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Head-Centred But No Body-Centered Modulation of Horizontal Space Misrepresentation in Neglect and in Hemianopia
ABSTRACT HEAD-CENTRED BUT NO BODY-CENTERED MODULATION OF HORIZONTAL SPACE MISREPRESENTATION IN NEGLECT AND IN HEMIANOPIA Fabrizio Doricchi1,2, Paola Guariglia1, Alessandra Onida1 and Francesca Figliozzi1,2 (1Centro Ricerche di Neuropsicologia, Fondazione Santa Lucia IRCCS and L.E.N.A. – Laboratorio Europeo di Neuroscienze dell’Azione; 2Dipartimento di Psicologia, Università degli Studi di Roma “La Sapienza”, Italia)
INTRODUCTION Neglect patients fail to attend to stimuli or parts of stimuli in the space contralateral to their unilateral brain damage. Visual neglect is doubly dissociated from impairments due to damage of retinotopic representations of space in primary visual pathways (i.e. hemianopia) and is thought to depend on the disruption of extra-retinotopic multimodal representations. Anisometric representation of horizontal space with relative underestimation of contralesional object size or between-object distances and corresponding relative overestimation of equivalent ipsilesional ones, was recently hypothesised to be a relevant component of neglect (Bisiach et al., 1994; Milner et al., 1993; Halligan and Marshall, 1991; Ishiai et al., 1994). Bisiach et al. (1994), specifically emphasised that anisometric misrepresentation can explain the relative contralesional overextension and the ipsilesional underextension showed by neglect patients in the reproduction of horizontal distances. This finding seems indeed difficult to explain both by contralesional hypokinesia or representational scotoma and by ipsilesional attentional bias or defective disengagement. However, misreproduction of horizontal distances appears selectively marked only when neglect is accompanied by concomitant damage of retinotopic representations of contralesional space in occipital and parietal areas (Doricchi and Angelelli, 1999; Doricchi et al., 2002a and 2002b), whereas it can be completely absent in neglect patients without concomitant visual field defects (Karnath and Ferber, 1999). Compared with neglect patients affected by concomitant hemianopia, hemianopic patients without neglect have an opposite pattern of misrepresentation (i.e. contralesional overestimation/ ipsilesional underestimation; Zihl and Von Cramon, 1986; Barton et al., 1998; Kerkhoff, 1993). The aim of the present study was to identify the spatial coordinate system (or systems) whose disruption is responsible for space misrepresentation in neglect patients (with or without hemianopia) and in pure hemianopic patients. We used a visual version of the endpoint task (Bisiach et al. 1994). In this task any asymmetry in reproduction can be attributed to genuine space misperception because the patient is forced by the examiner to look at and check the endpoints of the distance being reproduced at each step of each trial. The same could not happen in size comparison or Cortex, (2002) 38, 849-853
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landmark tasks with a segment on either side of a central reference. In this case, attention and inspection could be preferentially attracted by the center of “mass” of stimuli rather than by their endpoints, leaving open the possibility of mistaking the effects due to defective attention and representation of the most contralesional section of stimuli for those genuinely linked to space misrepresentation. In experiment 1 we investigated whether changing the position of test stimuli with respect to the patient’s body midsagittal plane (corresponding to manipulations of proprioceptive information signalling the position of the trunk under the head) produces any change in the degree of horizontal space misrepresentation. In experiment 2 we evaluated the effect of changing the headcentered position of the test stimuli (separated and combined manipulation of eye and neck position) in order to define the influence of eye-neck proprioceptive inputs on space misrepresentation. METHODS Experiment 1 Five right brain damaged patients with contralesional neglect and no hemianopia (N+H–), five right brain damaged patients with contralesional neglect and hemianopia (N+H+), three hemianopic patients (N–H+, two with left and one with right damage) and five healthy controls (C) participated in the experiment. On each trial the patients had to verbally guide the displacement of a visual target (i.e. an unlit led moved by the examiner) on a horizontal bar. The task was to reproduce in the ipsilesional (10 trials) or in the contralesional (10 trials) side of the bar, taking as reference its centre, the distance (10 cm) between the centre of the bar and another fixed target presented in the opposite side of the bar. The centre of the bar was always aligned (A) to the head midsagittal plane whereas the trunk of patients could be aligned to or shifted 30° contralesionally (TC) or ipsilesionally (TI) with respect to the head midsagittal plane (see Figure 1). Experiment 2 Ten N+H–, four N+H+, five N–H+ (three right and two left brain damaged) and five C participated in the experiment. Distances were reproduced with the centre of the bar (see Figure 1): a) aligned to the head - body midsagittal plane (A); b) aligned to the body midsagittal plane and positioned in the ipsilesional (HC) or contralesional head hemispace (HI) (head turn = 30 degrees in each case); c) placed in the contralesional (BC) or ipsilesional (BI) head-body hemispace.
RESULTS Experiment 1 Trunk turns had no effect on distance reproduction (Group × Trunk position × Side of reproduction and Trunk × Side ANOVA interactions F < 1). N+H+ had relative contralesional overextension (contra 10.3, ipsi 8.6, planned comparison p < .001), N+H– had no lateral asymmetry and N–H+ showed relative contralesional underextension (contra 9.9, ipsi 10.69, planned comparison p = .002).
Cortex Forum
851
EXPERIMENT 1
EXPERIMENT 2
Fig. 1 – Effect of trunk turns (Experiment 1) and eye-head turns (Experiment 2) on visual distance reproduction in the contralesional (contra bar side) and ipsilesional (ipsi bar side) space. The grey line at 10 cm represents perfect distance reproduction.
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Experiment 2 Bar position had a different influence on the performance of the four groups of patients (Group × Bar position × Bar side ANOVA: F = 2.6, p = .004). In the baseline condition (A) N+H– had no asymmetry (contra 9.8, ipsi 10). In the same group the deviation of the eyes towards one side of space (BI or BC conditions), with or without concomitant head deviation in the opposed direction (HI or HC conditions), induced shifting of both endpoints toward the side of space opposite the direction of gaze shift and the appearence of a corresponding asymmetry of reproduction (see Figure 1; p < .01 in each comparison). In N+H+ relative contralesional overextension was not influenced by Bar position (Bar side effect p < .001 in each comparison). In N–H+, relative contralesional underextension was abolished when the head was deviated contralesionally and the centre of the bar remained aligned to the body midsagittal line (HC condition, P ns; in all other conditions p < .001). C showed no asymmetry. DISCUSSION In the baseline condition (A) of the distance reproduction task, N+H+ patients showed relative contralesional underestimation (overextension) and ipsilesional overestimation (underextension), N+H– patients had no lateral asymmetry and N–H+ had relative contralesional overestimation (underextension) and ipsilesional underestimation (overextension). These findings reconfirm, with a purely visual task, that massive damage to retinotopic representations of space predisposes neglect patients to suffer from horizontal space misperception in distance reproduction tasks (Doricchi and Angelelli, 1999; Doricchi et al., 2002a and 2002b; see also Doricchi, in press). The reverse pattern of space misperception found in pure hemianopics replicates previous findings by Zihl and Von Cramon (1986), is in keeping with the contralesional deviation of the subjective midline showed by hemianopics in the line bisection task (Kerkhoff, 1993; Barton et al.1998) and disconfirms the finding of underestimation of contralesional horizontal space in hemianopia recently reported by Ferber and Karnath (2001). The findings from the two experiments of the present study show that horizontal space misrepresentation is not modulated by changes in the body-centred position of stimuli while it is modulated both by combined (and directionally opposed) head/eye deviation and, to a lesser degree, by selective eye deviation. These results suggest that space misrepresentation in neglect patients depends on the concomitant damage of retinotopic and extraretinotopic information at a stage of visuospatial processing where the gain of eye-centered retinotopic and head-centered representation of space is not modulated by mechanisms underlying the body centered coding of space. The absence of any modulation from eye or neck proprioception on space misrepresentation in N+H+ confirms that the total unilateral loss of retinotopic representations of space predisposes neglect patients to the highest probability of suffering the most severe form of horizontal space misperception. Acknowledgements. This study was supported by a grant from the Fondazione Santa Lucia to Fabrizio Doricchi.
Cortex Forum
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REFERENCES BARTON JJS and BLACK SE. Line bisection in hemianopia. Journal of Neurology Neurosurgery and Psychiatry, 64: 660-662, 1998. BISIACH E, RUSCONI ML, PERETTI VA and VALLAR G. Challenging current accounts of unilateral neglect. Neuropsychologia, 32: 1431-1434, 1994. DORICCHI F. The contribution of retinotopic and multimodal coding of space to horizontal space misrepresentation in neglect and hemianopia. In HO Karnath, AD Milner and G Vallar (Eds), The cognitive and neural bases of spatial neglect. Oxford University Press, in press. DORICCHI F and ANGELELLI P. Misrepresentation of horizontal space in left unilateral neglect. Role of hemianopia. Neurology, 52: 1845-1852, 1999. DORICCHI F, GALATI G, DELUCA L, NICO D and D’OLIMPIO F. Horizontal space misrepresentation in unilateral brain damage. Part I. Visual and proprioceptive – motor influences in left unilateral neglect. Neuropsychologia, 40: 1101-1117, 2002a. DORICCHI F, ONIDA A and GUARIGLIA P. Horizontal space misrepresentation in unilateral brain damage. Part II. Eye-head centered modulation of visual misrepresentation in hemianopia without neglect Neuropsychologia, 40: 1118-1128, 2002b. FERBER S and KARNATH HO. Size perception in hemianopia and neglect. Brain, 124: 527-536, 2001. HALLIGAN PW and MARSHALL JC. Spatial compression in visual neglect: A case study. Cortex, 27: 623629, 1991. ISHIAI S, SUGISHITA M, WATABIKI S, NAKAYAMA T, KOTERA M and GONO S. Improvement of left unilateral spatial neglect in a line extension task. Neurology, 44: 294-298, 1994. KARNATH HO and FERBER S. Is space representation distorted in neglect? Neuropsychologia, 37: 7-15, 1999. KERKHOFF G. Displacement of the egocentric visual midline in altitudinal postchiasmatic scotomata. Neuropsychologia, 31: 261-265, 1993. MILNER AD, HARVEY M, ROBERTS RC and FORSTER SV. Line bisection errors in visual neglect: Misguided action or size distortion? Neuropsychologia, 31: 39-49, 1993. ZIHL J and VON CRAMON D. Zerebrale Sehstörungen. Stuttgart: Kohlhammer; 1986. Fabrizio Doricchi, Centro Ricerche di Neuropsicologia – Fondazione Santa Lucia – IRCCS, Via Ardeatina 306 - 00179 Roma. Italia. e-mail: [email protected]
INTRODUCTION Neglect patients fail to attend to stimuli or parts of stimuli in the space contralateral to their unilateral brain damage. Visual neglect is doubly dissociated from impairments due to damage of retinotopic representations of space in primary visual pathways (i.e. hemianopia) and is thought to depend on the disruption of extra-retinotopic multimodal representations. Anisometric representation of horizontal space with relative underestimation of contralesional object size or between-object distances and corresponding relative overestimation of equivalent ipsilesional ones, was recently hypothesised to be a relevant component of neglect (Bisiach et al., 1994; Milner et al., 1993; Halligan and Marshall, 1991; Ishiai et al., 1994). Bisiach et al. (1994), specifically emphasised that anisometric misrepresentation can explain the relative contralesional overextension and the ipsilesional underextension showed by neglect patients in the reproduction of horizontal distances. This finding seems indeed difficult to explain both by contralesional hypokinesia or representational scotoma and by ipsilesional attentional bias or defective disengagement. However, misreproduction of horizontal distances appears selectively marked only when neglect is accompanied by concomitant damage of retinotopic representations of contralesional space in occipital and parietal areas (Doricchi and Angelelli, 1999; Doricchi et al., 2002a and 2002b), whereas it can be completely absent in neglect patients without concomitant visual field defects (Karnath and Ferber, 1999). Compared with neglect patients affected by concomitant hemianopia, hemianopic patients without neglect have an opposite pattern of misrepresentation (i.e. contralesional overestimation/ ipsilesional underestimation; Zihl and Von Cramon, 1986; Barton et al., 1998; Kerkhoff, 1993). The aim of the present study was to identify the spatial coordinate system (or systems) whose disruption is responsible for space misrepresentation in neglect patients (with or without hemianopia) and in pure hemianopic patients. We used a visual version of the endpoint task (Bisiach et al. 1994). In this task any asymmetry in reproduction can be attributed to genuine space misperception because the patient is forced by the examiner to look at and check the endpoints of the distance being reproduced at each step of each trial. The same could not happen in size comparison or Cortex, (2002) 38, 849-853
850
Fabrizio Doricchi and Others
landmark tasks with a segment on either side of a central reference. In this case, attention and inspection could be preferentially attracted by the center of “mass” of stimuli rather than by their endpoints, leaving open the possibility of mistaking the effects due to defective attention and representation of the most contralesional section of stimuli for those genuinely linked to space misrepresentation. In experiment 1 we investigated whether changing the position of test stimuli with respect to the patient’s body midsagittal plane (corresponding to manipulations of proprioceptive information signalling the position of the trunk under the head) produces any change in the degree of horizontal space misrepresentation. In experiment 2 we evaluated the effect of changing the headcentered position of the test stimuli (separated and combined manipulation of eye and neck position) in order to define the influence of eye-neck proprioceptive inputs on space misrepresentation. METHODS Experiment 1 Five right brain damaged patients with contralesional neglect and no hemianopia (N+H–), five right brain damaged patients with contralesional neglect and hemianopia (N+H+), three hemianopic patients (N–H+, two with left and one with right damage) and five healthy controls (C) participated in the experiment. On each trial the patients had to verbally guide the displacement of a visual target (i.e. an unlit led moved by the examiner) on a horizontal bar. The task was to reproduce in the ipsilesional (10 trials) or in the contralesional (10 trials) side of the bar, taking as reference its centre, the distance (10 cm) between the centre of the bar and another fixed target presented in the opposite side of the bar. The centre of the bar was always aligned (A) to the head midsagittal plane whereas the trunk of patients could be aligned to or shifted 30° contralesionally (TC) or ipsilesionally (TI) with respect to the head midsagittal plane (see Figure 1). Experiment 2 Ten N+H–, four N+H+, five N–H+ (three right and two left brain damaged) and five C participated in the experiment. Distances were reproduced with the centre of the bar (see Figure 1): a) aligned to the head - body midsagittal plane (A); b) aligned to the body midsagittal plane and positioned in the ipsilesional (HC) or contralesional head hemispace (HI) (head turn = 30 degrees in each case); c) placed in the contralesional (BC) or ipsilesional (BI) head-body hemispace.
RESULTS Experiment 1 Trunk turns had no effect on distance reproduction (Group × Trunk position × Side of reproduction and Trunk × Side ANOVA interactions F < 1). N+H+ had relative contralesional overextension (contra 10.3, ipsi 8.6, planned comparison p < .001), N+H– had no lateral asymmetry and N–H+ showed relative contralesional underextension (contra 9.9, ipsi 10.69, planned comparison p = .002).
Cortex Forum
851
EXPERIMENT 1
EXPERIMENT 2
Fig. 1 – Effect of trunk turns (Experiment 1) and eye-head turns (Experiment 2) on visual distance reproduction in the contralesional (contra bar side) and ipsilesional (ipsi bar side) space. The grey line at 10 cm represents perfect distance reproduction.
852
Fabrizio Doricchi and Others
Experiment 2 Bar position had a different influence on the performance of the four groups of patients (Group × Bar position × Bar side ANOVA: F = 2.6, p = .004). In the baseline condition (A) N+H– had no asymmetry (contra 9.8, ipsi 10). In the same group the deviation of the eyes towards one side of space (BI or BC conditions), with or without concomitant head deviation in the opposed direction (HI or HC conditions), induced shifting of both endpoints toward the side of space opposite the direction of gaze shift and the appearence of a corresponding asymmetry of reproduction (see Figure 1; p < .01 in each comparison). In N+H+ relative contralesional overextension was not influenced by Bar position (Bar side effect p < .001 in each comparison). In N–H+, relative contralesional underextension was abolished when the head was deviated contralesionally and the centre of the bar remained aligned to the body midsagittal line (HC condition, P ns; in all other conditions p < .001). C showed no asymmetry. DISCUSSION In the baseline condition (A) of the distance reproduction task, N+H+ patients showed relative contralesional underestimation (overextension) and ipsilesional overestimation (underextension), N+H– patients had no lateral asymmetry and N–H+ had relative contralesional overestimation (underextension) and ipsilesional underestimation (overextension). These findings reconfirm, with a purely visual task, that massive damage to retinotopic representations of space predisposes neglect patients to suffer from horizontal space misperception in distance reproduction tasks (Doricchi and Angelelli, 1999; Doricchi et al., 2002a and 2002b; see also Doricchi, in press). The reverse pattern of space misperception found in pure hemianopics replicates previous findings by Zihl and Von Cramon (1986), is in keeping with the contralesional deviation of the subjective midline showed by hemianopics in the line bisection task (Kerkhoff, 1993; Barton et al.1998) and disconfirms the finding of underestimation of contralesional horizontal space in hemianopia recently reported by Ferber and Karnath (2001). The findings from the two experiments of the present study show that horizontal space misrepresentation is not modulated by changes in the body-centred position of stimuli while it is modulated both by combined (and directionally opposed) head/eye deviation and, to a lesser degree, by selective eye deviation. These results suggest that space misrepresentation in neglect patients depends on the concomitant damage of retinotopic and extraretinotopic information at a stage of visuospatial processing where the gain of eye-centered retinotopic and head-centered representation of space is not modulated by mechanisms underlying the body centered coding of space. The absence of any modulation from eye or neck proprioception on space misrepresentation in N+H+ confirms that the total unilateral loss of retinotopic representations of space predisposes neglect patients to the highest probability of suffering the most severe form of horizontal space misperception. Acknowledgements. This study was supported by a grant from the Fondazione Santa Lucia to Fabrizio Doricchi.
Cortex Forum
853
REFERENCES BARTON JJS and BLACK SE. Line bisection in hemianopia. Journal of Neurology Neurosurgery and Psychiatry, 64: 660-662, 1998. BISIACH E, RUSCONI ML, PERETTI VA and VALLAR G. Challenging current accounts of unilateral neglect. Neuropsychologia, 32: 1431-1434, 1994. DORICCHI F. The contribution of retinotopic and multimodal coding of space to horizontal space misrepresentation in neglect and hemianopia. In HO Karnath, AD Milner and G Vallar (Eds), The cognitive and neural bases of spatial neglect. Oxford University Press, in press. DORICCHI F and ANGELELLI P. Misrepresentation of horizontal space in left unilateral neglect. Role of hemianopia. Neurology, 52: 1845-1852, 1999. DORICCHI F, GALATI G, DELUCA L, NICO D and D’OLIMPIO F. Horizontal space misrepresentation in unilateral brain damage. Part I. Visual and proprioceptive – motor influences in left unilateral neglect. Neuropsychologia, 40: 1101-1117, 2002a. DORICCHI F, ONIDA A and GUARIGLIA P. Horizontal space misrepresentation in unilateral brain damage. Part II. Eye-head centered modulation of visual misrepresentation in hemianopia without neglect Neuropsychologia, 40: 1118-1128, 2002b. FERBER S and KARNATH HO. Size perception in hemianopia and neglect. Brain, 124: 527-536, 2001. HALLIGAN PW and MARSHALL JC. Spatial compression in visual neglect: A case study. Cortex, 27: 623629, 1991. ISHIAI S, SUGISHITA M, WATABIKI S, NAKAYAMA T, KOTERA M and GONO S. Improvement of left unilateral spatial neglect in a line extension task. Neurology, 44: 294-298, 1994. KARNATH HO and FERBER S. Is space representation distorted in neglect? Neuropsychologia, 37: 7-15, 1999. KERKHOFF G. Displacement of the egocentric visual midline in altitudinal postchiasmatic scotomata. Neuropsychologia, 31: 261-265, 1993. MILNER AD, HARVEY M, ROBERTS RC and FORSTER SV. Line bisection errors in visual neglect: Misguided action or size distortion? Neuropsychologia, 31: 39-49, 1993. ZIHL J and VON CRAMON D. Zerebrale Sehstörungen. Stuttgart: Kohlhammer; 1986. Fabrizio Doricchi, Centro Ricerche di Neuropsicologia – Fondazione Santa Lucia – IRCCS, Via Ardeatina 306 - 00179 Roma. Italia. e-mail: [email protected]