Unilateral neglect and perceptual parsing: a large ... - Semantic Scholar

Neuropsychologia 40 (2002) 1918–1929

Unilateral neglect and perceptual parsing: a large-group study Marco Neppi-Mòdona a,∗ , Silvia Savazzi a , Raffaella Ricci a , Rosanna Genero b , Giuseppina Berruti b , Riccardo Pepi b a

Dipartimento di Psicologia, Università di Torino, Via Po 14, 10123 Torino, Italy b Casa di Cura Papa Giovanni XXIII, Pianezza, Italy Received 11 September 2001; accepted 1 May 2002

Abstract Array-centred and subarray-centred neglect were disambiguated in a group of 116 patients with left neglect by means of a modified version of the Albert test in which the central column of segments was deleted so as to create two separate sets of targets grouped by proximity. The results indicated that neglect was more frequent in array- than subarray-centred coordinates and that, in a minority of cases, neglect co-occurred in both coordinate-systems. The two types of neglect were functionally but not anatomically dissociated. Presence of visual field defects was not prevalent in one type of neglect with respect to the other. These data contribute further evidence to previous single-case and small-group studies by showing that neglect can occur in single or multiple reference frames simultaneously, in agreement with current neuropsychological, neurophysiological and computational concepts of space representation. © 2002 Elsevier Science Ltd. All rights reserved. Keywords: Array-centred neglect; Subarray-centred neglect; Perceptual parsing; Spatial reference frames

1. Introduction When presented with a stimulus array printed on a sheet of paper, e.g. Albert [1] or Diller and Weinberg [12] cancellation tasks, and asked to cross out the targets with a pencil, neglect patients usually omit the stimuli laying on the contralesional side of space. We will refer to this type of neglect as array-centred neglect (ACN). In drawing a figure, the same patients may produce an adequate representation of parts on the ipsilesional side, while omitting significant features on the contralesional side of its vertical axis. Interestingly, clinical and experimental evidence suggests that patients sometimes neglect the contralesional side of each component of a complex stimulus, rather than the contralesional side of that stimulus as a whole. For example, if left neglect patients are given a version of Albert line cancellation task where the lines are organised into two separate gestalten grouped by proximity and common colour [13] (see Fig. 2), they may either disregard contralesional targets over the visual array as a whole, or within each subgroup of targets. Similarly, patients who only copy the ipsilesional of two flowers originating from a common stem may omit the ∗

Corresponding author. Tel.: +39-11-6703064; fax: +39-11-8159039. E-mail address: [email protected] (M. Neppi-Mòdona).

contralesional side of each flower if the common stem is deleted so that the two flowers stand out as separate perceptual units [17,24]. We will refer to this latter type of behaviour as subarray-centred neglect (SACN) [14,18,19]. Manifestations of neglect relative to different coordinate frames can be double dissociated [9] or coexist within the same patient [5,6,29], their occurrence being modulated by task-related factors [7,22]. The neuropsychological evidence that neglect can occur within multiple or single reference frames (for a review see [25]) is consistent with neurophysiological data derived from the response properties of the primate’s cortex neurons which code the representation of space (for a review see [3,10]). These data indicate that different neurones can encode space in a number of different reference frames (viewer-, environment- [28] and object-centred [26]). Such cells are distributed in specific locations of the parietal and frontal cortex of the monkey, forming a well-defined parietal–frontal network [10,23]. Indeed, functional imaging studies in humans have confirmed the importance of these areas for the control of viewer-centred and object-centred visual attention [15], and egocentric and allocentric coding of space [16,21]. In addition, neurophysiological findings in the animal [2] and fMRI [11] and neuropsychological [4] data in man

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M. Neppi-Mòdona et al. / Neuropsychologia 40 (2002) 1918–1929

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Fig. 1. Letter H cancellation task. The stimulus array is composed by 104 Hs (53 in the left half and 51 in the right half of the sheet) and 208 distracting letters randomly distributed in 52 columns. The patient is asked, with no limitation of time, to cancel all Hs. The figure reproduces a typical left-neglect patient’s performance: the shaded surface represent the area of the array neglected by the patient.

indicate that the parietal cortex is capable of representing the position of an object in multiple reference frames simultaneously. Simultaneous encoding of a spatial location in multiple reference frames is also consistent with computational concepts of space representation [6,25]. Simulation studies based on the interpretation of the response properties of cortical neurons as basis function of their sensory inputs show that a single neuron can encode the spatial location of an object in various reference frames [27]. It is still debated, however, whether space- and objectbased spatial representations in man reflect the activity of discrete neural structures or, rather, of the same population of neurons. Besides, no data are presently available relative to the incidence of ACN and SACN following right hemisphere damage. To address these issues, we quantified the incidence of ACN and SACN following right hemisphere damage in a large group of patients and attempted to correlate these two types of neglect with lesion anatomy. One hundred and sixteen neglect Ss (N+) were recruited from several institutions and exposed to an extensive neuropsychological investigation using tasks commonly adopted to assess the presence of neglect. In addition, a specific task was introduced for assessing the presence of ACN and SACN. Line bisection and letter H cancellation (see Fig. 1) were used as screening tasks. A modified version of the Albert cancellation task [1] in which the central column of segments was deleted so as to create two separate sets of targets grouped by proximity (see Fig. 2) was used to evaluate the presence of ACN and SACN. Our choice was based on the consideration: (1) several single-case and small-group studies [13,17,20,24] suggest that copying tasks employing stimuli whose structure is defined by perceptual grouping can dissociate ACN from SACN; (2) the task is relatively easy and can be executed by most patients with severe neglect.

2. Methods 2.1. Subjects One hundred and eighty-four right brain-damaged subjects recruited from several institutions on the basis of clinical and (in most cases) neuroradiological evidence of a right sided brain lesion consented to participate in the experiment. One hundred and sixteen of them were subsequently selected on the basis of the presence of left unilateral neglect. Neglect was defined according to either or both of the following criteria: (1) mean rightward bisection error (see procedure) exceeding 10.34 mm (i.e. three S.D. from the control’s mean, that was 1.01 mm to the right of the true centre); (2) left side minus right side omissions on a modified version of Diller and Weinberg [12] cancellation task (see procedure) equal to 5 or more. As control, we used data collected in a previous study on neglect [8] from a group constituted of 40 healthy right-handers (23 males and 17 females) with mean age (64.60 years; S.D. = 7.09) and education (8.88 years; S.D. = 4.50) approximately matching the levels found in group studies on unilateral neglect. Patients’ demographic and clinical data including sex (67 M, 49 F), age (mean = 66.08 years; S.D. = 13, 14) and educational level (mean = 7.09 years; S.D. = 3.62) are reported in Table 1. All patients were right-handers, with the exception of six left-handers. 2.2. Procedure 2.2.1. Screening tasks 2.2.1.1. Line bisection. Patients were required to bisect a series of five 180 mm long and 1 mm thick black horizontal lines printed at the centre of an A4 sheet of white paper and presented in turn on a desk. The pages were horizontally

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oriented and centred on the sagittal midplane of the patients’ trunk. Errors were measured with approximation to the nearest mm. For each patient a record was taken of the mean bisection error and S.D. (see Table 1). 2.2.1.2. Letter H cancellation task. Patients were presented with six rows of letters (104 Hs and 208 distracting letters) distributed in 52 columns, printed on an A3 sheet

of white paper, and asked to cross out all the Hs. The paper was centred on the patient’s sagittal midplane. The size of the letter H was approximately 4 mm both horizontally and vertically, and letter style was capital Times New Roman (see Fig. 1). A record was taken of the number of omitted Hs in the left and right side of the array of stimuli. In addition, we recorded the number of letters (Hs and non-Hs) in the neglected area of the stimulus array (defined as the area

Fig. 2. Examples of patients’ (A–E) performance on the Albert task. Roman symbols I–X indicate the column of pertinence of the targets. The shaded surfaces represent the area of the array neglected by the patient. A and B show the typical performance of a patient with moderate and severe ACN, respectively. An example (C) of co-occurrence of ACN and SACN, with the former prevailing over the latter. Two cases (D–E) of SACN without ACN.


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Fig. 2. (Continued ).

lying to the left of the boundary obtained by connecting the leftmost cancelled Hs of each row of stimuli) (see Fig. 1). 2.2.2. Evaluation of ACN and SACN 2.2.2.1. Albert cancellation task. Patients were presented with a modified version of the Albert cancellation task [1], composed of 50 short black segments (2 cm long and 0.5 mm thick) printed on an A4 sheet of paper placed in front of the

subject at reading distance. The segments, distributed in ten columns and five rows, were randomly oriented and grouped by proximity in two sets, each composed of 25 lines, separated by an empty gap, vertically oriented and 4 cm wide (see Fig. 2A).1 The subject’s task was to cross out all the 1 Our version of the task is modified after that of Driver and Halligan [13], where the two subarrays of targets were different in colour, one being printed in black and the other in red.

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Fig. 2. (Continued ).

segments by means of a pencil with no limitation of time. On the basis of the spatial distribution of the uncrossed segments over the stimulus array, two scores were computed: an ACN and an SACN score. In principle, ACN would result in a number of omissions (> = 1) homogeneously distributed in an area confined to the left subarray (as in Fig. 2A) or comprising the right subarray (as in Fig. 2B), depending on its severity. SACN, instead, would result in a number of omissions (> = 1) clustered on the left side of both subarrays, independently of its severity. 2.2.2.2. ACN score. For each individual, the array of segments was scanned row by row following a left to right direction in search of uncrossed segments. A record was taken of the number of uncrossed segments preceding the first crossed segment of each raw. The total number of uncrossed segments was held to represent ACN (possible range 1–50). A positive score was held to represent presence of ACN. In the case of the performance shown in Fig. 2A and B, the ACN score would thus be 9 and 38, respectively. Presence of undetected targets (> = 1) in insulated areas of the left half of the right subarray (as in Fig. 2C) was considered as indicative of possible co-occurrence of SACN. Omissions were computed as follows. The right subarray was scanned row by row following a left to right direction in search of uncrossed segments. A record was taken of the number of uncrossed targets preceding the first crossed segment of each raw and subtracted from the ACN score. The so obtained score, if positive, was held to represent the total ACN score, that is the ACN score cleaned from the contribution of SACN. In the case of the performance shown in Fig. 2C, the total ACN score would thus be 20 − 4 = 16.

Positive scores were held to represent presence and negative or 0 scores absence of ACN (see Fig. 2D and E, respectively). It must be noted, however, that a severe ACN, showing as a homogeneously neglected area of the stimulus array extending to the right subarray (as in Fig. 2B), would preclude any measure of (eventually) concomitant SACN. This was the case in 43/80 (53.75%) ACN patients. 2.2.2.3. SACN score. It was obtained subtracting the number of uncrossed segments in the 5th column from the number of uncrossed segments in the 6th column of the array (see Fig. 2A). We reasoned that, in presence of SACN, fewer omissions should appear in the 5th column, located at the extreme right of the left subarray, than in the 6th column, located at the extreme left of the right subarray. In the case of the performance shown in Fig. 2A, the SACN score would thus be 0 − 0 = 0; in the case of the performance shown in Fig. 2B, it would be 5 − 5 = 0; in the case of the performance shown in Fig. 2C, it would be 4 − 0 = 4. Positive scores (range 1–5) were considered indicative of SACN. The methods used for computing ACN and SACN rest on the assumption that these two types of neglect can be dissociated neuropsychologically. This assumption does not rule out the possibility that ACN and SACN are functionally related. Indeed, they might influence each other through additive or interactive effects. To this respect, our methodology for computing ACN and SACN has a potential limitation: it only provides a measure of separate or additive effects of both types of neglect, not of those due to an interaction. Theoretically, it is possible that a subarray-based neglect would increase in the left versus right subarray due to the influence of an array-based neglect (see Fig. 2C).


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Table 1 Demographic, Clinical, and Experimental Data Patient Sex

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

M M M M F M M M M M M F F M F F M M F F F F F M M F M F M M F F F M F F F F M M M F M M F M M F F F F M M M M M F M M M

Age (years)

Education Length (years) of illness (days)

Presence of Lesion visual field location defects

71 76 74 63 71 76 67 63 71 65 77 70 78 66 60 72 46 50 73 43 69 76 60 72 70 85 73 82 62 71 65 69 77 79 65 68 74 68 53 63 75 72 51 76 83 48 67 59 65 71 78 68 57 34 43 67 82 68 76 43

3 13 5 6 2 5 5 5 5 5 5 5 5 5 8 5 8 8 8 5 4 5 5 5 8 5 8 5 13 8 5 5 5 8 5 2 8 5 13 5 5 5 13 5 8 8 13 5 5 8 4 8 5 5 11 5 5 5 5 8

n.a. Yes Yes n.a. n.a. n.a. Yes No Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes No Yes Yes No n.a. No n.a. No No Yes No No n.a. Yes No No Yes No No n.a. Yes n.a. Yes n.a. n.a. No n.a. n.a. Yes Yes n.a. No Yes No Yes

28 62 259 n.a. 23 949 47 11 27 13 n.a. 617 22 n.a. 14 n.a. n.a. n.a. n.a. 6 n.a. 6 12 5 20 38 13 n.a. 5 44 279 n.a. 393 n.a. 90 33 64 1507 39 302 153 12 53 55 119 n.a. n.a. n.a. 61 131 n.a. 32 75 n.a. 12 n.a. 118 n.a. 33 18

P F, T, P T, P, O T, bg T, P F, T, P F, T P, O P, th, bg T, F Unapparent Unapparent T, O Unapparent cs, ci, th P F, T, P ci, bg cm, bg T, P cs, F cm bg T, P T, P, O T, P, ins P, O F, P, T F, bg ci P bg, cr ci, th F, T, P F, T, P F bg, ci T, P F, T, P T, P P Caps. Lentic. ci, th ci, ins P F, T, P, bg TP bg bg F bg, ci ins, F P ci F, T, P ins, P F F, T, P F, P F, P

Bisection error (mm) Diller Mean

19.60 −0.20 64.00 12.00 16.00 6.80 16.80 27.40 11.20 12.00 80.20 6.20 67.80 25.60 15.20 23.00 2.40 3.00 35.00 16.00 63.00 46.40 1.80 7.80 73.60 12.00 26.20 1.20 16.80 35.00 27.80 62.00 17.60 28.20 29.20 −4.80 15.00 15.40 8.60 0.20 11.00 3.80 15.60 22.40 3.00 7.80 74.80 0.00 −3.00 6.80 −0.80 13.80 44.20 80.20 12.00 33.20 23.60 5.40 17.20 0.60

Albert

S.D.

Left Right Neglected ACN SACN omissions omissions area (omitted Hs + non Hs)

5.55 4.39 7.60 2.55 8.97 5.59 6.50 10.42 6.76 7.78 6.61 6.14 8.73 16.99 7.05 4.74 7.70 8.51 12.86 4.18 17.49 19.40 6.76 2.59 4.22 5.57 15.32 10.85 4.21 8.97 9.26 8.97 4.77 4.76 7.98 6.02 5.52 9.76 7.96 4.97 0.82 3.56 11.15 13.65 6.44 7.60 2.68 2.74 3.39 8.07 3.11 2.05 9.58 1.10 6.96 23.61 11.48 8.71 2.39 5.90

10 53 53 17 27 14 53 n.a. n.a. n.a. n.a. 53 n.a. n.a. n.a. n.a. n.a. n.a. n.a. n.a. n.a. n.a. 53 39 53 n.a. n.a. 33 53 48 53 53 3 19 53 14 42 28 50 29 10 8 53 15 46 10 n.a. 6 36 19 14 n.a. 53 n.a. 9 53 52 15 16 53

0 34 23 9 5 5 40 n.a. n.a. n.a. n.a. 25 n.a. n.a. n.a. n.a. n.a. n.a. n.a. n.a. n.a. n.a. 38 0 43 n.a. n.a. 19 33 19 11 45 4 0 13 5 22 0 6 16 0 0 29 15 13 1 n.a. 0 9 7 3 n.a. 15 n.a. 4 24 41 7 15 15

28 225 205 n.a. 53 39 271 n.a. n.a. n.a. n.a. 232 n.a. n.a. n.a. n.a. n.a. n.a. n.a. n.a. n.a. n.a. 274 119 290 n.a. n.a. n.a. 261 177 194 299 4 58 200 29 173 80 161 82 20 24 250 26 161 2 n.a. 11 190 41 24 n.a. 205 n.a. 24 207 220 43 5 207

0 33 0 0 2 10 45 29 37 26 44 16 20 35 44 −1 26 23 41 45 47 44 21 29 41 16 31 44 5 26 3 39 0 0 3 0 34 3 5 3 0 0 12 0 0 −1 41 5 0 4 0 9 27 45 2 34 31 0 0 2

0 −4 2 0 0 0 0 −2 0 −4 0 4 0 −1 0 3 −4 0 0 0 0 0 0 −2 0 0 −1 0 1 −4 0 0 0 0 0 0 −2 0 0 0 0 0 −1 1 0 2 0 0 0 0 0 0 −3 0 0 −2 −2 0 0 0

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Table 1 (Continued ) Patient Sex

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116

F F F M M F M F M M F M M M M F F F M M F M M M M M M F M M M M F F M F M F F M F M F M M F F M F M M M F M F M

Age (years)

Education Length (years) of illness (days)

Presence of Lesion visual field location defects

69 79 47 60 56 66 77 62 75 62 34 68 55 24 67 52 68 78 66 32 75 62 61 86 71 69 62 64 59 59 22 64 52 71 75 75 56 81 83 28 54 62 71 75 63 69 83 69 84 82 82 77 91 70 75 70

3 3 5 8 5 5 5 5 13 17 5 8 13 8 5 8 3 8 3 5 5 13 4 8 3 5 13 11 8 8 13 5 8 8 11 5 8 5 5 13 8 5 0 5 18 5 8 13 13 5 18 5 8 5 16 17

No n.a. Yes Yes Yes Yes No No Yes Yes Yes Yes Yes Yes Yes Yes Yes n.a. Yes Yes No No No No Yes n.a. Yes Yes Yes Yes n.a. n.a. n.a. Yes Yes n.a. Yes Yes n.a. Yes Yes Yes n.a. n.a. n.a. n.a. n.a. Yes Yes Yes Yes Yes Yes Yes Yes Yes

759 n.a. 4 1 77 139 111 n.a. 37 89 196 58 31 169 51 73 25 122 151 3 471 305 659 79 60 37 38 25 n.a. n.a. 476 156 n.a. n.a. n.a. 1 16 4 3 15 69 114 2 36 n.a. n.a. n.a. 54 n.a. n.a. 12 n.a. 23 45 22 182

ci F, P F, T T, P F, P, bg ci T, P th cs P, T F, P th, O P, T T, P T, P, ce T, P bg, T, F bg T, F, P, O Unapparent ci, bg T, P T, P bg T, P, O ci, bg T, P T, P, O cm T, O F P, O T bg P T T, O, th, ci T, P bg bg, ci, th T, P P, F th, bg, ci cs T, P th, ci P cs P F, T, P F, T T, O th, bg T, P T, P T, P, O

Bisection error (mm) Diller Mean

16.40 9.00 9.00 11.00 14.00 15.20 33.40 15.40 8.60 54.60 14.80 18.20 2.60 29.20 12.40 8.20 22.40 20.80 11.00 11.60 15.80 15.40 16.80 15.40 30.20 16.60 10.80 14.20 13.40 78.60 53.40 34.40 11.40 −4.40 5.20 15.20 10.60 11.00 12.80 −3.60 7.80 12.40 −7.00 48.80 65.20 16.00 38.20 27.60 26.00 80.00 32.80 43.40 7.80 1.00 13.40 32.23

Albert

S.D.

Left Right Neglected ACN SACN omissions omissions area (omitted Hs + non Hs)

4.72 14.11 4.95 3.49 2.74 9.73 2.61 2.41 13.90 10.21 2.95 10.38 2.51 4.27 5.86 2.39 3.78 6.38 4.64 7.16 6.14 3.36 9.55 7.70 7.63 13.85 13.81 5.63 16.98 1.14 5.03 14.69 5.32 4.39 8.41 4.09 4.16 13.00 1.79 6.11 5.89 2.70 12.37 4.60 11.34 5.57 17.09 6.91 6.20 5.74 13.61 21.80 7.19 1.22 n.a. n.a.

53 49 13 0 27 12 9 21 53 50 46 45 27 53 43 20 13 53 10 3 45 15 10 13 43 51 24 53 52 53 13 24 53 53 53 14 0 45 17 31 22 2 53 53 47 35 53 53 47 53 11 52 21 53 53 53

37 3 8 0 5 0 4 12 35 22 21 18 2 22 25 8 0 40 6 1 11 0 1 0 10 28 2 9 4 46 4 14 48 13 31 12 0 17 11 8 1 0 20 41 22 10 38 23 13 48 7 19 13 27 21 43

2 150 41 2 39 28 27 49 260 215 142 133 77 217 151 37 43 284 23 2 167 37 27 29 117 241 70 187 179 301 32 39 307 215 257 15 2 141 53 89 50 6 185 285 185 94 269 230 174 302 30 161 47 246 225 286

26 9 4 0 0 0 0 1 29 28 27 0 3 30 2 0 0 29 10 0 2 0 0 0 4 27 36 13 30 43 1 2 46 0 26 1 0 0 4 0 0 0 2 38 27 0 29 9 6 32 −1 7 0 33 14 26

−4 1 0 0 1 1 0 0 −3 −4 −3 1 0 −3 2 0 0 −2 0 0 0 0 0 0 0 −3 0 −1 −3 0 0 1 0 0 −4 0 0 2 −1 0 0 0 0 0 −4 0 −2 1 1 0 1 0 −2 0 0 0

F = frontal; O = occipital; P = parietal; T = temporal; bg = basal ganglia; ci = capsula interna; cm = middle cerebral artery district; cs = centrum semiovale; ins = insula; th = thalamus; H = haemorrage; I = ischemia; Tr = trauma; N = neoplasm. Patient no. 2 also had a small lesion in the left hemisphere.


3. Results 3.1. Albert task Individual ACN and SACN scores are reported in Table 1. Twenty-nine patients made no omissions in the left and/or right side of the array, and therefore were no further considered in the analyses. 3.2. ACN group Eighty patients out of 116 (68.97%) showed ACN (ACN group). Among these, 43 (53.75%) showed severe ACN, with complete neglect of the left subarray and omissions extending to the right subarray (as in Fig. 2B); 30 (37.5%) showed mild or moderate ACN, with omissions confined to the left subarray (as in Fig. 2A); the remaining seven patients (8.75%) showed co-occurrence of ACN and SACN (as in Fig. 2C). Fig. 3A reports the mean number of crossed segments, from the leftmost to the rightmost column of the array, for the 73 patients with ACN (comprising 30 mild/moderate and 43 severe ACN patients): note that the number of hits progressively increases from left to right across the entire array. 3.3. SACN group Only 14 patients out of 116 (12.06%) showed SACN (SACN group). Among these, 7 (50%) showed it without ACN, the remaining 7 showed the co-occurrence of ACN. Fig. 3B reports the mean number of crossed segments, from the leftmost to the rightmost column of the array, for the seven patients with ‘pure’ SACN: note that the number of hits progressively increases from left to right within each subarray rather than across the entire array of targets. It must be noted, however, that incidence of SACN, as well as co-occurrence of SACN and ACN, might be underestimated here, given that 43/116 (37.07%) patients showed severe ACN, which might mask eventual presence of SACN. 3.4. Frequency of ACN and SACN Overall, the frequency of ACN (80/116) (68.97%) is significantly higher (P < 0.01 on a test of proportions) than the frequency of SACN (14/116) (12.06%). The existence of patients (N = 30) with ACN and absence of SACN and patients (N = 7) showing the opposite dissociation, evidences a functional double dissociation. Note that the 30 patients with ‘pure’ ACN all showed mild/moderate neglect on the Albert task. Indeed, the 43 severe ACN patients were excluded from this analysis: as they entirely neglected the left subarray and partly neglected the left side of the right subarray, eventual presence of SACN could be masked by ACN, thus leading to consider them, erroneously, as ‘pure’ ACN patients.

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The occurrence of ‘pure’ ACN (37.5%) is comparable to the occurrence of ‘pure’ SACN (50%) (P > 0.1 on a test of proportions). 3.5. ACN, SACN and severity of neglect Inspection of Fig. 3 shows that average performance on the rightmost stimuli of the right subarray is worse in the ACN than in the SACN group, suggesting the possibility that severity of neglect is higher in the ACN than in the SACN group. To ascertain whether this was the case, we compared the number of omissions in the rightmost columns (VIII–X) of the right subarray in the two groups of patients (considering the unequal size of the two groups, the non-parametric Mann–Whitney test was employed). The analysis yielded the following results: severe ACN patients (N = 43) (i.e. patients neglecting a homogeneous area of the stimulus array comprising the left subarray and extending to the right subarray) tend to omit, on average, more targets than SACN patients (N = 7) (omissionsACN = 3.88 versus omissionsSACN = 0.86, Z = −1.089; P = 0.078 (one tailed)). Instead, performance of mild-moderate ACN patients (N = 30), whose neglect is circumscribed within an homogeneous area of the left subarray, is comparable to that of SACN patients (omissionsACN = 0.57 versus omissionsSACN = 0.86, Z = −1.001; P = 0.391 (one tailed)). These data indicate that worse average performance in the rightmost side of the stimulus array reflects higher severity of neglect of a subgroup of ACN patients only, not of the ACN group as a whole. 3.6. ACN, SACN and visual field defects Presence of partial or complete visual field defects was evaluated through a ‘confrontation’ technique, as part of a standard neurological examination. The patients were given a randomised sequence of 20 single visual stimuli, 10 left- and 10 right-sided, intermixed with a sequence of 10 bilateral stimuli simultaneously presented. The experimenter stood in front of the patient and asked him to fixate the experimenter’s nose. Then, he/she raised his/her arms wide open at the patient’s head level, with the hands closed, and alternatively lifted his/her right or left index finger and quickly repositioned it in its initial position. The patient was asked to detect any index movement by answering ‘yes’ (or ‘no’ if no movement was perceived). The sequence of stimulation was repeated twice: once in correspondence of the upper visual field and once in correspondence of the lower visual field of the patient. A visual field defect was diagnosed in case three or more left single stimuli went undetected in one sequence and/or the other. Data were available for 21/30 patients manifesting pure ACN and for 7/7 with pure SACN. Presence of visual field defects in the upper and/or lower contralesional visual field

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Fig. 3. Roman symbols I–X represent (A–B) the column of pertinence of the targets, from the leftmost (I) to the rightmost (X) column. The shaded area between column V and VI represents the gap existing between the two subarrays of targets. A reports the mean number of crossed segments, from the leftmost to the rightmost column of the array of targets, for the 73 patients with ACN (comprising 43 patients with severe ACN and 30 patients with mild or moderate ACN). Note the progressive increment in the number of hits across the entire array from left to right. B, as in A but SACN patients’ performance is represented (N=7): note that the left to right gradient in the number of hits is now located within each subarray rather than across the entire array of targets.


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Table 2 F

P

T

O

sc

(A) Number (and %) of patients with damage confined to, or comprising different brain regions ACN (N = 30) 10 (33.33) 15 (50.00) 17 (56.67) SACN (N = 7) 3 (42.86) 5 (71.43) 4 (57.14) ACN + SACN (N = 6) 2 (33.33) 4 (66.67) 1 (16.67)

5 (16.67) 1 (14.29) 1 (16.67)

10 (33.33) 3 (42.86) 3 (50.00)

(B) Number (and %) of patients with damage confined to a single brain region ACN (N = 12) 2 (16.67) 1 (8.33) SACN (N = 2) 0 1 (50.00) CAN + SACN (N = 2) 0 1 (50.00)

0 0 0

1 (8.33.) 0 0

8 (66.67) 1 (50.00) 1 (50.00)

F = frontal; O = occipital; P = parietal; T = temporal; sc = subcortical (grouping lesions to basal ganglia, capsula interna, centrum semiovale, thalamus and white matter).

were apparent in 15/21 (71.43%) ACN patients and in 6/7 (85.71%) SACN patients. The difference was not significant on a test of proportions (P > 0.1). 3.7. ACN, SACN and lesion location Table 2A and B report the involvement of brain regions comprised by lesions giving rise to pure ACN, pure SACN or both in all patients with objectively demonstrated lesions by brain scans. In the ACN group (N = 30) (see Table 2A), lesion locations within the right hemisphere comprised especially temporal (56.67%) and parietal (50%) areas. Subcortical (33.33%) and frontal areas (33.33%) were less frequently involved. The occipital district was seldom compromised (16.67%). As for the SACN group (N = 7), the picture looked very similar. Parietal (71.43%) and temporal (57.14%) areas were most frequently involved. The frontal and subcortical regions were (relatively) less frequently compromised (42.86%) and the occipital district was seldom affected (14.29%). In the ACN + SACN group (N = 6), parietal (66.67%) and subcortical (50%) areas were most frequently affected, followed by frontal (33.33%), temporal (16.67%) and occipital areas (16.67%). In case of damage confined to a single brain area (see Table 2B), in presence of ACN (N = 12), the subcortical region was most frequently involved (66.67%), followed by frontal (16.67%), parietal (8.33%) and temporal (8.33%) areas. Due to the small number of patients, data relative to the presence of SACN (N = 2) and the co-occurrence of ACN and SACN (N = 2) are scarcely informative.

4. Discussion The main findings of this work can be summarized as follows: after a lesion circumscribed to the right hemisphere: (1) occurrence of ACN prevailed over that of SACN (ratio 5.7–1); (2) co-presence of both types of neglect

was a relatively infrequent event (8.75%);2 (3) ACN and SACN were double dissociated neuropsychologically but not anatomically; (4) presence of visual field defects was not prevalent in one type of neglect with respect to the other. These data contribute further evidence to previous singlecase and small-group studies by showing that neglect can occur in single or multiple reference frames simultaneously, in agreement with current neuropsychological, neurophysiological and computational concepts of space representation. Finally, this study individuates a widespread neural network—comprising frontal, parietal, temporal and subcortical areas of the right hemisphere—subserving array-centred and subarray-centred spatial representations. However, the lack, in our anatomical data, of graphic reconstructions of the patients’ lesions, did not permit us to clarify whether array- and subarray-centred spatial representations are sustained by discrete neural systems within this network or, rather, are distinct processes subserved by the same population of neurones. The functional double dissociation between ACN and SACN favours the first option, whereas the lack of an anatomical dissociation and the existence of patients with a lesion circumscribed to the parietal or subcortical area showing ‘pure’ ACN, ‘pure’ SACN or co-occurrence of both on the Albert task, is suggestive of the second option. Hence, a third, intermediate, possibility should be considered: that array- and subarray-centred spatial representations are activated in multiple neural networks, some devoted to subserve exclusively one type of spatial representation or the other and localized in distinct 2 It must be pointed out that occurrence of SACN and co-occurrence of ACN and SACN might be underestimated in this study due to the presence of a number of patients (N = 43) with severe ACN which might mask eventual presence of SACN neglect. Besides, the appearance of ACN and SACN is strongly dependent upon the perceptual properties of the stimuli employed and the task demands [7,22]. Hence, the validity of our results is circumscribed to the use of the present version of the Albert task as a tool to unconfound ACN and SACN. The use of other configurations of stimuli might lead to substantially different results. For example, increasing the perceptual-grouping effect of the two subarrays of stimuli by printing each subarray in a different colour, thus enhancing their salience, might increase the number of patients manifesting SACN.

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brain regions, others sustaining both types of spatial representations and localized in the same neural space. A recent fMRI study [16] devised to investigate the neural bases of ego- and allocentric frames of reference for the representation of space, contains data in favour of this possibility. Subjects were given a bisection task in which they had to discriminate whether the vertical bar transecting a segment presented on a computer monitor was located to the left or to the right of either the sagittal midplane of their body (egocentric task) or the midpoint of the horizontal line (allocentric task). It must be noted that these tasks differ in some relevant aspects from that employed in our experiment. First, the former are entirely visual decision-making spatial tasks, whereas ours is a visuo-motor spatial task. Second, in the former the reliance on ego- and allocentric reference frames is pre-determined by the nature of the task itself, because subjects are explicitly instructed to use either their subjective midline or the subjective midpoint of the segment as a reference frame to judge the position of the vertical bar transecting it. In our experiment, instead, patients are not instructed to use one reference system or the other. The comparison between egocentric and allocentric activations in Galati et al.’s experiment revealed the existence of separate (partly overlapping) areas [a similar finding has been reported by Fink et al. [15] using PET measures of regional cerebral blood flow (rCBF)]. Moreover, the right-hemisphere area involved in egocentric coding was found to be more than nine times wider than that involved in allocentric coding, suggesting that the neural substrate subserving egocentred spatial representations is more extended than that devoted to allocentred spatial representations. This datum is in accordance with our finding that the incidence of array-centred neglect is 5.7 times higher than that of subarray-centred neglect. As far as the existence of a partial overlap between the areas underlying the two types of spatial representations, the comparison between egocentric and allocentric activations revealed that 12% of the fronto-parietal network activated during the egocentric task was also activated during the allocentric task. This amount of co-activation is concordant with that we could expect on the basis of the rate of co-occurrence of array- and subarray-centred neglect in our group of patients (8.75%). Acknowledgements The authors are grateful to Marlene Behrmann for her comments on an earlier version of the manuscript and to two anonymous referees for their suggestions. The research was supported by a CNR (Grant No. 98.00557 CT11) to Edoardo Bisiach. References [1] Albert ML. A simple test of visual neglect. Neurology 1973;23:658– 64.

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