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Setting the midpoint of sentences: The role of the left hemisphere
Neuropsychologia 137 (2020) 107287
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Setting the midpoint of sentences: The role of the left hemisphere Laura Veronelli a, *, Lisa S. Arduino b, c, Verena Biscaro d, Massimo Corbo a, Giuseppe Vallar d, e a
Department of Neurorehabilitation Sciences, Casa di Cura del Policlinico, Milan, Italy Department of Human Sciences, LUMSA University, Rome, Italy c ISTC-CNR, Rome, Italy d Department of Psychology, University of Milano-Bicocca, Milan, Italy e Neuropsychological Laboratory, IRCCS Istituto Auxologico Italiano, Milan, Italy b
A R T I C L E I N F O
A B S T R A C T
Keywords: Unilateral spatial neglect Aphasia Sentence bisection Word bisection Line bisection Reading habits
The human brain has a remarkable capacity to focus processing resources based on the features and the relevance of the task at hand. The two cerebral hemispheres contribute differentially to this capacity, with the left hemisphere linguistic and right hemisphere visuo-spatial abilities each offering unique contributions. For example, previous research has established that healthy participants set the subjective mid-point of written sentences more leftwards of center, compared to unpronounceable letter strings or simple lines. Remarkably, patients with right hemisphere damage exhibiting unilateral spatial neglect also show this pattern, even though, as well known in the literature, they tend toward a rightward- bias for non-linguistic stimuli. This evidence suggests that the leftward bias for sentential material is due to linguistic, mainly left-hemisphere mediated processes, which are largely unimpaired in right brain-damaged patients, and intact in heathy participants. To test this hypothesis, we compared sentence bisection performance to that of letter strings and simple lines in left brain-damaged patients (with and without aphasia). If the larger leftward bias in the bisection of sentential material is based on linguistic processes, then the left brain-damaged patients should show a reduction or absence of a leftward bias in sentence bisection. We tested twenty-four left brain-damaged patients (12 with aphasia and 12 without aphasia), and 24 age-matched elderly participants (patients and controls were all righthanded). Participants were asked to bisect 240 stimuli, comprising: (i) affirmative and interrogative clauses, (ii) sentences with lexical and syntactic violations, (iii) letter strings and (iv) simple lines. As predicted, neurolog ically intact participants showed larger leftward biases in bisecting written readable sentences compared to strings of letters. In contrast, the left hemispheredamaged patients (both with and without aphasia) showed no differences in bisecting sentences and letter strings or lines. These findings indicate that the larger leftward bias exhibited by healthy participants in the bisection of sentences is likely due to ortho-phonological coding taking place implicitly during the bisection task. This ortho-phonological coding is impaired with left brain damage – also in absence of apparent aphasia – leading to the left hemispheredamaged patients showing a reduced leftward bias in sentence bisection. These findings support the hypothesis that the leftward bias in the bisection of written sentences is the result of ortho-phonological influences rather than visual-spatial biases.
1. Introduction Line bisection (Schenkenberg et al., 1980) is a clinical test for the detection of unilateral spatial neglect (USN). When required to set the midpoint of a horizontal segment, right brain-damaged patients with left USN may transect the line to the right of the objective midpoint of the stimulus (Bisiach et al., 1976; Heilman et al., 1983; Vallar et al., 2000). On the other hand, left brain-damaged patients can exhibit a dispro portionate leftward bias, interpreted as an indicator of right USN (Beis
et al., 2004; Kleinman et al., 2007; Sallard et al., 2012; Zilli and Heil man, 2016), although right USN after left brain damage is overall comparatively less frequent (Beume et al., 2017; Buxbaum et al., 2004), or severe (Ogden, 1985) than after right brain damage. A leftward bias (pseudoneglect), although smaller in size, has been found also in healthy participants, interpreted as due to a leftward orientation in a visuo-spatial task, supported by activity of the right hemisphere, and affected by a number of factors, including age, and scanning direction in reading (Bowers and Heilman, 1980; Jewell and McCourt, 2000, for
* Corresponding author. Department of Neurorehabilitation Sciences, Casa di Cura del Policlinico, via Dezza 48, 20144 Milan, Italy. E-mail address: [email protected] (L. Veronelli). https://doi.org/10.1016/j.neuropsychologia.2019.107287 Received 26 April 2018; Received in revised form 21 November 2019; Accepted 28 November 2019 Available online 19 December 2019 0028-3932/© 2019 Elsevier Ltd. All rights reserved.
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Neuropsychologia 137 (2020) 107287
review; Rinaldi et al., 2014). The relationship between spatial and linguistic (orthographic) pro cessing has been studied through tasks that require the bisection of words and sentences (Arduino et al., 2016, 2010; Fischer, 2000, 1996; Gabay et al., 2015; Veronelli et al., 2014a, 2014b; Fischer, 2004; Arduino et al., 2016; Veronelli et al., 2017). Neurologically unimpaired participants show pseudoneglect, namely a larger leftward bias, when bisecting words and pseudowords (i.e., legal non-words), but not letter strings (Fischer, 1996). This finding indicates an overestimation of the spatial extent of word beginnings, compared to letter strings, related to lexical access (Fischer, 2000, 2004, 1996; Gabay et al., 2015), which is necessary for establishing a cohort of potential entries in the mental lexicon (Paap et al., 1982). One study in neurologically unimpaired participants found a leftward bias for all types of discrete stimuli (whether they be Italian words, pseudowords, letter or symbol strings), as well as for continuous lines, with the only exception of short ortho graphic stimuli, which were bisected rightwards (Arduino et al., 2010). These findings indicate that a number of different processes may influ ence the bisection of a stimulus, including its lexical status, and its continuous vs. discrete perceptual structure (see also Girelli et al., 2017). The role of ortho-phonological information in modulating directional biases in stimulus bisection has been demonstrated in different lan guages. In Italian, a language with a shallow orthography (Ellis et al., 2004; Toraldo et al., 2006), words stressed on the penultimate syllable induce a larger rightward bias, compared to words stressed on the antepenultimate syllable in both USN patients and healthy participants (Veronelli et al., 2014b). In German, a language with a quite transparent orthography (Frith et al., 1998), participants perceive the midpoint of the string to be closer toward the side with more phonemes (Fischer, 2004), showing a grapheme-phoneme convergence effect on the perceived word centre (although only for the trigram SCH). Concerning lexical features, English and Hebrew readers show a written word fre quency effect, with larger leftward biases in the bisection of lower, as compared with higher frequency words (Gabay et al., 2015). In the last few decades, many studies on line bisection have shown that the magnitude of both pseudoneglect in healthy participants (Jewell and McCourt, 2000, for review) and of the rightward bias in patients with left USN (Bisiach et al., 1983; Halligan and Marshall, 1989; Vallar et al., 2000) is influenced by stimulus length, typically with a greater error with longer lines. Accordingly, sentences, which are longer in extent than words, may induce larger deviation biases, and help uncoupling spatial and linguistic factors. Veronelli and coworkers (2014a) have recently investigated the interaction between written language and spatial cognition using a sentence bisection task. Right brain-damaged patients with left USN and neurologically unimpaired participants were asked to set the subjective mid-point of declarative and interrogative sentences, of sentences with lexical and syntactic vi olations, of letter strings, and of lines. USN patients showed an overall rightward error, larger than the one exhibited by control participants, and affected by stimulus type, with larger rightward deviations with lines, moderate deviations with letter strings, and slight deviations with sentences. Letter strings and sentences were therefore bisected more leftward compared to lines. The smaller rightward deviation shown by USN patients with readable sentences might be indicative of a less asymmetrical spatial exploration, mediated by the linguistic features of the stimuli, and is in line with the left-to-right Italian reading habits (Chokron and Imbert, 1993; Girelli et al., 2017). The readability of the stimulus may be a factor to explain the ortho-phonological effect found in sentence bisection, with a reduction of the rightward deviation for sentential material compared to letter strings and lines in USN patients, and a leftward bias for control participants (see Veronelli et al., 2014a, for details). The aim of this study was to investigate the nature of this directional modulation during the bisection of orthographic material in a group of left brain-damaged patients with and without aphasia and dyslexia. Participants were asked to manually bisect different types of sentences,
namely: declarative, Yes/No interrogative, sentences with syntactic and with lexical violations, and, as control materials, letter strings and lines. Left brain-damaged patients underwent a baseline linguistic assessment of the status of the semantic-lexical system, of sub-lexical conversion functioning, and of grammatical competencies. We hypothesized that the presence of aphasic deficits might interfere with the putative lin guistic sentence processing during a length estimation task. Such lin guistic processing would affect the bisection performance in an implicit way, because the bisection task does not require an overt verbal pro cessing or response. We expected that patients with aphasia and dyslexia, differently from controls, would not show a difference in bisecting readable and unreadable material, or would exhibit a specific bisection pattern more in accordance with the linguistic impairment they have. Specifically, the evidence above suggests, for sentential ma terial, a leftward bias in neurologically unimpaired participants and a comparatively minor rightward error in USN patients, related to the linguistic features of the stimulus. In the light of these findings, we predicted that left brain damage could diminish or abolish such bias, particularly in patients with aphasia. This prediction implies that the most crucial differences are to be found comparing the bisection of sentential material vs. other types of stimuli, such as letter strings and lines, in patients and in control participants, rather than comparing different groups. The use of a variety of sentential material (declarative, interrogative sentences, non-syntactic and non-lexical sentence-like strings), and of letter strings, as in the study by Veronelli et al. (2014a), would allow to assess more specifically the effects of damage to the left hemisphere, which may impair language, on specific types of linguistic stimuli, in bisection tasks. Studies using tracking of eye movements suggest that patients with aphasia, as controls participants, are sensitive to both the structural frequency and the complexity of sentences in reading tasks, although patients may use different reading strategies (DeDe, 2017; Knilans and DeDe, 2015). To the best of our knowledge, this study is the first to investigate the performance of left brain-damaged patients in a sentence bisection task. 2. Material and methods 2.1. Participants Participants were recruited from the inpatient population of the Department of Neurorehabilitation Sciences of the Casa di Cura del Policlinico, Milan, Italy. A total of 24 left brain-damaged patients, and 24 age-matched participants (C) entered the study. Left hemispheredamaged patients had suffered a first-ever cerebrovascular stroke (20 ischemic, three haemorrhagic and one ischemic with haemorrhagic infarction). Patients were divided into two groups, according to their performance in a verbal comprehension task: patients with aphasia (Aþ), with a score � 22/50 (moderate impairment in auditory-verbal comprehension) at the Token Test (Luzzatti et al., 1994), and patients without aphasia (A-), with a score < 22/50. The Aþ group included 12 patients, six females, with a mean age of 70.75 years (SD � 9.20; range 55–83), and mean education of 9.92 years (SD � 3.63; range 5–17). Following a clinical evaluation and the administration of the Aachen Aphasia Test (Luzzatti et al., 1996), patients were classified as follows: five patients suffered from Broca’s aphasia (two with apraxia of speech), three from global aphasia, two from Wernicke aphasia, and one from anomic aphasia; one patient did not meet the criteria for any of the above-mentioned subtypes. The A- group included 12 patients, 9 females with a mean age of 72.58 years (SD � 13.79; range 60–85), and mean education of 11.67 years (SD � 3.75; range 5–17). The study also included twenty-four C participants (12 females), who were matched for age (M ¼ 72.58 years, SD � 9.36, range 65–85) and educational level (M ¼ 11.29 years, SD � 4.67, range 5–17) to the patients. One-way analyses of variance (ANOVAs) showed that age (F2,47 ¼ 0.13; p ¼ 0.87, η2 ¼ 0.01) and educational level (F2,47 ¼ 0.60; p ¼ 0.55, η2 ¼ 0.03) did not differ among groups (Aþ, A- and C). Lesion site was assessed for each left 2
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Neuropsychologia 137 (2020) 107287
brain-damaged patient by CT or MRI scan, and drawn manually by VB, supervised by LV, using the MRIcro software (Rorden and Brett, 2000), onto selected horizontal slices of a standard template brain. Scan images were not available for Aþ patient CL; medical records reported ischemic lesions in the left fronto-parietal areas. Overlapped lesion maps of 23 left-brain-damaged patients, subdivided in Aþ and A-groups are shown in Fig. 1. In Aþ patients lesions superimposed in the left insula, and in the temporal and frontal lobes (7 patients); in A- patients lesions super imposed in the left internal capsule and in the left insula (10 patients). Lesions were more extensive in Aþ (M ¼ 64.93 cm3, SD ¼ �51.91) than in A- (M ¼ 8.32 cm3, SD ¼ �7.69; t10 ¼ 3.58, p ¼ 0.005, η2 ¼ 0.38), and involved cortico-subcortical networks. In the A- group, lesions were limited to subcortical regions. Patients were right-handed, had normal or corrected-to-normal vision, and no history of previous neurological diseases or psychiatric disorders. Demographic and neurological infor mation of the Aþ and A- groups are shown in Table 1. The project was approved by the local Ethical Committee and informed consent was obtained from all participants, according with the Declaration of Helsinki (British Medical Journal, 302: 1194, 1991). 2.2. Baseline neuropsychological assessment. The presence and severity of aphasia were further assessed by a diagnostic battery, which included the following subtests of the Batteria per l’Analisi dei Deficit Afasici (BADA) (Miceli et al., 1994):
Table 1 Demographic and neurological data of 24 left brain-damaged patients (12 A þ and 12 A-). Sex/Age/ Education
Duration of disease (months)
Etiology/ Lesion site
Lesion volume (cc)
Neurological examination V
SS
M
I F/P I T/Bg/t/ ic/ec H F/P/T/ Bg/ic/ec IT I F/T/Bg I F/T/P/ ic/ec I T/t/Bg I/H F/T/ Bg I F/P/T H T/P/Bg I T/F/P I T/P
na 19.9
– –
ext þ
þ þ
83
ext
ext
þ
4.8 168.7 122.3
– – ext
– – þ
þ þ þ
8.1 77.8
– ext
– þ
þ þ
25.1 36 71 97.5
– – – –
– þ – –
þ þ þ þ
H T/t/Gb/ ic/ec I Bg I T/Bg/ic I F/P I T/Bg/ic I T/Bg/t/ ic I T/Bg/ic I T/t/Bg/ ic I T/t/Bg/ ic I T/t/Bg/ ic I T/t/Bg/ ic/ec I Bg/ic
22.6
–
–
þ
0.7 1.2 2.7 0.9 9.2
– – – – –
– – – – –
þ þ þ þ þ
8.4 1.9
– –
– –
þ þ
20.2
–
–
þ
9.5
–
ext
þ
16.2
–
–
þ
6.3
–
–
þ
Aþ patients CL CA
F/83/10 F/81/11
3 1
GV
F/69/5
4
AS SMC TF
F/67/13 F/60/9 M/69/8
1 49 2
GB MR
M/78/13 F/81/13
1 2
GA AS TCS CG
M/75/7 M/60/8 M/55/5 M/71/17
1 2 2 87
A- patients
(i) Pseudoword reading aloud (45 stimuli, from 1 to 3 syllables); pseudoword delayed copy (6 stimuli, from 1 to 3 syllables). These subtests evaluate sub-lexical conversion functioning; (ii) Visual lexical decision (80 stimuli, half pseudowords); word reading aloud (92 stimuli: 52 nouns, 20 verbs, 20 function words); visual noun comprehension (40 stimuli). These subtests evaluate lexical-semantic processing; (iii) Visual grammatical judgments (24 sentences); sentence reading aloud (6 stimuli); visual sentence comprehension (45 stimuli). These subtests evaluate grammatical competence. Neurologically unimpaired participants performed without errors the sentence reading aloud task, made no more than one error in the pseudoword delayed copy and visual noun comprehension tasks, and no more than two errors in the word and pseudoword reading aloud, visual lexical decision, visual grammatical judgments and visual sentence comprehension tasks (Miceli et al., 1994). The presence and severity of right USN were assessed by a diagnostic battery, which included the following tests:
MA
F/85/17
2
RA GE MC GE PS
F/84/9 F/85/13 M/76/12 F/60/8 F/71/17
96 1 1 1 1
MR GF
F/72/13 M/37/15
1 2
BR
F/66/8
1
CF
M/72/5
1
SN
F/79/10
1
NG
F/84/13
1
M/F: male/female. I/H: ischemic/haemorrhagic lesion; F: frontal; P: parietal; T: temporal; ic: internal capsule; ec: external capsule; Bg: basal ganglia; t: thal amus; na, not available for mapping. Neurological examination: M/SS/V, motor/somatosensory/visual half-field deficit contralateral to the damaged hemisphere; ext: extinction to double simultaneous stimulation (for visual and somatosensory deficit). þ: deficit; -: no deficit.
participants committed a maximum of one error, with the maximum difference between the number of omission errors in the two sides of the sheet being one target.
(i) Line cancellation (Albert, 1973). Participants were required to cross out all of the 21 black lines (25 mm in length and 1 mm in width), printed on an A3 sheet, 11 in the left hand-side, and 10 in the right-hand-side of the sheet. Neurologically unimpaired
Fig. 1. Superimposition of the left-hemispheric lesions in 11 left brain-damaged Aþ patients (a) and in 12 left brain-damaged A-patients (b). MNI coordinates for the shown axial slices are given. The number of overlapping lesions is indicated by different colors, with coding increasing frequencies (from violet, n ¼ 1, to red, n ¼ 112). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) 3
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Neuropsychologia 137 (2020) 107287
(ii) Bell cancellation (Gauthier et al., 1989). Patients were required to cross out all the ‘bell’ targets (18 targets printed on the left-hand side, and 17 on the right-hand side of the sheet). Neurologically unimpaired participants made a mean of 0.47 (1.3%, SD � 0.83, range 0–4) omission errors out of 35 targets. The maximum dif ference between omissions on the two sides of the sheet was four targets (Vallar et al., 1994). (iii) Line bisection. Patients were required to mark with a pencil the midpoint of six horizontal black lines (two 100 mm, two 150 mm, and two 250 mm in length, all 2 mm in width), presented in a random-fixed order. Each line was printed in the center of an A4 sheet, aligned with the mid-sagittal plane of the participant’s body. The length of the left-hand side of the line (i.e., from the left end of the line to the participant’s mark) was measured to the nearest mm. This measure was converted into a standardized score (percentage deviation), namely: measured left half minus objective half/objective half *100. This transformation yields positive numbers for marks placed to the right of the physical center, negative numbers for marks placed to the left of it. The mean percentage deviation score of 65 neurologically unim paired participants, matched for age (M ¼ 72.2, SD � 5.16, range 65–83) and years of education (M ¼ 9.5, SD � 4.48, range 5–18) was 1.21% (SD � 3.48, range 16.2%-þ6.2%) (Fortis et al., 2010). (iv) Complex Figure Drawing (Gainotti et al., 1972). Participants were required to copy a complex five-element figure: from left to right, two trees, a house, and two pine trees. The scoring procedure of Ronchi et al. (2009), adapted for the assessment of right USN, was used. A score was assigned in a range of 0–5: 0 for a flawless copy; 0.5 for each partial right-sided omission of one component (e.g., the right-hand-side of a tree); 1 for each complete omission of one component. The horizontal ground line was not considered for scoring.
baseline assessment for aphasia and USN, respectively. The Aþ group showed a moderate-to-severe impairment in all administered linguistic tests, thus exhibiting a damage involving the sub-lexical conversion processes, the lexical-semantic and grammatical systems. Concerning visuo-spatial evaluation, one Aþ patient and two A- patients exhibited signs of slight right USN. 2.2. Stimuli and procedures All participants were asked to set the subjective mid-point of different types of sentences, letter strings and lines, using the left hand. The stimuli of Veronelli et al. (2014a), that include different types of sentences, differing in their syntactic structure, were used. The 240 stimuli, divided into six groups of 40 stimuli each (see Veronelli et al., 2014a) included: (i) Forty declarative sentences with a full stop at the end, e.g.: “La mamma smarrisce il portafoglio.” (“The mother loses the wallet”). (ii) The same 40 sentences of (i), in the interrogative form (Yes/No interrogative sentences), e.g.: “La mamma smarrisce il portafo glio?” (‘Does the mother lose the wallet?‘) (iii) Forty non-syntactic sentences, namely words in scrambled order, with half of the stimuli taken from the declarative sentences and half from the Yes/No interrogative ones. Word order in each sentence was randomized, with each element (subject, object, verb) occupying each sentential position (initial, central, final) with the same frequency. Furthermore, articles were separated from the accompanying nouns [e.g., declarative: “La mamma smarrisce il portafoglio.” (“the mother loses the wallet.”); nonsyntactic: “Portafoglio il mamma smarrisce la.” (“Wallet the mother loses the.“)]. (iv) Forty non-lexical sentences; stimuli were generated by substitut ing letters in each word (in the left and in the right part of each word, minimum 2 letters, maximum all but 2 letters), without
Tables 2 and 3 show, for Aþ and A- patients, the results of the Table 2 Baseline assessment for aphasia. Number of errors are displayed. Sub-lexical conversion procedures
Lexical-semantic system
Non-word reading aloud
Non-word delayed copy
Visual lexical decision
Word reading aloud
Visual noun comprehension
Grammatical competence Visual grammatical judgments
Sentence reading aloud
Visual sentence comprehension
6/6a 6/6a 6/6a 1/6 ne 6/6a ne 5/6a 6/6a 6/6a 1/6 2/6a
21/80a ne 35/80a 35/80a 36/80a 40/80a 5/80a 11/80a 37/80a 13/80a 30/80a 16/80a
92/92a 47/92a 92/92a 26/92a 75/92a 89/92a 7/92a 92/92a 92/92a 4/92a 39/92a 92/92a
6/40a 12/40a 14/40a 0/40 10/40a 17/40a 6/40a 18/40a 11/40a 7/40a 5/40a 1/40
12/24a ne 12/24a 8/24a 13/24a 10/24a 6/24a 11/24a 12/24a 8/24a 10/24a 12/24a
6/6a 6/6a 6/6a 3/6a 6/6a 6/6a 2/6a 6/6a 6/6a 1/6a 4/6a 6/6a
17/45a 21/45a 20/45a 20/45a 19/45a 19/45a 8/45a 18/45a 22/45a 19/45a 16/45a 14/45a
0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 2/6a 2/6a 0/6
0/80 1/80 10/80a 2/80 2/80 0/80 1/80 0/80 1/80 17/80a 14/80a 0/80
0/92 0/92 1/92 0/92 0/92 0/92 0/92 0/92 3/92a 3/92a 2/92 2/92
3/40a 0/40 1/40 2/40a 0/40 1/40 0/40 0/40 1/40 1/40 2/40a 0/40
0/24 0/24 2/24 03/24a 0/24 1/24 1/24 0/24 5/24a 10/24a 4/24a 1/24
0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6
6/45a 2/45 15/45a 4/45a 0/45 1/45 2/45 1/45 4/45a 3/45a 12/45a 2/45
A þ patients CL CA GV AS SMC TF GB MR GA AS TCS CG
45/45a 31/45a 45/45a 15/45a 41/45a 44/45a 7/45a 45/45a 45/45a 3/45a 33/45a 45/45a
A- patients MA RA GE MC GE PS MR GF BR CF SN NG a
0/45 0/45 0/45 3/45a 0/45 0/45 0/45 0/45 0/45 5/45a 5/45a 1/45
Defective performance, as compared with normative data. ne, not evaluable. 4
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half vowel strings, e.g.: “Vbd fgnmrptc spdnnrdfg cv ngtrsddfrt.” or “Aoi auoi eooiuaie i aeuoieiae.” (vi) Forty lines of comparable length.
Table 3 Baseline assessment for right visual USN. Cancellation tasks: number of omis sions in the left/right (L/R) hand-side of the display. Line bisection: percent deviation (-/þleftward/rightward deviation); Complex figure drawing: 0/5 in dicates errorless performance. Line Cancellation
Bell Cancellation
Line bisection
L
R
L
R
0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10
0/17
0/17
0.81%
0/5
0/17
0/17
6.07%
0/5
Each stimulus was printed in lowercase, 26-pt, Arial font on an A4 sheet. Mean lengths for each condition were: (i and vi) M ¼ 117.9 mm (SD � 18.0, range 87.0–158.5); (ii) M ¼ 111.3 mm (SD � 18, range 80.0–151.5); (iii) M ¼ 116.9 mm (SD � 14.9, range 85.0–140.0); (iv) M ¼ 114.2 mm (SD � 20.1, 69.0–155.0); (v) M ¼ 116.2 mm (SD � 12.4, range 90.0–148.5). Stimuli sets were presented in a randomized order to each participant, following a latin square design for the four types of sentences, and randomizing the resulting three stimuli sets (sentences, letter strings, lines) with all possible permutations. Stimuli were pre sented in the center of a horizontal A4 sheet, each page containing four items, aligned with the mid-sagittal plane of the participant’s body at a viewing distance of 40 cm. A moveable window was used in order to present each stimulus one at a time. Patients were individually tested in a quiet room, with the experimenter sitting in front of them. They were required to bisect each sentence, string or line, marking the mid-point with a soft pen using the left-hand, ipsilateral to the left hemispheric lesion, and not affected by the neurological damage. Participants were informed that the vertical mark could be made in any point of the stimulus, irrespective of whether the center might fall between two words, two letters, or go through a letter. No time limits were set, and no feedback was given as to the accuracy of the response. The distance between the left end of each stimulus and the participant’s mark was measured to the nearest mm. Each measure in mm was converted into a standardized score (measured left half minus objective half/objective half *100), in order to equate the participants’ error with respect to stimulus length. This percent deviation from the objective midpoint of the stimulus yielded positive values for rightward deviations, negative values for leftward deviations (Rode et al., 2006).
Complex figure drawing
Aþ patients CL CA GV AS SMC TF GB MR GA AS TCS CG
0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11
a
0.5/5a
2/ 17a 3/17
7/ 17a 7/17
5/17
3/17
1.24%
0/5
0/17
2/17
1.13%
0/5
2/17
3/17
2.52%
0/5
0/17
0/17
2.24%
0/5
2/17
2/17
1.16%
0/5
3/17
3/17
1.03%
0/5
2/17
3/17
3%
0/5
1/17
0/17
1.84%
0/5
2/17
0/17
1.32%
0/5
8/17
8/17
2.40%
0/5
0/17
0/17
4.42%
0/5
0/17
0/17
8.34%a
0/5
1/17
1/17
0.43%
0/5
0/17
0/17
2.94%
0/5
1/17
0/17
3.43%
0/5
0/17
0/17
0.70%
0/5
0/17
0/17
10.80%a
0/5
0/17
0/17
1.21%
0/5
4/17
3/17
3.50%
0/5
0/17
0/17
3.05%
0/5
9.88% 4.78%
0/5
A- patients MA RA GE MC GE PS MR GF BR CF SN NG
0/ 11 0/ 11 1/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11
0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10
2.3. Statistical analyses Data were analysed using non-parametric Friedman ANOVAs for each group of participants and comparing different types of stimulus (declarative sentences, yes/no interrogative sentences, sentences with syntactic and lexical violations, letter strings, lines), because the assumption of the homogeneity of variances across groups (Levene, 1960) – in this study, left brain-damaged patients, Aþ and A-, C par ticipants- for a repeated-measures ANOVA was violated for letter strings (p < 0.001). Level of significance was set at p < 0.05. Post-hoc multiple comparisons were performed using Wilcoxon pairwise tests, with Bonferroni-adjusted level of significance p < 0.003, when appropriate. Each average standardized score was compared to the objective midline of the stimulus through one-sample t-tests against zero. Pearson’s cor relations, with Bonferroni correction for multiple comparisons (p < 0.003), were used in order to measure the association between bisection errors for the different types of stimuli in the three groups. Furthermore, differences between the bisection biases for letter strings and linguistic stimuli (affirmative, interrogative and non-lexical sentences) were compared: (i) among left brain-damaged-patients (LBD; Aþ and A-) and C participants, using a Mann-Whitney test, and (ii) among LBD and right brain-damaged patients with left USN (RBD, as described in the study by Veronelli et al., 2014a), using an independent-samples t-test.
a
Defective performance, as compared with normative data, indicating right USN.
changing the order of the original words in the sentence. Spe cifically, articles, gender/number agreement, consonant clusters and double consonants were maintained, as well as verb endings/ suffixes and noun suffixes, with changes being confined to the root [e.g.: “La cabba sterrisce il costapoglio.” (“the loster sares the pibbet.“)]. (v) Forty unreadable letter strings, generated in order to mimic the visuo-perceptual structure of a sentence in terms of spaces be tween letters and the full stop. The presence of double letters was also maintained; half of the stimuli were consonant strings, and
3. Results As shown in Fig. 2, all participants made a leftward error in bisection. In the C group, the Friedman ANOVA for stimulus type was significant (χ25 ¼ 23.91, p < 0.001, Kendall’s W ¼ 0.20). Post-hoc multiple com parisons revealed that letter strings (Mdn ¼ 1.78) were bisected more accurately, more rightward, than declarative sentences (Mdn ¼ 4.48, p < 0.003, η2 ¼ 0.37), Yes/No interrogative sentences (Mdn ¼ 6.03, p < 5
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bisection for non-syntactic sentences (M ¼ 2.22%, t11 ¼ 1.98, p ¼ 0 0.07, η2 ¼ 0.07), and lines (M ¼ 2.31%, t11 ¼ 1.78, p ¼ 0.10, η2 ¼ 0.06). In the C group, Bonferroni-corrected (p ¼ 0.003) Pearson’s correla tions performed on bisection deviations were significant between all types of stimuli (declarative and Yes-No interrogative, r ¼ 0.79, p < 0.001; declarative and non-lexical, r ¼ 0.80, p < 0.001; declarative and non-syntactic, r ¼ 0.77, p < 0.001; declarative and letter strings, r ¼ 0.83, p < 0.001; Yes-No interrogative and non-lexical, r ¼ 0.79, p < 0.001; Yes-No interrogative and non-syntactic, r ¼ 0.86, p < 0.001; YesNo interrogative and letter strings, r ¼ 0.81, p < 0.001; non-lexical and non-syntactic, r ¼ 0.82, p < 0.001; non-lexical and letter strings, r ¼ 0.83, p < 0.001; non-lexical and lines, r ¼ 0.66, p ¼ 0.001; non-syntactic and letter strings r ¼ 0.80, p < 0.001; letter strings and lines r ¼ 0.59, p ¼ 0.002), except between lines and declarative sentences (r ¼ 0.569, p ¼ 0.004, n.s.), lines and Yes-No interrogative sentences (r ¼ 0.47, p ¼ 0.02, n.s.) and lines and non-syntactic sentences (r ¼ 0.530, p ¼ 0.01, n. s.). In the A- group, significant correlations were found between the four types of linguistic stimuli: declarative and Yes-No interrogative (r ¼ 0.89, p < 0.001), declarative and non-lexical (r ¼ 0.89, p < 0.001), declarative and non-syntactic (r ¼ 0.80, p ¼ 0.002), Yes-No interrogative and non-lexical (r ¼ 0.97, p < 0.001), Yes-No interrogative and nonsyntactic (r ¼ 0.93, p < 0.001) and between non-lexical and nonsyntactic stimuli (r ¼ 0.89, p < 0.001). No significant correlations were found between letter strings and all the other types of linguistic stimuli, between lines and all the other types of linguistic stimuli, and between letter strings and lines (p > 0.003, in all cases, n.s.). In the Aþ group, correlations were significant between declarative and Yes-No interrogative sentences (r ¼ 0.81, p ¼ 0.001), declarative and nonlexical sentences (r ¼ 0.84, p ¼ 0.001), Yes-no interrogative and nonlexical sentences (r ¼ 0.89, p < 0.001) and between letter strings and lines (r ¼ 0.80, p ¼ 0.002). No other significant correlations were found (p > 0.003, in all cases). A Mann-Whitney test indicated that the difference between the average bisection deviations for letter strings and linguistic stimuli (affirmative, interrogative and non-semantic sentences) was larger for the C group (Mdn ¼ 2.08) than for the group of left brain-damagedpatients (Aþ and A-) (Mdn ¼ 0.47, U ¼ 190.5, p ¼ 0.04, η2 ¼ 0.084) (see Fig. 3A). The t-test performed in LBD and RBD patients (data from Veronelli et al., 2014a) on the difference between the average deviations for letter strings and linguistic stimuli revealed a significantly larger difference in RBD than in LBD patients (t28 ¼ 3.00; p ¼ 0.006, η2 ¼ 0.32; M ¼ 9.88%, M ¼ 0.13%, respectively), as shown in Fig. 3B. Summing up, healthy participants show larger leftward biases in the bisection of orthographic readable sentences, compared to unreadable letter strings. On the contrary, patients with and without aphasia set the mid-point of all types of stimuli to the left of the physical center, without a difference between readable and unreadable material.
Fig. 2. Median percent deviation error (upper and lower quartiles, maximum and minimum values) by participants’ group (Aþ/A-left brain-damaged pa tients and C participants), and by type of stimulus (declarative sentences, Yes/ No interrogative sentences, non-syntactic sentences, non-lexical sentences, letter strings, lines). � mild outliers.
0.001, η2 ¼ 0.55), and non-lexical sentences (Mdn ¼ 4.68, p < 0.002, η2 ¼ 0.42). On the other hand, the difference between letter strings (Mdn ¼ 1.78) and non-syntactic sentences (Mdn ¼ 3.79) was not significant after Bonferroni correction (p ¼ 0.013, η2 ¼ 0.26, n.s., with the level of significance after the correction being p < 0.003). No other significant differences were found after Bonferroni correction (p < 0.003, for all the comparisons). In both the Aþ and A- groups, the Friedman ANOVAs for the type of stimulus were not significant (Aþ: χ25 ¼ 6.14, p ¼ 0.29, W ¼ 0.10; A-: χ25 ¼ 5.87, p ¼ 0.32, W ¼ 0.10). In the C groups, all bisection scores differed significantly from ac curate bisection: declarative sentences, M ¼ 4.43%, t23 ¼ 4.81, p < 0.001, η2 ¼ 0.19; Yes/No interrogative sentences, M ¼ 5.48%, t23 ¼ 6.01, p < 0.001, η2 ¼ 0.27; non-syntactic sentences, M ¼ 4.45%, t23 ¼ 4.59, p < 0.001, η2 ¼ 0.18; non-lexical sentences, M ¼ 4.76%, t23 ¼ 4.89; p < 0.001, η2 ¼ 0.20; letter strings, M ¼ 2.77%, t23 ¼ 3.73, p ¼ 0.001, η2 ¼ 0.13; lines, M ¼ 2.84%, t23 ¼ 3.08, p ¼ 0.005, η2 ¼ 0.09. Aþ participants exhibited significantly leftward deviations from accurate bisection with Yes/No interrogative sentences (M ¼ 4.94%, t11 ¼ 3.65, p ¼ 0.004, η2 ¼ 0.22), non-syntactic sentences (M ¼ 5.25%, t11 ¼ 4.67, p ¼ 0.001, η2 ¼ 0.31), non-lexical sentences (M ¼ 5.21%, t1 ¼ 3.65; p ¼ 0.004, η2 ¼ 0.22), and lines (M ¼ 4.22%, t11 ¼ 2.55, p ¼ 0.03, η2 ¼ 0.12). The leftward directional bias did not differ from accurate bisection for declarative sentences (M ¼ 3.22%, t11 ¼ 1.68, p ¼ 0.12, η2 ¼ 0.05), and letter strings (M ¼ 4.67%, t11 ¼ 1.61, p ¼ 0.14, η2 ¼ 0.05). In the A- group bisection performances significantly differed from accurate bisection, with a leftward deviation for declarative sentences (M ¼ 3.55%, t11 ¼ 3.38, p ¼ 0.006, η2 ¼ 0.19), Yes/No interrogative sentences (M ¼ 3.78%, t11 ¼ 3.02, p ¼ 0.012, η2 ¼ 0.16), non-lexical sentences (M ¼ 3.99%, t11 ¼ 3.70, p ¼ 0.003, η2 ¼ 0.22), and letter strings (M ¼ 3.30%, t11 ¼ 3.13, p ¼ 0.01, η2 ¼ 0.17). The leftward directional bias did not differ from accurate
4. Discussion This study investigated whether the presence of an acquired lin guistic impairment (aphasia of various types and degrees) could modulate the patients’ estimation of the lateral extent of linguistic material presented visually, as assessed by a task requiring the manual bisection of orthographic strings. The evidence reviewed in the introduction indicates that the leftward bias in the bisection of both single words and sentences may be driven not only by asymmetries in the orientation of spatial attention, related to hemispheric differences and specifically, to a major role of the right hemisphere (see a recent review and discussion in Bartolomeo and Seidel Malkinson, 2019), but may be also dependent on language pro cessing (Fischer, 2000, 2004, 1996; Veronelli et al., 2014a). Based on this evidence, the prediction was made that patients with a linguistic disorder could show a less marked leftward bias when bisecting readable 6
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assessed by tasks that directly and explicitly probe these performances. Conversely, the processing of linguistic material in bisection tasks is not directly and explicitly assessed by the task of setting the mid-point of a string. In non-aphasic patients, ortho-phonological conversion abilities (as assessed through pseudoword reading aloud, see Table 2) are spared. Nevertheless, these patients do not exhibit any differences in bisecting readable and unreadable (other than by letter-by-letter reading) mate rial. This indicates that intact reading abilities are not sufficient for, or do not provide an adequate support to, the language-related effect of a larger leftward bias in the bisection of readable vs. unreadable material. This effect can be altered in the presence of a left brain-lesion, even in absence of apparent aphasia. While including orthographic stimuli, sentence bisection is per se a length estimation task, where linguistic processing is not directly required. Notwithstanding, also the perfor mances of control participants indicate that orthographic processing, although not explicitly required by the task, takes place, as shown by the different bisection biases in the case of readable vs. unreadable senten ces. In sum, as a consequence of left hemispheric brain damage, the language-related implicit processes that modulate the setting of the subjective mid-point in sentence bisection, may be less effective. The possibility that the lack of significant differences between sentential and letter string material within Aþ and A- left brain-damaged patients might just reflect random variability of performance is countered by the finding that the patients’ bisection is overall significantly deviated leftward, as compared to the objective center of the stimulus to be bisected, as in control participants, with most of the stimuli. Particu larly, control participants show significant leftward biases with all types of stimuli, Aþ patients with all stimuli, but declarative sentences and letter strings, A– patients with all stimuli, but non-syntactic sentences and lines. Also the presence of significant correlations between bisection biases for linguistic stimuli in all groups argues against interpretations of the patients’ performances in terms of random variability. Eye tracking studies suggest that aphasic patients do not construct an online mental representation of the sentence with the same time course as control participants. Effects of structural complexity emerge on the first pass through the sentence for controls, but only in rereading times for patients (DeDe, 2017; Knilans and DeDe, 2015). While the sentence reading and bisection tasks definitely differ in important respects, a shared finding concerns abnormalities in the linguistic processing of sentences. In conclusion, in the visuo-spatial task of bisecting sentences neurologically unimpaired participants show a language-related effect, bisecting readable sentences more leftward than unreadable ones. This effect, even in the absence of apparent aphasia, is disrupted by left hemispheric lesions, which alter the processes, likely linguistic in na ture, that modulate sentence bisection.
Fig. 3. A) Median difference of percent deviation errors (upper and lower quartiles, maximum and minimum values) between letter strings and linguistic stimuli in LBD patients and C participants. B) Mean difference of percent de viation errors (�SE) in RBD (data from Veronelli et al., 2014a) and LBD pa tients. � mild outliers; * extreme outliers.
sentences, as compared to unreadable ones. Patients and neurologically unimpaired participants were required to bisect different types of stimuli (declarative sentences, Yes/No interrogative sentences, non-syntactic sentences, non-lexical sentences, unreadable letter strings and lines). Healthy participants exhibited a leftward deviation with all stimuli, namely different types of sentences, letter strings and lines, showing larger leftward biases with orthographic readable sentences, as compared to unreadable letter strings. These findings confirm previous evidence (Fischer, 1996; Veronelli et al., 2014a) that the presence of readable material may induce a more pro nounced leftward shift of attention, possibly through an activation of left hemisphere-based linguistic processes, that orient more leftward, to ward the beginning of the to-be-bisected letter string, readable in Italian from left to right (see Chokron et al., 1998; Chokron and Imbert, 1993). Furthermore, the leftward biases in bisection for lines and words, that mark the performance of neurologically unimpaired adults, develop with different directional patterns between three and eight years of age, suggesting that different factors, including visuo-spatial attention and linguistic processes, may be involved (Girelli et al., 2017). In the present study, left-brain-damaged patients, both with and without aphasia, do not show the significant difference between read able and unreadable material found both in neurologically unimpaired participants and in right-brain damaged patients (Veronelli et al., 2014a). The lack of significant differences in the biases for the different types of readable stimuli in both aphasic and not aphasic left-brain-damaged patients contrasts with the larger leftward biases found in control participants and in right-brain damaged patients with left USN. These findings suggest that left brain damage may impair the linguistic processes involved in the bisection of sentential material, in dependent of the presence of a clinically apparent aphasic deficit. The linguistic processing (and its impairments) that features speech pro duction and comprehension (and aphasia) is explicit in nature, and
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Neuropsychologia journal homepage: http://www.elsevier.com/locate/neuropsychologia
Setting the midpoint of sentences: The role of the left hemisphere Laura Veronelli a, *, Lisa S. Arduino b, c, Verena Biscaro d, Massimo Corbo a, Giuseppe Vallar d, e a
Department of Neurorehabilitation Sciences, Casa di Cura del Policlinico, Milan, Italy Department of Human Sciences, LUMSA University, Rome, Italy c ISTC-CNR, Rome, Italy d Department of Psychology, University of Milano-Bicocca, Milan, Italy e Neuropsychological Laboratory, IRCCS Istituto Auxologico Italiano, Milan, Italy b
A R T I C L E I N F O
A B S T R A C T
Keywords: Unilateral spatial neglect Aphasia Sentence bisection Word bisection Line bisection Reading habits
The human brain has a remarkable capacity to focus processing resources based on the features and the relevance of the task at hand. The two cerebral hemispheres contribute differentially to this capacity, with the left hemisphere linguistic and right hemisphere visuo-spatial abilities each offering unique contributions. For example, previous research has established that healthy participants set the subjective mid-point of written sentences more leftwards of center, compared to unpronounceable letter strings or simple lines. Remarkably, patients with right hemisphere damage exhibiting unilateral spatial neglect also show this pattern, even though, as well known in the literature, they tend toward a rightward- bias for non-linguistic stimuli. This evidence suggests that the leftward bias for sentential material is due to linguistic, mainly left-hemisphere mediated processes, which are largely unimpaired in right brain-damaged patients, and intact in heathy participants. To test this hypothesis, we compared sentence bisection performance to that of letter strings and simple lines in left brain-damaged patients (with and without aphasia). If the larger leftward bias in the bisection of sentential material is based on linguistic processes, then the left brain-damaged patients should show a reduction or absence of a leftward bias in sentence bisection. We tested twenty-four left brain-damaged patients (12 with aphasia and 12 without aphasia), and 24 age-matched elderly participants (patients and controls were all righthanded). Participants were asked to bisect 240 stimuli, comprising: (i) affirmative and interrogative clauses, (ii) sentences with lexical and syntactic violations, (iii) letter strings and (iv) simple lines. As predicted, neurolog ically intact participants showed larger leftward biases in bisecting written readable sentences compared to strings of letters. In contrast, the left hemispheredamaged patients (both with and without aphasia) showed no differences in bisecting sentences and letter strings or lines. These findings indicate that the larger leftward bias exhibited by healthy participants in the bisection of sentences is likely due to ortho-phonological coding taking place implicitly during the bisection task. This ortho-phonological coding is impaired with left brain damage – also in absence of apparent aphasia – leading to the left hemispheredamaged patients showing a reduced leftward bias in sentence bisection. These findings support the hypothesis that the leftward bias in the bisection of written sentences is the result of ortho-phonological influences rather than visual-spatial biases.
1. Introduction Line bisection (Schenkenberg et al., 1980) is a clinical test for the detection of unilateral spatial neglect (USN). When required to set the midpoint of a horizontal segment, right brain-damaged patients with left USN may transect the line to the right of the objective midpoint of the stimulus (Bisiach et al., 1976; Heilman et al., 1983; Vallar et al., 2000). On the other hand, left brain-damaged patients can exhibit a dispro portionate leftward bias, interpreted as an indicator of right USN (Beis
et al., 2004; Kleinman et al., 2007; Sallard et al., 2012; Zilli and Heil man, 2016), although right USN after left brain damage is overall comparatively less frequent (Beume et al., 2017; Buxbaum et al., 2004), or severe (Ogden, 1985) than after right brain damage. A leftward bias (pseudoneglect), although smaller in size, has been found also in healthy participants, interpreted as due to a leftward orientation in a visuo-spatial task, supported by activity of the right hemisphere, and affected by a number of factors, including age, and scanning direction in reading (Bowers and Heilman, 1980; Jewell and McCourt, 2000, for
* Corresponding author. Department of Neurorehabilitation Sciences, Casa di Cura del Policlinico, via Dezza 48, 20144 Milan, Italy. E-mail address: [email protected] (L. Veronelli). https://doi.org/10.1016/j.neuropsychologia.2019.107287 Received 26 April 2018; Received in revised form 21 November 2019; Accepted 28 November 2019 Available online 19 December 2019 0028-3932/© 2019 Elsevier Ltd. All rights reserved.
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review; Rinaldi et al., 2014). The relationship between spatial and linguistic (orthographic) pro cessing has been studied through tasks that require the bisection of words and sentences (Arduino et al., 2016, 2010; Fischer, 2000, 1996; Gabay et al., 2015; Veronelli et al., 2014a, 2014b; Fischer, 2004; Arduino et al., 2016; Veronelli et al., 2017). Neurologically unimpaired participants show pseudoneglect, namely a larger leftward bias, when bisecting words and pseudowords (i.e., legal non-words), but not letter strings (Fischer, 1996). This finding indicates an overestimation of the spatial extent of word beginnings, compared to letter strings, related to lexical access (Fischer, 2000, 2004, 1996; Gabay et al., 2015), which is necessary for establishing a cohort of potential entries in the mental lexicon (Paap et al., 1982). One study in neurologically unimpaired participants found a leftward bias for all types of discrete stimuli (whether they be Italian words, pseudowords, letter or symbol strings), as well as for continuous lines, with the only exception of short ortho graphic stimuli, which were bisected rightwards (Arduino et al., 2010). These findings indicate that a number of different processes may influ ence the bisection of a stimulus, including its lexical status, and its continuous vs. discrete perceptual structure (see also Girelli et al., 2017). The role of ortho-phonological information in modulating directional biases in stimulus bisection has been demonstrated in different lan guages. In Italian, a language with a shallow orthography (Ellis et al., 2004; Toraldo et al., 2006), words stressed on the penultimate syllable induce a larger rightward bias, compared to words stressed on the antepenultimate syllable in both USN patients and healthy participants (Veronelli et al., 2014b). In German, a language with a quite transparent orthography (Frith et al., 1998), participants perceive the midpoint of the string to be closer toward the side with more phonemes (Fischer, 2004), showing a grapheme-phoneme convergence effect on the perceived word centre (although only for the trigram SCH). Concerning lexical features, English and Hebrew readers show a written word fre quency effect, with larger leftward biases in the bisection of lower, as compared with higher frequency words (Gabay et al., 2015). In the last few decades, many studies on line bisection have shown that the magnitude of both pseudoneglect in healthy participants (Jewell and McCourt, 2000, for review) and of the rightward bias in patients with left USN (Bisiach et al., 1983; Halligan and Marshall, 1989; Vallar et al., 2000) is influenced by stimulus length, typically with a greater error with longer lines. Accordingly, sentences, which are longer in extent than words, may induce larger deviation biases, and help uncoupling spatial and linguistic factors. Veronelli and coworkers (2014a) have recently investigated the interaction between written language and spatial cognition using a sentence bisection task. Right brain-damaged patients with left USN and neurologically unimpaired participants were asked to set the subjective mid-point of declarative and interrogative sentences, of sentences with lexical and syntactic vi olations, of letter strings, and of lines. USN patients showed an overall rightward error, larger than the one exhibited by control participants, and affected by stimulus type, with larger rightward deviations with lines, moderate deviations with letter strings, and slight deviations with sentences. Letter strings and sentences were therefore bisected more leftward compared to lines. The smaller rightward deviation shown by USN patients with readable sentences might be indicative of a less asymmetrical spatial exploration, mediated by the linguistic features of the stimuli, and is in line with the left-to-right Italian reading habits (Chokron and Imbert, 1993; Girelli et al., 2017). The readability of the stimulus may be a factor to explain the ortho-phonological effect found in sentence bisection, with a reduction of the rightward deviation for sentential material compared to letter strings and lines in USN patients, and a leftward bias for control participants (see Veronelli et al., 2014a, for details). The aim of this study was to investigate the nature of this directional modulation during the bisection of orthographic material in a group of left brain-damaged patients with and without aphasia and dyslexia. Participants were asked to manually bisect different types of sentences,
namely: declarative, Yes/No interrogative, sentences with syntactic and with lexical violations, and, as control materials, letter strings and lines. Left brain-damaged patients underwent a baseline linguistic assessment of the status of the semantic-lexical system, of sub-lexical conversion functioning, and of grammatical competencies. We hypothesized that the presence of aphasic deficits might interfere with the putative lin guistic sentence processing during a length estimation task. Such lin guistic processing would affect the bisection performance in an implicit way, because the bisection task does not require an overt verbal pro cessing or response. We expected that patients with aphasia and dyslexia, differently from controls, would not show a difference in bisecting readable and unreadable material, or would exhibit a specific bisection pattern more in accordance with the linguistic impairment they have. Specifically, the evidence above suggests, for sentential ma terial, a leftward bias in neurologically unimpaired participants and a comparatively minor rightward error in USN patients, related to the linguistic features of the stimulus. In the light of these findings, we predicted that left brain damage could diminish or abolish such bias, particularly in patients with aphasia. This prediction implies that the most crucial differences are to be found comparing the bisection of sentential material vs. other types of stimuli, such as letter strings and lines, in patients and in control participants, rather than comparing different groups. The use of a variety of sentential material (declarative, interrogative sentences, non-syntactic and non-lexical sentence-like strings), and of letter strings, as in the study by Veronelli et al. (2014a), would allow to assess more specifically the effects of damage to the left hemisphere, which may impair language, on specific types of linguistic stimuli, in bisection tasks. Studies using tracking of eye movements suggest that patients with aphasia, as controls participants, are sensitive to both the structural frequency and the complexity of sentences in reading tasks, although patients may use different reading strategies (DeDe, 2017; Knilans and DeDe, 2015). To the best of our knowledge, this study is the first to investigate the performance of left brain-damaged patients in a sentence bisection task. 2. Material and methods 2.1. Participants Participants were recruited from the inpatient population of the Department of Neurorehabilitation Sciences of the Casa di Cura del Policlinico, Milan, Italy. A total of 24 left brain-damaged patients, and 24 age-matched participants (C) entered the study. Left hemispheredamaged patients had suffered a first-ever cerebrovascular stroke (20 ischemic, three haemorrhagic and one ischemic with haemorrhagic infarction). Patients were divided into two groups, according to their performance in a verbal comprehension task: patients with aphasia (Aþ), with a score � 22/50 (moderate impairment in auditory-verbal comprehension) at the Token Test (Luzzatti et al., 1994), and patients without aphasia (A-), with a score < 22/50. The Aþ group included 12 patients, six females, with a mean age of 70.75 years (SD � 9.20; range 55–83), and mean education of 9.92 years (SD � 3.63; range 5–17). Following a clinical evaluation and the administration of the Aachen Aphasia Test (Luzzatti et al., 1996), patients were classified as follows: five patients suffered from Broca’s aphasia (two with apraxia of speech), three from global aphasia, two from Wernicke aphasia, and one from anomic aphasia; one patient did not meet the criteria for any of the above-mentioned subtypes. The A- group included 12 patients, 9 females with a mean age of 72.58 years (SD � 13.79; range 60–85), and mean education of 11.67 years (SD � 3.75; range 5–17). The study also included twenty-four C participants (12 females), who were matched for age (M ¼ 72.58 years, SD � 9.36, range 65–85) and educational level (M ¼ 11.29 years, SD � 4.67, range 5–17) to the patients. One-way analyses of variance (ANOVAs) showed that age (F2,47 ¼ 0.13; p ¼ 0.87, η2 ¼ 0.01) and educational level (F2,47 ¼ 0.60; p ¼ 0.55, η2 ¼ 0.03) did not differ among groups (Aþ, A- and C). Lesion site was assessed for each left 2
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brain-damaged patient by CT or MRI scan, and drawn manually by VB, supervised by LV, using the MRIcro software (Rorden and Brett, 2000), onto selected horizontal slices of a standard template brain. Scan images were not available for Aþ patient CL; medical records reported ischemic lesions in the left fronto-parietal areas. Overlapped lesion maps of 23 left-brain-damaged patients, subdivided in Aþ and A-groups are shown in Fig. 1. In Aþ patients lesions superimposed in the left insula, and in the temporal and frontal lobes (7 patients); in A- patients lesions super imposed in the left internal capsule and in the left insula (10 patients). Lesions were more extensive in Aþ (M ¼ 64.93 cm3, SD ¼ �51.91) than in A- (M ¼ 8.32 cm3, SD ¼ �7.69; t10 ¼ 3.58, p ¼ 0.005, η2 ¼ 0.38), and involved cortico-subcortical networks. In the A- group, lesions were limited to subcortical regions. Patients were right-handed, had normal or corrected-to-normal vision, and no history of previous neurological diseases or psychiatric disorders. Demographic and neurological infor mation of the Aþ and A- groups are shown in Table 1. The project was approved by the local Ethical Committee and informed consent was obtained from all participants, according with the Declaration of Helsinki (British Medical Journal, 302: 1194, 1991). 2.2. Baseline neuropsychological assessment. The presence and severity of aphasia were further assessed by a diagnostic battery, which included the following subtests of the Batteria per l’Analisi dei Deficit Afasici (BADA) (Miceli et al., 1994):
Table 1 Demographic and neurological data of 24 left brain-damaged patients (12 A þ and 12 A-). Sex/Age/ Education
Duration of disease (months)
Etiology/ Lesion site
Lesion volume (cc)
Neurological examination V
SS
M
I F/P I T/Bg/t/ ic/ec H F/P/T/ Bg/ic/ec IT I F/T/Bg I F/T/P/ ic/ec I T/t/Bg I/H F/T/ Bg I F/P/T H T/P/Bg I T/F/P I T/P
na 19.9
– –
ext þ
þ þ
83
ext
ext
þ
4.8 168.7 122.3
– – ext
– – þ
þ þ þ
8.1 77.8
– ext
– þ
þ þ
25.1 36 71 97.5
– – – –
– þ – –
þ þ þ þ
H T/t/Gb/ ic/ec I Bg I T/Bg/ic I F/P I T/Bg/ic I T/Bg/t/ ic I T/Bg/ic I T/t/Bg/ ic I T/t/Bg/ ic I T/t/Bg/ ic I T/t/Bg/ ic/ec I Bg/ic
22.6
–
–
þ
0.7 1.2 2.7 0.9 9.2
– – – – –
– – – – –
þ þ þ þ þ
8.4 1.9
– –
– –
þ þ
20.2
–
–
þ
9.5
–
ext
þ
16.2
–
–
þ
6.3
–
–
þ
Aþ patients CL CA
F/83/10 F/81/11
3 1
GV
F/69/5
4
AS SMC TF
F/67/13 F/60/9 M/69/8
1 49 2
GB MR
M/78/13 F/81/13
1 2
GA AS TCS CG
M/75/7 M/60/8 M/55/5 M/71/17
1 2 2 87
A- patients
(i) Pseudoword reading aloud (45 stimuli, from 1 to 3 syllables); pseudoword delayed copy (6 stimuli, from 1 to 3 syllables). These subtests evaluate sub-lexical conversion functioning; (ii) Visual lexical decision (80 stimuli, half pseudowords); word reading aloud (92 stimuli: 52 nouns, 20 verbs, 20 function words); visual noun comprehension (40 stimuli). These subtests evaluate lexical-semantic processing; (iii) Visual grammatical judgments (24 sentences); sentence reading aloud (6 stimuli); visual sentence comprehension (45 stimuli). These subtests evaluate grammatical competence. Neurologically unimpaired participants performed without errors the sentence reading aloud task, made no more than one error in the pseudoword delayed copy and visual noun comprehension tasks, and no more than two errors in the word and pseudoword reading aloud, visual lexical decision, visual grammatical judgments and visual sentence comprehension tasks (Miceli et al., 1994). The presence and severity of right USN were assessed by a diagnostic battery, which included the following tests:
MA
F/85/17
2
RA GE MC GE PS
F/84/9 F/85/13 M/76/12 F/60/8 F/71/17
96 1 1 1 1
MR GF
F/72/13 M/37/15
1 2
BR
F/66/8
1
CF
M/72/5
1
SN
F/79/10
1
NG
F/84/13
1
M/F: male/female. I/H: ischemic/haemorrhagic lesion; F: frontal; P: parietal; T: temporal; ic: internal capsule; ec: external capsule; Bg: basal ganglia; t: thal amus; na, not available for mapping. Neurological examination: M/SS/V, motor/somatosensory/visual half-field deficit contralateral to the damaged hemisphere; ext: extinction to double simultaneous stimulation (for visual and somatosensory deficit). þ: deficit; -: no deficit.
participants committed a maximum of one error, with the maximum difference between the number of omission errors in the two sides of the sheet being one target.
(i) Line cancellation (Albert, 1973). Participants were required to cross out all of the 21 black lines (25 mm in length and 1 mm in width), printed on an A3 sheet, 11 in the left hand-side, and 10 in the right-hand-side of the sheet. Neurologically unimpaired
Fig. 1. Superimposition of the left-hemispheric lesions in 11 left brain-damaged Aþ patients (a) and in 12 left brain-damaged A-patients (b). MNI coordinates for the shown axial slices are given. The number of overlapping lesions is indicated by different colors, with coding increasing frequencies (from violet, n ¼ 1, to red, n ¼ 112). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) 3
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(ii) Bell cancellation (Gauthier et al., 1989). Patients were required to cross out all the ‘bell’ targets (18 targets printed on the left-hand side, and 17 on the right-hand side of the sheet). Neurologically unimpaired participants made a mean of 0.47 (1.3%, SD � 0.83, range 0–4) omission errors out of 35 targets. The maximum dif ference between omissions on the two sides of the sheet was four targets (Vallar et al., 1994). (iii) Line bisection. Patients were required to mark with a pencil the midpoint of six horizontal black lines (two 100 mm, two 150 mm, and two 250 mm in length, all 2 mm in width), presented in a random-fixed order. Each line was printed in the center of an A4 sheet, aligned with the mid-sagittal plane of the participant’s body. The length of the left-hand side of the line (i.e., from the left end of the line to the participant’s mark) was measured to the nearest mm. This measure was converted into a standardized score (percentage deviation), namely: measured left half minus objective half/objective half *100. This transformation yields positive numbers for marks placed to the right of the physical center, negative numbers for marks placed to the left of it. The mean percentage deviation score of 65 neurologically unim paired participants, matched for age (M ¼ 72.2, SD � 5.16, range 65–83) and years of education (M ¼ 9.5, SD � 4.48, range 5–18) was 1.21% (SD � 3.48, range 16.2%-þ6.2%) (Fortis et al., 2010). (iv) Complex Figure Drawing (Gainotti et al., 1972). Participants were required to copy a complex five-element figure: from left to right, two trees, a house, and two pine trees. The scoring procedure of Ronchi et al. (2009), adapted for the assessment of right USN, was used. A score was assigned in a range of 0–5: 0 for a flawless copy; 0.5 for each partial right-sided omission of one component (e.g., the right-hand-side of a tree); 1 for each complete omission of one component. The horizontal ground line was not considered for scoring.
baseline assessment for aphasia and USN, respectively. The Aþ group showed a moderate-to-severe impairment in all administered linguistic tests, thus exhibiting a damage involving the sub-lexical conversion processes, the lexical-semantic and grammatical systems. Concerning visuo-spatial evaluation, one Aþ patient and two A- patients exhibited signs of slight right USN. 2.2. Stimuli and procedures All participants were asked to set the subjective mid-point of different types of sentences, letter strings and lines, using the left hand. The stimuli of Veronelli et al. (2014a), that include different types of sentences, differing in their syntactic structure, were used. The 240 stimuli, divided into six groups of 40 stimuli each (see Veronelli et al., 2014a) included: (i) Forty declarative sentences with a full stop at the end, e.g.: “La mamma smarrisce il portafoglio.” (“The mother loses the wallet”). (ii) The same 40 sentences of (i), in the interrogative form (Yes/No interrogative sentences), e.g.: “La mamma smarrisce il portafo glio?” (‘Does the mother lose the wallet?‘) (iii) Forty non-syntactic sentences, namely words in scrambled order, with half of the stimuli taken from the declarative sentences and half from the Yes/No interrogative ones. Word order in each sentence was randomized, with each element (subject, object, verb) occupying each sentential position (initial, central, final) with the same frequency. Furthermore, articles were separated from the accompanying nouns [e.g., declarative: “La mamma smarrisce il portafoglio.” (“the mother loses the wallet.”); nonsyntactic: “Portafoglio il mamma smarrisce la.” (“Wallet the mother loses the.“)]. (iv) Forty non-lexical sentences; stimuli were generated by substitut ing letters in each word (in the left and in the right part of each word, minimum 2 letters, maximum all but 2 letters), without
Tables 2 and 3 show, for Aþ and A- patients, the results of the Table 2 Baseline assessment for aphasia. Number of errors are displayed. Sub-lexical conversion procedures
Lexical-semantic system
Non-word reading aloud
Non-word delayed copy
Visual lexical decision
Word reading aloud
Visual noun comprehension
Grammatical competence Visual grammatical judgments
Sentence reading aloud
Visual sentence comprehension
6/6a 6/6a 6/6a 1/6 ne 6/6a ne 5/6a 6/6a 6/6a 1/6 2/6a
21/80a ne 35/80a 35/80a 36/80a 40/80a 5/80a 11/80a 37/80a 13/80a 30/80a 16/80a
92/92a 47/92a 92/92a 26/92a 75/92a 89/92a 7/92a 92/92a 92/92a 4/92a 39/92a 92/92a
6/40a 12/40a 14/40a 0/40 10/40a 17/40a 6/40a 18/40a 11/40a 7/40a 5/40a 1/40
12/24a ne 12/24a 8/24a 13/24a 10/24a 6/24a 11/24a 12/24a 8/24a 10/24a 12/24a
6/6a 6/6a 6/6a 3/6a 6/6a 6/6a 2/6a 6/6a 6/6a 1/6a 4/6a 6/6a
17/45a 21/45a 20/45a 20/45a 19/45a 19/45a 8/45a 18/45a 22/45a 19/45a 16/45a 14/45a
0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 2/6a 2/6a 0/6
0/80 1/80 10/80a 2/80 2/80 0/80 1/80 0/80 1/80 17/80a 14/80a 0/80
0/92 0/92 1/92 0/92 0/92 0/92 0/92 0/92 3/92a 3/92a 2/92 2/92
3/40a 0/40 1/40 2/40a 0/40 1/40 0/40 0/40 1/40 1/40 2/40a 0/40
0/24 0/24 2/24 03/24a 0/24 1/24 1/24 0/24 5/24a 10/24a 4/24a 1/24
0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6 0/6
6/45a 2/45 15/45a 4/45a 0/45 1/45 2/45 1/45 4/45a 3/45a 12/45a 2/45
A þ patients CL CA GV AS SMC TF GB MR GA AS TCS CG
45/45a 31/45a 45/45a 15/45a 41/45a 44/45a 7/45a 45/45a 45/45a 3/45a 33/45a 45/45a
A- patients MA RA GE MC GE PS MR GF BR CF SN NG a
0/45 0/45 0/45 3/45a 0/45 0/45 0/45 0/45 0/45 5/45a 5/45a 1/45
Defective performance, as compared with normative data. ne, not evaluable. 4
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half vowel strings, e.g.: “Vbd fgnmrptc spdnnrdfg cv ngtrsddfrt.” or “Aoi auoi eooiuaie i aeuoieiae.” (vi) Forty lines of comparable length.
Table 3 Baseline assessment for right visual USN. Cancellation tasks: number of omis sions in the left/right (L/R) hand-side of the display. Line bisection: percent deviation (-/þleftward/rightward deviation); Complex figure drawing: 0/5 in dicates errorless performance. Line Cancellation
Bell Cancellation
Line bisection
L
R
L
R
0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10
0/17
0/17
0.81%
0/5
0/17
0/17
6.07%
0/5
Each stimulus was printed in lowercase, 26-pt, Arial font on an A4 sheet. Mean lengths for each condition were: (i and vi) M ¼ 117.9 mm (SD � 18.0, range 87.0–158.5); (ii) M ¼ 111.3 mm (SD � 18, range 80.0–151.5); (iii) M ¼ 116.9 mm (SD � 14.9, range 85.0–140.0); (iv) M ¼ 114.2 mm (SD � 20.1, 69.0–155.0); (v) M ¼ 116.2 mm (SD � 12.4, range 90.0–148.5). Stimuli sets were presented in a randomized order to each participant, following a latin square design for the four types of sentences, and randomizing the resulting three stimuli sets (sentences, letter strings, lines) with all possible permutations. Stimuli were pre sented in the center of a horizontal A4 sheet, each page containing four items, aligned with the mid-sagittal plane of the participant’s body at a viewing distance of 40 cm. A moveable window was used in order to present each stimulus one at a time. Patients were individually tested in a quiet room, with the experimenter sitting in front of them. They were required to bisect each sentence, string or line, marking the mid-point with a soft pen using the left-hand, ipsilateral to the left hemispheric lesion, and not affected by the neurological damage. Participants were informed that the vertical mark could be made in any point of the stimulus, irrespective of whether the center might fall between two words, two letters, or go through a letter. No time limits were set, and no feedback was given as to the accuracy of the response. The distance between the left end of each stimulus and the participant’s mark was measured to the nearest mm. Each measure in mm was converted into a standardized score (measured left half minus objective half/objective half *100), in order to equate the participants’ error with respect to stimulus length. This percent deviation from the objective midpoint of the stimulus yielded positive values for rightward deviations, negative values for leftward deviations (Rode et al., 2006).
Complex figure drawing
Aþ patients CL CA GV AS SMC TF GB MR GA AS TCS CG
0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11
a
0.5/5a
2/ 17a 3/17
7/ 17a 7/17
5/17
3/17
1.24%
0/5
0/17
2/17
1.13%
0/5
2/17
3/17
2.52%
0/5
0/17
0/17
2.24%
0/5
2/17
2/17
1.16%
0/5
3/17
3/17
1.03%
0/5
2/17
3/17
3%
0/5
1/17
0/17
1.84%
0/5
2/17
0/17
1.32%
0/5
8/17
8/17
2.40%
0/5
0/17
0/17
4.42%
0/5
0/17
0/17
8.34%a
0/5
1/17
1/17
0.43%
0/5
0/17
0/17
2.94%
0/5
1/17
0/17
3.43%
0/5
0/17
0/17
0.70%
0/5
0/17
0/17
10.80%a
0/5
0/17
0/17
1.21%
0/5
4/17
3/17
3.50%
0/5
0/17
0/17
3.05%
0/5
9.88% 4.78%
0/5
A- patients MA RA GE MC GE PS MR GF BR CF SN NG
0/ 11 0/ 11 1/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11 0/ 11
0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10 0/ 10
2.3. Statistical analyses Data were analysed using non-parametric Friedman ANOVAs for each group of participants and comparing different types of stimulus (declarative sentences, yes/no interrogative sentences, sentences with syntactic and lexical violations, letter strings, lines), because the assumption of the homogeneity of variances across groups (Levene, 1960) – in this study, left brain-damaged patients, Aþ and A-, C par ticipants- for a repeated-measures ANOVA was violated for letter strings (p < 0.001). Level of significance was set at p < 0.05. Post-hoc multiple comparisons were performed using Wilcoxon pairwise tests, with Bonferroni-adjusted level of significance p < 0.003, when appropriate. Each average standardized score was compared to the objective midline of the stimulus through one-sample t-tests against zero. Pearson’s cor relations, with Bonferroni correction for multiple comparisons (p < 0.003), were used in order to measure the association between bisection errors for the different types of stimuli in the three groups. Furthermore, differences between the bisection biases for letter strings and linguistic stimuli (affirmative, interrogative and non-lexical sentences) were compared: (i) among left brain-damaged-patients (LBD; Aþ and A-) and C participants, using a Mann-Whitney test, and (ii) among LBD and right brain-damaged patients with left USN (RBD, as described in the study by Veronelli et al., 2014a), using an independent-samples t-test.
a
Defective performance, as compared with normative data, indicating right USN.
changing the order of the original words in the sentence. Spe cifically, articles, gender/number agreement, consonant clusters and double consonants were maintained, as well as verb endings/ suffixes and noun suffixes, with changes being confined to the root [e.g.: “La cabba sterrisce il costapoglio.” (“the loster sares the pibbet.“)]. (v) Forty unreadable letter strings, generated in order to mimic the visuo-perceptual structure of a sentence in terms of spaces be tween letters and the full stop. The presence of double letters was also maintained; half of the stimuli were consonant strings, and
3. Results As shown in Fig. 2, all participants made a leftward error in bisection. In the C group, the Friedman ANOVA for stimulus type was significant (χ25 ¼ 23.91, p < 0.001, Kendall’s W ¼ 0.20). Post-hoc multiple com parisons revealed that letter strings (Mdn ¼ 1.78) were bisected more accurately, more rightward, than declarative sentences (Mdn ¼ 4.48, p < 0.003, η2 ¼ 0.37), Yes/No interrogative sentences (Mdn ¼ 6.03, p < 5
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bisection for non-syntactic sentences (M ¼ 2.22%, t11 ¼ 1.98, p ¼ 0 0.07, η2 ¼ 0.07), and lines (M ¼ 2.31%, t11 ¼ 1.78, p ¼ 0.10, η2 ¼ 0.06). In the C group, Bonferroni-corrected (p ¼ 0.003) Pearson’s correla tions performed on bisection deviations were significant between all types of stimuli (declarative and Yes-No interrogative, r ¼ 0.79, p < 0.001; declarative and non-lexical, r ¼ 0.80, p < 0.001; declarative and non-syntactic, r ¼ 0.77, p < 0.001; declarative and letter strings, r ¼ 0.83, p < 0.001; Yes-No interrogative and non-lexical, r ¼ 0.79, p < 0.001; Yes-No interrogative and non-syntactic, r ¼ 0.86, p < 0.001; YesNo interrogative and letter strings, r ¼ 0.81, p < 0.001; non-lexical and non-syntactic, r ¼ 0.82, p < 0.001; non-lexical and letter strings, r ¼ 0.83, p < 0.001; non-lexical and lines, r ¼ 0.66, p ¼ 0.001; non-syntactic and letter strings r ¼ 0.80, p < 0.001; letter strings and lines r ¼ 0.59, p ¼ 0.002), except between lines and declarative sentences (r ¼ 0.569, p ¼ 0.004, n.s.), lines and Yes-No interrogative sentences (r ¼ 0.47, p ¼ 0.02, n.s.) and lines and non-syntactic sentences (r ¼ 0.530, p ¼ 0.01, n. s.). In the A- group, significant correlations were found between the four types of linguistic stimuli: declarative and Yes-No interrogative (r ¼ 0.89, p < 0.001), declarative and non-lexical (r ¼ 0.89, p < 0.001), declarative and non-syntactic (r ¼ 0.80, p ¼ 0.002), Yes-No interrogative and non-lexical (r ¼ 0.97, p < 0.001), Yes-No interrogative and nonsyntactic (r ¼ 0.93, p < 0.001) and between non-lexical and nonsyntactic stimuli (r ¼ 0.89, p < 0.001). No significant correlations were found between letter strings and all the other types of linguistic stimuli, between lines and all the other types of linguistic stimuli, and between letter strings and lines (p > 0.003, in all cases, n.s.). In the Aþ group, correlations were significant between declarative and Yes-No interrogative sentences (r ¼ 0.81, p ¼ 0.001), declarative and nonlexical sentences (r ¼ 0.84, p ¼ 0.001), Yes-no interrogative and nonlexical sentences (r ¼ 0.89, p < 0.001) and between letter strings and lines (r ¼ 0.80, p ¼ 0.002). No other significant correlations were found (p > 0.003, in all cases). A Mann-Whitney test indicated that the difference between the average bisection deviations for letter strings and linguistic stimuli (affirmative, interrogative and non-semantic sentences) was larger for the C group (Mdn ¼ 2.08) than for the group of left brain-damagedpatients (Aþ and A-) (Mdn ¼ 0.47, U ¼ 190.5, p ¼ 0.04, η2 ¼ 0.084) (see Fig. 3A). The t-test performed in LBD and RBD patients (data from Veronelli et al., 2014a) on the difference between the average deviations for letter strings and linguistic stimuli revealed a significantly larger difference in RBD than in LBD patients (t28 ¼ 3.00; p ¼ 0.006, η2 ¼ 0.32; M ¼ 9.88%, M ¼ 0.13%, respectively), as shown in Fig. 3B. Summing up, healthy participants show larger leftward biases in the bisection of orthographic readable sentences, compared to unreadable letter strings. On the contrary, patients with and without aphasia set the mid-point of all types of stimuli to the left of the physical center, without a difference between readable and unreadable material.
Fig. 2. Median percent deviation error (upper and lower quartiles, maximum and minimum values) by participants’ group (Aþ/A-left brain-damaged pa tients and C participants), and by type of stimulus (declarative sentences, Yes/ No interrogative sentences, non-syntactic sentences, non-lexical sentences, letter strings, lines). � mild outliers.
0.001, η2 ¼ 0.55), and non-lexical sentences (Mdn ¼ 4.68, p < 0.002, η2 ¼ 0.42). On the other hand, the difference between letter strings (Mdn ¼ 1.78) and non-syntactic sentences (Mdn ¼ 3.79) was not significant after Bonferroni correction (p ¼ 0.013, η2 ¼ 0.26, n.s., with the level of significance after the correction being p < 0.003). No other significant differences were found after Bonferroni correction (p < 0.003, for all the comparisons). In both the Aþ and A- groups, the Friedman ANOVAs for the type of stimulus were not significant (Aþ: χ25 ¼ 6.14, p ¼ 0.29, W ¼ 0.10; A-: χ25 ¼ 5.87, p ¼ 0.32, W ¼ 0.10). In the C groups, all bisection scores differed significantly from ac curate bisection: declarative sentences, M ¼ 4.43%, t23 ¼ 4.81, p < 0.001, η2 ¼ 0.19; Yes/No interrogative sentences, M ¼ 5.48%, t23 ¼ 6.01, p < 0.001, η2 ¼ 0.27; non-syntactic sentences, M ¼ 4.45%, t23 ¼ 4.59, p < 0.001, η2 ¼ 0.18; non-lexical sentences, M ¼ 4.76%, t23 ¼ 4.89; p < 0.001, η2 ¼ 0.20; letter strings, M ¼ 2.77%, t23 ¼ 3.73, p ¼ 0.001, η2 ¼ 0.13; lines, M ¼ 2.84%, t23 ¼ 3.08, p ¼ 0.005, η2 ¼ 0.09. Aþ participants exhibited significantly leftward deviations from accurate bisection with Yes/No interrogative sentences (M ¼ 4.94%, t11 ¼ 3.65, p ¼ 0.004, η2 ¼ 0.22), non-syntactic sentences (M ¼ 5.25%, t11 ¼ 4.67, p ¼ 0.001, η2 ¼ 0.31), non-lexical sentences (M ¼ 5.21%, t1 ¼ 3.65; p ¼ 0.004, η2 ¼ 0.22), and lines (M ¼ 4.22%, t11 ¼ 2.55, p ¼ 0.03, η2 ¼ 0.12). The leftward directional bias did not differ from accurate bisection for declarative sentences (M ¼ 3.22%, t11 ¼ 1.68, p ¼ 0.12, η2 ¼ 0.05), and letter strings (M ¼ 4.67%, t11 ¼ 1.61, p ¼ 0.14, η2 ¼ 0.05). In the A- group bisection performances significantly differed from accurate bisection, with a leftward deviation for declarative sentences (M ¼ 3.55%, t11 ¼ 3.38, p ¼ 0.006, η2 ¼ 0.19), Yes/No interrogative sentences (M ¼ 3.78%, t11 ¼ 3.02, p ¼ 0.012, η2 ¼ 0.16), non-lexical sentences (M ¼ 3.99%, t11 ¼ 3.70, p ¼ 0.003, η2 ¼ 0.22), and letter strings (M ¼ 3.30%, t11 ¼ 3.13, p ¼ 0.01, η2 ¼ 0.17). The leftward directional bias did not differ from accurate
4. Discussion This study investigated whether the presence of an acquired lin guistic impairment (aphasia of various types and degrees) could modulate the patients’ estimation of the lateral extent of linguistic material presented visually, as assessed by a task requiring the manual bisection of orthographic strings. The evidence reviewed in the introduction indicates that the leftward bias in the bisection of both single words and sentences may be driven not only by asymmetries in the orientation of spatial attention, related to hemispheric differences and specifically, to a major role of the right hemisphere (see a recent review and discussion in Bartolomeo and Seidel Malkinson, 2019), but may be also dependent on language pro cessing (Fischer, 2000, 2004, 1996; Veronelli et al., 2014a). Based on this evidence, the prediction was made that patients with a linguistic disorder could show a less marked leftward bias when bisecting readable 6
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assessed by tasks that directly and explicitly probe these performances. Conversely, the processing of linguistic material in bisection tasks is not directly and explicitly assessed by the task of setting the mid-point of a string. In non-aphasic patients, ortho-phonological conversion abilities (as assessed through pseudoword reading aloud, see Table 2) are spared. Nevertheless, these patients do not exhibit any differences in bisecting readable and unreadable (other than by letter-by-letter reading) mate rial. This indicates that intact reading abilities are not sufficient for, or do not provide an adequate support to, the language-related effect of a larger leftward bias in the bisection of readable vs. unreadable material. This effect can be altered in the presence of a left brain-lesion, even in absence of apparent aphasia. While including orthographic stimuli, sentence bisection is per se a length estimation task, where linguistic processing is not directly required. Notwithstanding, also the perfor mances of control participants indicate that orthographic processing, although not explicitly required by the task, takes place, as shown by the different bisection biases in the case of readable vs. unreadable senten ces. In sum, as a consequence of left hemispheric brain damage, the language-related implicit processes that modulate the setting of the subjective mid-point in sentence bisection, may be less effective. The possibility that the lack of significant differences between sentential and letter string material within Aþ and A- left brain-damaged patients might just reflect random variability of performance is countered by the finding that the patients’ bisection is overall significantly deviated leftward, as compared to the objective center of the stimulus to be bisected, as in control participants, with most of the stimuli. Particu larly, control participants show significant leftward biases with all types of stimuli, Aþ patients with all stimuli, but declarative sentences and letter strings, A– patients with all stimuli, but non-syntactic sentences and lines. Also the presence of significant correlations between bisection biases for linguistic stimuli in all groups argues against interpretations of the patients’ performances in terms of random variability. Eye tracking studies suggest that aphasic patients do not construct an online mental representation of the sentence with the same time course as control participants. Effects of structural complexity emerge on the first pass through the sentence for controls, but only in rereading times for patients (DeDe, 2017; Knilans and DeDe, 2015). While the sentence reading and bisection tasks definitely differ in important respects, a shared finding concerns abnormalities in the linguistic processing of sentences. In conclusion, in the visuo-spatial task of bisecting sentences neurologically unimpaired participants show a language-related effect, bisecting readable sentences more leftward than unreadable ones. This effect, even in the absence of apparent aphasia, is disrupted by left hemispheric lesions, which alter the processes, likely linguistic in na ture, that modulate sentence bisection.
Fig. 3. A) Median difference of percent deviation errors (upper and lower quartiles, maximum and minimum values) between letter strings and linguistic stimuli in LBD patients and C participants. B) Mean difference of percent de viation errors (�SE) in RBD (data from Veronelli et al., 2014a) and LBD pa tients. � mild outliers; * extreme outliers.
sentences, as compared to unreadable ones. Patients and neurologically unimpaired participants were required to bisect different types of stimuli (declarative sentences, Yes/No interrogative sentences, non-syntactic sentences, non-lexical sentences, unreadable letter strings and lines). Healthy participants exhibited a leftward deviation with all stimuli, namely different types of sentences, letter strings and lines, showing larger leftward biases with orthographic readable sentences, as compared to unreadable letter strings. These findings confirm previous evidence (Fischer, 1996; Veronelli et al., 2014a) that the presence of readable material may induce a more pro nounced leftward shift of attention, possibly through an activation of left hemisphere-based linguistic processes, that orient more leftward, to ward the beginning of the to-be-bisected letter string, readable in Italian from left to right (see Chokron et al., 1998; Chokron and Imbert, 1993). Furthermore, the leftward biases in bisection for lines and words, that mark the performance of neurologically unimpaired adults, develop with different directional patterns between three and eight years of age, suggesting that different factors, including visuo-spatial attention and linguistic processes, may be involved (Girelli et al., 2017). In the present study, left-brain-damaged patients, both with and without aphasia, do not show the significant difference between read able and unreadable material found both in neurologically unimpaired participants and in right-brain damaged patients (Veronelli et al., 2014a). The lack of significant differences in the biases for the different types of readable stimuli in both aphasic and not aphasic left-brain-damaged patients contrasts with the larger leftward biases found in control participants and in right-brain damaged patients with left USN. These findings suggest that left brain damage may impair the linguistic processes involved in the bisection of sentential material, in dependent of the presence of a clinically apparent aphasic deficit. The linguistic processing (and its impairments) that features speech pro duction and comprehension (and aphasia) is explicit in nature, and
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