Elsevier

Neuropsychologia

Volume 37, Issue 8, 1 July 1999, Pages 881-894
Neuropsychologia

Egocentric frame of reference: its role in spatial biasafter right hemisphere lesions

https://doi.org/10.1016/S0028-3932(98)00150-XGet rights and content

Abstract

The reference shift hypothesis of unilateral neglect holds that spatial bias in left neglectstems from a rightward deviation of patients egocentric frame of reference (ER). Twenty fiveunselected right brain-damaged patients participated in a straight-ahead pointing task to assessthe position of their ER (Experiment 1). A rightward ER shift emerged only in the subgroup ofpatients with extensive parietal lesions. In Experiment 2, we found that the position of the ER didnot predict the outcome of various visuospatial neglect tests (r = 0.07 to 0.27). In Experiment 3,no significant positive correlation emerged between the ER position and visual (r = 0.26) ortactile (r = −0.48) extinction. Two further experiments examined the relationships between theER position and patients performance on a reaction time test of directional motor bias(Experiment 4), and on a test of response times to lateralised visual stimuli (Experiment 5).Results showed that the ER position did not predict the distribution of accuracy scores orresponse times in either task (Experiment 3: accuracy: r = 0.06; response times: r = 0.16;Experiment 4: accuracy: r = 0.09; response times: r = 0.04). We concluded that the position ofthe ER plays no crucial role in the behavioural consequences of spatial bias induced by righthemisphere lesions.

Introduction

Patients with right hemisphere brain lesion who suffer from left hemineglect show a directionalbias toward the right side of space when perceiving and acting in their environment. A number oftheories have been advanced to account for this often dramatic and pervasive behavioural pattern,but neglect has up to now proved elusive for a unitary explanation, and there is no consensus aboutits causal mechanisms [25]. Recently the hypothesis has been proposed that the crucial mechanismleading to neglect is the disturbed transformation of sensory input into a supramodal egocentricframe of reference (ER), causing in turn a deviation of this reference frame toward the side ipsilateralto the brain lesion 36, 58. We shall refer to this as the reference shift hypothesis of neglect. Thishypothesis draws on the more general notion that spatially-directed behaviour is coded in a systemof coordinates (a motor map of space) referred to the body axis, different from the visual map onwhich the retinal position of objects is specified [[31], p. 87]. This egocentric coordinate system isnormally superimposed to the sagittal middle, but a unilateral brain lesion would produce a deviationof the ER through an imbalance between the bilateral neural processes which build thisrepresentation 31, 62.

The concept of a supramodal coordinate system used for visuomotor and exploratory behaviourhas been postulated on the grounds that the integration of data from different sources of sensoryinput (visual, tactile, vestibular, auditory, proprioceptive) is necessary for an organism to interacteffectively with its environment. A unique representation would perform the computations to solve,for example, the problems posed by the spatial distortion of sensory and motor primary corticalrepresentations (e.g., there is no isomorphism between the retina and its cortical projections, thefovea being overrepresentated in V1), by the fact that receptive surfaces are constantly moving, andby the different coordinate systems used by different primary sensory and motor maps [56].

An efficient way of building this single coherent frame of reference would be to code it in termsof egocentric coordinates relative to the sagittal middle; this putative space representation is theegocentric frame of reference postulated by the reference shift hypothesis of neglect. It has to benoted, however, that it is not necessary to postulate such a single central representation of the ER;multisensory integration could be performed by a distributed mechanism, as a neural network fortransforming one set of sensory vectors into other sensory reference frames [56]. Furthermore, severalindependent mechanisms of this type could be at work in parallel in different brain areas [55].Whatever the mechanism in use, it should provide the possibility of locating stimuli relative to theobserver, of acting with reference to them and of representing the position of the body in space. Inthe hypothesis of a frame of reference coded in egocentric coordinates, it has been suggested that thetrunk vertical midline, and not the head or visual field midlines, constitutes the anchor of thisrepresentation [42]. Thus, the usual way of testing the perceived direction of the ER is to ask subjectsto point straight ahead while blindfolded and to record this subjective position 31, 63.

If left neglect patients suffer from an ipsilesional deviation of their ER, then they are expectedto point to the right of the objective midline on this task. This pattern of performance has indeedbeen described in some studies. Heilman, Bowers and Watson [30] tested five right brain-damaged(RBD) patients with left neglect and five left brain-damaged patients, and found that both groupserred toward the side ipsilateral to the brain lesion; RBD neglect patients, however, showed a greateripsilesional deviation than left brain-dmaged patients. Because the pointing task did not requirevisual of somesthetic input, Heilman and coworkers interpreted their results in neglect patients interms of a directional motor disorder (hemispatial akinesia). The finding of an ipsilesional shift ofthe subjective sagittal middle in left neglect was replicated in one patient with a proprioceptivestraight-ahead pointing task [13] and in three patients with a visual straight-ahead pointing task [36].Perenin found a mean rightward deviation of about 9° in a group of 25 left neglect patients using astraight-ahead pointing task performed in darkness [50].

These findings support the reference shift hypothesis of neglect, which predicts an associationbetween left neglect and rightward deviation on the straight-ahead pointing task, both phenomenabeing consequent upon an underlying distortion of the ER. However, recent evidence suggests thatthis association may not be the rule. Hasselbach and Butter [28] found an ipsilesional bias inperceiving straight ahead (in a visual condition) in two patients with extensive right parietal lesions,but not in three RBD patients whose lesions largely spared the parietal lobe, even though the latterpatients showed left neglect signs. A dissociation between left neglect and rightward shift of the ERwas thus demonstrated. Moreover, in another study [18] employing a similar visual paradigm (inwhich patients were required to stop a moving spot as it crossed their perceived midline), a rightwardER deviation was observed only when the direction of the spot was from the right to the left, and notin the opposite condition, in which neglect patients were accurate in locating their perceivedegocentre; on the other hand, in a proprioceptive straight-ahead pointing task no evidence of ERdisplacement was found in the neglect group.

In a recent study [10] we addressed more directly the issue of the interaction between neglect andER position, by examining the relationship between the proprioceptive straight-ahead pointing taskand a battery of neglect tests. We studied a series of six RBD patients, three showing signs of leftunilateral neglect, three without signs of neglect. Results showed that all patterns of dissociationwere possible between left neglect and rightward deviation in the pointing task. Patients showedleftward, rightward or no significant deviation when pointing straight ahead, irrespective of thepresence or absence of neglect signs. Particularly impressive was the performance of a left neglectpatient (case 2), who pointed significantly to the left (that is, toward his neglected hemispace). Case2 thus showed a deviation of his ER in the opposite direction for that predicted by the reference shifthypothesis of neglect. Our findings thereby suggested that there is no causal relationship betweenthe position of the ER and left neglect. This conclusion was based on the classicalneuropsychological method of inferring the functional independence between two signs by findingdouble dissociations between these signs in individual case studies. Nevertheless, our data could inprinciple have suffered from possible idiosyncratic differences, because they were obtained in asmall series of patients, and hence could not be conclusive to disprove the reference shift hypothesisof neglect (note, however, that also data showing an ipsilesional ER deviation in neglect were mostlybased on small groups of patients). An alternative approach for determining whether two tasks loadon the same process is to examine the correlation between these tasks in a group study [53]. Thus,for example, low correlations between the direction and magnitude of the deviation of the ER andbehavioural measures of neglect in a group of RBD patients would provide converging evidence thatthe position of the ER is not causally related to neglect. Experiments 1 and 2 of the present studyexamined the position of the ER in a group of 25 unselected RBD patients and the relationship ofthis position with patients performance on several neglect tests.

Another issue was left open by our previous study [10]. We found that RBD patients withoutclinical signs of neglect may show an ipsilesional shift of their ER. Thus, this deviation might berelated to forms of spatial bias other than clinically manifest neglect. To address this issue, weinvestigated whether the position of the ER was related to visual or tactile extinction (Experiment3), to a directional motor bias in producing lateralised arm movements (Experiment 4), or to a biaswhen producing central manual responses to lateralised visual stimuli (Experiment 5). In this way,we explored the relationships between the position of the ER and patients performance in each ofseveral levels of spatial processing ranging from perception to action.

Section snippets

Subjects

Twenty five right brain-damaged patients and 22 age-matched control subjects free ofneurological damage (mean age: 62 years; range 47–80) consented to participate in this study.Patients were consecutively tested upon their admission in neurological or rehabilitation units. Theonly inclusion criteria was their ability to perform all the experimental tasks. Patients did not showany clinical evidence for ipsilesional motor or proprioceptive deficit, or misreaching with the rightarm. Table 1

Experiment 1: straight-ahead pointing task

The aim of the present experiment was to assess the position of the egocentric reference in anunselected group of RBD patients, by using the classic proprioceptive straight-ahead pointing task31, 63.

Most previous studies testing the link between the position of the subjective median plane andleft neglect signs have employed relatively small groups of brain-damaged patients, who wereselected on the basis of the presence or absence of left neglect signs 10, 13, 30, 35, 36, 37, 38. Thefact that

Experiment 2: neglect tests

Following the reference shift hypothesis, in left neglect the subjective body midline is shiftedtowards the right side because the system which builds the egocentric frame of reference works witha systematic rightward error [35]. Consequently, patients subjective space is split into a left and aright half by what they now perceive as their body midline. In turn, this distortion determines asystematic rightward bias in exploratory behaviour, which results in signs of left neglect. Thus,

Experiment 3: visual and tactile extinction

Contralesional extinction, or the failure to report the contralesional stimulus on doublesimultaneous simulation with normal detection on single presentation, is often described in neglectpatients, both in the visual and tactile modalities (it can also be present in the auditory and olfactivemodalities).

The relationships between neglect and extinction are not clear, neither are the causal mechanismsof extinction [4]. Although neglect patients usually show visual extinction [20], and may

Experiment 4: directional motor bias

Left neglect patients may be reluctant to perform arm movements in or toward the left hemispace5, 29, 45, 46, 57. Although the role of this directional motor disorder in neglect is far from beingclear [3], a distinction has been proposed between forms of neglect more linked to a perceptual (oroculomotor) bias and forms of neglect more based on a deficit in executing arm movements towardthe neglected space 8, 57.

The weak correlations between the position of the ER and the results of visuospatial

Experiment 5: subclinical spatial bias

The data presented thus far strongly suggest that there is no causal relationship between deviationof the egocentric reference and clinical signs of neglect (Experiment 2) or extinction (Experiment3), nor between the position of the ER and a directional motor bias for goal-directed arm movements(Experiment 4). However, the possibility remains open that a deviation of the ER might determinea form of spatial bias which is not necessarily accompanied by signs of neglect, extinction, ordirectional

General discussion

In the present study, we assessed the position of the egocentric frame of reference in a group ofunselected right brain-damaged patients (Experiment 1). Consistent with earlier observations [28],we found an overall rightward shift of the perceived midline only in the subgroup of patients withextensive parietal lesions. We subsequently investigated the relationships between the position ofthe egocentric frame of reference and several measures of spatial bias. We found that the directionand

Acknowledgements

This research was supported by grants from the Consiglio Nazionale delle Ricerche to the firstauthor and the Région Rhône-Alpes to the second author, and was presented at the 16th EuropeanWorkshop on Cognitive Neuropsychology, Bressanone, Italy, January 1998. We thank Prof. J-D.Degos, Dr C. Loeper-Jény, and the administration and staff of Henri-Mondor and Saint-MauriceHospitals, for permission to study patients under their care. We are grateful to Prof. E. Bisiach forhis critical reading of a

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