Personal and extrapersonal space: A case of neglect dissociation

0

PERSONAL

CO?&3932;92 $5 00 + 0.W 1992 Pergamon Prrs* Ltd

AND EXTRAPERSONAL SPACE: A CASE OF NEGLECT DISSOCIATION

CECILIA GUARIGLIA* and GABRIELLA ANTONUCCI Dip. Psicologia,

UniversitB

“La Sapienza”

(Received 18 February

1992;

and Clinica accrpted

S. Lucia,

Roma,

Italy

21 Ju/$ 1992)

Abstract--Dissociation between personal and extrapersonal neglect has rarely been observed in man. In this study we present a case of severe personal neglect in the absence of a deficit for extrapersonal space. An extensive neuropsychological assessment demonstrates the absence of cognitive impairments in visuo-spatial processing and confirms the selective presence of a severe representational deficit of the left side of the body.

INTRODUCTION IN UNILATERALNEGLECTthe presence of deficits relative to the side of the body contralateral to the lesion (personal neglect) has often been described (e.g. Refs [4] and [17]). These patients do not recognize their own paretic limbs and are unable to use their left limbs even if they are not affected by motor impairments (motoric aspontaneity); and often they are unable to represent the left side of their body or to describe and represent its position in space

C181. Personal neglect is often associated with the inability to discriminate the contralesional arm position. This deficit was present in 40% of 55 right brain-damaged patients studied by WILLANGER et al. [ 181; 45% of them also showed anosognosia for motor impairments. Five patients with a defective sense of position and/or anosognosia were also affected by visual neglect. Ten patients showed visual neglect dissociated from personal neglect and five patients personal neglect without any explorative defects. C~SLETT [S] demonstrated the presence of a specific impairment in the representation of the left side of the body; he presented colour pictures of left and right hands seen from the palm or from the back to right brain-damaged patients with and without neglect. Neglect patient selectively failed in recognizing the left but not the right hand. His performances were significantly worse than those of left and right brain-damaged patients without neglect, especially when presented with the left back of the hand. Coslett interpreted these results by stating that discriminating left and right hands requires a matching between perceptual information and body representations; low performance on this task reflects a defect in the body schema representation of the side of the body contralateral to the lesion. Thus it may be that a specific module for the representation of the body exists; when this module is damaged by a cerebral lesion there is a distortion in the representation of the spatial relationship between body parts and a deficit in the recognition of their relative positions. *Address for reprint Roma, Italy.

requests:

C. Guariglia,

Dip. Psicologia,

1001

Universiti

“La Sapienza”,

Via dei Marsi, 78,00185

1002

C.

GUAKGLIA

and G. ANTONLKTI

Several experimental and clinical studies have tried to evaluate the independence of deficits relative to extrapersonal space and to body spatial representation. As several different words are used in the literature for indicating different portions of the space, in this paper we will indicate the subject’s body as persor~ul spuce and both peripersonal or reaching space and the far space as rxtruprrsonal spuce. Experimental studies have demonstrated a dissociation between disorders in processing extrapersonal and personal space. In monkeys a lesion of the right area six produces defects in exploring the perioral and the reaching left side of the space; while a lesion of the right frontal eye field produces a defect in exploring the far left side of the space without affecting the personal and the peripersonal space [14]. In man, dissociation between personal and extrapersonal neglect are quite rare. BISIACHet al. [4] analysed the performances of 96 right brain-damaged patients in a test of personal neglect, requiring patients to touch the left hand with the right hand, and in a test of extrapersonal neglect, consisting of a cancellation task. They found 37 cases of extrapersonal and 36 cases of personal neglect; only one out of two patients with severe personal neglect failed to show any sign of comparable extrapersonal neglect, while nine patients with severe extrapersonal neglect were unaffected by a comparable deficit for personal space. If we also consider the patients with moderate neglect, there are 30 out of 36 cases of extrapersonal neglect without personal deficits; however, there is no increase in personal neglect without extrapersonal deficits. Using the same test of personal neglect, PIZZAMIGLIO et a/. [12] failed to find cases of personal neglect in 18 acute and 48 chronic patients with cerebrovascular lesions in the left hemisphere. No evidence of dissociation similar to that demonstrated in monkeys by RIZZOLATTI et ul. [14] was found in this group. PIZZAMIGLIO et al. [12] studied the performances of 28 neglect patients in a neglect test [ 1 l] which allows for the presentation of stimuli in different portions of space without changing presentation and response modalities.* The authors did not find any dissociated case in which the exploration deficit was present only for far or for near extrapersonal space. They conclude that different systems do not exist for processing different portions of inputs from extrapersonal space: however, they suggest the possibility that this differentiation may exist when the subject organizes a motor response in near or far extrapersonal space. ZOCCOLOTTIand JUDICA [ 191developed a functional scale for evaluating neglect in daily life which consists of two separate scales for personal and extrapersonal defects. On the extrapersonal scale patients are required to perform tasks relative to near space (servir_g tea, dealing cards, describing complex scenes) or to far space (describing a room), while on the personal scale patients are required to use some objects (comb, razor, powder, eyeglasses) on their own. In a group of vascular patients, Zoccolotti and Judica found a significant correlation between the extrapersonal scale and a standardized battery for neglect while no significant correlation was present between the standardized battery and the scale of personal neglect suggesting a dissociation between the neglect deficit for personal and extrapersonal space. Therefore, Zoccolotti and Judica’s scale seems to provide a useful means for singling out and evaluating dissociation between external and body space representations.

*In this test stimuli consist of circular fans of the same size, which appear to be different in size when placed in a particular space relationship (Wundt Jastrow Illusion). Neglect patients typically fail to perceive the illusion when the part of the stimulus critical for the illusory elrect IS in the neglected hemispace.

PERSONAL

AND EXTRAPERSONAL

SPACE

1003

To date, in the clinical setting, the lack of measures for evaluating defective processing of the side of the body contralateral to the lesion has prevented the identification of cases with a clear dissociation between personal and extrapersonal space. With the use of the new functional scale, a single case of personal neglect was identified without any impairment in the extrapersonal space. This was a chronic patient with a unilateral right hemispheric lesion. The description that follows may also contribute to further clarifying the relationship between the representation of the body and personal neglect.

PATIENT

AND METHODS

Case descriptinn E.D.S. is a JZ-year-old right-handed male with 5 years of education. In December 1989 he underwent surgical removal of a spontaneous hematoma in the right parietal lobe. Following surgery a CT scan showed an internal capsular lesion in the right hemisphere involving basal nuclei. A SPECT study evidenced hypoperfusion of the whole right hemisphere, greater in the parieto-frontal areas. involving both cortical and subcortical regions. Four months later a new CT and a new SPECT study confirmed the previous results. In January 1990 E.D.S. became an in-patient at our rehabilitation center. Upon admission. a standard neurological examination evidenced the presence of left hemiplegia. Neither sensorial nor visual field defects were observed. The patient was subjected to a screening battery of tests for neglect [I 31 2 months after onset. In three out of four tests (Letter Cancellation, Line Cancellation and Sentence Reading) no sign of heminattention was evident, being subject’s performances on these tests within normal limits. When given the Wundt-Jastrow Area Illusion test [I I]. the patient gave one response inconsistent with the illusory effect when the stimulus was oriented toward the left and none when it was oriented toward the right. This pattern of performance is within normal limits [1 I]. When the patient was again administered the same battery a month later, only correct responses were observed. In April 1990 the patient was referred to the Neuropsychological Unit by his physical therapist who reported severe neglect interfering with the physical rehabilitative program. The patient was unable to look at his own left leg while walking with a cane and was unable to utilize the residual movement skills of the left side of the body. Further evaluation with the standard screening battery again showed the absence of extrapersonal neglect. E.D.S. was then administered the Semistructured Functional Evaluation Scale [l9], obtaining a score of 3 (severe neglect) in two out of three items on the personal subscale. In particular, on the personal subscale he failed to comb on the left and to shave the left cheek. On the extrapersonal scale he described a room completely, with some perseverative description of the right elements during the description of the elements on the left. No sign of neglect was found in other heminattention tests (i.e. copying of drawings, sentences, etc.). Extinction was present in two out of 10 tactile double stimulations [3] and the patient reported a simultaneous tactile stimulation after one out of 10 single tactile stimuli on the right hand. No error was present in 10 single tactile stimuli on the left hand. No extinction was present in a task of visual double stimulations [3]. When requested to explain why he is an in-patient, E.D.S. always promptly reports the presence ofa motor deficit in the left side of the body resulting from a cerebral hematoma. However, he does not demonstrate any awareness of the future consequences of his deficit (i.e. the impossibility of returning to his job) or awareness of personal neglect. To confirm the selectivity of persona1 neglect and exclude the presence of more general deficits, E.D.S. was administered a number of tests to evaluate mental deterioration and other visuo-spatial disturbances. His performance on the Raven PM38 (modified by GAINOTTI et al. 191) is normal, indicating the absence of mental deterioration. E.D.S. was not visuo-spatially impaired on a test of unusual perspective recognition [13], on the Street test [7], the Line Orientation test [l], or on a test of mental unfolding [8]. The patient’s performance on the Face Recognition test [2] was borderline. There was no sign of constructional, ideational or ideomotor apraxia on standardized tests 1161. In a test of linger agnosia [16] (which will be described in detail later), E.D.S.‘s performances for the left, but not for the right hand were clearly defective. suggesting the presence of a specilic involvement of body schema. Recognition

of,finyers

Tactile threshold was measured by means of an extesiometer with the “limit method” before subjecting the patient to the task. The threshold was 0.1 g on the right and 5 g on the left hand. For this task we utilized a stimulus with a weight of 22.5 g, clearly perceptible on both hands. For each hand five stimulations were performed on the first phalanx of each finger, while the patient was blindfolded. Subject’s task was to verbally name the stimulated finger. Each hand was tested in two experimental conditions: (a) full extension and spreading of the fingers; (b) since the plegia makes it difficult to hold the left fingers

C. GUARIGLIA and G. ANTONUCCI

1004

in the prescribed position, the patient was asked to assume the natural position of the left hand and to replicate the same position with the right hand. Each hand was tested separately with a randomized (extended-natural&natural extended) sequence of hand conditions. E.D.S. did not Fail in recognizing the right hand fingers in the first condition, but he made 9 errors with the left hand. Fifty-five per cent of the errors consisted of pointing to fingers not contiguous to those stimulated (i.e. for stimulation the left ring finger he responded he had been touched on the index finger). In the natural positions, E.D.S. made 6 errors on the right and 14 errors on the left hand (see Table 1).

Table 1. E.D.S.‘s performances (error percentage for 25 items) on the finger recognition test Position

Left hand

Extended Natural

36”/n 28%

Right hand 0% 120/b

Test of body schema [6] This test for the evaluation of body representation in children includes the denomination and the evocation-localization of body parts as well as reconstruction of the frontal and profile view of a body and a head. E.D.S.‘s performance on this test was highly defective, corresponding to that of a 4.6- and 8.5-year-old child for frontal and profile views. The patient did not fail in naming single parts, but was quite impaired on all tasks involving mental representation of the body. For example, he chose 8 out of 12 wrong parts for reconstructing the body profile and 10 out of24 wrong parts for reconstructing the head profile. He was unable to correctly locate the parts and he produced pictures which were hardly recognizable as human bodies or faces (see Fig. 1). In the frontal face reconstruction, for example, eyes were upside-down with the inner canthi revolving toward the ears in a vertical rather than a horizontal array. In the frontal body reconstruction parts were badly arranged and so far from each other that the arms were off the test board. When asked to correct his performance, E.D.S. answered that nothing was wrong, showing he was unable to judge the incongruences produced in his reconstructions. Test

of aurotopoagnosia [ 151

SEMENZAand GOODGLASS [lS] developed and standardized a test for autotopoagnosia using a population of brain-damaged patients; the test provides for verbal and nonverbal modalities of presentation and response, with subtests to indicate parts of the patient’s body on a model and on a multiple-choice response sheet, following an oral. visual or tactile request (the patient with eyes closed is touched on the part to be indicated). For use with E.D.S., the test was slightly modified, using the items referring to lateralized parts (e.g. eyes or arms) twice, specifying the side. The patient made 21 errors (11%) out ofa total of 192 stimuli (see Appendix). The errors were more frequent in the subtests where the patient was asked to indicate on himself the part the examiner pointed out on the model and on the model the spot where he was touched while blindfolded. Mainly he failed in localizing parts on the left side of the body, indicating the homologous right part (e.g. the right shoulder instead of the left one) or parts contiguous to those requested (e.g. when touched on the left wrist, he indicated the back of the left hand; in one case, the patient indicated the left hip when touched on the left shoulder). He also made some errors in localizing parts on the right side of the body; in this case, however, errors never consisted of inversions of side (e.g. the left hand rather than the right hand).

DISCUSSION The results of the present study serve to document the existence of independent systems for exploring distinct portions of space. In this patient, dissociation is evident between his capacity for orientation in extrapersonal space and his behavior when he is asked to use objects on his own body. No deficit emerges in any of the trials which evaluate the presence of neglect in extrapersonal space. E.D.S. only presents a pathological performance on ZOCCOLOTTI and JUDICA’S [19] personal scale; however, on their extrapersonal scale no asymmetries in exploration emerge. Neuropsychological evaluation allows for the exclusion

PERSONAL

AND EXTRAPERSONAL

Fig. 1.

SPACE

1005

PERSONAL

AND

EXTRAPERSONAL

SPACE

1007

of the presence of other types of cognitive deficits; it demonstrates the absence of deterioration, apraxia, and the integrity of visuo-spatial abilities also in complex tasks. One of the most important findings is that even after many months from the onset of pathology the deficit is still present. Although E.D.S. has achieved good motor recovery which permits him to walk without support, he still has such serious personal neglect after 18 months that his wife complains he wakes her during the night and asks her to look for his left arm. At the beginning of the physiotherapy, the exploration of personal space deficit interfered very seriously with possible motor recovery. Residual motor abilities forecast good recovery which was obtained only by turning to specific strategies which took advantage of the integrity of his abilities to explore extrapersonal space. In fact, only external visual aids made possible the muscle control necessary for producing correct movements. For example, E.D.S. managed to put his weight on his left leg only when he could visually control the effect of this action by looking at the needle of the scale on which his left foot was placed. At the end of his re-education, E.D.S. had completely recovered the ability to walk correctly. However, motor recovery was not accompanied by any modification in his ability to explore his body, which could be shown with specific evaluation trials, even many months after the onset of pathology. The cases described in the literature which present personal neglect in the absence of extrapersonal deficits [4, 171 refer only to patients in the acute phase. In the cited works, the patients were asked to touch their left hand with their right hand and on the basis of this performance the presence and severity of personal neglect was defined by means of an evaluation scale from 0 (no deficit) to 3 (serious deficit). It should be noted that on this trial of personal neglect E.D.S. -- similar to PIZZAMIGLI~ et al.‘s [12] chronic patients - did not present any deficit. This results seem to indicate that a single item evaluation, such as that in BISIACH et al. [4], is insufficient for detecting personal neglect in chronic patients. On the other side, a more articulated scale developed by ZOCCOLOTTIand JULNCA[19] is capable of clinically identifying such a disorder, or segregating it from spatial extrapersonal impairments. One point which emerges from the analysis of this case is the association between serious personal neglect and the alteration of bodily spatial relations. E.D.S.‘s pathological performances on DAURAT-HMELJAK et ~1,‘s [6] trials and on the localization of body parts [lS] demonstrates a general disturbance of body schema. The deficits shown during the execution of the reconstruction ofa body and a face trial are rather surprising considering the absence of constructive apraxia and E.D.S.‘s good abilities of perceptual analysis and spatial processing in other tests. Although perfectly capable of carrying out correct processing of noncorporeal visualLspatia1 stimuli, E.D.S. was incapable of correctly judging the result of his performances on reconstruction trials. Repeatedly invited to look for and correct possible errors following completion of the task, he was not able to single out either choice errors (on the reconstruction of the body in profile. for example, he chose the parts showing two legs seen from the front rather than the left leg) or errors in orientation of the parts, showing an inability in perceptual analysis for corporeal stimuli which was absent for other categories of stimuli. The presence of personal neglect is also evident in E.D.S.‘s performance in all the tasks which compare responses for the left and right side of the body: in fact, the percentage of errors is greater when the representative ability of the left side of the body is involved. Since asymmetry in perceiving and using one side of the body cannot be completely explained by

1008

C. GUARIC;LIA and G.

AN~ONUCCI

the presence of disorders in body representation, it may be concluded that two separate processes are impaired in the present case, one concerning body schema in general and the other referring to the inability to deal with information coming from the body contralateral to the lesion. One consideration concerns the site of the lesion. In animals, distinct lesions produce exploration deficits for distinct portions of space. Lesions in man are not comparable to those obtained experimentally in animals; usually the former are very large vascular lesions which involve more than one cerebral area. Therefore, the study of lesions in patients who show selective exploration deficits has not yet permitted anatomical localization of single deficits. Also in our patient, in spite of a clinically clear dissociation, the lesion in the right parietal lobe extending to the basal ganglia can, in large part, be superimposed over those observed in patients with extrapersonal neglect. This does not permit any consideration of the neural substrates involved in different spatial representations for different portions of space. In conclusion, dissociations between explorative deficits for distinct portions of space can be demonstrated in man. Apart from dissociation between limited deficits of personal or extrapersonal space [4,12,17], HALLIGAN and MARSHALL’S[lo] case also shows a selective deficit for the exploration of peripersonal space in the absence of a deficit for personal and extrapersonal space. All the cited cases refer to patients in the acute phase. Our case constitutes a first confirmation of the presence of a dissociation between personal and extrapersonal space even many months after the onset of pathology. These results allow for the proposal of interesting hypotheses on the relations between spatial and bodily representations which can be clarified with the study of other patients with deficits limited to only one portion of space (personal or extrapersonal). Acknowledyements-~This work was supported by grants from Clinica S. Lucia and the Consiglio Nazionale Ricerche. The authors are grateful to E. Bisiach for his comments on a preliminary version of the paper.

delle

REFERENCES 1. BENTON, A. L., VARNEY, N. R. and HAMSHER, K., DE S. Judgment qf Line Orient&ion, Form V. University of Iowa Hospital, Iowa City, 1977. 2. BENTON, A. L., VAN ALLEN, M. W., HAMSHER,K., L)ES. and LEVIN, H. S. Test of’Fucia1 Recognition, Form S.L. Manual. Benton Laboratory of Neurology, Department of Neurology, University of Iowa Hospital and Clinics, Iowa City, 1975. 3. BISIACH,E., CAPPA, S. and VALLAK, G. Guida All’esamr Neuropsicologico. RatTaello Cortina, Milano, 1983. 4. BISIATH, E., PF.RANI, D., VALLAK, G. and BERTI, A. Unilateral neglect: personal and extrapersonal. Neuropsycholoqiu 24, 759-767, 1986. 5. COSLETT, B. H. The role of the body image in neglect. .I. clin. exp. Neuropsychol., 11, 79, 1989. 6. DAURAT-HMELJIAK, C., STAMBAK,M. and BEKGES,J. I1 te.st dello schema corporeo. Una prow di conoscenzu e di costruzione dell’immugine del corpo. Organizzazioni Speciali, Firenze, 1978. 7. DE RENZI, E. and SPINNLEK, H. Visual recognition in patients with unilateral cerebral disease. J. new. mental. Dis. 142, 515-523, 1966. 8. EKSTROM, R. B., FRENCH, J. W., HARMAN, H. H. and DERMEN, D. Manual,for kit of,~uctor-referenced cognitioe tests. Educational Testing Service, Princeton, 1976. 9. GAINOTTI, G., D’ERME, P., VILLA, G. and CALTAGIRONE, C. Focal brain lesions and Intelligence: a study with a new version of Raven’s Colored Matrices. J. clin. exp. Neuropsychol. 8, 37-50, 1986. IO. HALLIGAN, P. W. and MARSHALL, J. C. Left neglect for near but not far space in man. Nature 350,49& 500,199 1. Il. MASSIRONI, M., ANTONUCCI, G., PIZZAMIGLIO, L., VITALE, M. V. and ZOCCOLOTTI, P. The Wundt Jastrow illusion in the study of spatial heminattention. Neuropsychologia 26, 161-166, 1988. 12. PIZZAMIGLIO, L., CAPPA, S., VALLAR, G., ZOCTOLOTTI, P., BOTTINI, G., CIUKLI, P., GUAKIGLIA, C. and ANTONIJCTI, G. Visual neglect for far and near extra-personal space in humans. Cortex 25, 471477, 1989a. 13. PIZZAMIGLIO, L., JUDITA, A., RAZZANO, C. and ZOCCOLOTTI,P. Toward a comprehensive diagnosis of visuospatial disorders in unilateral brain damaged patients. Psychol. Assess. 5, 199-218, 1989b.

PERSONALAND EXTRAPERSONALSPACE

1009

14. RIZZOLATTI, G., MATELLI, M. and PAVESI, G. Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106, 655473, 1983. 15. SEMENZA, C. and GOODGLASS, H. Localization of body parts in brain injured patients. Neuropsycholoyia 23, 161-175, 1985. 16. SPINNLER, H. and TOGNONI,G. Standardizzazione e taratura italiana di test neuropsicologici. Ital. J. neural. Sci. 6 (supp.), 1987. 17. VALLAR,G., STERZI,R., BOTTINI,G., CAPPA,S. and RUSTONI,M. L. Temporary remission ofleft hemianesthesia after vestibular stimulation. A sensory neglect phenomenon. Cortex 26, 123-131, 1990. 18. WILLANGER, R., DANIELSEN,U. T. and ANKERHKJS,.I. Denial and neglect ofhemiparesis in right-sided apoplectic patients. .4cta neural. stand. 64, 31&326, 1981. 19. ZOCCOLOTTI, P. and JUDICA, A. Functional evaluation of hemi-neglect by means of a semi-structured scale: personal extrapersonal differentiation. Neuropsychol. Rehah. 1, 3344, 1991.