Characterization of atypical language activation patterns in focal epilepsy

Berl, Madison M.; Zimmaro, Lauren A.; Khan, Omar; Dustin, Irene; Ritzl, Eva K.; Duke, Elizabeth S.; Sepeta, Leigh N.; Satô, Susumu; Theodore, William H.; Gaillard, William D.

doi:10.1002/ana.24015

Cited by 131 publications

(187 citation statements)

References 59 publications

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“…DeSalvo et al language networks, which has been previously observed (16). Although language networks of patients with atypical language dominance included more brain regions, their classification by using this method was robust, at 100% (four of four), assuming that the patient with discordant classification had typical language laterality.…”

Section: Technical Developments: Resting-state Functional Mr Imaging mentioning

confidence: 77%

Resting-State Functional MR Imaging for Determining Language Laterality in Intractable Epilepsy

DeSalvo¹,

Tanaka²,

Douw

et al. 2016

Radiology

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Purpose:To measure the accuracy of resting-state functional magnetic resonance (MR) imaging in determining hemispheric language dominance in patients with medically intractable focal epilepsies against the results of an intracarotid amobarbital procedure (IAP). Materials and Methods:This study was approved by the institutional review board, and all subjects gave signed informed consent. Data in 23 patients with medically intractable focal epilepsy were retrospectively analyzed. All 23 patients were candidates for epilepsy surgery and underwent both IAP and resting-state functional MR imaging as part of presurgical evaluation. Language dominance was determined from functional MR imaging data by calculating a laterality index (LI) after using independent component analysis. The accuracy of this method was assessed against that of IAP by using a variety of thresholds. Sensitivity and specificity were calculated by using leave-one-out cross validation. Spatial maps of language components were qualitatively compared among each hemispheric language dominance group. Results:Measurement of hemispheric language dominance with resting-state functional MR imaging was highly concordant with IAP results, with up to 96% (22 of 23) accuracy, 96% (22 of 23) sensitivity, and 96% (22 of 23) specificity. Composite language component maps in patients with typical language laterality consistently included classic language areas such as the inferior frontal gyrus, the posterior superior temporal gyrus, and the inferior parietal lobule, while those of patients with atypical language laterality also included non-classical language areas such as the superior and middle frontal gyri, the insula, and the occipital cortex. Conclusion:Resting-state functional MR imaging can be used to measure language laterality in patients with medically intractable focal epilepsy.q RSNA, 2016

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Section: Technical Developments: Resting-state Functional Mr Imaging mentioning

confidence: 77%

Resting-State Functional MR Imaging for Determining Language Laterality in Intractable Epilepsy

DeSalvo¹,

Tanaka²,

Douw

et al. 2016

Radiology

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“…Different patterns of language organization are described in the literature (Goldmann and Golby, 2005;Dijkstra and Ferrier, 2013;Berl et al, 2014). Here, we consider (see Figure 3) three atypical patterns of hemispheric lateralization.…”

Section: Patterns Of Language Reorganizationmentioning

confidence: 94%

“…Neuroimaging methods have provided more precise function-to-structure mapping (Price, 2012) and suggested that language operations are supported by a large, flexible cerebral network (i.e., including areas located outside the classical language regions) distributed within and across hemispheres (Vigneau et al, 2011;Price, 2012). Moreover, the concept of hemispheric dominance has also evolved from dichotomized (left vs. right) processing toward the idea that continuous participation of both hemispheres is the norm (Jung-Beeman, 2005;Berl et al, 2014). According to this idea, the hemispheres interact continuously (Banich, 1995;Gazzaniga, 2000;Bloom and Hynd, 2005;van der Knaap and van der Ham, 2011;Perrone-Bertolotti et al, 2013a,b).…”

Section: General Considerationsmentioning

confidence: 99%

“…The typical left-hemisphere (LH) language lateralization (see Figure 2) may be modulated in neurological condition (Rasmussen and Milner, 1977;Springer et al, 1999), and language representation may be atypical in patients with disorders such as epilepsy (Billingsley et al, 2001;Adcock et al, 2003;Sabbah et al, 2003;Berl et al, 2005Berl et al, , 2014Brázdil et al, 2005;Goldmann and Golby, 2005;Thiel et al, 2006;Lee et al, 2008;Rosenberger et al, 2009;Yu et al, 2011;Dijkstra and Ferrier, 2013).…”

Section: Patterns Of Language Reorganizationmentioning

confidence: 99%

“…Here, we consider (see Figure 3) three atypical patterns of hemispheric lateralization. One atypical pattern is the RH dominance which suggests that language networks do 'shift' from the LH to the RH, usually between homologous regions (Gaillard et al, 2002;Thivard et al, 2005;Dijkstra and Ferrier, 2013;Berl et al, 2014). This pattern may be attributed to the removal or the reduction of normal transcallosal inhibition (Chiarello and Maxfield, 1996;Bloom and Hynd, 2005; van der Knaap and van der Ham, 2011) responsible for the LH dominance.…”

Section: Patterns Of Language Reorganizationmentioning

confidence: 99%

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What do patients with epilepsy tell us about language dynamics? A review of fMRI studies

Baciu

Perrone‐Bertolotti

2015

Reviews in the Neurosciences

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AbstractThe objective of this review is to resume major neuroimaging findings on language organization and plasticity in patients with focal and refractory epilepsy, to discuss the effect of modulatory variables that should be considered alongside patterns of reorganization, and to propose possible models of language reorganization. The focal and refractory epilepsy provides a real opportunity to investigate various types of language reorganization in different conditions. The ‘chronic’ condition (induced by the epileptogenic zone or EZ) is associated with either recruitment of homologous regions of the opposite hemisphere or recruitment of intrahemispheric, nonlinguistic regions. In the ‘acute’ condition (neurosurgery and EZ resection), the initial interhemispheric shift (induced by the chronic EZ) could follow a reverse direction, back to the initial hemisphere. These different patterns depend on several modulatory factors and are associated with various levels of language performance. As a neuroimaging tool, functional magnetic resonance imaging enables the detailed investigation of both hemispheres simultaneously and allows for comparison with healthy controls, potentially creating a more comprehensive and more realistic picture of brain-language relations. Importantly, functional neuroimaging approaches demonstrate a good degree of concordance on a theoretical level, but also a considerable degree of individual variability, attesting to the clinical importance with these methods to establish, empirically, language localization in individual patients. Overall, the unique features of epilepsy, combined with ongoing advances in technology, promise further improvement in understanding of language substrate.

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Naming fMRI predicts the effect of temporal lobe resection on language decline

Trimmel

Graan

Gonzálvez

et al. 2019

Ann Clin Transl Neurol

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Objective: To develop language functional MRI (fMRI) methods that accurately predict postsurgical naming decline in temporal lobe epilepsy (TLE). Methods: Forty-six patients with TLE (25 left) and 19 controls underwent two overt fMRI paradigms (auditory naming and picture naming, both with active baseline conditions) and one covert task (verbal fluency). Clinical naming performance was assessed preoperatively and 4 months following anterior temporal lobe resection. Preoperative fMRI activations were correlated with postoperative naming decline. Individual laterality indices (LI) were calculated for temporal (auditory and picture naming) and frontal regions (verbal fluency) and were considered as predictors of naming decline in multiple regression models, along with other clinical variables (age at onset of seizures, preoperative naming scores, hippocampal volume, age). Results: In left TLE patients, activation of the left posterior inferior temporal gyrus during auditory naming and activation of left fusiform gyrus during picture naming were related to greater postoperative naming decline. Activation LI were the best individual predictors of naming decline in a multivariate regression model. For picture naming, an LI of higher than 0.34 gave 100% sensitivity and 92% specificity (positive predictive value (PPV) 91.6%). For auditory naming, a temporal lobe LI higher than 0.18 identified all patients with a clinically significant naming decline with 100% sensitivity and 58% specificity (PPV: 58.3%). No effect was seen for verbal fluency. Interpretation: Auditory and picture naming fMRI are clinically applicable to predict postoperative naming decline after left temporal lobe resection in individual patients, with picture naming being more specific. 2186

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Characterization of atypical language activation patterns in focal epilepsy

Cited by 131 publications

References 59 publications

Resting-State Functional MR Imaging for Determining Language Laterality in Intractable Epilepsy

Resting-State Functional MR Imaging for Determining Language Laterality in Intractable Epilepsy

What do patients with epilepsy tell us about language dynamics? A review of fMRI studies

Naming fMRI predicts the effect of temporal lobe resection on language decline

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