Elsevier

NeuroImage

Volume 18, Issue 4, April 2003, Pages 837-846
NeuroImage

Regular article
Are action and perception in near and far space additive or interactive factors?

https://doi.org/10.1016/S1053-8119(03)00018-1Get rights and content

Abstract

Functional imaging has revealed differential neural mechanisms underlying action directed toward near or far space. Because some neuropsychological studies of patients with visuospatial neglect failed to show near/far dissociations with perceptual tasks, we investigated whether action and perception elicit distinct cerebral representations in near and far space. We measured regional cerebral blood flow with positron emission tomography in normal volunteers who performed manual line bisection (action) and made line bisection judgments (perception). Stimuli were presented in near space or far space. Far space presentation enhanced activations in occipital cortex extending into the medial occipitotemporal cortex bilaterally, while near space presentation enhanced left occipital–parietal, parietal, and premotor cortex activity. Manual bisection activated the extrastriate, superior parietal, and premotor cortex bilaterally, while bisection judgments activated the right inferior parietal cortex, anterior cingulate, right dorsolateral prefrontal cortex, and extrastriate and superior temporal cortex bilaterally. The neural mechanisms responsible for the two tasks (perceptual/motor) were not differentially modulated by space of presentation.

Introduction

For nonhuman primates, differential neuronal populations subserving attention to and action in near space (within reaching distance, peripersonal space) versus far space (beyond reaching distance, extrapersonal space) have been described (Rizzolatti et al., 1983). Dissociations of task performance in near and far space are also observed in neurological patients Barrett et al 2000, Cowey et al 1994, Halligan and Marshall 1991, Vuilleumier et al 1998. Based on electrophysiological data in monkeys and neuropsychological observation in patients, it has then been postulated that the dorsal and ventral processing streams (Ungerleider and Mishkin, 1982) are differentially involved in the neural representations of near and far space, respectively (Previc, 1998).

Using positron emission tomography (PET) in normal volunteers, we recently demonstrated differential neural bases for acting in near versus far space in normal volunteers (Weiss et al., 2000). In that study, two different motor tasks were performed in near versus far space: manual line bisection and dot pointing. Thus the design did not allow us to distinguish whether the observed differential neural mechanisms were related to computing the relevant spatial positions or acting on the result of those computations when the stimulus is in near versus far space. By contrast, the current study, which uses both a visuospatial motor task (manual bisection, emphasizing the action component) and a visuospatial perceptual task (bisection judgments, emphasizing the perceptual/computational component), enabled us to investigate whether presentation in near versus far space does or does not have a differential impact on the neural representations of the motor and perceptual tasks. We accordingly use additive-factors logic (Sternberg, 1969), in which the variables of task and space of presentation are factorially crossed. To find an interaction between these variables suggests that one processing component (at least) is held in common in the regions implicated by the main variables; to find no interaction suggests that no distinct processing components are held in common by the four simple main effects (but see McClelland (1979) for complications when cascade effects or feedback systems are involved). This issue is of clinical significance with respect to dissociations between impaired and preserved abilities in patients with spatial disorders: there has been considerable controversy over whether it is only action tasks that show major discrepancies in accuracy of performance in near versus far space Brain 1941, Paterson and Zangwill 1944, Pitzalis et al 2001, Pizzamiglio et al 1989, Vuilleumier et al 1998.

Section snippets

Subjects

Twelve healthy, right-handed male volunteers (age 24.3 ± 3.7 years) with no history of neurological or psychiatric illness were recruited. We studied only male volunteers to avoid the normal variation in brain size and shape between the sexes and hence improve image normalization (see below). Similarly, we did not wish to encounter any problems related to the interaction of neural mechanisms underlying cognitive tasks with hormone levels in female subjects (Dietrich et al., 2001). Informed

Effect of SPACE: far space versus near space (and vice versa)

The main effect of far space [relative to near space; (manual line bisection, far space, FLB + line bisection judgment task, far space, FLBJ) > (manual line bisection, near space, NLB + line bisection judgment task, near space, NLBJ)] showed enhanced activation of occipital cortex bilaterally (P ≤ 0.05, corrected for multiple comparisons across the whole brain) extending bilaterally via the lingual and fusiform gyri (P ≤ 0.05, corrected for multiple comparisons across the whole brain) to the

Discussion

The fact that task performance in near space draws differentially on the dorsal visuomotor processing stream and performance in far space draws differentially on the ventral visuoperceptual stream replicates and extends our previous findings (Weiss et al., 2000). We have also replicated earlier findings of a closer coupling between performance in near space and the activation of the left hemisphere Barrett et al 2000, Weiss et al 2000. Because, in our experiment, responses were made by the

Acknowledgements

The authors thank Lutz Tellmann and the radiographers from the Institute of Medicine for their help with data acquisition. J.C.M. is supported by the Medical Research Council; K.Z. and G.R.F. are supported by the Deutsche Forschungsgemeinschaft (KFO-112). Additional support from the VolkswagenStiftung is gratefully acknowledged.

References (37)

  • I. Toni et al.

    Movement preparation and motor intention

    NeuroImage

    (2001)
  • A. Berti et al.

    When far becomes nearre-mapping of space by tool use

    J. Cogn. Neurosci.

    (2000)
  • O. Bjoertomt et al.

    Spatial neglect in near and far space investigated by repetitive transcranial magnetic stimulation

    Brain

    (2002)
  • W.R. Brain

    Visual disorientation with special reference to lesions of the right hemisphere

    Brain

    (1941)
  • B.G. Cumming

    An unexpected specialization for horizontal disparity in primate primary visual cortex

    Nature

    (2002)
  • B.G. Cumming et al.

    The physiology of stereopsis

    Annu. Rev. Neurosci.

    (2001)
  • G.R. Fink et al.

    Line bisection judgements implicate right parietal cortex and cerebellum as assessed by fMRI

    Neurology

    (2000)
  • K.J. Friston

    Testing for anatomically specified regional effects

    Hum. Brain Mapp.

    (1997)
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