Superior Written Over Spoken Picture Naming in a Case of Frontotemporal Dementia

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Superior written over spoken picture naming in a case of
fronto-temporal dementia


Marie-Josèphe Tainturier1, Olivier Moreaud2,3, Danielle David3, E. Charles Leek1 & Jacques Pellat2,3


1 School of Psychology, University of Wales, Bangor, North Wales

2 Laboratoire de psychologie expérimentale, Université Pierre Mendès France, Grenoble, France

3 Service de neurologie et neuropsychologie, Centre hospitalier universitaire de Grenoble
















Running title: Superior written naming in fronto-temporal dementia



Address correspondence to:

Marie-Josèphe Tainturier
School of Psychology
University of Wales Bangor
Bangor, Gwynedd, LL57 2DG, UK
e-mail: [email protected]
Fax: +44 (0)1248 382599

Abstract
Two main hypotheses have been proposed regarding the role of phonology in written word production. According to the phonological mediation hypothesis, the retrieval of the lexical phonological representation of a word is an obligatory prerequisite to the retrieval of its spelling. Therefore, deficits to the phonological lexicon should affect both spoken and written picture naming. In contrast, the orthographic autonomy hypothesis posits that the lexical orthographic representations of words can be accessed without any necessary phonological mediation. In support of this view, cases of preserved written naming despite impaired lexical phonology have been reported following brain damage (Bub & Kertesz, 1982; Hier & Mohr, 1977; Levine et al, 1982). In this report, we replicate this basic pattern of performance in case YP, a 60-year-old woman with a pattern of fronto-temporal dementia. As her disease progressed, YP's ability to write down the names of pictures remained very good despite a severe decline of oral naming. Further testing indicated that this deficit was not primarily due to an articulatory or post-lexical phonological deficit. YP's case provides strong additional support for the orthographic autonomy hypothesis. The significance of this case with respect to the characterization of dementia syndromes is discussed.



Introduction
When brain damage affects spoken language it usually affects written language to a similar or greater extent (Basso et al., 1978). Actually, spelling is seen as one of the most vulnerable skills in aphasia (e.g., Patterson & Shewell, 1987). Nevertheless, several cases of superior or even entirely preserved written language have been reported (for reviews, see Basso et al., 1978; Rapp et al., 1997; Tainturier & Rapp, 2000). The existence of such cases raises questions regarding the organization of the cognitive processes that underlie spoken and written word production.
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Insert Figure 1 (a & b)
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Figure 1 depicts a set of hypotheses about the cognitive processes involved in the oral or written naming of a picture. According to the orthographic autonomy hypothesis (Fig. 1a), word spellings can be retrieved from the orthographic lexicon through direct link with semantics, with no necessary involvement of phonology. An alternative view is that written naming necessarily involves some form of phonological mediation (e.g., Geshwind, 1969; Perfetti, 1997; Van Orden et al, 1997). Under that view, semantic representations will activate the phonological forms of words, which then activate the corresponding orthographic forms. On both hypotheses, the retrieval of the orthographic or phonological lexical representations of words is followed by the application of postlexical processes specific to each modality of output; these processes are responsible for the transformation of abstract lexical representations into specific motor patterns.
These contrasting views about the role of phonology in producing written words make different predictions about the possible patterns of impairment that could be observed following brain damage. According to the phonological mediation hypothesis, a deficit at the level of the phonological lexicon should necessarily produce a deficit in both oral and written picture naming. According to the orthographic autonomy hypothesis however, it should be possible to observe patients with preserved written naming but impaired oral naming.
As noted earlier, a number of cases of brain damaged individuals with superior written over spoken naming have been reported. However, most of these cases do not speak directly to the issue of the autonomy of orthography because the lexical versus post-lexical origin of the spoken deficit is not clearly established. Since post-lexical deficits should not affect written naming under any account, we will now review cases in which preserved written naming occurred despite a spoken naming disorder that was most likely due to a lexical deficit.
One convincing pattern was exhibited by case RGB (Caramazza & Hillis, 1990) who produced many semantic errors in his oral naming of pictures (e.g., picture of a tiger -> "lion") but none in his written naming. It is unlikely that semantic errors would arise as a result of a post-lexical phonological deficit, phonemic errors or neologisms being generally seen as the characteristic error types at this level (for a discussion, see Rapp & Goldrick, in press). Rather, spoken semantic errors are usually considered to have a lexical origin, resulting from deficits to either the lexico-semantic system itself or, as was argued in the case of RGB, to the phonological lexicon. Under the phonological mediation hypothesis, one would therefore expect that a patient producing semantic errors in his spoken output would also produce them in his written output. By showing that this is not necessarily the case, Caramazza & Hillis (1990) provided direct support for the orthographic autonomy hypothesis. Similar cases have been reported since (Beaton et al, 1997; Hillis & Caramazza, 1995; Miceli et al, 1997; Miceli et al, 1999; Nickels, 1992; Rapp et al, 1997; Shelton & Weinrich, 1997).
Another pattern of impairment supporting the orthographic autonomy hypothesis was reported by Bub and Kertesz (1982). MH could write down the names of 15/20 pictures, but named only one orally, producing no response at all in the remaining cases. Crucially, different aspects of her performance suggested that the source of her spoken naming disorder was at the level of the phonological lexicon rather than at a more peripheral level. Her speech was very reduced but well articulated and without phonemic errors. Furthermore, she was very poor in tasks that do not involve overt production but that do require internal access to lexical phonology (e.g., judging whether or not two pictures correspond to rhyming words). Similar cases have been described by Hier & Mohr (1977) and Levine et al (1982).
The case of a brain-damaged woman with a remarkable sparing of written picture naming in the face of an almost total incapacity to produce words orally will now be reported. We will argue that her pattern of performance provides additional support for the orthographic autonomy hypothesis. An interesting feature of this case is that the preservation of written over oral naming occurs within the context of a degenerative pathology (fronto-temporal dementia) contrary to previous cases that all resulted from vascular accidents.
Striking neuropsychological dissociations are typically the result of focal brain lesions. Nevertheless, various cognitive abilities can be differentially impaired in neuro-degenerative diseases. For example, primary progressive aphasia is characterized by a selective impairment of language skills (Mesulam, 1982). Interestingly, finer dissociations have also been reported. For example, primary progressive aphasia can either take the form of nonfluent aphasia with impaired phonology and syntax or else be characterized by a selective breakdown of semantic representations (Hodges & Patterson, 1996). There are several other examples, such as the progressive dysgraphia case reported by Graham et al (1997) who initially showed a marked surface dysgraphia with mild word finding difficulties.
To our knowledge, the pattern of dissociation that will be described in this article has not been reported in cases of degenerative disease. To the extent that it may be observed in other cases, this observation could contribute to the early differential diagnosis of fronto-temporal dementia as opposed to dementia of the Alzheimer's type. Indeed, it has been argued that written language disorders develop earlier than oral language disorders in DAT (Appel et al., 1982; Cummings et al., 1985; Faber et al., 1988). Some cases of preserved spelling in mild DAT have been reported, but the individual performance of these patients in spoken naming tasks was not specified (Hughes et al, 1997).
Case Report
Initial Assessment - Autumn 1993
YP, a 59 year-old right-handed retired accountant, was referred to the Centre Hospitalier Universitaire de Grenoble for neurological assessment in October 1993. She had shown signs of increasing memory loss in the previous two years. Her husband also reported behavioral disturbances since 1988. Initially, YP became increasingly apathetic and indifferent to previously enjoyed activities. Her eating patterns also changed: she never refused food and would nibble all day long which led to significant weight gain. During the summer of 1988, her husband noticed that she constantly put the heat on to maximum intensity; if questioned about it, YP would blame some absent family member. Her condition worsened, and she had to quit work. YP had to be stimulated in daily life activities that she could no longer accomplish spontaneously. In 1991-92, disorders of memory and language started, and their aggravation led to her physician's referral. When first seen, standard neurological examination was normal. However, YP scored 24/30 on the MMSE (Folstein et al, 1975), indicative of a mild cognitive dysfunction. Further testing showed that language and verbal memory skills were primarily affected, together with frontal "executive" functions.
Language and verbal memory skills. YP's scores on the Aphasia Examination Battery of the Centre Hospitalier Universitaire de Grenoble revealed a severe impoverishment of spontaneous speech, verbal fluency, and verbal memory. Spontaneous expression was very reduced and YP frequently offered single-word responses to questions. However, she showed no signs of bucco-facial apraxia. She had a limited capacity to give definitions of words, providing either no (3/9) or very sketchy responses (e.g., fork -> "to eat", blind -> "all black, all black"). Her verbal fluency was also reduced: She could only name 13 pieces of clothing (control mean = 24, SD=6) and 6 words starting with the letter P (control mean = 24, SD=8) within two minutes in each case. However, she was still able to name 75/80 pictures. Her reading aloud and repetition were good, although sometimes hesitant and with occasional palilalias or phonemic errors. Overall, she could repeat 16/20 phonologically complex words. Writing to dictation of three sentences was perfect, as was spontaneous writing. Oral and written comprehension of single words and sentences was preserved. For example, she could match sentences to pictured actions (7/8 spoken; 8/8 written; task taken from Nespoulous et al, 1986) and execute complex arbitrary orders (3/3 spoken; 5/5 written). YP's short-term memory was reduced, with a word span of 2 and a digit span of 4 forwards and 2 backwards. YP could only produce 3/16 elements of a short story in immediate recall. In a recognition task of a list of 10 words, her performance was also below normal range (6/10 on the first trial, and 9/10 on the second and third trials). Delayed recall of lists of words was more severely impaired.
Other cognitive skills. There was significant decline in tasks assessing executive functions: Stroop task (Perret et al, 1974), gestual series (Luria, 1978), verbal fluency (see above). YP also showed a very mild deficit of ideational and ideomotor praxis and of visuo-constructive abilities (Poppelreuter task, see Lezak, 1983; incomplete figures test). Results on the subtests of the Mattis scale (Mattis, 1976) aimed at measuring selective attention were within the normal range (35/37) although performance on the visual recognition memory subtest of the same scale was slightly impaired (3/4). There were no signs of constructional apraxia. Mental calculation was normal.
Follow up- Autumn 1994
Over the course of the following year, YP's condition severely deteriorated. The most obvious consequence of the progression of her disease was that she lost all capacity to express herself through speech. Palilalias (e.g., "lalalala", "tatatat") and often inappropriate yes/no responses were all that YP could produce when encouraged to speak. In addition, she had become severely apragmatic and could not perform everyday life activities like eating or dressing by herself. Her husband reported that she would carry on eating unless he stopped her. Her affect was also disturbed, and she alternated between crying episodes and more frequent periods of constant smiling. An MRI scan performed in February of 1995 showed a diffuse cortical and sub-cortical atrophy predominant in the fronto-temporal regions of both hemispheres (see Figure 2).
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Insert Figure 2
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At this stage, most standard neuropsychological tests could no longer be carried out due to YP's incapacity to produce any speech or to follow test instructions. It also became increasingly difficult and finally impossible for YP to come to her hospital appointments, which limited the amount of testing that could be performed.
The language examination showed that spoken expression skills had severely deteriorated. Her spontaneous speech was reduced to palilalias and a few word starts. She could only name 2/20 pictures (see Table 1 and below for more data). In contrast, repetition was better preserved (9/11 phonologically complex words; 4/4 short sentences) and spoken word comprehension was normal. In a task in which she had to choose which of a set of 10 pictures from the same semantic category corresponded to a spoken word, she scored 10/10 for animals, 9/10 for fruits and vegetables and 10/10 for artifacts. She could also point to pictures (6/6) based on a short definition of the object's use. Matching sentences to pictured actions was also within normal range (7/8; task taken from Nespoulous et al, 1986). Written comprehension was also good, for both single words (12/12) and sentences (7/8). As further evidence of the preservation of her semantic knowledge, she performed flawlessly in a task that required her to sort 24 images into 3 unnamed categories (8 fruits, 8 flowers, 8 vegetables).
In striking contrast to her spoken production, YP's written expression remained surprisingly good. For example, she could write down the names of 19/20 pictures although she could only name 2 aloud ( 2(1) = 28.96, p < 0.001). Although she made some mistakes in writing sentences to dictation (1/3 sentences correct, with a total of 7 errors out of 44 words), her errors were restricted to function words and affixes. For example, upon hearing the sentence "The children are in class" YP wrote "My children are in class". YP's difficulties with function words were also apparent in single-word writing to dictation (14/20) where she substituted target words with other function words or with homophonic content words. Interestingly, difficulties with function words and affixes have been reported in other patients with superior written over oral naming (e.g., Bub & Kertesz, 1982; Rapp & Caramazza, 1996).
The next section focuses on an analysis of YP's preserved written naming skills in an attempt to evaluate whether her case could be taken as support for the orthographic autonomy hypothesis.
The superiority of written picture naming.
The superiority of written over oral naming of pictures (see preliminary data above) was confirmed by assessing YP's performance in these two tasks on an additional set of items (21/25 vs. 2/25, 2(1) = 29.08, p < 0.001). In oral naming, YP generally failed to produce any response to the target (17/25) even though she was strongly encouraged to do so. When she did, she produced palilalias in three cases, the first phoneme in two cases, and one semantic error (picture of a helicopter -> "plane"). In written naming, YP produced 3 semantic errors [a picture of a violin was named "mandolin" (in French: violon -> mandoline), a coffee maker was named "coffee" (cafetière -> café), and a mandarine was named "apple" (mandarine -> pomme)] and one phonologically implausible error ("hélicoptère" was spelled "hécutère"). It should be noted that not only was YP's performance level far superior in written naming, but that she accomplished the task quickly and with no apparent effort.
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Insert Table 1
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As stated in the introduction, superior written over oral naming can only be seen as supporting the orthographic autonomy hypothesis if it can be established that the spoken naming disorder is not primarily due to postlexical phonological or articulatory impairments. Three pieces of evidence suggest that YP's spoken naming deficit is mainly related to a lexical impairment.
First, her repetition of the test items was far better than her oral naming (22/25 vs. 2/25, 2(1) = 32.04, p < 0.001). All words were properly articulated, although the 3 errors were phonologically related nonwords (/SosEt/ -> /sosEt/, /grënuj/ -> /dënuj/, /bruEt/ -> /ruEtr/). It is generally considered that all speech production tasks (e.g., naming, repetition, reading aloud) involve the same post-lexical components (e.g., Butterworth, 1992). Therefore, YP's relatively preserved performance in repetition suggests that a post-lexical deficit is not the main source of her poor spoken naming.
Second, YP's naming performance improved significantly with cueing (18/25 vs. 2/25, 2(1) = 21.34, p < 0.001). In 13 cases, the correct response was produced following a phonemic cue (first phoneme) and in 5 cases with a combination of phonemic and semantic cues (sentence context + first phoneme). For example, when presented with a picture of a frog (/grënuj/), YP could produce no response whatsoever. However, telling her "that's a /g/..." was sufficient to elicit a well-articulated, phonologically accurate response. Of the 7 items for which cueing was ineffective, 6 lead to a no response and only 1 to a phonemic error (/pusE$/ -> /pusE/). The all or none nature of YP's responses in cued naming adds to the repetition data in suggesting that postlexical processes are not primarily impaired, as it is difficult to see how providing a single phoneme would be sufficient to eliminate all potential phonemic errors. However, YP's cued naming performance is consistent with a lexical retrieval deficit if one believes that the cues can increase the accessibility of otherwise irrecoverable lexical representations or help in the selection of the appropriate response among a set of rival lexical candidates (Nickels, 1992).
A third line of evidence in favor of a lexical deficit comes from an inspection of YP's responses in reading aloud the same test items. YP's reading was poor (10/25) and qualitatively similar to her oral naming. Reading errors were mostly palilalias (n=7) and aborted responses (n=3, e.g., violon (/vjolO$/) -> /vja lalalala .../). There was only one clear phonemic error (botte /bOt/ -> /but/). In the 5 remaining cases, YP did not produce anything. As in oral naming, YP's reading improved markedly with phonemic cueing (10/25 vs. 24/25, 2(1) = 18.00, p < 0.001) and no partial responses or phonemic errors were produced. Here again, this error pattern does not seem to be consistent with a post-lexical language production impairment. However, it is consistent with a lexical impairment if one reasons that the effect of the cue is to help in the selection of a lexical unit. It should be noted that YP could not read nonwords (0/20) suggesting that her capacity to derive phonology from print non-lexically was severely impaired. Therefore, YP's reading of words must have relied at least partly on lexical processing, hence the similarity in error patterns between reading and naming. It remains to be explained why YP's reading aloud, although clearly impaired, was better preserved than her oral naming (10/25 vs. 2/25, 2(1) = 7.02, p < 0.01). It has been proposed that better performance in reading as compared to picture naming could reflect the integration of partial lexical information with partial information from sublexical grapheme/phoneme conversion processes (Hillis & Caramazza, 1995). This explanation may apply to YP (note that YP's failure to read nonwords does not preclude that residual sublexical information is available).
Finally, it should be noted that at no time in the evolution of her spoken production impairment did YP show signs of a post-lexical deficit. That is, she went from good naming performance to very poor naming performance without going through a stage where she produced a significant amount of phonemic or articulatory errors.
In summary, the evidence that we have presented suggests that a lexical deficit is the main source of YP's spoken naming disorder. However, it cannot be ruled out that YP suffers from some additional post-lexical phonological impairment. The occasional phonological errors observed in repetition, reading aloud, and naming are consistent with such an interpretation (although they are also consistent with a lexical impairment that would prevent the full phonological specification of some words; see Butterworth, 1992). However, it is very unlikely that a post-lexical deficit alone can account for YP's oral naming deficit because (a) phonological errors were produced at a very low rate at all stages of her disease, (b) repetition was much better preserved than naming and (c) cueing elicited a significant amount of correct responses but very few phonemic approximations. One might argue that YP's naming disorder could be related to a disconnection between lexical and post-lexical phonology, which would explain the relative preservation of repetition. On this account, YP's preserved spelling would not speak to the issue of orthographic autonomy because the preserved phonological lexicon might still mediate access to orthographic lexemes. Although we cannot entirely dismiss this hypothesis, we feel that it fails to explain the very low rate of phonological errors in naming and reading tasks. According to current models of language production, deficits to the connections between lexical and post-lexical phonology should often lead to the production of phonemic errors. This hypothesis was supported in several studies of patients with neologistic jargon, as well as following "disconnection lesions" in computer simulations (Dell et al, 1997; Croot et al, 1998; Hillis et al, 1999).
It would have been interesting to know more about YP's knowledge of the phonological forms of words in tasks that do not involve overt production. Failure on such tasks has been used to support to hypothesis of damage to lexical representations (e.g., Bub & Kertesz, 1982), although post-lexical deficits might also interfere with "covert" access to phonological word forms. We did submit YP to simple rhyme judgment and phoneme detection tasks, but these tasks proved so difficult for her that they could not be completed. Although this is consistent with a lexical impairment, the reasons for YP's failure on these tasks are unclear. For example, she was just as poor at deciding whether or not two words rhymed when both stimuli were presented auditorially (which does not require lexical mediation) as when she had to retrieve the names from pictures.
General discussion
We have presented the case of YP, a woman with fronto-temporal dementia who showed a striking preservation of written picture naming in the face of severely impaired spoken naming. We have argued that this deficit was primarily caused by a lexical phonological deficit. Therefore, the evidence from YP and from previously reported cases (see above) suggests that access to the orthographic lexicon does not require phonological mediation. Of course, it remains entirely possible that phonological mediation plays some role in normal writing. The relatively high proportion of real-word homophone substitutions (e.g., writing "piece" for "peace") in the "slips of the pen" of normal writers supports this hypothesis (Ellis, 1982).
We might also consider how YP's pattern of performance fits with two-stage models of lexical access (e.g., Butterworth, 1992; Dell & O'Seaghdha, 1992; Jescheniak & Levelt, 1994; Roelofs, 1992). Although there is variation in the specific implementations of this general hypothesis, it is commonly assumed that access to a word's phonological form (p-lexeme) or orthographic form (o-lexeme) is mediated by prior access to a modality-neutral specification of the word's syntactic features (lemma). Within this framework, one could postulate direct connections between lemmas and o-lexemes (orthographic autonomy) and/or connections between p-lexemes and o-lexemes (phonological mediation). Under both accounts, damage to the modality-neutral lemma level should affect both spoken and written naming (for a discussion, see Caramazza, 1997). Therefore, YP's performance – superior written over oral naming – is not consistent with a deficit at the lemma level. Rather, her deficit would have to involve the p-lexeme level, or the connections between lemmas and lexemes. In either case, the retrieval of o-lexemes should be disturbed if phonological mediation is obligatory. Therefore, YP's performance suggests direct connections between lemmas and o-lexemes. An interesting prediction of two-stage models is that YP should have preserved access to the syntactic properties of words that she cannot name (e.g., grammatical category, gender). Unfortunately, we were unable to examine this possibility.
Contrary to previously reported cases of relative preservation of spelling that all followed from vascular accidents, YP presented with a progressive pattern of behavioral and neuropsychological impairment consistent with a clinical diagnosis of fronto-temporal dementia (Brun, Englund, Gustavson, et al. 1994; Miller et al, 1997; Neary & Snowden, 1996; Neary et al, 1998). According to Hodges et al's (1999) classification (see also Gregory, Serra-Mestres & Hodges, 1999; Hodges & Miller, in press), YP's profile corresponds to the frontal variant of FTD, as opposed to the temporal variant (semantic dementia). In support of this diagnosis, the initial stages of her disease were mainly characterised by progressive changes in behavior that led to a profound personality change, severe apragmatism, inertia, stereotypies, hyperphagia, and a disturbed expression of affect. These symptoms may have reflected an initial involvement of orbitomedial frontal regions (e.g., Gregory et al, 1999). The behavioral disturbances were first noticed by the family in 1988, and it is only 5 years later than increasing cognitive dysfunction prompted referal for neurological assessment. At that stage, YP showed a moderate impairment of frontal executive functions and verbal memory with reduced verbal fluency in the context of normal neurological examination.Within a year, the dissolution of spoken language progressed , with anomia, palilalias, reduced fluency, and ultimately mutism. However, language comprehension and repetition remained relatively preserved. An MRI performed in 1995 showed diffuse bilateral atrophy predominant in the fronto-temporal regions.
The nature of language disorders in the frontal variant of FTD is not as well documented as it is in other forms of degenerative diseases. Patients usually present with a progressive reduction of language leading to mutism (Miller et al, 1997; Neary & Snowden, 1996; Neary et al, 1998), as was the case in YP, although pressure for speech can also be observed in patients with an overactive, disinhibited pattern of behavioral disturbance. The language disorders that emerge in the later stages of the frontal variant of FTD may reflect in part the extension of cortical atrophy to the temporal lobe. Indeed, the late MRI of YP shows atrophy that is not limited to the frontal regions. However, even in the latest stages, her pattern of language impairments was still very different from what is observed in other forms of progressive dementia. Most noticeably, she showed no clear deficit of word or sentence comprehension nor of nonverbal semantic processing. Also, her speech output reduced to the point of mutism, but at no stage of her disease did she produce a high rate of paraphasias, although phonemic and semantic errors were occasionally produced in picture naming or repetition.
The superiority of written over oral language production is not currently seen as a characteristic feature of the frontal variant of FTD although it should be noted that spelling is not systematically assessed and/or reported in the late stages of the disease. Neary et al (1998) include agraphia as one of the core features of progressive nonfluent aphasia. In the case of semantic dementia, spelling is relatively preserved except for orthographically irregular words that give rise to phonologically plausible errors like "phone" written as "fone" (Graham, Patterson & Hodges, 1999; Neary et al, 1998). YP produced no such errors and did not show an effect of regularity. In FTD (frontal variant), it has been assumed that written output should mirror spoken output (Snowden et al., 1996). Clearly, YP's case presents a challenge to this view. Further studies of spelling in fronto-temporal dementia should help to clarify this issue.
Acknowledgements: We are grateful to Isabelle Fluchaire for her contribution to YP's neuropsychological assessment and to Annick Charnallet and anonymous reviewers for their comments on previous versions of this article.
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Figure 1: Cognitive processes involved in spoken and written picture naming. A. Orthographic autonomy hypothesis. B. Phonological mediation hypothesis.

Figure 2: Axial (left) and coronal (right) MRI slices showing diffuse cerebral atrophy, predominant in the fronto-temporal regions.




Table 1

Summary of YP's performance on identical sets of stimuli in different tasks

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Task Number of correct responses

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Written picture naming 19/20

Spoken picture naming 2/20

Written picture naming 21/25

Spoken picture naming 2/25

Oral picture naming with cueing1 18/25

Reading aloud 10/25

Reading aloud with phonemic cueing 24/25

Repetition 22/25

Written word/picture matching 24/25

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1 13 items were retrieved with phonemic cueing only (first phoneme) and 5 with phonemic cueing plus sentence context.






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