Elsevier

Cortex

Volume 48, Issue 10, November–December 2012, Pages 1320-1328
Cortex

Research report
Paradoxical extension into the contralesional hemispace in spatial neglect

https://doi.org/10.1016/j.cortex.2011.10.003Get rights and content

Abstract

To explore the idea of a perceptual distortion of space in spatial neglect, neglect patients, age-matched healthy controls and right hemisphere control patients judged the vanishing point of horizontally and vertically-moving stimuli. Hemifield of presentation and movement direction of the stimulus presentation was manipulated. The results suggest that neglect patients show a stronger response bias in the direction of the moving stimuli (“representational momentum”) than healthy and right hemisphere controls. Furthermore, neglect patients, but not the control groups, showed a direction-specific response whereby the presence of neglect was associated with a larger representational momentum for leftward-moving stimuli. The one left-hemisphere patient with right-sided neglect showed the opposite effect. Thus, neglect patients showed a relative overextension into their neglected side of space. While these findings are in line with the idea of an extension in the representation of contralesional space, other explanations such as deficient spatial remapping, impairments in smooth pursuit and distortions in memorized visuo-motor movements are considered.

Introduction

Spatial neglect is a puzzling disorder, which often accompanies damage to the right parietal cortex. While neglect is primarily characterised by a failure to report, respond or orient to stimuli presented to the contralesional side (Heilman, 1979), there are occasions where excessive perceptual/motor activity is directed towards the neglected hemispace. Such counterintuitive behaviour was demonstrated by Bisiach et al. (1994) when they presented a single point (corresponding to the midpoint of a previously presented line) to patients with left-sided neglect. When asked to mark the complementary endpoints of the virtual line, patients placed the left endpoint significantly further away from the centre than the right one. That is, there was an overextension instead of a neglect towards the left. This surprising finding was subsequently confirmed in a number of studies using the same or related techniques (e.g., Bisiach et al., 1996, Bisiach et al., 1998, Irving-Bell et al., 1999, Kerkhoff, 2000, Latini Corazzini et al., 2005). These studies also revealed that, although the leftward extension is frequently found, not all patients with neglect show this behaviour. Furthermore, a number of factors are known to affect the extent of overshooting, including hemianopia, stimulus position and scanning direction (e.g., Doricchi and Angelelli, 1999, Geminiani et al., 2002, Ishiai et al., 1994, Nico et al., 1999).

According to Bisiach et al. (1994), leftward extension in the endpoint task was not compatible with many common theories of spatial neglect, which attribute the disorder to attentional impairments (Heilman and Van Den Abell, 1980, Mesulam, 1981), deficits in planning and the execution of movements (Heilman et al., 1985, Watson et al., 1978) and/or disruption of space representation (Bisiach and Luzzatti, 1978). Instead, Bisiach et al., 1996, Bisiach et al., 1998) speculated that a distortion of perceived space caused the leftward overextension. Specifically, they suggested that the representation of contralesional space would be logarithmically expanded, whereas the ipsilesional side would be compressed. Consequently, for two equal horizontal line segments in representational space, the left segment would map onto a larger physical extension than the right segment. Conversely, for two equal line segments presented in physical space, the left segment is perceived as shorter than the right counterpart (see Chatterjee, 2002). The assumption of an anisometric space representation provides a theoretical framework to understand why patients with neglect overshoot towards the left in the endpoint task and why they deviate rightwards in line bisection tasks. Related accounts of a perceptually shrunken left side of physical space have also been put forward by other investigators (Halligan and Marshall, 1991, Milner and Harvey, 1995). Others, however, have questioned this account and, if acknowledged at all, a distorted space representation is seen as a mere epiphenomenon of spatial neglect (Karnath and Ferber, 1998, Perri et al., 2000; Rode et al., 2006, Rode et al., 2008).

The current study explored the hypothesis of a distorted space using the phenomenon of “representational momentum”. Representational momentum (RM) refers to the observation that, when people judge the vanishing point of a moving object that suddenly disappears, they misplace its final position in the direction of the movement (Freyd and Finke, 1984, Thornton and Hubbard, 2002). While RM has been extensively studied in healthy participants, it has only been studied once in neglect patients (McGeorge et al., 2006). In healthy subjects, variables such as velocity and direction of target motion and context of the display have been shown to modify RM. For example, a target that is believed to move faster (e.g., a rocket) results in a larger forward displacement than an object that is believed to move more slowly [e.g., a steeple (Thornton and Hubbard, 2002)]. For a review of the empirical literature on RM, see Hubbard (2005).

The standard paradigm of RM requires participants to memorize the final position of a moving target that suddenly disappears. Since a distorted space representation in neglect necessarily leads to inaccurate task performance, RM seems particularly suited to uncover such distortions. We tested this idea in a group of patients with spatial neglect, in age-matched healthy controls and in a further control group of patients with right hemisphere lesions, but no neglect symptoms (right hemisphere (RH) controls).

Prior to the main task, we assessed how accurately participants point to stationary targets presented in a variety of locations on a touch screen. This test allowed us to demonstrate that the basic ability to detect targets and accurately point to them was preserved in neglect patients.

The main task assessed RM as a function of movement direction and side of stimuli presentation. Participants pointed to the location where a moving target (moving either horizontally or vertically) suddenly vanished. For horizontal movements, a number of predictions were made. The account of distorted space representation in left neglect maintains that the left side of represented space is enlarged whereas the right side of space is compressed (Bisiach et al., 1996, Bisiach et al., 1998). If this account is correct, we expected neglect patients to show an enhanced overestimation (i.e., judging the final position further to the left than healthy participants or RH control patients) for targets moving leftwards and an underestimation for rightward movements. We also investigated whether the RM in neglect patients is modulated by the side on which the stimuli are presented (centre, left, and right hemispace). Given the inconsistent findings of position effects in the line extension task (e.g., Geminiani et al., 2002, Nico et al., 1999), no specific predictions were made for the side of stimulus presentation. Bisiach et al., 1996, Bisiach et al., 1998) framework only predicts distortions in the horizontal dimension. For vertical movements we therefore predicted no difference between healthy, control patients and neglect patients.

The RM task was also applied to a single patient with the relatively rare condition of right-sided neglect after left brain damage. For this patient, we hypothesized the reversed pattern compared to left-sided neglect patients for the horizontal conditions, but not for the vertical conditions.

Section snippets

Subjects

Nine patients with left hemi-neglect after right-hemisphere brain damage (five women; mean age 64.5 years, standard error of mean (SEM) 5.0), nine sex- and age-matched healthy controls (five women; mean age 64.5 years, SEM 4.7) and nine age-matched RH controls (four women; mean age 59.5, SEM 5.2), as well as one patient with right hemi-neglect after left-hemisphere brain damage (a 58-years old man) participated in this study. As in our previous study (Loetscher and Brugger, 2009), neglect was

Pointing accuracy task

Horizontal Deviations. The data were analysed with a 3 × 3 ANOVA with the factors Group (neglect, healthy, RH controls) and Side (left, centre, right). There was a significant effect for Side [F(2,48) = 7.5, p = .003, ηp2=.40]. Post-hoc tests demonstrated that pointing to right-sided targets (mean −.4 mm, p = .003) was more accurate than to central targets (mean −1.7 mm). Furthermore there was a main effect of Group [F(2,24) = 4.0, p < .03, ηp2=.25] with a slightly better PA in healthy (mean

Discussion

In the PA task, we established that the neglect patients was just as accurate as the controls when pointing to visible stationary targets. Importantly, we demonstrated that the equivalence between the neglect and control populations was the same irrespective of where the target appeared. This finding is in line with previous research with neglect patients, which demonstrates an absence of pointing/reaching impairments in terms of accuracy or deviation (Himmelbach and Karnath, 2003, Karnath

Conclusions

While the current study reports an apparently anomalous contralesional overshooting effect in patients with spatial neglect, the study cannot unravel the underlying processes. The reported findings are in part compatible with the idea of a distorted space representation (Bisiach et al., 1996, Bisiach et al., 1998). However, the findings can also be explained with reference to impairments in smooth pursuit of a visual target (Doricchi et al., 2007) or the maintenance of memorized target

Acknowledgement

We thank Enrique Wintsch (Zurich) for programming assistance. We are further indebted to Professor Fabrizio Doricchi and two anonymous reviewers for their valuable comments on the manuscript. BL and TL were supported by the Swiss National Science Foundation.

References (55)

  • L. Irving-Bell et al.

    A distortion of perceived space in patients with right-hemisphere lesions and visual hemineglect

    Neuropsychologia

    (1999)
  • H.O. Karnath et al.

    Kinematics of goal-directed arm movements in neglect: Control of hand in space

    Neuropsychologia

    (1997)
  • H.O. Karnath et al.

    Is space representation distorted in neglect?

    Neuropsychologia

    (1998)
  • G. Kerkhoff

    Multiple perceptual distortions and their modulation in leftsided visual neglect

    Neuropsychologia

    (2000)
  • D. Kerzel

    Eye movements and visible persistence explain the mislocalization of the final position of a moving target

    Vision Research

    (2000)
  • D. Kerzel

    Attention maintains mental extrapolation of target position: Irrelevant distractors eliminate forward displacement after implied motion

    Cognition

    (2003)
  • T. Loetscher et al.

    Random number generation in neglect patients reveals enhanced response stereotypy, but no neglect in number space

    Neuropsychologia

    (2009)
  • Ad Milner et al.

    Distortion of size perception in visuospatial neglect

    Current Biology

    (1995)
  • D. Nico et al.

    The endpoints’ task: An analysis of length reproduction in unilateral neglect

    Neuropsychologia

    (1999)
  • J.A. Ogden

    Anterior-posterior interhemispheric differences in the loci of lesions producing visual hemineglect

    Brain and Cognition

    (1985)
  • L. Pisella et al.

    Impaired working memory for location but not for colour or shape in visual neglect: A comparison of parietal and non-parietal lesions

    Cortex

    (2004)
  • S. Rossit et al.

    The neural basis of visuomotor deficits in hemispatial neglect

    Neuropsychologia

    (2009)
  • S. Rossit et al.

    Immediate and delayed reaching in hemispatial neglect

    Neuropsychologia

    (2009)
  • P. Azouvi et al.

    Sensitivity of clinical and behavioural tests of spatial neglect after right hemisphere stroke

    Journal of Neurology, Neurosurgery and Psychiatry

    (2002)
  • R.W. Baloh et al.

    Optokinetic nystagmus and parietal lobe lesions

    Annals of Neurology

    (1980)
  • E. Bisiach et al.

    Beyond unilateral neglect

    Brain

    (1996)
  • A. Chatterjee

    Spatial anisometry and representational release in neglect

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