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Rapid recovery of aphasia and deep dyslexia after cerebrovascular left-hemisphere damage in childhood
Pergamon 0911-6044(95)00002-X
J. Neurolinguistics, Vol. 9, No. 1, pp.9-22, 1995 Copyright0 1995 Elscvierscience Ltd Printedin GreatBritain.All rightsmewed 0911~m/95 $9.50+0.00
RAPID RECOVERY OF APHASIA AND DEEP DYSLEXIA AFTER CEREBROVASCULAR LEFT-HEMISPHERE DAMAGE IN CHILDHOOD R. DE BLESER,* J. FAISS~ and M. SCHWARZ$. *Departmentof Cognitive Neurolinguistics, Potsdam; TDepartmentof Neuroradiology, Essen; *Department of Neurology, Aachen, Germany Abstract-This paper reports a case of acquired language impairment in an 85year-old right-handed Belgian boy (BV). He had normally acquired his native language (Flemish/Belgian Dutch) as well as a second language (French), and he was a very good pupil in school. Following a vascular accident in the left hemisphere, the patient initially presented a pure pattern of deep dyslexia associated with a non-fluent aphasia with phonemic paraphasias. The deep dyslexic symptoms disappeared within six weeks, and the aphasic impairments were no longer observable after 4.5 months. One year after the cerehro-vascular accident, the boy reached top-level academic records in school. The initial combination of a transient deep dyslexia and subsequent rapid recovery from aphasia will be discussed with reference to theories on right hemisphere reading in deep dyslexia and inter-hemispheric linguistic transferability. Results of functional magnetic resonance spectroscopy taken during speech stimulation one year post onset do not support the notion that rapid recovery in this case of childhood aphasia was due to a right hemisphere take-over of language.
INTRODUCTION DYSLEXIAS AND APHASIAS acquired during childhood have so far rarely been studied within the paradigm of cognitive neuropsychology . One particularly interesting exception is a case report by Patterson et al. [ 1] . The patient showed the typical symptoms of deep dyslexia after a left hemidecortication during puberty, when questions of cerebral plasticity are no longer relevant for interpretation [ 1 ] . The patient’s reading profile after removal of the left hemisphere could be explained in terms of damage to the non-lexical and lexical phonological components of the reading system, whereas the isolated right hemisphere was apparently capable of semantically processing high frequency nouns. Since in pre-adolescents the language substrate may be less fixed and may be even equipotentially available in both hemispheres [ 2,3] , patterns of preserved and impaired linguistic performance might not map straightforwardly onto components of normal processing models. In fact, the study of organically caused aphasia in children has been restricted almost exclusively to questions of cerebral plasticity, which has variously been reported to end between the ages of 1 and 15 years. Major issues were the incidence (rarer than in adults [4]), the lesion side (more crossed aphasias [ 51) and the course of recovery (rapid, spontaneous, and age-related [2]). None of these conclusions have remained unequivocal, however. Aphasia in children, it was argued, is only apparently rarer because the etiologies (vascular and neoplastic) leading to the relevant lesions occur less frequently [6,7] , crossed aphasia in right-handed children is as rare as in adults [ 7,8] and the course of recovery of childhood
Address for correspondence: Prof. Dr. R. De Bleser, Cognitive Neurolinguistics, Institute of Linguistics, Potsdam University, PF 601553, D-14415 Potsdam, Germany. 9
10
R.
DE BLESER ef al.
aphasias seems to depend on variables such as etiology and lesion size more so than on age [9, lo]. Thus, the data from childhood aphasia apparently supported theories of genetically endowed left-hemispheric linguistic specialization [ 111 rather than cerebral equipotentiality . At the same time, studies of children with developmental dyslexia in single cases [ 121 and in larger samples [ 131 identified performance profiles (surface or phonological dyslexia) which corresponded to those of acquired disorders in adults. This suggested that patterns of developmental dyslexia in pre-adolescents could be explained with reference to a normal (adult) modular model of reading and that specific components of the system were not acquired adequately. Since a cognitive approach to childhood impairments of language did not seem to be marred by issues of cerebral plasticity, it was used as a framework for the present case study.
METHOD Subject
BV is a right-handed Belgian boy who had normally acquired Flemish as his first language and French as a second language, and who obtained good grades in school. At 8.5 years of age, he was found on the bedroom floor early in the morning with right hemiplegia, right-sided facial paralysis and aphasia. A first tentative neurological diagnosis of migraine accompagn& in the local Belgian hospital was rejected the next day when a CT-scan showed a large left-hemispheric vascular lesion in the territory of the middle cerebral artery. Two days after onset, the patient was transferred to the neuropediatric clinic in Aachen, Germany. Transfemoral angiography revealed a subtotal embolic occlusion of the right internal carotid artery and an embolism (approximately 1 cm) of the left middle cerebral artery suspected to be of cardial origin, However, subsequent cardiological examinations showed no abnormalities, so that the cause for the embolism remained unknown. The patient still presented with right hemiplegia, facial paralysis, and aphasia. The CT-scan three days post onset showed low density areas in the left basal ganglia, the frontal operculum, and the subcortical precentral area. Figure la shows the angiography taken at 2 days post onset, Fig. lb the CT-lesion at 3 days post onset. Aphasia screening
The patient’s language was examined informally during the first and second weeks post onset. Whereas BV’s spontaneous speech was initially restricted to “Yes”, he was able to express himself quite well three days later with the assistance of the examiner, although speech production was sparse, with simplified syntax and characterized by severe word finding problems, occasional semantic paraphasias, frequent phonemic paraphasias but no dysarthric signs. Phonemic errors were also predominant in the patient’s repetition and picture naming. Communicative comprehension seemed to be relatively well preserved. The patient’s reading aloud was seriously defective and he often produced words which were semantically but not phonologically similar to the target. BV’s language impairment was formally examined with the Dutch version of the Aachen Aphasia Test (Dutch AAT [ 141) at three weeks post onset when the patient was still on the ward. He was reexamined after discharge at 1.5 months and 4.5 months post onset. Samples of spontaneous speech in Flemish (Belgian Dutch) at the three testing sessions are given in Appendix 1 with their approximate English translations. The results of the three AATexaminations are given in Table 1. The patient was clearly aphasic at time 1 (3 weeks) and time 2 (1.5 months post onset) in spontaneous speech as well as in the AAT-subtests. However, at time 2, phonemic paraphasias had all but disappeared, so that there was a significant improvement of repetition and reading aloud. The major symptom in spontaneous speech was still its spars@ and the presence of frequent pauses due to word finding problems. At time 3 (4.5 months post onset), there were no longer any obvious aphasic symptoms in spontaneous speech nor in the subtests of the AAT. The only impaired performance was found in writing to dictation. However, since BV could string together letter blocks into dictated words and morpheme blocks into sentences, the mild impairment in handwriting dictated words and sentences was likely due to motor difficulties in writing with the hemiplegic right hand. On the Edinburgh dexterity questionnaire, BV was an outspoken righthander and he refused to use his left hand for writing after his stroke, although he now used the non-dominant hand for pointing and other manipulations. Given the boy’s frustration about his spastic hand, writing was not further examined in the psycholinguistic testing reported below.
RAPID
RECOVERY
OF APHASIA
AND
DEEP DYSLEXIA
Fig. la. Transfemoral angiography 2 days post onset showing (top) a subtotal embolic occlusion of the right internal coratis with collateralization of the right middle cerebral artery via the anterior Ramus corn, nunicans and (bottom) an embolic occlusion of approximately 1 cm in the anterior main branch of the left middle cerebral artery.
R. DE BLESERet al. Table 1. BV: AAT results (percentiles) Time post onset
Time 1 3 weeks
Time 2 1.5 months
Time 3 4.5 months
Token test
65
74
93*$
Repetition (phones, words, sentences)
51
14*
95*1
Reading/writing (words, sentences)
33
63*
87*$
Naming (objects, colours, scenes)
12
94
99*p
Comprehension (auditory: words/sentences) (reading: words/sentences)
75
79
98*$
*Significant difference between time 1 and 2 and/or 2 and 3. %Significantdifference between time 1 and 3.
PSYCHOLINGUISTIC ASSESSMENT OF SPOKEN AND WRITTEN WORD AND NONWORD PROCESSING In order to investigate BV’s language impairments in more detail, selected parts of the Dutch version of the PALPA test [ 151 were administered at all three sessions. The PALPA is an instrument for psycholinguistic assessment of language processing in aphasia based on the logogen model. This model was originally developed to account for experimental results on word reading by normal subjects and aphasic patients [ 16, 171, but later versions included word processing in repetition, writing to dictation, and oral and written picture naming [ 18-231. The version of the logogen model used in the PALPA is depicted in Fig. 2. The model makes a distinction between receptive and productive word form stores, and it assumes that written language does not depend on spoken language but that it is processed in a functionally independent system. Thus, modality-specific impairments are predicted such as preserved auditory but impaired visual lexical decision if only the graphemic input lexicon is impaired. The lexica are interconnected with each other and-in this version of the modelwith a central semantic component. It contains meaning structures without their corresponding word forms. The connections between the lexica and the semantic system allow that word forms are mapped with their meaning as is required, for example, in auditory or visual word-topicture matching and in oral or written naming. In addition to the lexical word processing systems, the logogen model adopts non-lexical systems for the segmental processing of auditory and graphemic stimuli. As nonwords do not have a lexical entry, they can only be processed in this way. The segmental processing of words and nonwords in repetition is based on auditory-phonological conversion (APC), in reading aloud on grapheme-phoneme conversion rules (GPC) and in writing to dictation on phonemegrapheme conversion rules (PGC). Lexical as well as non-lexical processing of words and neologisms are based on prelexical pattern recognition processes for the perception, identification and categorization of linguistic elements. There are two modality-specific analysis systems, one for auditory-phonological analysis, the other for visual-graphemic analysis. Auditory and visual discrimination tests of word pairs and nonword pairs examine the functioning of the auditory and visual analysis systems, respectively. The material consisted of 36 identical pairs of monosyllabic CVC-stimuli (e.g., nonwords: peit/peit; words: pihpil) randomized with 36 pairs of items having a minimal difference either initially (e.g., pef/def), finally (e.g., pit/pil), or as a metathesis (e.g., peit/teip) (12 items each). The patient’s task was
RAPID
Fig. lb. CT-scan
RECOVERY
OF APHASIA
AND
13
DEEP DYSLEXIA
3 days post onset showing low density areas in the left basal ganglia, operculum and the subcortical precentral area.
the frontal
to decide whether they were the same. BV made no errors in any of the sessions. The paradigm of lexical decision examines the functioning of the phonological and graphemic input lexicon. Eighty words and 80 nonwords were presented randomly, and the patient had to decide whether the stimulus was a word. Word-items were systematically varied for frequency and concreteness, and the nonwords were derived by minimal substitutions. Results for auditory and visual lexical decision at the three testing times are given in Table 2. The patient was able to identify nonwords in all sessions and he could identify the 20 highfrequent concrete nouns from the beginning, but there was a clear effect both of frequency and of abstractness, so that low frequent abstract nouns (e.g., irritatie: “irritation”; “dogma”; “satire”, etc.) were seldom identified as words. The consistency of the reactions over the two modalities and across the three sessions make it plausible that these words did not yet belong to the boy’s premorbid passive vocabulary. It can thus be assumed that auditory and graphemic recognition of the words used in this set, i.e. access to the input lexica, was basically normal for the boy’s age.
R.
14
Spoken Word
DE BLESERet
al.
Written Word
Sub-Word Level Orthographic-toPhonological Conversion
Speech
Writing
Fig. 2. The logogen model of word processing.
In order to examine non-lexical segmental processing, nonwords of different lengths were presented for reading and repetition. The reading material consisted of stimuli with 3, 4, 5 and 6 letters, the repetition material of stimuli with 1, 2 or 3 syllables. The results for the different testing times are given in Table 3a. At time 1, the boy was unable to read any nonword and he produced no response, but from test time 2 onwards his performance was normal. Repetition of nonwords was in principle possible from the very beginning but it was characterized by phonemic paraphasias (responses are given in Appendix 2), which were hardly present any more at time 2. At no time was there any effect of length which would have indicated impaired memory as a possible cause of phonemic paraphasias. Words with the same characteristics as the nonwords and minimally differing from them were also presented for reading and repetition. The results are given in Table 3b. Repetition at time 1 is characterized by phonemic paraphasias (see Appendix 2) without length effect for words as well as nonwords and there was no difference between the two sets of items. Such a difference did show up in reading, however. In contrast to his nonword reading at time 1, the patient was able to read some words correctly, and he produced semantic
RAPID
RECOVERY
OF APHASIA
Table 2. BV: lexical decision: (Number
AND DEEP DYSLEXIA
auditory
and visual
Auditorv
correct)
15
Visual
Words (n = 80) C/H (n = 20)
Time I Time 2 Time 3
19 20 20
19 20 20
C/L (n = 20)
Time I Time 2 Time 3
13 14 14
12 13 14
A/H (n = 20)
Time I Time 2 Time 3
12 13 13
12 13 I3
A/L (n = 20)
Time I Time 2 Time 3
6 7 6
7 6 5
Nonwords (n = 80)
Time 1 Time 2 Time 3
76 78 78
75 76 16
Words: C/H: Concrete/High frequency: school (school) C/L: Concrete/Low frequency: bijl (axe) A/H: Abstract/High frequency: daad (deed) A/L: Abstract/Low frequency: smart (pain) Non words: sprool, bijf, died, smalt
Table 3a. BV: nonwords
varying in length: reading versus repetition (number correct)
Reading Time 1 Errors: omissions Time 2 Time 3
3 (kos) 016
4 (wank) 016
5 (proet) 016
6 (blaans) 016
616 516
516 616
616 616
516 616
Repetition Time 1 Errors: phonological Time 2 Time 3
I (prink) 6110
2 (wuiten) 7110
3 (anito) 6110
9110 IO/IO
lo/lo lo/lo
9110 IO/l0
Number of letters
Number of syllables
errors to the other items (see Appendix 3), not zero-responses as in the case of nonwords. Obviously, three weeks post onset the patient could process written words semantically but he was unable to process graphemic stimuli segmentally, even though the graphemic analysis system itself was unaffected (see “discrimination” above). Individual letter naming examined by means of upper case and lower case letters was also impossible at time 1. At time 2, the characteristic features of so-called deep dyslexia-the inability to read nonwords and the production of semantic paralexias to words-were no longer apparent. The boy now also named 22/26 single letters consistently in the set of upper and lower case letters, and at time 3 he had normal performance for letter naming as well as word and nonword reading.
R.
DE
BLESER et al.
Table 3b. BV: nouns varying in length: reading versus repetition (number correct) Number of letters Reading Time 1 Errors: semantic Time 2 Time 3
3 (kop) 316
4 (wand) 216
5 (broek) 216
6 (straat) 216
616 616
616 616
616 616
516 616
Repetition Time 1 Errors: phonological Time 2 Time 3
1 (brood) 7110
2 (kamer) 6/10
3 (arena) 6/10
9/10 10/10
IO/10 10/10
lO/lO 10/10
Number of syllables
In order to further examine lexical variables in the patient’s reading impairment, the words of the auditory and visual lexical decision tasks, which were controlled for frequency and concreteness, were also presented for reading and repetition. Table 4 gives the results. In contrast to lexical decision, there were clear modality-specific differences at time 1. On the whole, repetition was better preserved than reading and was characterized by phonemic paraphasias. Reading errors were exclusively semantic for high frequency concrete nouns (see Appendix 3). The low-frequent and/or abstract nouns which were identified in lexical decision also triggered semantic paralexias, whereas no response occurred in reading the misidentified items. There was no such effect of frequency and abstractness in word repetition, suggesting that word repetition used the non-lexical APC-procedures in addition to the lexical ones. By test time two, the phonemic paraphasias in repetition had seriously decreased, and the semantic errors in reading had disappeared in favour of correct responses even in the case of still misidentified low frequent abstract words. This indicates a refunctioning of the non-lexical reading route at time 2. Performance at test time three was normal in all respects. Access to semantics from the input lexica was examined by means of a synonym decision task as well as an auditory and a reading comprehension task requiring that a word be matched to one of four pictures. Table 4. BV: reading versus repetition frequency and concreteness
Repetition
Reading Correct
of nouns:
Semant.
0
Correct
Phonol
-
14 18 20
6 2 -
7 4
12 19 20
8 1 -
C/H
Time 1 Time 2 Time 3
9 20 20
11 -
C/L
Time 1 Time 2 Time 3
6 16 20
-
Time 1 Time 2 Time 3
4 17 20
-
8 3 -
13 17 20
7 3 -
Time 1 Time 2 Time 3
17 18
-
20 3 2
15 17 20
5 3 -
A/H
A/L
7 8
RAPID
RECOVERY
OF APHASIA
AND DEEP DYSLEXIA
17
The synonym decision task consisted of 60 pairs of words, 30 synonyms and 30 semantically unrelated stimuli. In each set, 15 pairs were highly imageable and 15 were of low imageability. The stimuli were randomized and presented in auditory and written form in different sessions. The patient’s performance on synonym judgement at all three testing sessions was perfect in both versions for highly imageable pairs (e.g., “oceaan’‘-“zee”: ocean-sea versus “oceaan”-“gift”: ocean-present). A few errors (between 3-5/15) merely occurred for low imageable synonyms in both modes of presentation which were classified by BV as nonsynonymous (e.g., “vergiffenis’‘-“gratie”: forgiving-pardon). As with low frequent abstract nouns in lexical decision, the items triggering errors were consistent over modalities and test sessions, so that it is likely that BV did not have premorbid knowledge of these words and their meanings. The auditory and visual word-to-picture matching tasks contained one target picture and three distracters, which were either semantically, phonologically or visually similar to the target. Since not all of the concrete items of the lexical decision task could be adequately drawn or had unanimous name agreement, a different set of 40 concrete nouns, 20 high and 20 low frequency ones, was selected in the comprehension tasks. The patient’s performance was errorless in both modalities on all three sessions. Thus, the semantics of concrete nouns could be accessed from both input lexica already at time 1. The drawings of the 40 target items were also used in oral naming of pictures, which investigates access to the phonological output lexicon from semantics. Table 5 summarizes the results. As in the repetition tasks at time 1, there was no frequency effect in oral naming either. Nearly half of the responses in each frequency set were phonemic paraphasias which were always close to the target. They had almost disappeared at time 2, and performance was normal at time 3. A further reading and repetition task examined BV’s performance on words belonging to different parts of speech. Patients with so-called deep dyslexia are reported to show a hierarchy in their reading, with nouns being read better than adjectives and verbs, and function words are affected most severely. The material consisted of 20 nouns, 20 adjectives, 20 verb infinitives, and 20 function words which were controlled for syllable number (from 1 to 4) and frequency (7 high frequent, 13 low frequent items in each set), and the different parts of speech were randomized. Table 6 summarizes the results. There was no obvious part of speech effect in reading or repetition at any testing time. This was hardly possible in reading at time 1, given the low level of correct performance. However, there was a qualitative difference in the reading errors. BV was unable to read any function word and did not produce a response even to the 7 highly frequent items. 417 high frequency nouns and 317 verbs were read correctly. Due to the high proportion of relatively low frequent Table 5. BV: oral picture naming: Correct
frequency Phonemic
High frequent (n = 20) Time 1 Time 2 Time 3
12 17 20
8 3 -
Low frequent Time 1 Time 2 Time 3
11 18 20
9 2 -
(n = 20)
R. DE BLESER et al.
18
Table 6. BV: different parts of speech: reading versus repetition
(number correct)
Reading Noun e.g.
hemel bescheidenheit
Time 1 Errors:
Adject.
Verb inf.
Functor
heftig ondergeschikt
hangen financieren
heen integendeel
O/20
s/20
O/20
16/20 18/20
15120 18120
16120 17120
14120 17120
13120
14120
13120
13120
17120 19120
16120 18120
16120 19120
18120 20120
4120 omissions/semantic
Time 2 Time 3
Repetition Time 1 Errors: Time 2 Time 3
phonological
(and abstract) items in the lists, there were rather few semantic paralexias and many omissions for all content words. The semantic paralexias always preserved the syntactic category of the target (see Appendix 3). Reading had significantly improved for all parts of speech by test times 2 and 3, and the paralexias were now restricted to some visual/phonemic errors for low frequency abstract items The (e.g., meermalen: “often” +meer halen: fetch more; prioriteit “priority+poriteit). phonemic errors in repetition significantly decreased between test times 1 and 2. To summarize: BV’s oral speech output in spontaneous speech, word and nonword repetition and oral naming was characterized by phonemic errors at 3 weeks post onset. Such errors did not occur in reading tasks, where BV’s output was phonologically correct but semantic paralexias were produced to highly frequent concrete nouns, whereas nonwords, function words, as well as low frequent abstract words led to omissions. These deep dyslexic symptoms disappeared at such a pace that 1.5 months post onset BV was able to read words and nonwords almost perfectly. By that time, the phonological impairment in speech had also recovered.
DISCUSSION The pattern of linguistic impairment and recovery of BV following a left hemisphere stroke during childhood suggests that the phonemic difficulties in speech in the period immediately following the stroke resulted from BV’s quite extensive left hemisphere lesion, and that the semantic responses to graphemic stimuli were given by his healthy right hemisphere. The subsequent rapid recovery could certainly not be accounted for by the assumption of the so-called “displacement mechanism” [ 241. This assumption proposes that, if certain cortical areas in the immature brain are still functionally uncommitted, they may receive the functions of a committed but damaged area. However, BV’s recovery was too rapid to have involved relearning. Another assumption is that rapid recovery in childhood aphasia may be due to the bilateral representation of linguistic functions in children and the “inhibitory release mechanisms” [25] . According to this assumption, the right hemisphere has been learning language during a critical period but could not express itself due to inhibitory effects from the dominant left hemisphere. Upon damage to this hemisphere, the right hemisphere is allowed to demonstrate its linguistic abilities.
RAPID RECOVERYOF APHASIA AND
DEEP DYSLEXIA
19
In the case of BV, the right hemisphere release account was all the more attractive because the initial deep dyslexia seemed to show the generally noninhibited right hemisphere semantic functions [ 1 ] whereas it was only set free to process phonology at a later stage. If this were an adequate account of BV’s recovery pattern, functional MRI-imageing, for example, should show predominantly right-hemisphere activation during linguistic tasks such as verb generation. In order to verify this prediction, BV was given such an examination one year post-onset. The results are given in Fig. 3. Subtraction of activation during the resting stage from that during verb generation showed increased activation only in the left hemisphere, namely, in the left fronto-temporal area adjacent to BV’s chronic lesion. This suggests that his rapid recovery was due to intrahemispheric rather than interhemispheric plasticity and that, after a brief period of right hemisphere language production with semantic paralexias and phonemic paraphasias, the left hemisphere-though lesioned in the language relevant areas-had regained linguistic control. Acknowledgemenrs-The Dr. med. F. Kotlarek,
authors wish to acknowledge Dr. J. Reul, Department Department of Neuropediatrics, Aachen.
of Neuroradiology,
Aachen, and Prof.
REFERENCES PATTERSON, K., VARGHA-KHADEM, F. and POLKEY, CH.E. Reading with one hemisphere. Bruin 112, 39-63, 1989. BASSER, L. S. Hemiplegia of early onset and the faculty of speech with special reference to the effects of hemispherectomy. Bruin 85, 427-460, 1962. LENNEBERG, E. H. Biological Founaiztions of Language. Wiley, New York, 1967. DENCKLA, M. Childhood learning disabilities. In Cfinicui Neuropsychology, K. HEILMAN and E. VALENSTEIN (Editors). Oxford University Press, New York, 1979.
Fig. 3. Functional MRI-activation during verb generation compared to resting taken 1 year post onset shows increased left fronto-temporal activity in the neighbourhood of the signal-reduced lesion.
R. DE BLESER et al.
20
9. 10. 11. 12. 13. 14. 15. 16. 17. 18.
19. 20. 21. 22. 23. 24. 25.
HI?CAEN, H. Language representation and brain development. In Brain, Feral and Infant, S. R. BERENBERG (Editor). Martinus Nijhoff, The Hague, 112-123, 1976. HEILMAN, K. and VALENSTEIN, E. Clinical Neuropsychology. Oxford University Press, New York, 1979. SATZ, P. and BULLARD-BATES, C. Acquired aphasia in children. In Acquired Aphasia, M. TAYLOR SARNO (Editor). Academic Press, New York, 1981. DENNIS, M. and WHITAKER, H. A. Hemispheric equipotentiality and language acquisition. In Language Development and Neurological Theory, S. J. SEGALOWITZ and F. A. GRUBER (Editors). Academic Press, New York, 1977. VAN Dongen, H. R. and LOONEN, M.C. Neurological factors related to prognosis of acquired aphasia in childhood. In Recovery in Aphasics, Y. LEBRUN and R. Hoops (Editors). Swets and Zeitlinger, Amsterdam, 1979. ST. JAMES ROBERTS, I. A reinterpretation of hemispherectomy data without functional plasticity of the brain. I. Intellectual function. Bruin and Language 13, 31-53, 1981. GALABURDA, A. M., LE MAY, M., KEMPER, T. L. and GESCHWIND, N. Right-left asymmetries in the brain. Structural differences between the hemispheres may underlie cerebral dominance. Science 199, 852-857, 1978. TEMPLE, C. M. Developmental analogues to acquired phonological dyslexia. In Dyslexia: A Global Issue, R. N. MALATESHA and H. A. WHITAKER (Editors). Martinus Nijhoff, The Hague, 1984. CASTLES, A. and COLTHEART, M. Varieties of developmental dyslexia. Cognirion 47, 149-180, 1993. GRAETZ, P., DE BLESER, R. and WILLMES, K. Akense Afasie Test. Nederlandstalige Versie. Swets & Zeitlinger, Lisse, 1992. KAY, J., LESSER, R. and COLTHEART, M. Psycholinguistic Assessment of Language Processing in Aphasia (PALPA). Lawrence Erlbaum, London, 1992. MORTON, J. A functional model for memory. In Models of Human Memory, D. A. NORMAN (Editor). Academic Press, New York, 1970. MORTON, J. Word recognition. In Psycholingistic Series, Vol. 2, J. MORTON and J. C. MARSHALL (Editors). Elek Science, London, 1979. MORTON, J. Facilitation in word recognition: Experiments causing change in the logogen model. In Processing of Visible Language, Vol. 1, P. A. KOLERS, M. WROLSTADand H. BOUMA (Editors). Plenum Press, New York, 1979b. MORTON, J. The logogen model and orthographic structure. In Cognitive Processes in Spelling, U. FROTH(Editor). Academic Press, London, 1980a. MORTON, J. Two auditory parallels to deep dyslexia. In Deep Dyslexia, M. COLTHEART, K. E. PATTERSONand J. C. MARSHALL (Editors). Routledge & Kegan Paul, London, 198Ob. NEWCOMBE, F. and MARSHALL, J. Transcoding and lexical stabilization. In Deep Dyslexia, M. COLTHEART, K. PATTERSONand J. C. MARSHALL (Editors). Routledge & Kegan Paul, London, 1980. ELLIS, A. W. Reading, Writing and Dyslexia: A Cognitive Analysis. Lawrence Erlbaum, London, 1984. PATTERSON, K. E. Acquired disorders of spelling. In Perspectives on Cognitive Neuropschology, G. DENES, C. SEMENZA and P. BISSIACHI (Editors). Lawrence Erlbaum, London, 1988. GOLDMAN, P. S. Functional development of the prefrontal cortex in early life and the problem of neuronal plasticity. Experimental Neurology 32, 366-387, 1972. Geschwind, N. Disorders of the higher cortical function in children. Clinical Proceedings of the Children’s Hospital 28, 261-272, 1972.
APPENDIX 1: SAMPLES OF SPONTANEOUS SPEECH OF BV fime I-3
weeks post onset
(Do you have any sisters or brothers?) Ehm ehm .ja. ik . heb. broekjes (phon. for “broertjes”) ehm Uhm uhm. .yes. . .I. have, .panties (phon. for “little brothers”) uhm. uhm . sisters. (How many?) Ehm .een. twee .O .dina Olila. Olifia (phon. for “Olivia”) uhm... Uhm.. .one...two...O.dina...Olila.Olifiaand
ehm
.zussen.
en ehm . .
(What do you like to eat?) Ehm. .ehm. .nopporn ehm. .ehm. .popporn .popcom ehm . .das alles. Uhm uhm. nopporn uhm uhm. .popporn .popcom uhm. .that is all. (What do you do in school?) Ehm.. .ik.. . “kuster” ehm “knustel” (phon. for “knutsel”) dikwijls en. “neken” (phon. for “teken”) ehm .ehm. .das alles. Uhm.. .I. (phon. for “knutsel”: work at hobby). often and. (phon. for draw) uhm.uhm. .that is all.
RAPID
Time 2-2.5
RECOVERY OF APHASIA AND DEEP DYSLEXIA
21
months post onset
(What do you do during the day?) Ja ehm.
mijn.
kleren aandoen, en dan naar beneden gaan.
.ehm.
Yes uhm. put on. .my .clothes and then go down. .uhm. . dan .ehm boterhammetjes eten .en .ehm .en dan. met de lego spelen en then .uhm. .eat sandwiches .and.uhm. .and then.pIay with the lego.and dan. ehm ehm. met. .de het auto naar het ziekenhuis. rijden .en dan. then.uhm. .uhm. .ride. .in. the. the car to the hospital.and then. en. ik heb. schoon (phon. for “school”). kine. ergo .en .dan eten. and. I have. pretty (phon. for “school”). physio .ergo .and. then eat. (What is the name of your sisters and what do they do?) ehm. Bieke en Olivia en ehm. ze zijn lief en. .ehm. van van ehm uhm. Bieke and Olivia and. uhm. they are cute. and. uhm. this this uhm van .morgen vanmorgen ehm. hebben .ze. .ehm. .ik opgestaan en this. morning this morning uhm. they. got. uhm. I woken up and naar moeke geweest .ehm want. ik moet vroeg opstaan .omdat ehm. gone to. mommy. uhm. because 1 have to get up early. .because uhm. naar hier te komen en ehm en. Olivia en Bieke hebben ook opgestaan en come here. and uhm and. Olivia and Bieke. have. also got up. and ehm naar beneden gekomen om. 7 uur nee nee ehm .6 uur. uhm come downstairs. at. 7 o’clock no no uhm .6 o’clock.
Time 3-4.5
months post onset
(What do you do in the rehabilitation centre during the day?) Eerst naar school gaan. .rekenen en taal .en dan.naar de kine. First go to school. mathematics and language .and then in physio. oefeningen doen. en dan. naar ergo. en dan knutselen do exercises.and then. in ergo. and then practice hobbies. (How was the party last weekend?) Ehm mijn familie is gekomen en. ‘K heb 6en boot gekregen en. Uhm my family came and. .I have received a boat.and. ‘k heb dermee in de vijver gevaren.en w’hebben spagetti en w’hebben I went with it on the lake. and we had. spaghetti and we played gevoetbald met Anton. mijn neef. maar hij is nog een beetje klein. hij is twee jaar. football with Anton. my cousin. but he is still somewhat little. he is two years old.
APPENDIX
2: PHONEMIC
PARAPHASIAS
Nonwords (different syllable number)
Target
Target
splu:t jarst sxreip Ra:rt
spru:t jast stre:p fena:
sxil fluit sma: k
sxin fruit smak
to:per lorde hike1
toper lonke hindel
ho’tel bo:ter kerel a:vont
ke’tel boter kegel na:vo
e:gula: eilium inima: 0te:ra
e:kladi: e:der anika: ame:rika:
0:pera: opium are:na: hie:na
rapata: pius re:ka:ra: hie:sa
3: SEMANTIC
List of words varying in letter number mes (knife): vork (fork)
AT TIME
Words (different syllable number)
Target
APPENDIX
IN REPETITION
PARALEXIAS
IN READING
AT TIME
1
1
22
R. DE BLESERet al.
wet (law): politie (police) bes (berry): kriek (cherry) wand (wall): muur (wall) neef (nephew): broer (brother) nier (kidney): lever (liver) boom (tree): stam (trunk) broek (trousers): kleed (dress) spun (waterhose): water plein (market place): markt (market place) kunst (art): schilderij (painting) strand (beach): zee (sea) herfst (autumn): seizoen (season) straat (street): weg (street) vrucht (fruit): appel (apple)
List of words varying in frequency and concreteness Target: high frequent, concrete: ziekenhuis (hospital): kliniek (clinic) kamer (room): zaal (room) fiets (bicycle): velo (bicycle) zomer (summer): zon (sun) pastoor (priest): kerk (church) bodem (floor): vloer (floor) kerk (church): mis (mass) koffie (coffee): melk (milk) dorp (village): stad (town) rommel (junk): afval (garbage) blad (leaf): boom (tree)
Target: high frequent, abstract: ding (thing): zaak (object) idee (idea): gedacht (thought) opleiding (education): school (school) moment (moment): vandaag (today) toekomst (future): morgen (tomorrow) behoefte (need): nood (need) dood (death): sterven (die) voorbeeld (model): braaf (good)
Target: low frequent, concrete: elleboog (elbow): arm (arm) kever (beetle): beest (beast) snavel (beak): mond (mouth) patat (patatoe): fritten (French fries) pil (pill): doktor (doctor) wortel (carrot): peeke (carrot) giraffe (giraffe): dier (animal)
List of words of different part of speech Target noun: mens (person): man (man) toneel (theater): theater verdriet (unhappiness): tranen (tears) komkommer (cucumber): groente (vegetable)
Target verb: drijven (float): zwemmen (swim) stinken (stink): rieken (smell) binden (tie); toedoen (close)
Target adjective: groot (big): lang (tall) vrolijk (happy): gelukkig (happy) verkeerd (wrong): mis (wrong) lekker (tasty): goed (good)
J. Neurolinguistics, Vol. 9, No. 1, pp.9-22, 1995 Copyright0 1995 Elscvierscience Ltd Printedin GreatBritain.All rightsmewed 0911~m/95 $9.50+0.00
RAPID RECOVERY OF APHASIA AND DEEP DYSLEXIA AFTER CEREBROVASCULAR LEFT-HEMISPHERE DAMAGE IN CHILDHOOD R. DE BLESER,* J. FAISS~ and M. SCHWARZ$. *Departmentof Cognitive Neurolinguistics, Potsdam; TDepartmentof Neuroradiology, Essen; *Department of Neurology, Aachen, Germany Abstract-This paper reports a case of acquired language impairment in an 85year-old right-handed Belgian boy (BV). He had normally acquired his native language (Flemish/Belgian Dutch) as well as a second language (French), and he was a very good pupil in school. Following a vascular accident in the left hemisphere, the patient initially presented a pure pattern of deep dyslexia associated with a non-fluent aphasia with phonemic paraphasias. The deep dyslexic symptoms disappeared within six weeks, and the aphasic impairments were no longer observable after 4.5 months. One year after the cerehro-vascular accident, the boy reached top-level academic records in school. The initial combination of a transient deep dyslexia and subsequent rapid recovery from aphasia will be discussed with reference to theories on right hemisphere reading in deep dyslexia and inter-hemispheric linguistic transferability. Results of functional magnetic resonance spectroscopy taken during speech stimulation one year post onset do not support the notion that rapid recovery in this case of childhood aphasia was due to a right hemisphere take-over of language.
INTRODUCTION DYSLEXIAS AND APHASIAS acquired during childhood have so far rarely been studied within the paradigm of cognitive neuropsychology . One particularly interesting exception is a case report by Patterson et al. [ 1] . The patient showed the typical symptoms of deep dyslexia after a left hemidecortication during puberty, when questions of cerebral plasticity are no longer relevant for interpretation [ 1 ] . The patient’s reading profile after removal of the left hemisphere could be explained in terms of damage to the non-lexical and lexical phonological components of the reading system, whereas the isolated right hemisphere was apparently capable of semantically processing high frequency nouns. Since in pre-adolescents the language substrate may be less fixed and may be even equipotentially available in both hemispheres [ 2,3] , patterns of preserved and impaired linguistic performance might not map straightforwardly onto components of normal processing models. In fact, the study of organically caused aphasia in children has been restricted almost exclusively to questions of cerebral plasticity, which has variously been reported to end between the ages of 1 and 15 years. Major issues were the incidence (rarer than in adults [4]), the lesion side (more crossed aphasias [ 51) and the course of recovery (rapid, spontaneous, and age-related [2]). None of these conclusions have remained unequivocal, however. Aphasia in children, it was argued, is only apparently rarer because the etiologies (vascular and neoplastic) leading to the relevant lesions occur less frequently [6,7] , crossed aphasia in right-handed children is as rare as in adults [ 7,8] and the course of recovery of childhood
Address for correspondence: Prof. Dr. R. De Bleser, Cognitive Neurolinguistics, Institute of Linguistics, Potsdam University, PF 601553, D-14415 Potsdam, Germany. 9
10
R.
DE BLESER ef al.
aphasias seems to depend on variables such as etiology and lesion size more so than on age [9, lo]. Thus, the data from childhood aphasia apparently supported theories of genetically endowed left-hemispheric linguistic specialization [ 111 rather than cerebral equipotentiality . At the same time, studies of children with developmental dyslexia in single cases [ 121 and in larger samples [ 131 identified performance profiles (surface or phonological dyslexia) which corresponded to those of acquired disorders in adults. This suggested that patterns of developmental dyslexia in pre-adolescents could be explained with reference to a normal (adult) modular model of reading and that specific components of the system were not acquired adequately. Since a cognitive approach to childhood impairments of language did not seem to be marred by issues of cerebral plasticity, it was used as a framework for the present case study.
METHOD Subject
BV is a right-handed Belgian boy who had normally acquired Flemish as his first language and French as a second language, and who obtained good grades in school. At 8.5 years of age, he was found on the bedroom floor early in the morning with right hemiplegia, right-sided facial paralysis and aphasia. A first tentative neurological diagnosis of migraine accompagn& in the local Belgian hospital was rejected the next day when a CT-scan showed a large left-hemispheric vascular lesion in the territory of the middle cerebral artery. Two days after onset, the patient was transferred to the neuropediatric clinic in Aachen, Germany. Transfemoral angiography revealed a subtotal embolic occlusion of the right internal carotid artery and an embolism (approximately 1 cm) of the left middle cerebral artery suspected to be of cardial origin, However, subsequent cardiological examinations showed no abnormalities, so that the cause for the embolism remained unknown. The patient still presented with right hemiplegia, facial paralysis, and aphasia. The CT-scan three days post onset showed low density areas in the left basal ganglia, the frontal operculum, and the subcortical precentral area. Figure la shows the angiography taken at 2 days post onset, Fig. lb the CT-lesion at 3 days post onset. Aphasia screening
The patient’s language was examined informally during the first and second weeks post onset. Whereas BV’s spontaneous speech was initially restricted to “Yes”, he was able to express himself quite well three days later with the assistance of the examiner, although speech production was sparse, with simplified syntax and characterized by severe word finding problems, occasional semantic paraphasias, frequent phonemic paraphasias but no dysarthric signs. Phonemic errors were also predominant in the patient’s repetition and picture naming. Communicative comprehension seemed to be relatively well preserved. The patient’s reading aloud was seriously defective and he often produced words which were semantically but not phonologically similar to the target. BV’s language impairment was formally examined with the Dutch version of the Aachen Aphasia Test (Dutch AAT [ 141) at three weeks post onset when the patient was still on the ward. He was reexamined after discharge at 1.5 months and 4.5 months post onset. Samples of spontaneous speech in Flemish (Belgian Dutch) at the three testing sessions are given in Appendix 1 with their approximate English translations. The results of the three AATexaminations are given in Table 1. The patient was clearly aphasic at time 1 (3 weeks) and time 2 (1.5 months post onset) in spontaneous speech as well as in the AAT-subtests. However, at time 2, phonemic paraphasias had all but disappeared, so that there was a significant improvement of repetition and reading aloud. The major symptom in spontaneous speech was still its spars@ and the presence of frequent pauses due to word finding problems. At time 3 (4.5 months post onset), there were no longer any obvious aphasic symptoms in spontaneous speech nor in the subtests of the AAT. The only impaired performance was found in writing to dictation. However, since BV could string together letter blocks into dictated words and morpheme blocks into sentences, the mild impairment in handwriting dictated words and sentences was likely due to motor difficulties in writing with the hemiplegic right hand. On the Edinburgh dexterity questionnaire, BV was an outspoken righthander and he refused to use his left hand for writing after his stroke, although he now used the non-dominant hand for pointing and other manipulations. Given the boy’s frustration about his spastic hand, writing was not further examined in the psycholinguistic testing reported below.
RAPID
RECOVERY
OF APHASIA
AND
DEEP DYSLEXIA
Fig. la. Transfemoral angiography 2 days post onset showing (top) a subtotal embolic occlusion of the right internal coratis with collateralization of the right middle cerebral artery via the anterior Ramus corn, nunicans and (bottom) an embolic occlusion of approximately 1 cm in the anterior main branch of the left middle cerebral artery.
R. DE BLESERet al. Table 1. BV: AAT results (percentiles) Time post onset
Time 1 3 weeks
Time 2 1.5 months
Time 3 4.5 months
Token test
65
74
93*$
Repetition (phones, words, sentences)
51
14*
95*1
Reading/writing (words, sentences)
33
63*
87*$
Naming (objects, colours, scenes)
12
94
99*p
Comprehension (auditory: words/sentences) (reading: words/sentences)
75
79
98*$
*Significant difference between time 1 and 2 and/or 2 and 3. %Significantdifference between time 1 and 3.
PSYCHOLINGUISTIC ASSESSMENT OF SPOKEN AND WRITTEN WORD AND NONWORD PROCESSING In order to investigate BV’s language impairments in more detail, selected parts of the Dutch version of the PALPA test [ 151 were administered at all three sessions. The PALPA is an instrument for psycholinguistic assessment of language processing in aphasia based on the logogen model. This model was originally developed to account for experimental results on word reading by normal subjects and aphasic patients [ 16, 171, but later versions included word processing in repetition, writing to dictation, and oral and written picture naming [ 18-231. The version of the logogen model used in the PALPA is depicted in Fig. 2. The model makes a distinction between receptive and productive word form stores, and it assumes that written language does not depend on spoken language but that it is processed in a functionally independent system. Thus, modality-specific impairments are predicted such as preserved auditory but impaired visual lexical decision if only the graphemic input lexicon is impaired. The lexica are interconnected with each other and-in this version of the modelwith a central semantic component. It contains meaning structures without their corresponding word forms. The connections between the lexica and the semantic system allow that word forms are mapped with their meaning as is required, for example, in auditory or visual word-topicture matching and in oral or written naming. In addition to the lexical word processing systems, the logogen model adopts non-lexical systems for the segmental processing of auditory and graphemic stimuli. As nonwords do not have a lexical entry, they can only be processed in this way. The segmental processing of words and nonwords in repetition is based on auditory-phonological conversion (APC), in reading aloud on grapheme-phoneme conversion rules (GPC) and in writing to dictation on phonemegrapheme conversion rules (PGC). Lexical as well as non-lexical processing of words and neologisms are based on prelexical pattern recognition processes for the perception, identification and categorization of linguistic elements. There are two modality-specific analysis systems, one for auditory-phonological analysis, the other for visual-graphemic analysis. Auditory and visual discrimination tests of word pairs and nonword pairs examine the functioning of the auditory and visual analysis systems, respectively. The material consisted of 36 identical pairs of monosyllabic CVC-stimuli (e.g., nonwords: peit/peit; words: pihpil) randomized with 36 pairs of items having a minimal difference either initially (e.g., pef/def), finally (e.g., pit/pil), or as a metathesis (e.g., peit/teip) (12 items each). The patient’s task was
RAPID
Fig. lb. CT-scan
RECOVERY
OF APHASIA
AND
13
DEEP DYSLEXIA
3 days post onset showing low density areas in the left basal ganglia, operculum and the subcortical precentral area.
the frontal
to decide whether they were the same. BV made no errors in any of the sessions. The paradigm of lexical decision examines the functioning of the phonological and graphemic input lexicon. Eighty words and 80 nonwords were presented randomly, and the patient had to decide whether the stimulus was a word. Word-items were systematically varied for frequency and concreteness, and the nonwords were derived by minimal substitutions. Results for auditory and visual lexical decision at the three testing times are given in Table 2. The patient was able to identify nonwords in all sessions and he could identify the 20 highfrequent concrete nouns from the beginning, but there was a clear effect both of frequency and of abstractness, so that low frequent abstract nouns (e.g., irritatie: “irritation”; “dogma”; “satire”, etc.) were seldom identified as words. The consistency of the reactions over the two modalities and across the three sessions make it plausible that these words did not yet belong to the boy’s premorbid passive vocabulary. It can thus be assumed that auditory and graphemic recognition of the words used in this set, i.e. access to the input lexica, was basically normal for the boy’s age.
R.
14
Spoken Word
DE BLESERet
al.
Written Word
Sub-Word Level Orthographic-toPhonological Conversion
Speech
Writing
Fig. 2. The logogen model of word processing.
In order to examine non-lexical segmental processing, nonwords of different lengths were presented for reading and repetition. The reading material consisted of stimuli with 3, 4, 5 and 6 letters, the repetition material of stimuli with 1, 2 or 3 syllables. The results for the different testing times are given in Table 3a. At time 1, the boy was unable to read any nonword and he produced no response, but from test time 2 onwards his performance was normal. Repetition of nonwords was in principle possible from the very beginning but it was characterized by phonemic paraphasias (responses are given in Appendix 2), which were hardly present any more at time 2. At no time was there any effect of length which would have indicated impaired memory as a possible cause of phonemic paraphasias. Words with the same characteristics as the nonwords and minimally differing from them were also presented for reading and repetition. The results are given in Table 3b. Repetition at time 1 is characterized by phonemic paraphasias (see Appendix 2) without length effect for words as well as nonwords and there was no difference between the two sets of items. Such a difference did show up in reading, however. In contrast to his nonword reading at time 1, the patient was able to read some words correctly, and he produced semantic
RAPID
RECOVERY
OF APHASIA
Table 2. BV: lexical decision: (Number
AND DEEP DYSLEXIA
auditory
and visual
Auditorv
correct)
15
Visual
Words (n = 80) C/H (n = 20)
Time I Time 2 Time 3
19 20 20
19 20 20
C/L (n = 20)
Time I Time 2 Time 3
13 14 14
12 13 14
A/H (n = 20)
Time I Time 2 Time 3
12 13 13
12 13 I3
A/L (n = 20)
Time I Time 2 Time 3
6 7 6
7 6 5
Nonwords (n = 80)
Time 1 Time 2 Time 3
76 78 78
75 76 16
Words: C/H: Concrete/High frequency: school (school) C/L: Concrete/Low frequency: bijl (axe) A/H: Abstract/High frequency: daad (deed) A/L: Abstract/Low frequency: smart (pain) Non words: sprool, bijf, died, smalt
Table 3a. BV: nonwords
varying in length: reading versus repetition (number correct)
Reading Time 1 Errors: omissions Time 2 Time 3
3 (kos) 016
4 (wank) 016
5 (proet) 016
6 (blaans) 016
616 516
516 616
616 616
516 616
Repetition Time 1 Errors: phonological Time 2 Time 3
I (prink) 6110
2 (wuiten) 7110
3 (anito) 6110
9110 IO/IO
lo/lo lo/lo
9110 IO/l0
Number of letters
Number of syllables
errors to the other items (see Appendix 3), not zero-responses as in the case of nonwords. Obviously, three weeks post onset the patient could process written words semantically but he was unable to process graphemic stimuli segmentally, even though the graphemic analysis system itself was unaffected (see “discrimination” above). Individual letter naming examined by means of upper case and lower case letters was also impossible at time 1. At time 2, the characteristic features of so-called deep dyslexia-the inability to read nonwords and the production of semantic paralexias to words-were no longer apparent. The boy now also named 22/26 single letters consistently in the set of upper and lower case letters, and at time 3 he had normal performance for letter naming as well as word and nonword reading.
R.
DE
BLESER et al.
Table 3b. BV: nouns varying in length: reading versus repetition (number correct) Number of letters Reading Time 1 Errors: semantic Time 2 Time 3
3 (kop) 316
4 (wand) 216
5 (broek) 216
6 (straat) 216
616 616
616 616
616 616
516 616
Repetition Time 1 Errors: phonological Time 2 Time 3
1 (brood) 7110
2 (kamer) 6/10
3 (arena) 6/10
9/10 10/10
IO/10 10/10
lO/lO 10/10
Number of syllables
In order to further examine lexical variables in the patient’s reading impairment, the words of the auditory and visual lexical decision tasks, which were controlled for frequency and concreteness, were also presented for reading and repetition. Table 4 gives the results. In contrast to lexical decision, there were clear modality-specific differences at time 1. On the whole, repetition was better preserved than reading and was characterized by phonemic paraphasias. Reading errors were exclusively semantic for high frequency concrete nouns (see Appendix 3). The low-frequent and/or abstract nouns which were identified in lexical decision also triggered semantic paralexias, whereas no response occurred in reading the misidentified items. There was no such effect of frequency and abstractness in word repetition, suggesting that word repetition used the non-lexical APC-procedures in addition to the lexical ones. By test time two, the phonemic paraphasias in repetition had seriously decreased, and the semantic errors in reading had disappeared in favour of correct responses even in the case of still misidentified low frequent abstract words. This indicates a refunctioning of the non-lexical reading route at time 2. Performance at test time three was normal in all respects. Access to semantics from the input lexica was examined by means of a synonym decision task as well as an auditory and a reading comprehension task requiring that a word be matched to one of four pictures. Table 4. BV: reading versus repetition frequency and concreteness
Repetition
Reading Correct
of nouns:
Semant.
0
Correct
Phonol
-
14 18 20
6 2 -
7 4
12 19 20
8 1 -
C/H
Time 1 Time 2 Time 3
9 20 20
11 -
C/L
Time 1 Time 2 Time 3
6 16 20
-
Time 1 Time 2 Time 3
4 17 20
-
8 3 -
13 17 20
7 3 -
Time 1 Time 2 Time 3
17 18
-
20 3 2
15 17 20
5 3 -
A/H
A/L
7 8
RAPID
RECOVERY
OF APHASIA
AND DEEP DYSLEXIA
17
The synonym decision task consisted of 60 pairs of words, 30 synonyms and 30 semantically unrelated stimuli. In each set, 15 pairs were highly imageable and 15 were of low imageability. The stimuli were randomized and presented in auditory and written form in different sessions. The patient’s performance on synonym judgement at all three testing sessions was perfect in both versions for highly imageable pairs (e.g., “oceaan’‘-“zee”: ocean-sea versus “oceaan”-“gift”: ocean-present). A few errors (between 3-5/15) merely occurred for low imageable synonyms in both modes of presentation which were classified by BV as nonsynonymous (e.g., “vergiffenis’‘-“gratie”: forgiving-pardon). As with low frequent abstract nouns in lexical decision, the items triggering errors were consistent over modalities and test sessions, so that it is likely that BV did not have premorbid knowledge of these words and their meanings. The auditory and visual word-to-picture matching tasks contained one target picture and three distracters, which were either semantically, phonologically or visually similar to the target. Since not all of the concrete items of the lexical decision task could be adequately drawn or had unanimous name agreement, a different set of 40 concrete nouns, 20 high and 20 low frequency ones, was selected in the comprehension tasks. The patient’s performance was errorless in both modalities on all three sessions. Thus, the semantics of concrete nouns could be accessed from both input lexica already at time 1. The drawings of the 40 target items were also used in oral naming of pictures, which investigates access to the phonological output lexicon from semantics. Table 5 summarizes the results. As in the repetition tasks at time 1, there was no frequency effect in oral naming either. Nearly half of the responses in each frequency set were phonemic paraphasias which were always close to the target. They had almost disappeared at time 2, and performance was normal at time 3. A further reading and repetition task examined BV’s performance on words belonging to different parts of speech. Patients with so-called deep dyslexia are reported to show a hierarchy in their reading, with nouns being read better than adjectives and verbs, and function words are affected most severely. The material consisted of 20 nouns, 20 adjectives, 20 verb infinitives, and 20 function words which were controlled for syllable number (from 1 to 4) and frequency (7 high frequent, 13 low frequent items in each set), and the different parts of speech were randomized. Table 6 summarizes the results. There was no obvious part of speech effect in reading or repetition at any testing time. This was hardly possible in reading at time 1, given the low level of correct performance. However, there was a qualitative difference in the reading errors. BV was unable to read any function word and did not produce a response even to the 7 highly frequent items. 417 high frequency nouns and 317 verbs were read correctly. Due to the high proportion of relatively low frequent Table 5. BV: oral picture naming: Correct
frequency Phonemic
High frequent (n = 20) Time 1 Time 2 Time 3
12 17 20
8 3 -
Low frequent Time 1 Time 2 Time 3
11 18 20
9 2 -
(n = 20)
R. DE BLESER et al.
18
Table 6. BV: different parts of speech: reading versus repetition
(number correct)
Reading Noun e.g.
hemel bescheidenheit
Time 1 Errors:
Adject.
Verb inf.
Functor
heftig ondergeschikt
hangen financieren
heen integendeel
O/20
s/20
O/20
16/20 18/20
15120 18120
16120 17120
14120 17120
13120
14120
13120
13120
17120 19120
16120 18120
16120 19120
18120 20120
4120 omissions/semantic
Time 2 Time 3
Repetition Time 1 Errors: Time 2 Time 3
phonological
(and abstract) items in the lists, there were rather few semantic paralexias and many omissions for all content words. The semantic paralexias always preserved the syntactic category of the target (see Appendix 3). Reading had significantly improved for all parts of speech by test times 2 and 3, and the paralexias were now restricted to some visual/phonemic errors for low frequency abstract items The (e.g., meermalen: “often” +meer halen: fetch more; prioriteit “priority+poriteit). phonemic errors in repetition significantly decreased between test times 1 and 2. To summarize: BV’s oral speech output in spontaneous speech, word and nonword repetition and oral naming was characterized by phonemic errors at 3 weeks post onset. Such errors did not occur in reading tasks, where BV’s output was phonologically correct but semantic paralexias were produced to highly frequent concrete nouns, whereas nonwords, function words, as well as low frequent abstract words led to omissions. These deep dyslexic symptoms disappeared at such a pace that 1.5 months post onset BV was able to read words and nonwords almost perfectly. By that time, the phonological impairment in speech had also recovered.
DISCUSSION The pattern of linguistic impairment and recovery of BV following a left hemisphere stroke during childhood suggests that the phonemic difficulties in speech in the period immediately following the stroke resulted from BV’s quite extensive left hemisphere lesion, and that the semantic responses to graphemic stimuli were given by his healthy right hemisphere. The subsequent rapid recovery could certainly not be accounted for by the assumption of the so-called “displacement mechanism” [ 241. This assumption proposes that, if certain cortical areas in the immature brain are still functionally uncommitted, they may receive the functions of a committed but damaged area. However, BV’s recovery was too rapid to have involved relearning. Another assumption is that rapid recovery in childhood aphasia may be due to the bilateral representation of linguistic functions in children and the “inhibitory release mechanisms” [25] . According to this assumption, the right hemisphere has been learning language during a critical period but could not express itself due to inhibitory effects from the dominant left hemisphere. Upon damage to this hemisphere, the right hemisphere is allowed to demonstrate its linguistic abilities.
RAPID RECOVERYOF APHASIA AND
DEEP DYSLEXIA
19
In the case of BV, the right hemisphere release account was all the more attractive because the initial deep dyslexia seemed to show the generally noninhibited right hemisphere semantic functions [ 1 ] whereas it was only set free to process phonology at a later stage. If this were an adequate account of BV’s recovery pattern, functional MRI-imageing, for example, should show predominantly right-hemisphere activation during linguistic tasks such as verb generation. In order to verify this prediction, BV was given such an examination one year post-onset. The results are given in Fig. 3. Subtraction of activation during the resting stage from that during verb generation showed increased activation only in the left hemisphere, namely, in the left fronto-temporal area adjacent to BV’s chronic lesion. This suggests that his rapid recovery was due to intrahemispheric rather than interhemispheric plasticity and that, after a brief period of right hemisphere language production with semantic paralexias and phonemic paraphasias, the left hemisphere-though lesioned in the language relevant areas-had regained linguistic control. Acknowledgemenrs-The Dr. med. F. Kotlarek,
authors wish to acknowledge Dr. J. Reul, Department Department of Neuropediatrics, Aachen.
of Neuroradiology,
Aachen, and Prof.
REFERENCES PATTERSON, K., VARGHA-KHADEM, F. and POLKEY, CH.E. Reading with one hemisphere. Bruin 112, 39-63, 1989. BASSER, L. S. Hemiplegia of early onset and the faculty of speech with special reference to the effects of hemispherectomy. Bruin 85, 427-460, 1962. LENNEBERG, E. H. Biological Founaiztions of Language. Wiley, New York, 1967. DENCKLA, M. Childhood learning disabilities. In Cfinicui Neuropsychology, K. HEILMAN and E. VALENSTEIN (Editors). Oxford University Press, New York, 1979.
Fig. 3. Functional MRI-activation during verb generation compared to resting taken 1 year post onset shows increased left fronto-temporal activity in the neighbourhood of the signal-reduced lesion.
R. DE BLESER et al.
20
9. 10. 11. 12. 13. 14. 15. 16. 17. 18.
19. 20. 21. 22. 23. 24. 25.
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APPENDIX 1: SAMPLES OF SPONTANEOUS SPEECH OF BV fime I-3
weeks post onset
(Do you have any sisters or brothers?) Ehm ehm .ja. ik . heb. broekjes (phon. for “broertjes”) ehm Uhm uhm. .yes. . .I. have, .panties (phon. for “little brothers”) uhm. uhm . sisters. (How many?) Ehm .een. twee .O .dina Olila. Olifia (phon. for “Olivia”) uhm... Uhm.. .one...two...O.dina...Olila.Olifiaand
ehm
.zussen.
en ehm . .
(What do you like to eat?) Ehm. .ehm. .nopporn ehm. .ehm. .popporn .popcom ehm . .das alles. Uhm uhm. nopporn uhm uhm. .popporn .popcom uhm. .that is all. (What do you do in school?) Ehm.. .ik.. . “kuster” ehm “knustel” (phon. for “knutsel”) dikwijls en. “neken” (phon. for “teken”) ehm .ehm. .das alles. Uhm.. .I. (phon. for “knutsel”: work at hobby). often and. (phon. for draw) uhm.uhm. .that is all.
RAPID
Time 2-2.5
RECOVERY OF APHASIA AND DEEP DYSLEXIA
21
months post onset
(What do you do during the day?) Ja ehm.
mijn.
kleren aandoen, en dan naar beneden gaan.
.ehm.
Yes uhm. put on. .my .clothes and then go down. .uhm. . dan .ehm boterhammetjes eten .en .ehm .en dan. met de lego spelen en then .uhm. .eat sandwiches .and.uhm. .and then.pIay with the lego.and dan. ehm ehm. met. .de het auto naar het ziekenhuis. rijden .en dan. then.uhm. .uhm. .ride. .in. the. the car to the hospital.and then. en. ik heb. schoon (phon. for “school”). kine. ergo .en .dan eten. and. I have. pretty (phon. for “school”). physio .ergo .and. then eat. (What is the name of your sisters and what do they do?) ehm. Bieke en Olivia en ehm. ze zijn lief en. .ehm. van van ehm uhm. Bieke and Olivia and. uhm. they are cute. and. uhm. this this uhm van .morgen vanmorgen ehm. hebben .ze. .ehm. .ik opgestaan en this. morning this morning uhm. they. got. uhm. I woken up and naar moeke geweest .ehm want. ik moet vroeg opstaan .omdat ehm. gone to. mommy. uhm. because 1 have to get up early. .because uhm. naar hier te komen en ehm en. Olivia en Bieke hebben ook opgestaan en come here. and uhm and. Olivia and Bieke. have. also got up. and ehm naar beneden gekomen om. 7 uur nee nee ehm .6 uur. uhm come downstairs. at. 7 o’clock no no uhm .6 o’clock.
Time 3-4.5
months post onset
(What do you do in the rehabilitation centre during the day?) Eerst naar school gaan. .rekenen en taal .en dan.naar de kine. First go to school. mathematics and language .and then in physio. oefeningen doen. en dan. naar ergo. en dan knutselen do exercises.and then. in ergo. and then practice hobbies. (How was the party last weekend?) Ehm mijn familie is gekomen en. ‘K heb 6en boot gekregen en. Uhm my family came and. .I have received a boat.and. ‘k heb dermee in de vijver gevaren.en w’hebben spagetti en w’hebben I went with it on the lake. and we had. spaghetti and we played gevoetbald met Anton. mijn neef. maar hij is nog een beetje klein. hij is twee jaar. football with Anton. my cousin. but he is still somewhat little. he is two years old.
APPENDIX
2: PHONEMIC
PARAPHASIAS
Nonwords (different syllable number)
Target
Target
splu:t jarst sxreip Ra:rt
spru:t jast stre:p fena:
sxil fluit sma: k
sxin fruit smak
to:per lorde hike1
toper lonke hindel
ho’tel bo:ter kerel a:vont
ke’tel boter kegel na:vo
e:gula: eilium inima: 0te:ra
e:kladi: e:der anika: ame:rika:
0:pera: opium are:na: hie:na
rapata: pius re:ka:ra: hie:sa
3: SEMANTIC
List of words varying in letter number mes (knife): vork (fork)
AT TIME
Words (different syllable number)
Target
APPENDIX
IN REPETITION
PARALEXIAS
IN READING
AT TIME
1
1
22
R. DE BLESERet al.
wet (law): politie (police) bes (berry): kriek (cherry) wand (wall): muur (wall) neef (nephew): broer (brother) nier (kidney): lever (liver) boom (tree): stam (trunk) broek (trousers): kleed (dress) spun (waterhose): water plein (market place): markt (market place) kunst (art): schilderij (painting) strand (beach): zee (sea) herfst (autumn): seizoen (season) straat (street): weg (street) vrucht (fruit): appel (apple)
List of words varying in frequency and concreteness Target: high frequent, concrete: ziekenhuis (hospital): kliniek (clinic) kamer (room): zaal (room) fiets (bicycle): velo (bicycle) zomer (summer): zon (sun) pastoor (priest): kerk (church) bodem (floor): vloer (floor) kerk (church): mis (mass) koffie (coffee): melk (milk) dorp (village): stad (town) rommel (junk): afval (garbage) blad (leaf): boom (tree)
Target: high frequent, abstract: ding (thing): zaak (object) idee (idea): gedacht (thought) opleiding (education): school (school) moment (moment): vandaag (today) toekomst (future): morgen (tomorrow) behoefte (need): nood (need) dood (death): sterven (die) voorbeeld (model): braaf (good)
Target: low frequent, concrete: elleboog (elbow): arm (arm) kever (beetle): beest (beast) snavel (beak): mond (mouth) patat (patatoe): fritten (French fries) pil (pill): doktor (doctor) wortel (carrot): peeke (carrot) giraffe (giraffe): dier (animal)
List of words of different part of speech Target noun: mens (person): man (man) toneel (theater): theater verdriet (unhappiness): tranen (tears) komkommer (cucumber): groente (vegetable)
Target verb: drijven (float): zwemmen (swim) stinken (stink): rieken (smell) binden (tie); toedoen (close)
Target adjective: groot (big): lang (tall) vrolijk (happy): gelukkig (happy) verkeerd (wrong): mis (wrong) lekker (tasty): goed (good)