NOTE PURE TOPOGRAPHICAL DISORIENTATION DUE TO A DEEP-SEATED LESION WITH CORTICAL REMOTE EFFECTS* Claude Hublet and Guy Demeurisse (Hopital Universitaire Brugmann, Service de Revalidation Neurologique, Bruxelles) INTRODUCTION In most cases topographical disorientation is- observed within the context of more global disorganization of behaviour (confusional states, dementia, global amnesia, visual agnosia, ... ). More rarely it may occur as an isolated phenomenon. The clinical signs are then restricted to ambulatory disorders: in some cases, the patients lose their way in familiar surroundings, in others, the disorder is present only in unfamiliar surroundings. Studies in cognitive neuropsychology have shown that topographical disorientation is not the consequence of a single cognitive process disturbance, but of disorders of perception of environmental data, or of disorders of recognition of places, or of spatial memory disturbances. The anatomical location of the lesions responsible for the syndrome is not readily identifiable (see discussion), but the lesions are generally cortico-subcortical, situated in the posterior part of the right hemisphere (De Renzi, 1982). To our knowledge, isolated topographical disorientation due to a right internal capsule lesion has never been described. Such was the case in the present study. In order to try to understand the pathophysiology of neuropsychological disorders in this case, we also studied cortical neuronal activity by measuring regional cerebral blood flow. CASE REPORT The patient, a 72 year-old retired clerk, was right-handed (1000/0 according to the Edinburgh inventory), with no history of any previous neurological event. He had suffered from heart infarction and diabetes mellitus had been diagnosed three years earlier. He also presented arterial hypertension and atrial fibrillation. He was admitted to our department for sudden onset of left hemiparesis predominating in the upper limb. The patient was alert and cooperative. There was no sensory disturbance nor visual field defect (at instrumental perimetry). Symbolic function disorders were observed (see neuropsychological examination). Two CT scans were carried out (at three weeks and six months after onset), and revealed one small infarct in the posterior limb of the right internal capsule (Figure 1). The neuropsychological assessment involved standard global investigation of the cognitive functions and more specific tests for spatial disorientation. Two weeks after onset, orientation in time and memory for old and recent events were normal. The Wechsler Adult Intelligence Scale showed a Full Scale Intelligence Quotient (IQ) of 119, a verbal IQ of 121 and a Performance IQ of 115. Neurolinguistic examination was normal except for the presence of some iterations of strokes during writing. Bucco-linguofacial, ideomotor, ideational and constructional praxis were all preserved. There was no difficulty in recognizing objects, pictures, faces and colours. Somatognosis was normal. How- • This work was presented at the 13th European Conference of the International Neuropsychological Society in Innsbruck on July 6, 1990. Cortex, (1992) 28, 123-128 124 C. Hublet and G. Demeurisse Fig. 1 - CT scan: Small ischemic hypodense lesion in the right internal capsule (see marker). ever, the patient suffered from major spatial disorientation when walking in the department and in the hospital gardens; this disorder was still present six months after onset. Spatial Perception Assessment The patient had no difficulty judging relative or absolute object's location. His subjective visual coordinates, estimated by alignment of a luminous rod to vertical and horizontal positions in the absence of visual cues (total darkness), were normal. The map of the testing room was drawed with precision. The copy of Rey-Osterrieth figure was normal (perc. 60). There was no unilateral spatial agnosia during cancellation and bisection of lines tasks. Maze tests (on paper) were rapidly and correctly performed. Mnestic Function Assessment Memorization of a series of 15 words, figurative drawings and photographs of unfamiliar faces was normal. The Wechsler Full Scale Memory Quotient was 115. In the spatial position Memory Test (De Renzi, Faglioni and Scotti, 1969), learning in three consecutive trials the positions of six geometrical shapes in two rows was excellent. However, he scored very poorly in the Benton Visual Memory Test (3 correct replies in a total of 10) and for the recall from memory of Rey-Osterrieth's figure (2 SD below the mean). The failure was total in the Milner visual test (Milner, 1965) which involves a network of 100 electric boltheads arranged in a square through which the patient has to discover the correct route. Beginning in the lower left corner the patient has to find his way to the upper right corner by successively touching 29 boltheads with a metal stylus. Discriminative feedback is auditory and a tone sounds whenever an incorrect bolthead is touched . Normal right-handed control subjects (n = 12, 5 males and 7 females, mean age: 57) performed three consecutive errorless runs after, at most, 24 trials. Our patient was unable to find his way through the maze without error, even after three sessions of 25 consecutive trials (Figure 2). Major orientation difficulties, especially in new surroundings, were also observed during locomotor tasks. When placed in surroundings unknown before the stroke, for instance the hospital department in which he had been for more than a month, the patient was unable on his own to find simple paths covered several times everyday with an investigator. Mental evocation of the paths was wrong most of the time. This contrasted with very good ability to Topographical disorientation 125 Fig. 2 - Milner Visual Maze Test: Patient's learning curves after 25 consecutive trials grouped in five blocks (I, l/, III, IV, V) of five trials. Results are expressed as mean number of errors by block. Three different sessions of measurements (a, b, c) were performed at 190 days after stroke (a: a.m.; b: p.m.) and 191 days after onset (c: a.m.). 2. 18 16 I I mw Y I I mN v .:n :m: .Ill Y BLOCKS OF 5 CONSECUTIVE TRIALS evoke or indicate on a map familiar paths covered by the patient before his stroke. He also located correctly the principal Belgian cities on a blank map and recognized unhesitatingly photographs of various old and new districts of Brussels. The assessment of orientation in extrapersonal space was completed by using a simplified version of the route-finding test of Hecaen, Tzortzis and Masure (1972). In this test, the patient is asked to walk between landmarks taped on the walls with the aid of a guide map indicating a route with arrowed segments. This task requires the ability to re-orientate the plan so that it always corresponds to the orientation of the examination room during the successive changes of direction of the subjects. Two types of landmark were available to our patient: simple, identical geometrical shapes (black squares) and verbalizable concrete figures (ex. cat, aeroplane, violin). The results showed numerous errors of orientation when the landmarks were identical (Figure 3) but normal performance in the presence of verbalizable landmarks. CORRECT PATH. . PATH FOLLOWED BY THE PATIENT Fig. 3 - Routefinding test with non-verbalizable landmarks (* starting point). 126 C. Hublet and G. Demeurisse Regional Cerebral Blood Flow Measurements (rCBF) were made at rest using the two-dimensional 133 Xenon inhalation method. The detector-holding blocks carried 32 head detectors situated in parallel planes making an 11 0 angle with the cantho-meatalline. Flow values were expressed as Initial Slope Index (lSI) (Risberg, Ali, Wilson et ai., 1975) calculated between 30 and 90 sec. after the beginning of the washout. The CO 2 concentration in the expired air was recorded by a capnograph and the results corrected for pC0 2 according to Maximilian, Prohovnik and Risberg (1980) (i.e. 0.75 lSI units for each mmHg deviation from 40 mm Hg). Our criteria of normality for average hemispheric flow and loco-regional distribution were published earlier (Demeurisse, Verhas, Capon et aI., 1983). Given that in most stroke patients there is a flow decrease involving the whole brain (Naritomi, Meyer, Sakai et aI. , 1979; Demeurisse et ai., 1983; Demeurisse, Verhas and Capon, 1984; Meyer, Rogers and Mortel, 1984), rCBF results were also expressed in Ufo of the hemispheric mean value in order to identify regional low flow areas. In the patient mean hemispheric flow values (30,0 lSI units in the left hemisphere and 29,8 in the right one) were below normal (normality±S.D.: 64,9± 10,1). Regional hypoperfusion was considered as significant when the relative flow value was at least two S.D. under the normal value in a given area. Such was the case in the right parietal region (value between 2 S.D. and 2,5 S.D. below normal) (Figure 4). R L Fig. 4 -rCBF landscape at rest: Deviations from mean hemispheric value are represented as "clock symbols"; 90 ° correspond to 15% deviation. Dotted area: significant loco-regional hypoperfusion in the right parietal region. DISCUSSION Our patient presented a clinical picture in which topographic disorientation was the main disorder. It only occurred in surroundings unknown before the stroke. In terms of spatial perception the patient's performance was within the normal range, while deficits of spatial memory were apparent. During the route-finding test, performance was impaired only with non-verbalizable landmarks. If this test is deemed not to involve memory as suggested by Hecaen, Tzortzis and Rondot (1980), the topographic disorientation of our patient cannot be explained by a selective deficit of spatial memory. However, closer analysis of our patient's performance during the route-finding test reveals that the first segments were correctly negotiated, indicating that the patient had preserved the ability to maintain the correct orientation of the plan in relation to the examination room puring the first changes of direction. Beyond the fourth segment, on the contrary, his performance became abnormal suggesting that the simple ability to correctly manipulate the spatial data was not sufficient for successful completion of the entire test. Thus contrary to Hecaen et al. (1980), we take the view that this test cannot be accomplished without the involvement of memory. Therefore, Topographical disorientation 127 the topographic disorientation of our patient could be attributed to selective loss of spatial memory. This was also the case for the patients of De Renzi, Faglioni and Villa (1977) and Whiteley and Warrington (1978). In most of literature cases, topographical disorientation is accompanied by other clinical signs and accurate anatomical location of the lesions likely to have produced the syndrome is therefore difficult. However, according to Cummings, Landis and Benson (1983), most orientation disturbances were due to lesions involving the postero-medial region of the right hemisphere. Three years later, the same team (Landis, Cummings, Benson et aI., 1986) reported on 16 cases of loss of topographic familiarity: all the lesions involved right medialtemp oro-occipital areas; in some cases, they were bilateral. Also, in the four cases reported by Habib and Sirigu (1987), damage was restricted to the right parahippocampal gyrus, a region supplied by inferior branches of the right posterior cerebral artery. The role of the right hippocampus in spatial memory has also been demonstrated in epileptic patients undergoing removal of this structure, who performed poorly on the maze learning test (Milner, 1965) and spatial location tests (Smith and Milner, 1981), though not presenting clinical topographical disorientation. According to De Renzi (1982), in most pathologically-verified cases of topographical disorientation, the injured region of the right hemisphere involves the posterior parietal and adjacent lateral temporal and occipital cortex. Spatial memory deficits have also been correlated with lesions, located in the right parietal region (Newcombe and Russel, 1969). The syndrome of spatial disorientation has thus been observed in right-sided corticosubcortical lesions located either in the parietal region or in the parahippocampal region. This was not the case in our patient. CT scan showed a deep-seated lesion that did not reach the cortex. The rCBF study, however, showed a significant hypoperfusion akin to "diaschisis" in the right parietal region. (See for a recent review of this phenomenon, Feeney and Baron, 1986). In patients with deep-seated lesions remote cortical dysfunction has already been considered to be responsible for the appearance of symbolic function disorders, such as language disorders (Metter, Riege, Hanson et aI., 1983; Skinhoj Olsen, Bruhn and Oberg, 1986; Demeurisse, Capon, Verhas et aI., 1990), severe multi modal neglect (Bogousslavsky, Miklossy, Regli et aI., 1988), and frontal lobe syndrome (Pozzilli, Passafiume, Bastianello et aI., 1987). We submit that in the present case, topographical disorientation was related to decreased neuronal activity in the right parietal region. In rhesus monkeys, there are important reciprocal connections between the parahippocampal gyrus and the parietal cortex. Topographical disorientation could thus be caused by damage or dysfunction in one of these structures or perhaps also in the tracts linking them. It is tempting to speculate that, if rCBF or metabolism measurements had been taken in cases where lesions were situated in the right parahippocampal gyrus, a remote decrease in neuronal activity might have been observed in the parietal region. ABSTRACT Lesions producing pure topographical disorientation syndromes are classically located either in the right parietal region either in the right parahippocampal gyrus. The patient described in the present study was admitted to hospital after sudden onset of a left hemiparesis. The lesion at CT scan was located in the posterior limb of the right internal capsule. Neuropsychological assessment was normal except for the presence of a major topographical disorientation and of mnestic disturbances for vi suo-spatial material leading us to attribute topographical disorientation to a specific loss of topographical memory. Regional cerebral blood flow measurements disclosed a right parietal hypoperfusion. 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Claude Hublet, Service de Revalidation Neurologique, H&pital Universitaire Brugmann, 4, place A. Van Gehuchten, 1020 Brussels, Belgium.