Elsevier

Neuropsychologia

Volume 37, Issue 12, November 1999, Pages 1387-1405
Neuropsychologia

Multimodal spatial orientation deficits in left-sided visual neglect

https://doi.org/10.1016/S0028-3932(99)00031-7Get rights and content

Abstract

Patients with right-sided temporo-parietal lesions often show contralesional neglect. However, neglect patients may also show spatial–perceptual deficits beyond the bisection and space exploration deficits frequently assessed in the horizontal plane, that is, deficits in the judgment of the subjective visual vertical or horizontal. In a recent study (Kerkhoff, G. & Zoelch, C., Disorders of visuo–spatial orientation in the frontal plane in patients with visual neglect following right or left parietal lesions. Exp. Brain Res., 1998;122:108–120) we found significant perturbations in the perception of these three visual–spatial axes in patients with contralesional neglect from right or left parietal lesions. To examine if this finding extends also to another modality we investigated how neglect patients perform tasks of visual– and tactile–spatial judgments of axis-orientation in the frontal plane. Visual–spatial and tactile–spatial judgments of the subjective vertical, horizontal and a right oblique orientation were obtained from patients with and without neglect as well as from normal subjects. Patients with left neglect showed a significant, contraversive tilt of all three visual–spatial axes (+5.6° to +9.5°, counterclockwise), and of the three tactile–spatial axes as well (+5.2° to +10.5°, counterclockwise). In contrast, right and left hemisphere lesioned control patients without neglect and normal control subjects showed unimpaired visual and tactile–spatial judgments (constant errors: <1.0°). Difference thresholds in the visual–spatial tasks and unsigned errors in the tactile–spatial tasks were selectively elevated in the neglect group in contrast to all other subject groups. Spatial orientation deficits were significantly associated with the severity of clinical neglect (r=0.55–0.88), and with the patients’ ambulation performance (r=0.45–0.70). Furthermore, crossmodal axis orientation tests in two neglect patients showed a similar counterclockwise tilt of +5° to +15°, suggesting a similar spatial deficit in both modalities. Orientation judgments were significantly aggravated by a 25°-tilt of the head to the left, as tested in one neglect patient, while a comparable rightward head-tilt improved spatial judgments in both modalities. This suggests that spatial orientation judgments are significantly modulated by gravitational input in neglect patients. Together these results are interpreted as evidence for multisensory spatial orientation deficits in neglect patients which are modulated by head-position and are related to their accompanying postural impairment.

Introduction

Patients with hemispatial neglect fail to detect or respond to visual, acoustic or tactile stimuli in their contralesional hemispace [7]. Some current models of neglect focus on deficits in the patient’s horizontal plane which are apparent as omissions of critical targets in left hemispace during visual search, or a rightward deviation both in pointing straight ahead or in line bisection.

Within this horizontal plane several abnormalities of spatial perception or representation have been demonstrated in neglect patients ranging from a selective deficit in horizontal size perception in left hemispace [39], [40], a deviation of space representation towards the right ipsilesional hemispace [7] to a compression of left hemispace [22], [42] or both hemispaces in one case [26]. While most studies have focused on deviations in left/right terms in the horizontal plane a few emphasized perception in the vertical dimension [39], [57]. Milner and Harvey [39], [40] found normal size judgments in three neglect patients in the vertical domain whereas [57] found deficits of position sense in neglect patients in the horizontal and vertical domain. Their neglect patients showed impairments in judging the position of their occluded left and right arm when it was positioned passively by the experimenter to different positions in the horizontal and vertical plane. This deficit was significantly reduced by optokinetic stimulation towards the left, neglected side.

However, patients with parietal lesions may show more than neglect of contralesional hemispace. Numerous studies have demonstrated deficits in visual–spatial perception and visuomotor performance in this patient group (for a review see [14]. Patients with right parietal lesions often show most pronounced deficits in visual orientation discrimination and position estimation [53], [54], [61]. Disturbances in the judgment of the principal visual axes [28], the Subjective Visual Vertical and Horizontal (further abbreviated as SVV and SVH), have been documented repeatedly in this patient group [16], [34], [56]. Deficits in the judgment of line orientations, especially oblique orientations, are found with right parietotemporal lesions [32] and are especially frequent in patients with right hemispheric lesions [4]. Evidence from positron emission tomography (PET) suggests an important although not exclusive, role of the right parietal cortex in oblique orientation discrimination [59]. In a recent investigation Brandt and colleagues [8] tested 71 patients with unilateral hemispheric lesions in the judgment of the SVV and found that the most impaired patients had lesions centering on an area considered as the human homologue of the monkey parieto-insular-vestibular cortex (PIVC, cf. [24]). Hence, both clinical and more detailed lesion evidence using MRI analyses suggest that patients with parietal lesions show more than a displacement of an egocentric reference frame to the ipsilesional side of space. Patients with such, or very similar lesions, may also present with abnormal visual–spatial perception of the SVV and oblique line orientations in another spatial plane, the frontal plane. Surprisingly, possible relations between disturbances in these two spatial planes (horizontal and frontal plane) have rarely been studied together in the same sample.

In a recent study [31] we investigated visual–spatial orientation in the frontal plane in neglect patients using a novel PC-based measurement system. Twelve of thirteen patients with left-sided, and all three patients with right-sided visual neglect showed significant deficits in visual–spatial judgments of axis-orientation in the vertical, horizontal and a right oblique orientation whereas left or right hemisphere lesioned control patients performed indistinguishably from normal subjects. While these findings indicate a significant error in the central representation of space in the frontal plane they did not allow conclusions as to whether this deficit extends also to another modality, thus indicating a possible multisensory or even supramodal disorder. In the present study we addressed three questions by investigating visual–spatial and tactile–spatial axis-orientation in neglect patients, control patients and normal subjects:

  • 1.

    Are neglect patients similarly impaired in tactile orientation as in visual–spatial orientation?

  • 2.

    Are spatial orientation deficits related to the severity of neglect?

  • 3.

    Are these deficits related to motor activities requiring accurate perception of verticality, that is, ambulation?

  • 4.

    Is there evidence for a supramodal deficit, when subjects are required to perform crossmodal orientation matches? 5. Is the deficit of axis orientation modulated by gravitational input? Results to the first and fourth question would allow conclusions about the nature of the spatial deficit (modality-specific or supramodal deficit?) while results to the remaining questions would indicate a significant influence of these deficits on the clinical symptomatology of neglect.

Earlier studies on tactile perception of the vertical and horizontal [16], [38] and about visual and tactile orientation discrimination [12], [21] indicated that patients with right posterior, probably temporo-parietal lesions are significantly impaired in both modalities when tested with their non-paretic right hand. De Renzi and coworkers [16] found similar deficits in the judgment of the vertical and horizontal axis in the tactile and visual domain in patients with ‘right posterior brain’ lesions whereas all other patient groups performed like normal controls. Unfortunately, they did not comment on the relationship of these spatial disturbances to neglect in their study. However, they noted that ‘the available evidence points to the right parietal lobe as the crucial area involved in this function’ ([16], p. 494). As in the visual modality, it has rarely been investigated in one sample if neglect patients are also impaired in such spatial tasks in the frontal plane although the most frequent lesion location for patients with left neglect is the right temporo-parietal cortex and its underlying white matter [58].

Three experiments are described in the present article. First, a group study was conducted to test for visual– and tactile–spatial orientation deficits in patients with and without left visual neglect, as well as in normal subjects. In the second experiment, crossmodal spatial orientation judgments were obtained in two neglect patients and one normal subject, to test more directly whether there is a supramodal deficit in spatial orientation in neglect. In the third experiment, one neglect patient and one normal subject were tested with different levels of lateral head inclination (head upright, head tilted to the left or right by 25°) to study the possible effects of gravitational influences (through head orientation) on visual and tactile–spatial orientation judgments.

Section snippets

Subjects

Eleven patients with right hemispheric, vascular lesions and left spatial neglect documented by clinical tests (number cancellation, object search, line bisection, drawing, reading, see below), 12 patients with right hemispheric vascular lesions and 11 patients with left hemispheric lesions without spatial neglect in these tests (further referred to as RBD or LBD controls or simply as control patients) and 22 normal subjects were tested. Eleven normal subjects were tested in the tactile tests

Neglect tests

All neglect subjects showed the typical rightward deviation in horizontal line bisection (mean deviation=11.8 mm to the right), as well as a profound visual exploration deficit in object search with prolonged search times in the left, contralesional hemispace (mean=36.3 s) than in their ipsilesional, right hemispace (mean=13.7 s; t=10.79, P<0.0001). Neither the LBD controls (mean search time left/right hemispace=12.7/12.3 s) nor the RBD controls showed any significant asymmetry in object search

Experiment 2: crossmodal spatial judgments

To evaluate whether neglect patients show a similar pattern of results when required to match the spatial orientation perceived in one modality (visual or tactile) in the other modality and vice-versa two neglect patients and one normal subject were tested. It was hypothesized that both patients—but not the normal subject—should show a similar counterclockwise tilt of their spatial axes when performing the task crossmodally.

Modality-specific or supramodal spatial disorders in neglect?

Our neglect patients with predominantly parietal lesions showed visual- and tactile–spatial orientation deficits in axes other than the horizontal. The significant correlations between the visual and tactile variants of the spatial tasks indicate a significant relationship, although not necessarily supramodality in the sense that visual and tactile perceptual tilts are of identical magnitude. However, the direction of tilts was identical in nearly all neglect subjects suggesting a mechanism

Acknowledgements

I am grateful to Charles Heywood, PhD, from Durham, UK for his helpful comments, and two anonymous reviewers for suggesting Experiments 2 and 3.

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