al. [2], it is important to determine whether any aftereffects of prismatic adaptation are restricted to perceptual representations of peripersonal space (within which visuomotor adaptation takes place), or whether they extend to perceptual representations of extrapersonal space. In a study of prism adaptation in normals, Tietz and Gogel [33] compared the magnitude of adaptive aftereffects induced by manual pointing toward visual targets projected at two different depths (33.0 cm versus 55.9 cm). They observed significant generalisation of aftereffects across the two depths, the magnitude of which depended on whether the space between the participant and the targets was visible. Note however that the targets in this study were always within reaching distance (participants used a pen to mark their locations on a board), and so the results do not indicate whether adaptive aftereffects extend into extrapersonal space. The first aim of the present study, therefore, was to determine whether the visual aftereffects of prismatic adaptation, as measured by the landmark task, occur in extrapersonal space as well as in peripersonal space.

A second aim of this study was to determine whether prismatic aftereffects result directly from an egocentric bias in judgements of the subjective midline. In the study by Colent et al. [2], horizontal lines were always centred on the participants’ body midline. Thus, the rightward bias in landmark judgements found after adaptation to left-deviating prisms may have been due to a shift in participants’ egocentric midline, rather than to a bias in the allocentric representation of the lines themselves. To address this issue, we presented line stimuli so that they were either aligned with the participants’ body midline, or displaced horizontally toward the left or right hemispace. We also measured participants’ perception of their egocentric midline by having them point straight-ahead, without visual guidance, before and after prismatic adaptation. This permitted us to compare individuals’ egocentric judgements of straight-ahead with their allocentric judgements on the landmark stimuli.

Finally, in order to avoid any unwanted influences from extraneous marks or distractions in the environment, we projected the lines onto a white viewing screen in an otherwise darkened room. By moving the participant and projector between blocks, we were also able to ensure that the landmark stimuli were precisely matched for retinal angle across peripersonal and extrapersonal space conditions.

Section snippets

Participants

Thirty-two undergraduate students (12 males 20 females; age range 18–35 years) from the University of Melbourne participated for course credit. All participants were right-handed and had normal or corrected-to-normal vision.

Prismatic adaptation

Participants wore a pair of Cebe™ binocular prisms to induce a left- or right-lateral displacement of the visual field. Each circular eyepiece contained a clear wedge prism that displaced the visual field horizontally by 10° to the left or right. Black leather covers

Results

For ease of exposition, we report the findings for peripersonal and extrapersonal space separately, even though data for each viewing distance were obtained during a single testing session. We first report the direct effects of prismatic adaptation, and compare open-loop pointing responses obtained in the pre- and post-adaptation phases. We then report the effects of prismatic adaptation on spatial judgements of horizontal extent, as measured by the landmark task. We focus our discussion

Discussion

The purpose of this study was to examine whether visuomotor adaptation to a lateral shift of the visual field can influence visual judgements of spatial extent in normals. Our findings confirm those of Colent et al. [2] by showing that bisection judgements on the landmark task are shifted significantly to the right following adaptation to left-deviating prisms. Our results are also consistent with Colent et al.’s finding that adaptation to a right-prismatic shift does not induce a corresponding

Acknowledgements

Findings from this study were presented at the 28th Australian Experimental Psychology Conference, Melbourne, April 2001. Prism lenses were supplied by Optique Peter (France). We thank Patrick Wilken for his technical assistance, and Laure Pisella and Melissa Slavin for many helpful discussions. This work was supported by a grant from the Australian Research Council to JBM.

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