Anomalous Cerebral Language Organization: Acquired Crossed Aphasia in a Dextral Child

Brain and Language 76, 145–157 (2001) doi:10.1006/brln.2000.2437, available online at http://www.idealibrary.com on

Anomalous Cerebral Language Organization: Acquired Crossed Aphasia in a Dextral Child Peter Marien,* Sebastiaan Engelborghs,* Philippe Paquier,† and Peter P. De Deyn* *Department of Neurology, General Hospital Middelheim, Antwerp, Belgium, and Laboratory of Neurochemistry and Behavior, Born-Bunge Foundation, University of Antwerp, Belgium; and †Service de Neurologie, Hoˆpital Universitaire Erasme, Bruxelles, and School of Medicine, Department of ENT Surgery, University of Antwerp, Belgium

Following a dramatic change of its reported incidence, it was only recently recognized that acquired crossed aphasia in dextral children represents a highly exceptional phenomenon. We describe in a three epoch time-frame model the aphasic and neurocognitive manifestations of an additional case and focus briefly on its anatomoclinical configurations. In our patient, a right parietal cortico-subcortical hemorrhagic lesion caused an initially severe aphasia. After remission of the global aphasic symptoms in the acute phase, an adynamic output disorder with relatively severe auditory–verbal comprehension disturbances developed. In addition to the adynamia of self-generated speech, formal language investigations performed 3 weeks postonset, revealed agrammatism, hypertonic dysarthria, and dysprosodia. A substantial improvement of the aphasic disorder was objectified 83 days postonset. Neuropsychological investigations disclosed both dominant and nondominant hemisphere dysfunctions. Reassessment of neurocognitive functions after a 10-year period evidenced discrete residual anomia, confined to visual confrontational naming and a discrete visuo-perceptual syndrome. Given the posterior localization of the lesion, the syndrome shift from global to predominantly adynamic aphasia represents a finding beyond the plausible anatomoclinical expectations holding in general for the uncrossed, classic types of childhood and adult aphasia. As the first representative of crossed aphasia in dextral children with an anomalous lesion–aphasia profile, our case provides evidence to enrich the discussion on lateralization and intrahemispherical organization of language functions in both childhood and adult aphasia.  2001 Academic Press

1. INTRODUCTION

A century ago Byrom Bramwell (1899) coined the term crossed aphasia (CA) to refer to the condition in which the aphasia-producing lesion is located ipsilateral to the dominant hand. Stating that CA is common as an evanescent phenomenon but always confined to sinistrals in case the aphasic manifestations persist, Bramwell (1899) had apparently not fully considered last century’s prevailing insights on childhood aphasia. Indeed, in the early literature acquired childhood aphasia (ACA) had been similarly defined as a transient syndrome (Cotard, 1868) often induced by righthemisphere lesions (Wallenberg, 1886; Sachs & Peterson, 1890; Freud, 1897). Despite several, even early, contestations this view on ACA was incorporated in a standard doctrine that gave rise to the long-standing belief that irrespectively of lesion The authors gratefully acknowledge the editorial assistance of Louis Marie¨n. Address correspondence and reprint requests to Peter Marie¨n, A. Z. Middelheim, Department of Neurology, Lindendreef 1, 2020 Antwerp, Belgium. Fax: 0032/3/281.37.48. E-mail: [email protected]. 145 0093-934X/01 $35.00 Copyright  2001 by Academic Press All rights of reproduction in any form reserved.

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localization ACA is a unitary, transient, and nonfluent (motor type) aphasic syndrome commonly found in association with right-hemisphere lesions. From the semiological point of view it was further claimed that ACA is characterized by a dissociation between relatively preserved receptive and severely reduced expressive abilities ranging from mere mutism to articulatory defects. On the basis of overt resemblances with this doctrine several influencial studies (e.g., Brown & Wilson, 1973; Brown & He´caen, 1976) propagated that crossed aphasia in dextrals (CAD) represents a similar syndrome in adults. However, while CAD in adults was considered from its initial description onward a highly exceptional phenomenon (estimated incidence between 2 and 5%), it was not in children. In the studies published before the 1930s one-third of the childhood aphasic cases were reported to be CAD representatives. In the studies undertaken after 1940 this proportion spectacularly dropped to 5% (Woods & Teuber, 1978) and even less (Carter, Hohenegger, & Satz, 1982). From 1975 on, a starting-point chosen because Faglia, Rottoli, and Vignolo (1990) showed that all fully acceptable CAD cases were published thereafter, we encountered only four dextral children (2.3%) in a corpus of 169 aphasic cases with righthemisphere injury. The first childhood case was published in 1977 by Assal and Deonna and was reinvestigated 10 years later (Assal, 1987). The other cases were reported by Martins, Ferro, and Trindale (1987); Martins, Antunes, Castro-Caldas, and Antunes (1995); and Burd, Gascon, Swenson, and Hankey (1990). In view of the scarcity of fully documented cases of childhood CAD, the primary aim of this article is twofold: (1) to add a new case with a longitudinal follow-up to the extreme small group of childhood CAD cases, and (2) to focus briefly on its unique anatomoclinical characteristics.

2. CASE REPORT 2.1. History EDC, a 13-year-old right-handed girl, lost consciousness during a play at school. On admission the girl had a score of nine on the Glasgow Coma Scale. The general physical examination was unremarkable. No secondary sexual characteristics were present. The elemental neurological examination revealed left hemiplegia with left-sided hyperreflexia and central facial nerve palsy. The remaining cranial nerves were intact. The left plantar response was extensor. Coordination and sensation could not be tested. Within 2 days, consiousness entirely normalized and the left-sided pyramidal symptoms ameliorated slightly. Medical history, growth, and developmental milestones were reported normal. She was born at term after normal gestation and labor and there had been no perinatal or postnatal problems. Her scholastic achievements had always been above average levels and there was no familial history of developmental disorder or learning disability. No familial strain of left-handedness was found after careful inquiry. Both the parents and the grandparents were reported strong dextrals. A computerized tomography (CT) scan of the brain on admission disclosed a right-sided hyperdens area that extended from the temporal region to the occipital horn of the lateral ventricle and to the parietal lobe. A panarteriography of the cerebral vessels revealed hemorrhagic dislocation of the branches of the right middle cerebral artery and a small parietal arteriovenous (AV) malformation supplied by the posterior parietal artery. Neurosurgical resection of the AV malformation and coagulation of its laterally supplying branch was performed 73 days after onset of neurological symptoms. Postoperatively, the neurological condition improved but a residual left-sided spastic hemiparesis remained. Magnetic resonance imaging (MRI) of the brain performed 10 years after onset of neurological symptoms (Figs. 1A and 1B) revealed an extensive right parietal porencephalic cyst surrounded by scar tissue and gliosis with attraction of the enlarged lateral ventricle. Structural integrity of the left hemisphere was ascertained.

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(A)

(B) FIG. 1. (A) Brain MRI parasagittal gradient T1-weighted (TR 360, TE 13) and (B) axial FLAIR slices (TR 7202, TI 1800, TE 101) demonstrate the sequellae of neurosurgical treatment of the intracerebral hemorrhage and vascular malformation in the right hemisphere. A large porencephalic cyst surrounded by scar tissue and gliosis (hypersignal) is shown with attraction of the enlarged right lateral ventricle and macroscopically relatively spared cortical structures.

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2.2. Neurocognitive Assessments

2.2.1. Method Language was examined on a temporal basis in agreement with the three epoch time-frame for models of aphasia (Mazzocchi & Vignolo, 1979; Basso, Capitani, Laiacona, & Zanobio, 1985; Alexander, 1989). In order to avoid remote functional effects of the hemorrhagic lesion, generally accounting for the instability of aphasic profiles during the first 2 or 3 weeks postonset (acute phase), extensive language examinations were performed in the lesion phase at 25 and 83 days after onset of neurological symptoms. During this phase, which might last up to 4 months, the most pure and robust anatomo clinical correlations are found. To capture the various effects of recovery and functional brain reorganization, a third neurolinguistic examination was performed during the late phase, 10 years after onset of neurological symptoms. The neurolinguistic test battery mainly consisted of the Dutch version of the Aachener Aphasie Test (Graetz, De Bleser, & Willmes, 1992), the Boston Diagnostic Aphasia Examination (BDAE) (Goodglass & Kaplan, 1983), the Token Test (De Renzi & Vignolo, 1962), and the Boston Naming Test (Kaplan, Goodglass, & Weintraub, 1983). Neurocognitive investigations based on standardized test batteries were performed preoperatively in the lesion phase at Day 27 and postoperatively in the lesion phase at Day 90 and in the late phase 10 years postonset of the neurological symptoms.

2.2.2. Acute Phase Findings: Neurolinguistic Observations In the acute phase language functions were merely evaluated by means of bedside screening instruments and close neurobehavioral observations. After the girl had regained full consciousness, the aphasiological tableau evolved to a nonfluent output syndrome characterized by complete absence of self-generated speech and severe auditory–verbal comprehension deficits. A few days after onset, only strong incentives to speak elicited short verbal responses that were contaminated by phonematic distortions and dysarthric symptoms. Although the girl was sufficiently cooperative, failure to perform two-step commands indicated that auditory–verbal comprehension was functional only at elementary levels.

2.2.3. Lesion Phase Findings Table 1 describes the AAT results obtained in the lesion phase at two different time periods: Day 25 and Day 83 postonset neurological symptoms. 2.2.3.1. Neurolinguistic findings: Day 25. Auditory–verbal comprehension examination revealed generalized slowness of understanding verbal material, agrammatism and diminution of semantic knowledge. In contrast to an only slightly defective score of 65/72 (cut-off ⫽ 67) (percentile 70) on the BDAE word discrimination task, the AAT word comprehension subtest (Table 1) revealed a more severely deficient score of 18/30 (percentile 44) resulting from semantic distraction and failures at more complex semantic levels. Syntactic complexity determined performances on the sentence level significantly. Comprehension of daily language turned out to be entirely normal (e.g., BDAE commands 15/15) but failed, as reflected by an AAT sentence comprehension score of 19/30 (percentile 46) for syntactic ambiguous or grammatically complex sentences. Failures on this subtest did not result from semantic misinterpretations but followed from mixing-up function words. Syntax disturbances were further illustrated by a deficient comprehension of spatial prepositions embedded in reversed sentences (33% correct) (Ombredane, 1950). The Token Test profile showed no errors for part I and II (20/20), but performance on the more syntactically loaded parts III, IV, and V yielded defective results (21/41). In comparison with an age-matched population of 30 native Flemish-speaking controls (Van Eerdenbrugh, 1998) the patient’s total score of 41/61 represents 5.5 standard deviations below the adjusted mean of 57.1 (standard deviation ⫽ ⫾2.9). Spontaneous and imposed oral language examination showed a bradylalic speaking rate associated with an often effortful, hypertonic-like articulation. Spontaneous output was characterized by decreased speech initiation and by fragmented attempts to formulate ideas. Although in self-generated speech these long pauses indicated word-retrieval problems, confrontational naming tasks did not objectify defects of anomic origin (AAT total naming ⫽ 108/120; BDAE responsive naming ⫽ 30/30). Speech was also characterized by syntactic impairments. Frequent deletion of verbs, mistakes on tense and person, deletion of pronouns, and difficulties selecting the right preposition indicated expressive agrammatism. Agrammatic errors occurred especially in spontaneous speech and less in ‘‘structured’’ settings. For instance, the AAT descriptive naming subtest of situations and actions scored 20/30 (percentile 73) which represents 1.5 standard deviations below the mean of 25.69 (standard deviation ⫽ ⫾3.72). As

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TABLE 1 AAT Test Results on Day 25 and 83 Postonset Neurological Symptoms

Aachener Aphasie Test Comprehension Auditory: words Auditory: sentences Total Written: words Written: sentences Total Spontaneous speech Communicative behavior Articulation and prosody Automatisms Semantic structure Fonematic structure Syntactic structure Imposed speech Total repetition Phonemes Monosyllabic words Loan- & foreign words Compounds Sentences Total naming Simple nouns Color names Composed nouns Sentences Written language Reading aloud Composing Dictational writing

Results day 25/83

Percentile

Max

Mean

⫾1 SD

90/104 18/24 19/24 37/48 28/28 25/28 53/56

61/86 44/70 46/69 32/71 83/83 82/95 86/95

120 30 30 60 30 30 60

108.5 26.49 26.79 53.28 28.30 26.91 55.21

10.24 3.30 3.41 6.08 2.29 3.39 4.90

5 5 5 5 5 5

4.63 4.63 4.59 4.59 4.54 4.41

0.54 0.67 0.65 0.53 0.56 0.55

150 30 30 30 30 30 120 30 30 30 30 90 30 30 30

144.1 28.91 29.22 28.94 28.45 28.55 109.3 27.92 27.69 28.04 25.69 85.52 28.95 28.57 28

8.07 2.09 1.32 2.31 2.22 1.90 8.42 2.90 1.99 2.61 3.72 7.63 1.93 2.75 3.67

3/4 2/3 5/5 4/5 5/5 2/5 148/149 30/29 30/30 30/30 30/30 28/30 108/114 30/30 30/30 28/28 20/26 90/90 30/30 30/30 30/30

98/99 88/72 93/93 95/95 98/98 93/99 92/99 97/97 98/98 91/91 73/94 100/100 96/96 98/98 99/99

further illustrated in Table 1, no pathological phenomena were found in automatic speech and repetition tasks. Reading aloud was characterized by a decreased rate and many deletional errors of function words and flexional morphemes. Agrammatic manifestations remained restricted to the textual level and did not affect sentences, clauses, or words when read in isolation. The patient obtained a maximum score on the AAT ‘‘reading aloud’’ subtest. On an experimental list of 30 words, consisting of 10 function words, 10 irregularly spelled words, and 10 nonwords, the girl obtained a score of 30/30. In addition, an experimental list of 50 words did equally not disclose any effect of the variables regularity, length, frequency, and imageability (50/50). Reading comprehension for words, sentences, and texts was within entirely normal limits (Table 1). The AAT word comprehension test scored 28/30 (percentile 83), and the AAT sentence comprehension test 25/30 (percentile 82). A short story read from a magazine was summarized adequately. Spelling to dictation was slightly defective at the level of sentence writing. The patient sporadically omitted function words. Agrammatic errors increased substantially in narrative writing. Orthography was characterized by visuo-spatial disturbances. Multiplication of downstrokes in letters as well as repetition of entire letters, and the inability to write on a horizontal line reflected afferent dysgraphia. 2.2.3.2. Neurocognitive findings: Day 27. A strong and consistent right-hand preference was confirmed by the Edinburgh Inventory (Oldfield, 1971) revealing a Laterality Quotient of ⫹100. In the absence of major sensory disturbances, lateralized left-sided gnostic deficits were found, consisting of an astereognosia, a fingeragnosia, and an autotopagnosia. The girl was well aware of the left-sided motor disturbances and did not show symptoms of an auditory or visuo-gnostic defect. Visuo-spatial defects had a major impact on the visuo-constructive level (e.g., WISC block design: scaled score ⫽ 6) but no apractogenic problems were encountered. Constructional, ideational, ideomotor, dressing, and bucco-

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FIG. 2. Extract from the patient’s narrative writing (BDAE situational plate). Deleted function words are placed between brackets; prepositions which are displaced or added are underlined. The translation of the Dutch sample to English is marked in italic. labio-lingual praxis were normal. On written calculation, visuo-spatial errors induced spatial acalculia. Misalignment of numerical data in multicolumn arithmetic tasks, number omission, difficulties with space value and decimals, and paragraphic errors (e.g., 232 instead of 223) interfered with normal calculation. A total score of 5/20 with eight errors concerning the lateralization on the 12 ‘‘own body’’ items of Benton’s ‘‘Right-Left Orientation Test’’ (Benton, deS Hamsher, Varney, & Spreen, 1983) reflected a generalized right–left orientation defect. Memory, evaluated by Rey’s 15 words and the Rey–Osterrieth Complex Figure, was normal. The patient respectively scored percentile 50, 70, and 99 on the first, second, and third instruction of the 15 words and obtained percentile 50 drawing the complex figure of Rey–Osterrieth from memory. 2.2.3.3. Neurolinguistic findings: Day 83. Auditory–verbal comprehension was normal except for persistence of agrammatic symptoms. Similar to prior findings, the Token Test profile disclosed selective difficulties on the more syntactically loaded parts III, IV, and V. A slightly increased total score of 44/ 61 represented 4.5 standard deviations below the age-adjusted mean of 57.1 (standard deviation ⫽ ⫾2.9) (Van Eerdenbrugh, 1998). No improvement was found on Ombredane’s (1950) spatial comprehension test (33% correct answers). However, as illustrated in Table 1, AAT scores for auditory–verbal comprehension normalized for both words and sentences (percentiles 70 and 69, respectively). The girl obtained also a normal score of 69/72 (cut-off ⫽ 67) on the BDAE word discrimination task. No evidence of slowness in understanding or arguments in favor of a persisting decline of receptive semantic knowledge were found. Spontaneous and imposed oral language remained bradylalic and dysprosodic. In contrast to prior investigations articulation was no longer hypertonic and agrammatism was not found. Adynamic symptoms in spontaneous speech (reduced verbal initiative, fragmented output, long pauzes, formulation difficulties) had almost completely resolved. Reading aloud had normalized. Reading comprehension was again normal. Spelling to dictation was normal at all levels (Table 1). Although the girl generated long and complex sentences, agrammatic symptoms again disturbed narrative writing (Fig. 2). As illustrated in Fig. 2, a variety of written syntax errors occurred to structure the Dutch subordinate clause ‘‘dat het water overloopt’’ (that the water overflows) or ‘‘het water dat overloopt’’ (the water that overflows). Besides deletion of five prepositions and two verbs, grammatical displacement and addition of prepositions occurred. Only one person–verb congruence error was found. The infinitive form of the verb ‘‘afdrogen’’ (to dry) was used instead of the third-person singular present tense (‘‘afdroogt’’ or ‘‘droogt af’’). The erronous clause ‘‘en ziet het niet op het water dat overloopt’’ (and does not see that the water overflows) intersperses two distinct syntactic frames: (1) ‘‘en ziet niet dat het water overloopt’’ and (2) ‘‘en ze merkt niet op dat het water overloopt.’’ The attempt to maintain these different syntactic frames in a simultaneous production induced grammatical unacceptable juxtapositions. 2.2.3.4. Neuropsychological findings: Day 90. Postoperative investigations revealed an amelioration of visuo-spatial defects but no basic changes were found with regard to the lateralized gnostic (autotopagnosia, finger agnosia, and astereognosis) and orientation disturbances. The WISC revealed a normal global intelligence quotient of 100 with a discrepancy of 14 points between the verbal (92) and performance intelligence level (106). Besides a depressed scaled score of 6 on the ‘‘block design’’ subtest and a decreased scaled score of 8 on the ‘‘substitution’’ subtest a consistent subtestprofile was found on both the verbal and the performance level.

2.2.4. Late-Phase Findings Following a period of intensive physical therapy and speech and language training the girl reattended school. Except for difficulties in mathematics and a ‘‘strange accent’’ in foreign language acquisition,

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TABLE 2 BDAE Subtest Summary Results 10 Years Postonset Subtest Severity Fluency

Auditory comprehension

Naming

Oral reading Repetition

Paraphasia

Automatic speech Reading comprehension

Writing

Music

Articulatory rating Phrase length Melodic line Oral nonverbal agility Verbal agility Word discrimination Body part identification Commands Complex ideational material Responsive naming Confrontation naming Animal naming Word reading Oral sentence reading Repetition of words High-probability Low-probability Neologistic Literal Verbal Extended Automatized sequences Reciting Symbol discrimination Word recognition Comprehension of oral spelling Word–picture matching Reading sentences & paragraphs Mechanics Serial writing Primer level dictation Spelling to dictation Written confrontation naming Sentences to dictation Narrative writing Rhythm

Raw score

Percentile

5/5 7/7 7/7 7/7 9/12 13/14 72/72 20/20 15/15 11/12 30/30 114/114 23/23 30/30 8/10 10/10 8/8 8/8 0/40 0/47 1/40 0/75 8/8 not evaluated 10/10 8/8 5/8 10/10 8/10 5/5 47/47 15/15 10/10 10/10 12/12 5/5 not evaluated

100 70 70 50 80 100 100 90 90 100 100 100 90 85 90 90 100 70 90 90 50 90 70 80 75 80 90 90 100 90 100 100 100 100

she did not experience scholastic problems. She successfully finished college without delay. Soon after she had left school she was employed as an insurance agent. Secondary to her physical incapacities, she developed feelings of inferiority and depressive stigmata. Although she remained somewhat shy, no obviously emotional, psychological, or social problems were mentioned when she was reexamined again 10 years after onset of the neurological symptoms. Table 2 displays the BDAE subtest summary results 10 years postonset neurological symptoms. Table 3 shows the results obtained during the same period on additional language tests and on a variety of tests exploring several neurocognitive domains. 2.2.4.1. Neurolinguistic findings: 10 years postonset. As reflected by entirely normal results on the BDAE (Table 2) no obvious aphasic symptoms were encountered anymore ten years postonset. Additional neurolinguistic investigations disclosed, however, a discrete residual anomic deficit. On the Boston Naming Test (Kaplan et al., 1983) (Table 3) she named 47 of the 60 items correctly. In comparison with the test performance of a group of native Flemish-speaking healthy volunteers (Marie¨n, Mampaey, Vervaet, Saerens, & De Deyn, 1998), this result is 2.9 standard deviations below the gender and education adjusted mean of 54.5 (standard deviation ⫽ ⫾2.6). According to a classic neurolinguistic taxonomy for error classification (Critchley, 1970; Lecours & Lhermite, 1979; Goodglass & Kaplan, 1983), most naming errors consisted of verbal semantic paraphasias (4/13) (e.g., ‘‘beaver’’ named as ‘‘squirrel’’).

TABLE 3 Neurocognitive Test Results 10 Years Postonset Neurocognitive Tests Mini-mental state examination Intelligence Tests Wechsler Global IQ (GIQ) Wechsler Verbal IQ (VIQ) Information Comprehension Digit Span Arithmetic Similarities Vocabulary Wechsler Performance IQ (PIQ) Digit Symbol Picture Completion Block Design Picture Arrangement Object Assembly Progressive Raven Matrices Memory Tests Wechsler Memory Scale (WMS) Memory Quotient Information Orientation Mental Control Logical Memory Digit Span Visual Stimuli Paired Associates Hierarchic Dementia Scale (HDS) Memory: Biographic: it. 17 Rey-Osterrieth Figure: memory Language Tests Boston Naming Test (BNT) Verbal Fluency Semantic Generation Animals, 1 minute Transportation, 1minute Vegetables, 1 minute Clothing, 1 minute Total number of perseverations Total number of intrusions Phonological Generation Phoneme F, 2 minutes Phoneme A, 2 minutes Phoneme S, 2 minutes Total number perseverations Total number intrusions Frontal Tests Wisconsin Card Sorting Stroop Color–Word Test Praxis Tests Rey-Osterrieth Figure Praxis: Ideational: it. 5 (HDS) Praxis: Ideomotor: it. 3 (HDS) Praxis: Drawing: it. 15 (HDS) Praxis: Constructional: it. 12 (HDS) Visual Tests Right–Left Orientation—Form A Judgment of Line Orientation Visual Form Discrimination Facial Recognition Test

Score/ Maximum

Percentile

Mean

⫾1 SD

29/30

29

99 100 12/22 15/28 9/24 10/16 19/26 33/60 98 49/115 14/20 12/26 14/20 20/82 105

100 100 9 14 11 7 12 29 100 52 10 13 12 39 100

15 15

106/143 6/6 5/5 8/9 14/22 9/15 11/12 16.5/22

100

15

10/10 23/36

10 25

0 3

47/60

54.5 56.1 60.5

2.6 15.13 7.14

41

15.23

52

10

62 54 31 73 88 62 38 86 45 66 13

62 23 11 12 16 1 0 62 15 15 32 2 0 Normal 33 32/36 10/10 10/10 9/10 10/10 20/20 21/30 30/32 45/54

22 33–59

1.3

15

15

35 9.79 9.94 9.81 10

3 0.17 0.23 0.52 0

19.3 25.3 29.9

2.3

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Three of 13 errors were ‘‘don’t-know responses,’’ which represent the absence of any response or the expression for not knowing the right target word. Two naming errors consisted of adequate circumlocutions (e.g., ‘‘an instrument used by a doctor to listen to your heart’’ for ‘‘stethoscope’’). Another two errors were mere visual misperceptions (e.g., ‘‘snake’’ for ‘‘pretzel’’). One erroneous answer highly resembled the target word with respect to its phonological structure and was therefore considered a verbal morphological paraphasia (‘‘lasser’’ (welder) for ‘‘passer’’ (compass)). One error consisting of a neologistic combination of lexical elements that have a meaning on their own was classified as a portemanteau word or semantic neologism (‘‘schilderspaneel’’ (painter’s panel) for ‘‘palet’’ (palette)). As illustrated in Table 3, verbal fluency for 1-min semantic categories (animals, transport, vegetables, clothes) and 2-min phonological categories (phonemes /f/, /a/, and /s/) matched gender and education means (unpublished norms). 2.2.4.2. Neurocognitive findings: 10 years postonset. As shown in Table 3, general screening of cognitive functions by means of the Mini Mental State Examination (Folstein, Folstein, & McHugh, 1975) scored 29/30. This score matches normal age and education levels (mean ⫽ 29; standard deviation ⫾ 1.3) (Crum, Antony, Bassett, & Folstein, 1993). The Wechsler Adult Intelligence Scale yielded a normal global intelligence quotient of 99 with a consistent distribution of the verbal (VIQ ⫽ 100) and performance IQ (PIQ ⫽ 98). Comparison of the verbal subtests showed a significantly lower score for the subtest ‘‘digit span.’’ In agreement with this relatively poor performance, a result matching percentile 38 for the subtest ‘‘substitution’’ indicated poor visuo-motor concentration on the performance level as well. She further performed significantly worse on the visuo-constructive subtests ‘‘object assembly’’ and ‘‘block design’’ (percentile scores of respectively 13 and 45). As reflected by a memory quotient of 106, the Wechsler Memory Scale (Wechsler, 1987) matched the Wechsler IQ levels. On this memory test no differences were found between verbal and visual memory. Autobiographical memory and long-term memory were also normal. Except for the item ‘‘drawing praxis,’’ she obtained normal results on the praxis subtests of the Hierarchic Dementia Scale (HDS) (Cole & Dastoor, 1987). Residual visuo-constructive drawing problems were further illustrated by a poor performance matching percentile 10 for copying the Rey–Osterrieth complex figure. No evidence was found for a disturbance of dressing, bucco-labio-lingual, ideational, or ideomotor praxis. Benton’s visual tests (Benton, deS Hamsher, Varney, & Spreen, 1983) did not reveal an underlying visuo-perceptual or visuospatial deficit. She obtained normal results on mental and spatial calculation. Benton’s Right–Left Orientation Test (Benton et al., 1983), form A, scored normal. No behavioral or psychometric evidence (e.g., Wisconsin Card Sorting, Stroop Color–Word Test, Tower of Hanoi) was found indicative for frontal lobe dysfunction.

3. DISCUSSION

The aphasic manifestations in the patient reported represent a unique combination of ACA and CAD phenomena. The syndrome belongs to ACA since puberty was not reached at the time of injury. Since aphasic symptoms followed vascular damage confined to the right hemisphere in a natural and formally assessed dextral child with no history of familial sinistrality, early brain injury, or a seizure disorder, the aphasic syndrome also represents CAD. After rapid recovery from mutism in the presumed context of global aphasia, an adynamic output syndrome with relatively severe auditory–verbal comprehension defects dominated the aphasic syndrome in the acute phase. In the subsequent lesion phase, agrammatism was found in association with adynamia of self-generated speech, hypertonic dysarthria, and dysprosodia. Language assessments performed 83 days postonset disclosed a substantial improvement. The dynamic aphasia had almost completely resolved but prominent disturbances on the syntactic level remained. Bradylalic and dysprosodic symptoms characterized speech. Reassessment of speech and language functions after a 10-year period revealed only a discrete residual anomia, confined to visual confrontational naming. Some of these aphasic phenomena deserve some further comment. First, given the posterior localization of the lesion, the syndrome shift from global aphasia (in the early acute phase) to a predominantly adynamic output syndrome (in the lesion phase) represents a finding beyond the plausible anatomoclinical expectations holding in general for the uncrossed, classic types of childhood (Woods, 1995) and adult aphasia (Kirshner, 1995). While distant func-

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tional effects of the hemorrhagic lesion most likely accounted for the extent and severity of the language impairments during the acute phase, no such explanation can be offered for the lesion-phase findings. During the lesion phase, repeated brain scans (CT and MRI) delineated the area of actual brain tissue destruction and clearly illustrated absence of any visible mass effect. The pathology underlying Luria’s dynamic, or frontal aphasia (Luria & Tsvetkova, 1967, 1968; Luria, 1977), which closely relates to transcortical motor aphasia (TMA), most typically involves either of two distinct dominant hemisphere areas: the area situated anterior and/or superior to Broca’s area, and the territory supplied by the anterior cerebral artery. Some authors (Freedman, Alexander, & Naeser, 1984) consider TMA to result from a partial disconnection of the supplementary motor area from the motor speech area. Reduced spontaneous verbal output, as the core feature of dynamic aphasia, has also been described in association with extensive subcortical damage (antero-superior periventricular and the paraventricular white matter) and with focal right cerebellar lesions which induce deactivation of left cerebral structures (Marie¨n et al., 1996; Marie¨n, Engelborghs, Pickut, & De Deyn, 2000). In our patient none of the structures crucial to dynamic aphasia sustained damage. As a consequence, the anatomoclinical profile of our patient differs from the standard aphasic syndromes in terms of hemispheric language lateralization and intrahemispheric language representation. Alexander, Fischette, and Fisher (1989) introduced the term of ‘‘anomalous’’ case to refer to CAD patients with striking anomalies in the aphasia–lesion relationship. The term ‘‘mirror-image’’ case was conversely used to denote CAD cases with a standard aphasia syndrome associated with the lesion site expected in the left hemisphere. In adult CAD the mirror-image and anomalous subtype represent respectively 65 and 35% of the cases (Alexander et al., 1989; Coppens & Hungerford, 1998). Among the four childhood CAD cases reported in the literature only the two vascular cases reported by Assal (1987) and Burd et al. (1990) allow a similar analysis. Both cases reported by Martins and colleagues (1987, 1995) were excluded from this analysis because of their limited localization value (infiltrative neoplasm and traumatic brain damage). In the Assal case (1987), a CT scan of the brain disclosed an extensive fronto-parieto-temporal lesion involving the third frontal and first temporal convolution, the supramarginal gyrus, the anterior limb of the internal capsule, the anterior and middle parts of the caudate nucleus, and the putamen. Destruction of crucial parts of the language area explains the initially severe and long-lasting language impairments in this patient. Compatibility of the symptom–lesion profile in the lesion phase with the classical configurations of standard uncrossed aphasia, makes the case a mirror-image representative. Large cortico-subcortical damage to fronto-parietal and posterior parietal structures in the case described by Burd et al. (1990) initially caused a severe aphasia with equal involvement of expressive and receptive abilities. Since the lesion-phase findings in this patient correlated well with the anatomoclinical configurations holding for the standard aphasias, this case can also be considered a mirror-image representative. As a consequence, our patient represents within this still limited group, the first case of the ‘‘anomalous’’ childhood CAD variant. Our observations thus illustrate that similar to adult CAD, anatomoclinical ‘‘exceptions’’ can be discerned in childhood CAD as well. In our patient, the syntactic deficits constitute another prominent finding. Agrammatism has long been considered an essentially syntactic impairment of both language production and comprehension. Recent in-depth psycholinguistic investigations and anatomoclinical observations of agrammatic manifestations have expanded the traditional concept of agrammatism fundamentally. For instance, the observation of various types of differential syntax impairments (Tissot, Mounin, & Lhermitte, 1973; Miceli, Mazzucchi, Menn, & Goodglass, 1983; Kolk, vanGrunsven, & Keyser,

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1985; Jerema, Kadzielawa, & Waite, 1987; Caramazza & Hillis, 1989) led Nadeau (1988) and Nadeau and Gonzalez Rothi (1992) to hypothesize that a distinct neuroanatomic organization subserves these functional dissociations: a primarily syntactic component being localized frontally and a primarily morphological component being located in the dominant postcentral perisylvian cortex. In comparison with this view, the overall preserved ability of our patient to generate in speech as well as in written language syntactic long and complex sentences with embedded structures, the occurrence of grammatically unacceptable juxtapositions of words following attempts to produce more than one syntactic frame simultaneously, and the relatively frequent omission of free grammatical morphemes might be indicative of a structural impairment at the morphological selection level in expressive language. These ‘‘primarily morphological impairments of syntax’’ seem to be in congruence with the postcentral location of the lesion. Lesion-phase neurocognitive assessments disclosed in our patient a unilateral, leftsided agnostic syndrome consisting of astereognostic, fingeragnostic, and autotopagnostic symptoms. Since the recognition disturbances could not be attributed to unilateral sensory or major motor defects, the right parietal lesion might be considered causative. In coexistence with a generalized right–left discrimination disturbance the strictly unilateral agnostic deficits seem to provide evidence in support of the hypothesis that in our patient these dominant parietal features are distributed bilaterally. Aside from its dominant hemisphere qualities, destruction of the right parietal region also induced typical ‘‘minor’’ hemisphere symptoms. Constructional difficulties, spatial acalculia, and afferent dysgraphia constituted the core features of a visuo-perceptual syndrome. No visuo-spatial neglect or motor neglect phenomena were found. Ten years after the onset of neurological symptoms poor concentration was found in association with a discrete residual visuo-perceptual syndrome, consisting of isolated visuo-constructional difficulties. Whether the prosperous recuperation of the neurocognitive dysfunctions in our patient reflects the cross-over of these functions to the nonlesioned left hemisphere remains entirely speculative since intrahemispheric reorganization might be put forward as an alternative hypothesis as well. To shed some light on the patterns of neurocognitive reorganization, a functional neuroimaging study was proposed to the patient which she unfortunately refused. Further reports of clinical and neuroimaging studies of childhood CAD are needed to contribute to the understanding of the neurobiological mechanisms underlying lateralization, organization, and recovery of neurocognitive functions in this exceptional group of patients. 4. CONCLUSIONS

Summarizing our data we conclude the following: • in marked contrast to the longstanding conviction in behavioral neurology that acquired CAD in children represents a common finding, the paucity of childhood CAD representatives in the modern literature reflects the extreme rareness of this neurobiological entity • because of unexpected anatomoclinical correlations, our case constitutes the first representative of acquired childhood CAD with an anomalous lesion–aphasia profile • that anomalous lesion–aphasia configurations can be encountered in acquired childhood CAD not only enriches the phenomenon with the distinction of anomalous versus mirror-image patterns of cerebral language organization but also links childhood CAD explicitly to adult CAD

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• in contrast to its anomalous overall lesion–aphasia profile the anatomoclinical correlations holding for the agrammatic manifestations seem to be within plausible expectations • the neurocognitive profile of our patient, encompassing both dominant and nondominant hemisphere dysfunctions, provides support for the view that aside from its role in the genesis of the linguistic disturbances the right posterior brain region accommodates dominant as well as nondominant hemisphere functions; the unilateral aspect of the typically dominant hemisphere dysfunctions seems to indicate bilateral representation of at least some of the dominant hemisphere functions (stereognosis, fingergnosis, and autotopgnosis). 5. REFERENCES Alexander, M. P. (1989). Clinical–anatomical correlations of aphasia following predominantly subcortical lesions. In F. Boller & J. Grafman (Eds.), Handbook of neuropsychology (pp. 47–66). Amsterdam: Elsevier Science. Alexander, M. P., Fischette, M. R., & Fischer, R. S. (1989). Crossed aphasias can be mirror image or anomalous. Brain, 112, 953–973. Assal, G. (1987). Aphasie croise´e chez un enfant. Revue Neurologique, 143, 532–535. Assal, G., & Deonna, T. (1977). Aphasie par thrombose de la carotide interne droite, chez un enfant droitier. Oto-Neuro-Ophtalmologia, 49, 321–326. Basso, A., Capitani, E., Laiacona, M., & Zanobio, M. E. (1985). Crossed aphasia: One or more syndromes? Cortex, 21, 25–45. Benton, A. L., deS Hamsher, K., Varney, N. R., & Spreen, O. (1983). Contributions to neuropsychological assessment: A clinical manual. New York: Oxford Univ. Press. Bramwell, B. (1899). On ‘‘crossed’’ aphasia and the factors which go to determine whether the ‘‘leading’’ or ‘‘driving’’ speech-centres shall be located in the left or in the right hemisphere of the brain, with notes on a case of ‘‘crossed’’ aphasia (aphasia with right-sided hemiplegia in a left-handed man). Lancet, 1, 1473–1479. Brown, J. W., & He´caen, H. (1976). Lateralization and language representation: Observations on aphasia in children, left-handers, and ‘‘anomalous’’ dextrals. Neurology, 26, 183–189. Brown, J. W., & Wilson, F. R. (1973). Crossed aphasia in a dextral. Neurology, 23, 907–911. Burd, L., Gascon, G., Swenson, R., & Hankey, R. (1990). Crossed aphasia in early childhood. Developmental Medicine and Child Neurology, 32, 528–546. Caramazza, A., & Hillis, A. E. (1989). The disruption of sentence production: Some dissociations. Brain and Language, 36, 625–650. Carter, R. L., Hohenegger, M. K., & Satz, P. (1982). Aphasia and speech organization in children. Science, 218, 797–799. Cole, M. G., & Dastoor, D. (1987). A new hierarchic approach to the measurement of dementia. Psychosomatics, 28, 298–305. Coppens, P., & Hungerford, S. (1998). Crossed aphasia. In P. Coppens, Y. Lebrun, & A. Basso (Eds.), Aphasia in atypical populations (pp. 203–260). New Jersey: Erlbaum. Cotard, J. (1868). Etude sur l’atrophie ce´re´brale. Paris: Thesis, Faculte´ de Me´decine. Critchley, M. (1970). Aphasiology and other aspects of language. London: Arnold. Crum, R. M., Antony, J. C., Bassett, S. S., & Folstein, M. F. (1993). Population-based norms of the mini-mental state examination by age and educational level. JAMA, 269, 2386–2391. De Renzi, E., & Vignolo, L. A. (1962). The token test: A sensitive test to detect receptive disturbances in aphasia. Brain, 85, 665–678. Faglia, L., Rottoli, M. R., & Vignolo, L. A. (1990). Aphasia due to lesions confined to the right hemisphere in right handed patients: A review of the literature including the Italian cases. Italian Journal of Neurological Sciences, 11, 131–144. Folstein, M., Folstein, S., & McHugh, P. (1975). Mini-Mental State: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198. Freedman, M., Alexander, M. P., & Naeser, M. A. (1984). The anatomical basis of transcortical motor aphasia. Neurology, 34, 409–417.

ACQUIRED CROSSED APHASIA IN A DEXTRAL CHILD

157

Freud, S. (1897). Die infantile Cerebralla¨hmung. Wien: Alfred Ho¨lder. Goodglass, H., & Kaplan, E. (1983). The assessment of aphasia and related disorders. Philadelphia: Lea & Febiger. Graetz, P., De Bleser, R., & Willmes, K. (1992). De Akense Afasie Test. Lisse: Swets & Zeitlinger. Jerema, G., Kadzielawa, D., & Waite, J. (1987). On comprehension of active/passive sentences and language processing in a Polish agrammatic aphasic. Brain and Language, 32, 215–232. Kaplan, E., Goodglass, H., & Weintraub, S. (1983). The Boston Naming Test. Philadelphia: Lea & Febiger. Kirshner, H. S. (1995). Classical aphasia syndromes. In H. S. Kirshner (Ed.), Handbook of neurological speech and language disorders (pp. 57–89). New York: Dekker. Kolk, H. H. J., vanGrunsven, M. J. F., & Keyser, A. (1985). On parallelism between production and comprehension in agrammatism. In M. L. Kean (Ed.), Agrammatism. Orlando: Academic Press. Lecours, A. R., & Lhermitte, F. (1979). L’aphasie. Paris: Flammarion, Me´dicine Sciences. Luria, A. (1977). Neuropsychological studies in aphasia. Lisse: Swets & Zeitlinger. Luria, A., & Tsvetkova, L. (1967). Towards the mechanisms of ‘‘dynamic aphasia.’’ Acta Neurologica et Psychiatrica Belgica, 67, 1045–1057. Luria, A., & Tsvetkova, L. (1968). The mechanisms of ‘‘dynamic aphasia.’’ Foundations of Language, 4, 296–307. Marie¨n, P., Engelborghs, S., Pickut, B. A., & De Deyn, P. P. (2000). Aphasia following cerebellar damage: Fact of fallacy? Journal of Neurolinguistics, 13, 145–171. Marie¨n, P., Mampaey, E., Vervaet, A., Saerens, J., & De Deyn, P. P. (1998). Normative data for the Boston Naming Test in native Dutch-speaking Belgian elderly. Brain and Language, 65, 447–467. Marie¨n, P., Saerens, J., Nanhoe, R., Moens, E., Nagels, G., Pickut, B. A., Dierckx, R. A., & De Deyn, P. P. (1996). Cerebellar induced aphasia: Case report of cerebellar induced prefrontal aphasic language phenomena supported by SPECT findings. Journal of the Neurological Sciences, 144, 34–43. Martins, I. P., Antunes, N. l., Castro-Caldas, A., & Antunes, J. L. (1995). Atypical dominance for language in developmental aphasia. Developemental Medicine and Child Neurology, 37, 85–90. Martins, I. P., Ferro, J., & Trindale, A. (1987). Acquired crossed aphasia in a child. Developmental Medicine and Child Neurology, 29, 96–109. Mazzocchi, F., & Vignolo, L. A. (1979). Localization of lesions in aphasia: Clinical-CT scan correlations in stroke patients. Cortex, 15, 627–654. Miceli, G., Mazzucchi, A., Menn, L., & Goodglass, H. (1983). Contrasting cases of Italian agrammatic aphasia without comprehension disorder. Brain and Language, 19, 65–97. Nadeau, S. E. (1988). Impaired grammar with normal fluency and phonology. Implications for Broca’s aphasia. Brain, 111, 1111–1135. Nadeau, S. E., & Gonzalez Rothi, L. J. (1992). Morphological agrammatism following a right hemisphere stroke in a dextral patient. Brain and Language, 43, 642–667. Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97–113. Ombredane, A. (1950). L’aphasie et l’e´laboration de la pensee´ explicite. Paris: Presses Universitaires de France. Sachs, B., & Peterson, F. (1890). A study of cerebral palsies of early life, based upon analysis of one hundred and forty cases. Journal of Nervous and Mental Disease, 17, 295–332. Tissot, R., Mounin, G., & Lhermitte, F. (1973). L’Agrammatisme. Paris: Dessart. Van Eerdenbrugh, S. (1998). Tokentest bij kinderen. Unpublished thesis. School of Medicine. University of Ghent. Wallenberg, A. (1886). Ein Beitrag zur Lehre von den cerebralen Kinderla¨hmungen. Jahrbuch fu¨r Kinderheilkunde, 24, 384–439. Wechsler, D. (1987). Manual for the Wechsler Memory Scale—Revised. New York: Psychological Corp. Woods, B. T. (1995). Acquired childhood aphasia. In H. S. Kirshner (Ed.), Handbook of neurological speech and language disorders (pp. 415–430). New York: Dekker. Woods, B. T., & Teuber, L. (1978). Changing patterns of childhood aphasia. Annals of Neurology, 3, 273–280.