BRAIN

AND

COGNITION

15,

139-159 (1991)

Different Patterns of Dissociation in Unilateral Spatial Neglect ROBERTOCUBELLI Servizio di Riabilitazione,

Ospedale Maggiore,

VSL No. 27, Bologna, Italy

PAOLO NICHELLI Clinica Neurologica,

Vniversitli

di Modena, Italy

VIRGINIO BONITO Divisione

di Neurologia,

Ospedali Riuniti di Bergamo, Italy AND

ANTONIO DE TANTI

AND

MARIA GRAZIA INZAGHI

Ospedale Valduce, Como, Italy

The aim of this paper is to discuss the issue of dissociations found in unilateral spatial neglect according to the modality of space exploration and the nature of the task. For this purpose we present a reanalysis of the data from a recent paper of Gentilini et al. (1989) comparing visual and blindfolded exploration of a computer keyboard and discuss the performance of a left-brain-damaged patient with right visuospatial neglect and left-sided neglect dyslexia. We conclude that unilateral spatial neglect cannot be interpreted as a disruption of a single attentional mechanism, but rather it reflects impaired attentional mechanisms at several levels of Cognitive PrOCeSSing. 0 1991 Academic Press. Inc.

INTRODUCTION Patients with unilateral spatial neglect (USN) fail to report, respond to, or orient to stimuli presented on the side opposite a brain lesion. Although different sites of lesion may be causes of this defect, the lesion Research supported in part by a grant from Minister0 della Pubblica Istruzione to P.N. We thank Professor De Renzi for allowing us to analyze the original data from Gentilini et al.% (1989) paper. Address correspondence and reprint requests to Dr. Paolo Nichelli at Clinica Neurologica, via del Pozzo, 71, 41100 Modena, Italy. 139 0278-2626191$3.00

Copyright 0 1991 by Academic Press, Inc. All rights of reproduction in any form reserved.

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most frequently reported is located in the right parietal lobe (Vallar & Perani, 1987). Until the sixties USN was believed to be confined to the visual exploration of space. It was viewed mostly as a consequence of simpler deficits such as hemianopsia (Bay, 1953) and gaze palsy (Schott, Jeannerod, & Zahin, 1966), or alternatively, as due to the unawareness of visual defects because of anosognosia (Lurija & Skorodumova, 1950, quoted by Lurija, 1974), or to general mental deterioration (Battersby, Bender, Pollack, & Kahn, 1956). A different reductionist interpretation was proposed by Brain (1941), who considered USN to be an instance of defective visual localization of an object in external space related to a disordered body schema. Two influential papers in the late sixties helped to change the perspective by demonstrating that USN is an autonomous entity (Gainotti, 1968) and that posterior-right-brain-damaged patients also show left-sided neglect with tactile space exploration (De Renzi, Faglioni, & Scotti, 1970). Since then, any interpretation of neglect has to address the problem of the consistency of neglect across different sensory modalities of stimulus presentation and different ways of exploring external space (moving hands, eyes, or both). Current interpretations of neglect phenomena make different predictions concerning this issue. Three theories view USN as the consequence of the disruption of a single supraordinate mechanism that directs all space exploration. The “attentional” theory maintains that what is critically impaired in USN is the ability to allocate attention over space. There are multiple versions of this theory: Kinsbourne (1970a, 1970b) proposed that the contraversive tendency of the intact hemisphere in USN patients is no longer opposed by the damaged hemisphere; Posner and co-workers (1982, 1984, 1987) suggested that USN is due to an impairment in disengaging attention from the ipsilateral hemispace in order to direct it toward the contralateral one. The “intentional” theory, advanced by Heilman and co-workers (1983, 1985), claims that USN can be due to a unilateral defect of motor program activation which induces reduced and delayed movements to the contralateral hemispace. The “representational” theory, proposed by Bisiach and co-workers (1979, 1981, 1985a), assumes USN to be a breakdown of egocentric space representation. There is evidence supporting “attentional,” “intentional,” and representational mechanisms, although their relative contributions remain unclear. On this basis it has been recently proposed that the disruption of different mechanisms may underlie the performance of clinically indistinguishable USN patients (Bisiach, Bulgarelli, Sterzi, & Vallar, 1983; Coslett, Bowers, Fitzpatrick, Haws, & Heilman, 1990). Nevertheless all these theories view USN as a supramodal disorder and cannot predict patients

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exhibiting dissociated forms of neglect, for instance, neglect restricted to the visual exploration of space. Mcsulam (1981) hypothesized a network of complementary and interacting neural systems subserving directed attention and representation of extrapersonal space: a sensory representation located in posterior partietal cortex, a schema for distributing exploratory movements in the frontal cortex, and a motivational map in the cingulate cortex. In this framework one can expect forms of USN that differ according to the nature of the defect (sensory, motor, and motivational), but not according to the sensory modalities involved in space exploration. Rizzolatti and Camarda (1987) proposed a model of spatial attention based on a series of circuits that are essentially modality-specific, largely independent of each other, and formed by centers programming motor plans in a spatial framework.. As a matter of fact, one of these circuits conveys essentially proprioceptive information, while a second one is mostly involved in visually guided oculomotor behavior, and the third one is formed, at least in part, by polysensory neurons that respond to stimuli located in the peripersonal space. This seems to be the only theory which does not rule out modality-specific forms of USN. Neural systemsdevoted to directing attention to specific portion of space have been conceived as the substratum of space representation (Nichelli, Rinaldi, & Cubelli, 1989). Studies on line bisection (Nichelli et al., 1989) have shown that space representation is a dynamic process in both normal subjects and USN patients. Accordingly, USN can be defined as the outcome of a distorted distribution of the global pattern of attention over space. However, the issue of whether space exploration could be selectively affected by different sensory modalities remains unresolved. In any case, even those theories which predict modality-specific forms of neglect cannot explain domain-specific dissociations within the same sensory modality. A striking dissociation within the visual modality has been demonstrated by a patient described by Costello and Warrington (1987): after a bilateral parietal lobe lesion, the patient made reading errors at the beginning of the words (left-sided neglect dyslexia) but showed right-sided visuospatial neglect when copying drawings or in line bisection. In agreement with the suggestion that different neuropsychological mechanisms may underlie the various manifestations of USN, Costello and Warrington (1987) emphasize that the neglect dyslexic patient (J.A.F.) originally described by Baxter and Warrington (1983) showed no evidence of more general neglect. The same is true for patient M.T. reported by Bisiach, Vallar, Perani, Papagno, and Berti (1986), who read only the last two letters of a lo-letter word and yet was unimpaired in an item-cancellation task. A peculiar domain-specific dissociation was also

142

CUBELLI ET AL. TABLE 1 SUMMARYOF PAPERSDEALINGWITH THE ISSUE

OF MODALITY

EFFECTS IN

USN

Task similarity

Intrasubject analyses

Modalities tested

1. Supporting sovramodahty Bisiach et al., 1984 Bisiach et al., 1985b Weintraub & Mesulam, 1987

-

-

V; A V; T V; T

2. Supporting modality specificity Fagiioni et al., 1971 Chedru, 1976 Halsband et al., 1985 Pellat et al., 1986 Villardita, 1987 Barbieri and De Renzi, 1989 De Renzi et al., 1989 Gentilini et al., 1989

+

+ +

V; T V; T V; T; A; K; M V; T V; T V; T; M V; A V; T

Evidence

-

+ + + + -

Note. V, visual; T, tactile; A, acoustic; K, kinesthetic; M, motor. Most authors label “tactile” neglect the kind of neglect that is apparent in blindfold space exploration.

reported by Poizner, Klima, and Bellugi (1987), who tested deaf patients fluent in American Sign Language. Following right-brain damage these patients showed left neglect in the classical spatial tests but not during sign communication. Several experimental studies have shown that performance of USN patients can vary according to the nature of the task (Colombo, De Renzi, & Faglioni, 1976; Mark, Kooistra, & Heilman, 1988; Halligan, Marshall, & Wade, 1989) or to the stimulus type (Leicester, Sidman, Stoddard, and Moore, 1969; Chain, Leblanc, Chedru, & Lhermitte, 1979; Caplan, 1985; Weintraub & Mesulam, 1988). Two experimental criteria seem to be necessary in order to evaluate putative sensory modality effects in USN and to detect modality-specific forms of USN: (1) Experimental tasks must be the same except for the modality of space exploration. (2) A separate analysis of single subjects’ performance is required. Table 1 shows that no single study investigating the issue of modality effects in space exploration has met both these criteria. Only two papers met the criterion of task similarity, by comparing visual and blindfold exploration of the same space in brain-damaged patients. Chedru (1976) asked his subjects to tap all the keys of a teletype keyboard as quickly as possible and after 200 tappings computed how many rightand left-sided keys were tapped. In the task adopted by Gentilini, Barbieri, De Renzi, and Faglioni (1989) subjects, both viewing and blindfolded, searched for six target keys hidden in the keyboard of an Apple IIe

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personal computer. However, neither Chedru (1976) nor Gentilini et al. (1989) performed an analysis of single subjects’ performance. In conclusion the evidence supporting the claim that USN can be restricted to one sensory modality seems not to be sufficiently grounded. In order to discuss the issue of modality-specific effects in USN we report here a reanalysis of Gentilini et al.‘s data aimed to look for instances of intrasubject dissociations. To extend the discussion to the issue of domain-specific dissociation, we compared the performance at the keyboard task with that at a sentence reading task and at a cancellation task. A single case study showing opposite patterns of USN according to the task within the same sensory modality (a left-sided neglect dyslexia and a right-sided visuospatial neglect) was considered separately and taken into account in the general discussion about the origin of neglect phenomena. REANALYSIS OF GENTILINI ET AL.‘S (1989) DATA Apparatus and Procedure

A detailed description of the experimental sample and procedure has been reported by Gentilini et al. (1989). The analysis performed here concerns only the groups of control and right-brain-damaged patients. Subjects were seated in front of the keyboard of an Apple IIe microcomputer. A plywood shutter on the keyboard masked the most peripheral keys. They were informed that six keys, different from trial to trial and symmetrically arranged around the center of the keyboard, produced an acoustic signal when pressed. Their task was to find these keys by pressing one key at a time with the index finger of the hand ipsilateral to lesion. The computer recorded the keys pressed on each testing run and, by attributing a value of -2, - 1, + 1, + 2, respectively, to the number of leftmost (L), left intermediate (I), right intermediate (r), and rightmost (R) keys, calculated a percentage neglect score (N) according to N=2xL+l+r+2xRx100s L+l+r+R

In this way a neglect score of 0 represented an exploratory pattern of the keyboard perfectly balanced between the two halves of the space, a positive score corresponded to a preference for the right half of the keyboard, and a negative score, a preference for the left part of the keyboard. Greater absolute values of the score corresponded to stronger imbalance of the exploratory pattern. In order to detect possible evidence of dissociated performances between the two conditions of the keyboard exploration task, single subjects’ data analyses were carried out within the group of all right-brain-damaged

144

CUBELLI ET AL. 200 P z s 2 B 2

q q

El

loo-

q

1 El

4

. 0

-

”

.’

l*

q 8

*FM

q

l

El

q 0

•I

-100 -100

q s

l

* EP

_

l

I

I

0

100

200

N open eyes FIG. 1. For each subject N score obtained when exploring the keyboard with open eyes is plotted against N score when blindfolded. Positive values indicate preference for the right half of the keyboard and negative values, preference for the left half. Lines define the range of normal subjects’ performances.

patients (both those with and those without USN). For this purpose we took as evidence of impaired performance at a given task N scores exceeding the range of those obtained by normal controls. Dissociated performance was defined in a patient who showed a difference between the two N scores exceeding the maximum difference found in normal controls. As shown in Fig. 1, we found five patients (upper right quadrant) preferring the right side of the keyboard both with open eyes (N score > 53.12) and when blindfolded (N score > 59.37), while three patients (upper left quadrant) were found to be impaired only when blindfolded and four patients (lower right quadrant) only in the open eyes condition. Six patients had scores within the normal range. Of the remaining two patients, one subject showed a left-side preference both with open eyes (N score < -46.36) and when blindfolded (N score < -61.06; lower left quadrant), and the other one showed a left-side preference when blindfolded, but no side preference on the open eyes task. Dissociated performances were found in five patients whose difference between N score in the open eyes and N score in the blindfold condition exceeded the value of +58.75. Three of them (Fig. 2, upper right quadrant) showed an exaggerated preference for the right side of the keyboard in the open eyes condition and a normal performance in the blindfold condition, while, of the remaining two patients, one (Fig. 3, upper left quadrant) showed a normal performance in the open eyes condition and an exaggerated preference for the left side of the keyboard when blindfolded, and the last one obtained N scores within the normal limits on

DISSOCIATIONS

P 43 P 2 $ z t $

145

IN USN

200

100

El

I .

-100 -100

e

QQ

1

1

0

100

!

200

N open eyes FIG. 2. For each subject the difference between N score with open eyes and when blindfolded is plotted against N score in the open eyes condition. Dissociated performances were defined when the difference between the two scores exceeded the maximum difference found in normal controls. Lines define the range of normal subjects’ performance.

the two tasks. No patient showed dissociation indicating an exaggerated preference for the right side in the blindfold condition. Further comparisons were carried out between the performance on the open eyes exploration task and the sentence reading task. Seven patients were found to be impaired with both methods, while two patients were impaired only in the reading task, two subjects were impaired only in the keyboard exploration task, and eight subjects performed normally in both tests. The only right-brain-damaged patient that showed a left-side preference in the open eye task was normal in the reading task. DISCUSSION

There are two relevant findings from the analyses of single patients’ data from Gentilini et al.3 study (1989): (1) the extreme variability of performance according to the sensory modality involved in space exploration and (2) the dissociations within the visual modality between the reading and the exploratory task. The different theories proposed to give an account of USN cannot address this variability equally well. The representational theory (Bisiach, Cornacchia, Sterzi, & Vallar, 1984) anticipates that neglect phenomena are detectable in all modalities. A single task might be more sensitive in discovering USN, but dissociations of performance according to modality of exploration and type of test can hardly be reconciled with the view of USN as the result of the disruption of a unitary representational mechanism.

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-100

0

100

200

N blindfolded

FIG. 3. For each subject the difference between N score in the open eyes and in the blindfold condition is plotted against N score in the blindfold condition. Dissociated performances were defined when the difference between the two scores exceeded the maximum difference found in normal controls. Lines define the range of normal subjects’ performance.

The same holds true for the intentional theory, at least for those modalities that are involved in an active search for information. As to the “attentional” theory, Buchtel and Butter (1988), using a variant of Posner et al.3 (1982) spatial cueing task, found that the validity of visual and auditory cues influences the speed of response to visual targets but not to auditory targets, and they hypothesized that “crossmodal cueing of spatial position works only with modalities for which movement leads to improved sensory analysis.” This view emphasizes the linkage between the attentional system and the orienting of motor activity toward space location and implies the existence of modality-specific representations of visual and auditory space. Along the same lines, Butter, Buchtel, and Santucci (1989) proposed a supramodal organization of tactile and visual space representation since both these modalities can evoke orienting body movements that allow improved sensory analysis, a view which would not predict dissociations between blindfolded and visual exploration of extrapersonal space in USN patients. Note that we found one right-brain-damaged patient with an exaggerated preference for the left side of the keyboard when blindfolded. This unexpected finding cannot be explained by any of the current theories of neglect. The dissociation between keyboard exploration with open eyes and sentence reading seems to suggest that, in single patients, neglect phe-

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FIG. 4. CT scan. 28 April 1989.

nomena can vary within the same modality, according to the cognitive process involved. CASE REPORT

A.R., a 33-year-old right-handed bricklayer with 5 years of schooling, was admitted to the Rehabilitation Center “Villa Beretta” at Costamasnaga (Como, Italy) on May 10, 1989. He had been found unconscious on March 9, 1989, and referred to the Monza Hospital. Here a CT scan showed a large hematoma in the left parieto-occipital region with massive tetraventricular bleeding. After surgical evacuation of the clot at the Fatebenefratelli Hospital in Milan he regained consciousness, but he still showed mild dysphasia, severe right hemiparesis, impaired touch and position sense in the right limbs, and a dense right homonimous hemianopia. A control CT scan performed on April 28, 1989, showed a large hy-

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0

FIG. 5. (a) A.R.‘s copy of an array of three simple geometric shapes showing omission of the figure on the right. (b) A.R.‘s copy of a simple geometric pattern. (c) A.R.‘s marks of the hours on the dial of a clock (numbers inside the dial are those marked by A.R.; numbers outside the dial indicate the order of marking).

podense area in the site of the bleeding with dilatation of the left lateral ventricular system and especially of the left occipital horn (Fig. 4). When he was admitted to the rehabilitation center it appeared that he was insecurely oriented in time and place. On the WAIS his verbal IQ was 92, while his performance IQ was only 76. His spontaneous speech was normal with regard to phrase length, prosody, and syntax, but wordfinding difficulties were occasionally observed. On the Italian Version of the Aachener Aphasie Test (Huber, Poeck, Weniger, & Willmes, 1983; Luzzatti et al., 1987) he scored 116/120 on comprehension (which corresponded to the 98th percentile of the control population), 146/150 on

DISSOCIATIONS

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149

repetition (94th percentile), 108/120 on naming (94th percentile), 32/50 on the Token Test (69th percentile), and 50/90 on the written language (56th percentile). The poor performance at written language reflected an impairment both in reading (26/30) and in assembling written letters to form single words and sentences (24/30), but although he was able to use his left hand to write single letters he showed an almost complete inability to write words and sentences under dictation (O/30). Unfortunately, tactile naming of objects placed in his left hand was not tested. Nonetheless the pattern of writing impairment seems to suggest a functional disconnection between the two hemispheres. Reading errors always affected the left side of the word and of the sentence (for instance, he read “ciglia/eyelashes” instead of “biglia/marble” and “io te lo devo lasciare/I must leave this with you” instead of “dove te lo deve lasciare/where should he leave it”). He was able to copy simple and complex geometric forms (Fig. 5b), but when he had to copy an array of simple geometric shapes he tended to neglect those on the right (Fig. 5a). Asked to mark the hours on the dial of a clock, he began writing 12 at the top and 6 at the bottom and went on counterclockwise with the hours of the left side of the dial, then stopped and, after a delay of 10 set, marked 1, 2, and 3, but omitted 4 and 5, claiming he had completed his task (Fig. 5~). In summary, like the patient described by Costello and Warrington (1987), A.R. appeared to neglect the left space in reading and the right space in visuospatial tasks. In the following investigation we document this dissociation in more detail. Experimental

Investigations

A.R. was examined on several occasions between June 30 and August 16, 1989, and was presented with visuospatial tasks (Cancellation Task, Raven Coloured Progressive Matrices, Figure Search, Word Finding Task) and with a list of words to read. Cancellation

Task

This was a modified version of Albert’s test (Albert, 1973), consisting of 20 lines, each 30 mm in length, drawn in an apparently random manner on a 215 by 320-mm sheet of paper. However, the lines were not random, but arranged in four rows of 5 lines each and in such a way that 10 were to the left and 10 to the right of the center of the paper. The task of the subject was to cross out all lines on the page. All normal subjects perform the test without error (Nichelli et al., 1989). A.R. failed to cross out 2 lines on the right, a behavior that is indicative of USN. Raven-Colored

Progressive Matrices

Performance on this test was scored in terms of position preference only, without reference to whether the response was correct. The score

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was the difference between the number of response alternatives chosen on the left and those chosen on the right. Choices of alternatives in the center were disregarded. In a previous study (Colombo, De Renzi, & Faglioni, 1976) a difference greater than 8 was not found in normal controls. A.R. chose 16 alternatives on the left side and only 4 on the right: therefore he obtained a score of 12, which is indicative of right USN. Figure Search

This was a modified version of the test proposed by Colombo, De Renzi, and Gentilini (1982). The patient was seated in front of the examiner. His task was to find a target item among 20 alternatives. The display consisted of 20 photographs, each 10 x 10 cm, arranged vertically in five columns of 4 photographs each. At the beginning of the test the display was on the table and its central column was aligned with mid sagittal plane of the subject’s body. The subject had to look at the examiner until he/she asked the subject to find the target figure. The order of presentation of target items was pseudorandom and the examiner never asked for more than two items from the same column to be found successively. The mean searching time was 2.41, 4.99, 3.47, 5.85, and 7.53 set, respectively, for the leftmost, left middle, mid sagittal, right middle, and rightmost column. The score was determined by the sum of the searching time in the two right columns divided by the sum of the searching time in the two left columns and was therefore found equal to 1.81 (the values obtained by six normal male controls of the same age and level of schooling ranged from 0.79 to 1.22; mean = .95). Word-Finding

Task

The patient was seated in front of the screen of the computer and was asked to try to find a target word which appeared on the screen among other lexical items. Before the beginning of each trial, the superordinate of the word to be found was displayed (e.g., “a town” if the target word was “Milano”). The subject read the superordinate aloud and the examiner pressed a key only when he had read it correctly, causing the appearance of the target word among the distracters. For each trial a display of 12 words was presented to the subject. His task was to find and read aloud the target word. When he had done it the examiner pressed a key and the computer recorded the time elapsed from the beginning of the trial. The words on the display were equally distributed in three sectors of the screen (the central, the left, and the right sectors). Each sector contained one word written horizontally from left to right, one word vertically from top to bottom, one word diagonally from top-left to bottom-right, and one word diagonally from bottom-left to top-right. Each testing session consisted of 18 trials, so that 2 horizontal,

DISSOCIATIONS

IN USN

1.51

TABLE 2 A.R.3 SEARCHINGTIME OF WORDSIN THE LEFT, IN THE CENTRAL, AND IN THE RIGHTSECTOR OF THE SCREENAT THE WORD-FINDING TEST, COMPAREDWITH THE MEAN AND THE RANGE OF PERFORMANCEOBTAINED FROM A GROUP OF SIX MATCHED NORMAL CONTROLS

Left sector

Central sector

Right sector

A.R. First session Second sesson Third session

1.70 2.19 1.70

13.87 6.33

24.95 22.16

8.16

19.77

Mean

1.86

9.45

22.29

Controls Mean Range

3.26 2.06-4.28

4.30 2.42-8.87

4.39 2.18-7.17

and 2 diagonal target words had to be found for each sector in a random order. A.R. was examined at this test on three sessions, 2-3 days apart. Table 2 shows the mean searching time in seconds for target words presented in the left, in the central, or in the right sector of the screen, compared with the performances on two trials of a group of six matched controls. A.R.‘s performance at this task is strongly indicative of a right-sided USN, a fact which, in light of his difficulties on reading the leftmost part of the words, demonstrates that the side of neglect phenomena did not depend on the nature of the stimuli to be processed. 2 vertical,

Single Word Reading

A.R. was asked to read a set of 133 words that were presented one by one in the center of the screen of a PC computer. The subject had unlimited time to study the word before reading it aloud. The list was composed by the 40 concrete words taken from the reading test proposed by Basso, Capitani, and Vignolo (1979) and by the 96 nouns (controlled for length, frequency, and imagery value) of the list proposed by Job (1987). Three words were common to both lists and were presented once. The order of presentation was randomly determined. The total corpus of errors is given in the Appendix. Errors were classified according to the criteria of Ellis, Flude, and Young (1987) as follows: 1. Neglect errors: errors in which the target and error words are identical to the right of an identifiable neglect point, but in which there are no letters in common to the left of the neglect point (for example “suore/nuns” instead of “favore/favour”: in this case the neglect point occurred between “v” and “0”). 2. Nonneglect errors: other real-word errors which do not meet the

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CUBELLI ET AL. TABLE 3

ERROR ANALYSIS OF A.R. COMPAREDWITH THAT OF FOUR NEGLECT DYSLEXIC PATIENTS DESCRIBEDIN THE LITERATURE

A.R.

J.A.F.

V.B.

J.O.H.

Percentage of errors

19.5

22.5

15

27.7

Neglect errors Nonneglect errors Nonword errors

73 27 0

69 28 3

66 26 8

63 14 23

criteria for inclusion in the neglect category (e.g., “bionda/blond” for “bends/bandage”). 3. Nonword errors: responses which were neologisms. A.R. did not produce any error of this type. Table 3 shows the percentage of errors of A.R. compared with that of J.A.F. (Baxter & Warrington, 1983), V.B. (Ellis et al., 1987), and J.O.H. (Costello & Warrington, 1987). There is no great variability in the percentage of the different types of reading errors between A.R., V.B., and J.A.F. At variance with V.B. and J.A.F., J.O.H. showed a consistent proportion of nonword errors. A.R., who shared with this patient the association of left neglect dyslexia with visuospatial neglect on the opposite site, did not produce nonword errors. Table 4 shows the percentage of A.R.‘s reading errors as a function of word length and compares his performance with that of V.B. and J.O.H. Results show that, at least in these neglect dyslexic patients, word reading accuracy is not affected by word length. Furthermore, as some neglect dyslexic patients already described (Hillis & Caramazza, 1990), A.R. made fewer errors with high-frequency compared with low-frequency words, but the difference did not reach the level of statistical significance (with continuity correction, x2 = 3.659, 1 df, p < .lO). Word imageability did not affect his performance (with continuity correction, x2 = 2.058, 1 df, p -=c.20). DISCUSSION

Katz and Sevush (1989) have recently described two patients with lefthemisphere lesions who showed visual extinction on the right but reading difficulty on the left side of the words. One of them (J.M.) also showed some evidence of right USN (missed two letters in a letter-cancellation task and failed to draw the right portion of a daisy on one of two attempts). Katz and Sevush (1989) argue that dyslexia cannot be interpreted as a particular instance of ipsilateral spatial neglect both in their patients and in the patient described by Costello and Warrington (1987). They base

DISSOCIATIONS TABLE

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IN USN 4

PERCENTAGE OF ERRORS FOR WORDS OF EACH LETTER LENGTH BY A.R. COMPARED WITH THE PERFORMANCE OF Two DYSLEXIC PATIENTS DESCRIBED IN THE LITERATURE

A.R. J.O.H. V.B.

6

0 (17) 33.7 (157) 15 (20)

26 (19) 47 (79) 15 (20)

18 (22) 29 (41) 20 (20)

27 (18) 14 (22) 10 (20)

26 (57) 14 (49) 6 (30)

Note. The number of words of each letter is given in parentheses

their claim on the difference between the pattern of reading errors of these three patients and that of neglect dyslexics following right hemispheric damage. First, according to them, neglect dyslexics should make few nonword errors (i.e., they should not produce a nonword when trying to read a word), whereas all these three patients made a proportion of nonword errors, from 23% for J.O.H. to 38.5% for L.S. The reason for not accepting a nonword as an instance of neglect error is far from being clear; in any case, since A.R. did not produce a single nonword as a response to a word, this criterion cannot apply to all patients showing right USN and left neglect dyslexia. A second discrepancy is the claim that neglect dyslexics should make errors of omission or substitition affecting the entire half of compound words, while J.O.H. would make mistakes by substituting incorrect initial letters. We have not administered compound words to our patient, and therefore we can add nothing to this topic. However, a number of studies both on USN patients and on normal subjects biased to direct visual attention to one side (Sieroff & Michel, 1987; Sieroff, Pollatsek, & Posner, 1988; Sieroff & Posner, 1988) have not detected differences between compound words and other words; furthermore it is rather obscure on the basis of which theory of neglect a particular performance of neglect dyslexics with compound words should be predicted. The third discrepancy is the fact that J.O.H. made fewer errors on long words than on short words, but again, as shown in Table 4, this is far from being typical of patients showing neglect dyslexia contralateral to visuospatial neglect, as the same pattern of performance is shown by V.B., a neglect dyslexic patients who also showed general left neglect (Ellis et al., 1987). On this basis we must conclude that the claim that reading performance in neglect dyslexic patients showing general neglect on the same side reflects an impairment at a level different from that of those showing general neglect on the opposite side is not substantiated by empirical evidence. Left neglect in reading single words reflects a specific cognitive

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disorder, which can occur at different levels of representation, independently from the hemispheric side of lesion and from the cooccurrence and the side of general visuospatial neglect. It should be also emphasized that neglect in reading is not an instance of a material-specific deficit as demonstrated by the fact that A.R. showed right neglect when he had to find a word of a given category among distracters, but left neglect in single word reading. GENERAL DISCUSSION In a recent study Nichelli et al. (1989) have shown that line bisection can be affected, in normal subjects as well as in USN patients, by orienting attention to one side. They concluded that space representation, defined as the global pattern of attention distributed over space, is a dynamic function in both normal and pathological conditions. A number of studies have shown that the attentional demands of the task are important in determining the presence and the severity of neglect: USN patients’ line bisection is affected by a cue at the contralesional end of the line (Nichelli et al. 1989; Riddoch & Humphreys, 1983); Rapcsak, Verfaelie, Fleet, and Heilmann (1989) showed that increasing demands of visual selective attention adversely affects exploration of the left side of space; Aglioti and Barbieri (personal communication) demonstrated that USN is less severe with preattentive vision, i.e., when subjects had to detect conspicuous local feature or textons (Julesz, 1981) and more severe with attentive vision, which relies on serial processing and requires an effortful, sequential scanning of the display; Pierson-Savage, Bradshaw, and Nettleton (1988) showed that the rehabilitative effort to overcome difficulties in attending to events on the left can induce in USN patients an overcompensatory left-side advantage in vibrotactile reaction times in the open eyes condition, opposite to the right-side advantage at the same task that is found in nonrehabilitated patients. Concerning the role of attentional mechanisms in reading, many current models emphasize that meaningful letter strings can automatically attain an integrated word form, i.e., without any active scanning and with minimal allocation of attentional resources (LaBerge & Samuels, 1974; Posner, 1978). McClelland and Rumelhart (1981) proposed an interactive model of word reading, by which low-level visual information activates high-level word forms, which in turn feed-back to facilitate individual letter identification. While such a process would operate in parallel without active control by the subject, in the case of nonwords an elaborate serial scan requiring spatial attention would be needed (Sieroff et al., 1988). In this framework the creation of the “word form” should be spared from the attentional scanning deficit produced by parietal lesion (Sieroff & Michel, 1987). This interpretation is consistent with the observation of Sieroff et al. (1988), who reported neglect patients performing better at reading words than at spelling unpronouncable nonwords. Nevertheless,

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V.B. (Ellis et al., 1987) did not show any difference in accuracy when reading words and nonwords that were very similar to words. Furthermore Bisiach, Meregalli, and Berti (198%) have reported a left neglect patient, E.B., who made many neglect errors in reading lo-letter words and readable nonwords but was accurate in reporting lo-letter nonwords, the left half of which was constituted by an unreadable segment of five consonants. An alternative to the view that restricts the deficit of USN patients to the impairment of effortful attentional scanning is the proposal that spatial attention may differentially operate on different levels of representation (Caramazza & Hillis, 1990), and with very different requirements of cognitive resources. From this perspective the dissociation shown by J.O.H. and A.R. between left neglect in reading and right neglect in visuospatial tasks reflects not a material-specific deficit, but rather the disruption of separate systems involved in different cognitive operations. If this is the case, i.e., if there is not a single supramodal attentional system ruled by the opposing contraversive tendencies of the two hemispheres (Kinsbourne, 1977), one should view the distribution of attention over space as the result of a variety of neuronal systems that are called into action depending on the cognitive operation undertaken by the subject. Rizzolatti, Gentilucci, and Matelli (1985) have shown that, as far as systems directing attention toward specific portions of the space are concerned, each hemisphere includes neurons with both ipsilateral and contralateral receptive fields. Such an arrangement does not rule out the possibility of neglect disorders on the side ipsilateral to the lesion. Ipsilateral deficits have been reliably reported especially with regard to the symptom of extinction, both in the tactile (Schwartz, Marchok, Kreinick, & Flynn, 1979) and in the auditory modality (De Renzi, Gentilini, & Pattacini, 1984). Systematic studies are needed to confirm their possible occurrence and their clinical relevance in visuospatial neglect and in neglect dyslexia. A first conclusion from the analysis of all these possible dissociations is in agreement with the view (Hillis & Caramazza, 1989) that the term “unilateral spatial neglect” is indeed used in reference to a variety of phenomena that are not symptoms of a unitary deficit, but reflect impaired attentional mechanisms that may operate at several levels of cognitive processing. APPENDIX AR’s

Errors in Oral Reading of Words

Neglect Errors

Cospetto (presence) -+ Sospetto (suspicion) Falce (sickle) -+ Alce (elk) Essenza (essence) + Cosenza (Calabrian town)

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Agio (ease) + Ligio (true) Casa (house) + Borsa (bag) Evento (event) + Spent0 (extinguished) Marea (tide) + Idea (idea) Capretto (kid) + No (no) Fanale (lamp) + Canale (channel) Tatto (touch) + Gatto (cat) Monello (urchin) + Pennello (brush) Favore (favour) -+ Suore (nuns) Accord0 (agreement) + Ricordo (recollection) Aula (hall) + Bella (beautiful) Genere (gender) --+ Cenere (ash) Tuta (track-suit) + Muta (mute) Annata (year) + Renata (Renee) Garbo (grace) 4 Sgarbo (rudeness) Nonneglect Errors

Pace (peace) --+ Alce (elk) Assetto (trim) -+ Sospetto (suspicion) Ordine (order) + Rondine (swallow) Canone (canon) + Cannone (cannon) Benda (bandage) + Bionda (blond) Via (way) --+ Cava (quarry) Nozione (notion) 4 Nazione (nation) REFERENCES Albert, M. L. 1973. A simple test of visual neglect. Neurology, 23, 658-664. Barbieri, C., & De Renzi, E. 1989. Patterns of neglect dissociation. Behaviourul Neurology, 2, 13-24. Basso, A., Capitani, E., & Vignolo, L. A. 1979. Influence of rehabilitation on language skill in aphasic patients. Archives of Neurology, 36, 190-196. Battersby, W. S., Bender, M. B., Pollack, M., & Kahn, R. L. 1956. Unilateral “spatial agnosia” (inattention). Brain, 79, 68-93. Baxter, D. M., & Warrington, E. K. 1983. Neglect dysgraphia. Journal of Neurology, Neurosurgery and Psychiatry, 46, 1073-1078. Bay, E. 1953. Disturbances of visual perception and their examination. Brain, 76, 515-551. Bisiach, E., Berti, A., & Vallar, G. 1985a. Analogical and logical disorders underlying unilateral neglect of space. In M. I. Posner & 0. S. M. Marin (Eds.), Attention and performance XI. Hillsdale, NJ: LEA. Ch. 12, pp. 239-245. Bisiach, E., Bulgarelli, C., Sterzi, R., & Vallar, G. 1983. Line bisection and cognitive plasticity of unilateral neglect of space. Bruin & Cognition, 2, 32-38. Bisiach, E., Capitani, E., Luzzatti, C., & Perani, D. 1981. Brain and conscious representation of outside reality. Neuropsychologiu, 4, 543-551. Bisiach, E., Capitani, E., & Porta, E. 1985b. Two basic properties of space representation in the brain: Evidence from the unilateral neglect. Journal of Neurology, Neurosurgery and Psychiatry, 48, 141-144.

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