William T. Cahill. Wes Houston. Repetition and the arcuate fasciculus. Received: 3 October 1994. Accepted: 30 December 1994. J. E. Shuren (N~) ⢠B. K. Schefft.
J Neurol (1995) 242 : 596-598 © Springer-Verlag 1995
Jeffrey E. Shuren Bruce K. Schefft H w a - S h a i n Yeh M i c h a e l D. Privitera W i l l i a m T. Cahill Wes H o u s t o n
Received: 3 October 1994 Accepted: 30 December 1994 J. E. Shuren (N~) • B. K. Schefft M. D. Privitera • W. T. Cahill Department of Neurology, 4010 Medical Sciences Building (ML 525), University of Cincinnati College of Medicine, 231 Bethesda Avenue, Cincinnati, OH 45267-0525, USA H.-S. Yeh Department of Neurosurgery, 4411 Medical Sciences Building (ML 515), University of Cincinnati College of Medicine, 231 Bethesda Avenue, Cincinnati, OH 45267-0515, USA B. K. Schefft • W. Houston Department of Psychology, Dyer Hall 401-C (ML 376), University of Cincinnati, Cincinnati, OH 45221-0376, USA
Repetition and the arcuate fasciculus
A b s t r a c t According to the traditional m o d e l of language organization, repetition deficits arise following damage to the arcuate fasciculus of the d o m i n a n t hemisphere (conduction aphasia). C o n d u c t i o n aphasia m a y result from lesions that spare the arcuate fasciculus. However, these patients have atypical language organization. We describe a m a n with n o r m a l language architecture who u n d e r w e n t a resection of the anterior portion of his arcuate fasciculus and retained his ability to repeat words and sentences. We propose that the arcuate fasciculus is not necessary for speech repetition by the lexical route.
Introduction The arcuate fasciculus is a white matter tract that lies in the inferior portion of the superior l o n g i t u d i n a l fasciculus, superior to the insula and extreme capsule, c o n n e c t i n g temporal and frontal l a n g u a g e zones. Lesions of this structure are thought to produce impaired speech repetition [25]. We report the case of a m a n who retained the ability to repeat speech following anterior arcuate fasciculus resection as part of surgical treatment for his epilepsy.
Case report A 33-year-old right-handed man who underwent resection of a left frontal tumor in 1989 returned with a 1-year history of increasing seizure frequency, hesitancy and word-finding pauses in spontaneous speech, and right upper extremity weakness secondary to tu-
K e y w o r d s Repetition • Arcuate fasciculus • C o n d u c t i o n aphasia Magnetic resonance i m a g i n g Cortical stimulation
mor recurrence. Left hemisphere language dominance was established by cortical stimulation through chronically implanted subdural electrodes. Broca's and Wemicke's areas were identified by the patient's inability to read during cortical stimulation of these sites. Tumor resection (grade II gemistocytic astrocytoma) was performed with removal of the posterior segments of the left inferior and middle frontal cortices, the white matter deep to it and the white matter beneath the anterior somatosensory cortex including the anterior arcuate fasciculus and inferior two-thirds of the superior longitudinal fasciculus. The frontal operculum, supramarginal cortex, and superior temporal cortex were spared. This was confirmed by the neurosurgeon who performed the operation (H.Y.) and postsurgical MRI (Fig. 1). The lesion was mapped using the Damasio and Damasio templates [6]. On examination he had a slight pronator drift on the right and a slight decrease in fine motor movements of the right hand. On formal neuropsychological testing, performed 2 days and again at 3 weeks following surgery, the patient had a verbal IQ of 80, a performance IQ of 85, and a full-scale IQ of 81 on the Wechsler Adult Intelligence Scale-Revised (low average performance for his demographic group). He had fluent speech with occasional phonemic paraphasias (e.g., "plower" for "flower"). He had slight deficits in
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Fig. 1 Tl-weighted MRI in coronal and axial planes demonstrates left frontoparietal resection inclusive of the arcuate fasciculus confrontation naming [50/60 (lOth percentile) Boston Naming Test-Revised], syntactic production [53/60 (normal score 59.3) Inflectional Morphology TestJ, and oral/written spelling [2nd and 6th percentile respectively on the corresponding Multilingual Aphasia Examination (MAE) subtestsJ as well as a phonological alexia [he read 12 of 30 nonwords correctly on subtest 1, 28 of 30 regular words on subtest 2, and 25 of 30 irregular words on subtest 3 of the Battery of Adult Reading Function (Coslett et al. 1984; unpublished experimental edition)]. His verbal fluency on the MAE was profoundly impaired (< 1st percentile). His aural and reading comprehension (41 st and 59th percentile respectively on the MAE) were intact. He demonstrated normal speech repetition on the repetition sections of the MAE (11/14), Western Aphasia Battery (92/100), and Boston Diagnostic Aphasia Examination (10/10 Repetition of Words; 15/16 Repeating Phrases). The errors he made were either intrusions (e,g., "The phantom soared across the foggy heath" was repeated as "The phantom soared across the foggy phantom heath") or omissions (e.g., "'Pack my box with five dozen jugs of liquid veneer" was repeated as "Pack my box with five of"). Repetition of nonwords, however, was not assessed. The patient's immediate (21-32nd percentile) and delayed (21-32nd percentile) recall of the Denman Story were intact, as was his copy (17th percentile) and immediate (47-55th percentile) and delayed (21-32nd percentile) recall of the Rey Osterrieth Complex Figure consistent consistent with preserved verbal and nonverbal recent memory. However, his digit span was four forwards and three backwards, whereas his visual span was six forwards and six backwards consistent with impaired auditory-verbal (span) immediate memory. His visuoperceptual skills were preserved as assessed by the Facial Recognition Test (39th percentile) and the Visual Form Discrimination Test (84th percentile). His visuospatial skills as assessed by the Judgment of Line Orientation Test (9th percentile) were borderline but still within the range of normal for his demographic group. Oral and limb praxis, right-left orientation, and finger localization were intact. There was no evidence of extinction or hemispatial neglect.
Discussion According to the traditional model of language, Wernicke's area (speech comprehension) is connected to Broca's area (speech production) by a white matter tract purported to be the arcuate fasciculus [ 1, 24]. T h o u g h the existence o f the arcuate fasciculus as a distinct white mat-
ter tract has been debated, studies in rhesus m o n k e y s support the existence of white matter connections between Wernicke's area and Broca's area homologues running in the arcuate fasciculus [21]. Isolated damage to the arcuate fasciculus is thought to produce impaired repetition with relatively fluent speech and preserved comprehension (conduction aphasia) by disconnecting Broca's area from Wernicke's area [8, 24]. However, several cases have been reported in which the arcuate fasciculus was not damaged and yet a repetition disturbance was present [3, 10-13, 15, 18, 19, 25]. Most of these patients have had lesions of the superior temporal cortex. More recently, conduction aphasia has been attributed to mechanisms other than a disconnection syndrome [9, 17, 22, 23], such as damage to the phonological output system (see [16]). Repetition deficits m a y arise from several different mechanisms, including impaired phonological analysis (Wernicke's aphasia), impaired phonological memory, selection, or sequencing (conduction aphasia), or impaired motor speech programming and execution (Broca's aphasia). Repetition of speech m a y be mediated by at least two separate processes: one in which stored whole word representations are activated (lexical route) and one in which there is direct phonological encoding from immediate m e m o r y without the activation of stored whole word representations (nonlexical route).Words can be repeated by the lexical and nonlexical route, but nonwords can only be repeated by the nonlexical route. A third route m a y exist whereby repetition is performed by lexical-semantic processing. Patients with deep dysphasia make semantic errors when they try to repeat spoken words and cannot repeat nonwords [20], suggesting that there is damage to both the nonlexical and lexical routes. Coslett et al. [4] demonstrated that transcortical sensory aphasics with preserved processing by the lexical and nonlexical routes m a y spontaneously correct syntactic errors, whereas transcortical sensory aphasics with impaired lexical repetition do not correct syntactic errors in tests of repetition. The tendency to spontaneously correct syntactic errors in repetition m a y also occur in mixed transcortical motor aphasics ("isolation syndrome" [7]). Repetition of nonwords and of sentences with syntactic errors was not assessed in our patient. Therefore, whether or not the anterior arcuate fasciculus is important for repetition by the nonlexical route cannot be determined from this case. Because repetition by the lexical and nonlexical routes requires m a n y of the same processes as reading, the presence of a phonological alexia in our patient suggests that his nonlexical route for repetition m a y have been impaired. The findings in our patient represent a clinico-anatomical double dissociation. As mentioned above, several patients in the literature have been described who showed relatively isolated deficits in speech repetition (conduction aphasia) as the result of lesions that spared the arcuate fasciculus. This suggests that the arcuate fasciculus is
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not necessary for speech repetition but does not exclude a role in repetition. Our patient, on the other hand, had the anterior portion o f his arcuate fasciculus resected without evidence of impaired repetition. No case has ever been reported in which repetition deficits arose following isolated damage to the arcuate fasciculus. Therefore, it is unlikely that the arcuate fasciculus plays a significant, if any, role in speech repetition by the lexical route. Several authors have posited, based on patient studies, that right hemispheric pathways mediate speech repetition in some patients [2, 14, 15, 18]. These patients, however, also tended to have atypical language organization with auditory comprehension localized to the right hemisphere. Mendez and Benson [19] proposed that conduction aphasia, in at least some patients with left temporal lobe lesions sparing the arcuate fasciculus, arises owing to a disconnection o f auditory comprehension in the right hemisphere from the speech output area in the left hemisphere. It is possible that, as a result of the relatively slow growth of his tumor (as compared with an infarct), our patient's speech repetition was mediated by an atypical pathway in either his left or right hemisphere. However, the presence of increasing aphasia secondary to an enlarging left hemi-
sphere tumor, syntactic deficits and phonemic paraphasias following left frontal tumor resection, and mapping o f B r o c a ' s and W e m i c k e ' s areas in the left hemisphere by cortical stimulation support left hemisphere dominance for language as well as the presence of normal language architecture. Alternatively, speech repetition m a y be mediated by a white matter tract other than the arcuate fasciculus. Damasio and Damasio [5] noted that some conduction aphasics have lesions that spare the arcuate fasciculus but involve the supratemporal region. Conduction aphasia in these cases m a y have arisen from damage to a second white matter pathway extending from the superior temporal g y m s to Broca's area in the extreme capsule inferior to the insula. However, all these patients had lesions involving superior temporal cortex which m a y have resulted in the repetition deficits rather than involvement of the white matter tract itself. We suggest that the arcuate fasciculus by itself is not necessary for speech repetition by the lexical route. In accordance with current language models, cortical processing is probably responsible for speech repetition.
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