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Summary: Purpose: We sought to illustrate the value of functional magnetic resonance imaging (fMRI) in the presurgical assessment of hemispheric dominance for language by means of an illustrative case report.
Methods: fMRI with two language paradigms was performed in a right-handed patient without familial sinistrality suffering from a left frontal focal epilepsy.
Results: Both fMRI paradigms revealed unequivocally lateralized right hemispheric activation. Atypical language representation was confirmed by Wada test. The further presurgical workup could be restricted to subdural strip recordings instead of the initially intended grid implantation. After resective surgery, no language deficits were apparent.
Conclusions: Hemispheric dominance for language should be assessed by fMRI in all patients before surgery in areas potentially relevant for language in either cerebral hemisphere. fMRI may influence the further diagnostic workup and should be performed before other invasive diagnostic procedures.
Right hemispheric dominance for language is exceptional in right-handers without familial sinistrality, estimates of the incidence ranging from <2% (based on lesional studies) (1) to ∼4–5%(2–4) (based on Wada test studies). Functional magnetic resonance imaging (fMRI) allows noninvasive assessment of cerebral activation associated with language tasks. Several studies have shown a high correspondence between fMRI and the Wada test in the determination of hemispheric dominance for language (5–7). However, the clinical value of fMRI is still under debate.
We present a case in which fMRI unexpectedly revealed right hemispheric language dominance and influenced the further presurgical diagnostic assessment.
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A 39-year-old patient was admitted for presurgical assessment of a pharmacoresistant focal epilepsy with complex partial and secondarily generalized tonic–clonic seizures. At age 10 years, he had a severe head trauma with a left frontal contusion; seizure onset was at age 24 years. The patient had no focal neurologic deficits. The neuropsychological examination revealed average global intelligence and attention, average visuospatial memory performance, and marked verbal memory impairment. The patient was right-handed according to the Edinburgh inventory (8); there was no familial sinistrality.
Ictal surface EEG recordings revealed an extended regional left frontotemporal seizure onset. Because of the presumed left hemispheric language dominance, implantation of an extended left frontolateral subdural grid was planned to map the frontal language area. Before the grid implantation, fMRI was performed on a 1.5-T scanner. Two language paradigms were applied: (a) a paradigm requiring the finding of synonyms in a set of simultaneously presented words with parallel color-discrimination tasks as baseline condition (9); and (b) covert generation of verbs to visually presented nouns versus fixation of a crosshair as control condition (7). The paradigms were arranged as block designs with eight activation and nine control conditions, with every block lasting 20 s. Seventy-three volumes (five “dummy scans” at the beginning of every study) of a GE-EPI-sequence (slice thickness, 5 mm; gap, 0.5 mm; matrix, 128 × 128; FoV, 256 mm; TE, 66 ms; TR, 5 s) with 16 axial slices were acquired. For anatomic reference, a T1-weighted 3D magnetization-prepared rapid acquisition gradient echo (MPRAGE) sequence (TR, 9.7 ms; TE, 4 ms; TI, 300 ms; flip angle, 12 degrees) with isotropic 1-mm3 voxels was performed. Data evaluation [software BrainVoyager, Brain Innovation B.V., the Netherlands, and Max Planck Society e.V., Germany (10)] included 3D motion correction and spatial and temporal smoothing in the frequency domain. Statistical maps were calculated by correlation analysis and superimposed onto the anatomic images (threshold: correlation coefficient, r > 0.5). Lateralization indices (LI, right minus left/right plus left) (6) were calculated from the numbers of suprathreshold voxels in Broca's and Wernicke's areas and their right-hemispheric counterparts.
The semantic decision task elicited exclusive right-sided activations in the lateral frontal lobe, in the lateral temporal lobe, and in the dorsolateral prefrontal cortex (Fig.1); the LI was +1. In the verb-generation task, there was a minor additional activation focus in the left lateral frontal lobe, but no temporal activation on either side (Fig.2); the LI was +0.9. Additional activations were found with both paradigms in occipital visual areas, parietal association areas, and in the supplementary motor area (not shown). Right-hemispheric language dominance was confirmed by the Wada test [left carotid injection of 170 mg sodium amytal: no language deficit; right-sided injection (performed the next day): global aphasia].
Figure 1. Functional magnetic resonance imaging (fMRI) activation in the “semantic decision” paradigm. Activations in frontal and temporoparietal speech areas exclusively in the right hemisphere. Note left frontal contusion sparing the frontal operculum.
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Figure 2. In the verb-generation task, similar right frontal activation pattern; small additional activation focus in the left frontal operculum.
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Because of the exclusive right-hemispheric language dominance, only small subdural strips were implanted for the delineation of the seizure-onset zone instead of the initially intended grid. A wedge-shaped left frontopolar resection was performed extending from the cortical surface to the frontal horn of the lateral ventricle. The resection included the anterior two thirds of the gyrus rectus, the medial, anterior, and lateral orbital gyri, and the rostral parts of the superior and middle frontal gyri. The inferior frontal gyrus was spared.
After the operation, the patient had no neurologic deficit. Language deficits were excluded by standardized neuropsychological testing. To the present, the patient has remained seizure free (5 months after surgery).
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Our case illustrates that atypical language dominance has to be taken into consideration in right-handers without familial sinistrality.
Early left-brain injury may induce a shift of language skills to the right hemisphere (2). In right-handed epilepsy patients with early left-hemisheric lesions, atypical (i.e., right or bilateral) language representation occurs in ∼20%(2). According to Springer et al. (11), the frequency of atypical language representation in epilepsy patients strongly correlates with the age at onset of the seizures: in patients with late seizure onset (after age 15 years), atypical language dominance is not more frequent than in the normal population. Conversely, studies on reorganization of language functions after focal brain injury suggest that contrahemispheral contributions can emerge even in adulthood (12). Thus it remains open whether right-hemispheric language dominance in our patient was primary or induced by the trauma.
Because a left-hemispheric dominance was presumed, implantation of a subdural grid was thought to be inevitable, and initially we did not intend to perform a Wada test. The fMRI results changed the further diagnostic workup: instead of the large subdural grid, only subdural strip electrodes had to be implanted. This finding stresses the suggestion that fMRI should be performed before any invasive procedure in the assessment of cerebral language representation.
In addition, this case demonstrates the risk of aphasia induced by surgery in right-hemispheric areas potentially involved in language, even in right-handers without familial sinistrality. Therefore we propose performing fMRI in all patients before surgery (or any other interventional procedure) in areas potentially relevant for language in either cerebral hemisphere.
However, the degree and pattern of activation in fMRI strongly depend on the applied language paradigm and evaluation strategy. No generally accepted standard exists concerning fMRI language studies. Because the value of any method used to determine hemispheric language dominance depends on its sensitivity and specifity, further studies are mandatory to evaluate different fMRI task paradigms and evaluation strategies against established invasive procedures such as the Wada test or cortical stimulation.