Imaging language networks before and after anterior temporal lobe resection: Results of a longitudinal fMRI study

Bonelli, S; Thompson, Pamela J.; Yogarajah, Mahinda; Vollmar, Christian; Powell, Harrison; Symms, Mark R.; McEvoy, Andrew W.; Micallef, Caroline; Koepp, Matthias J.; Duncan, John S.

doi:10.1111/j.1528-1167.2012.03433.x

Cited by 149 publications

(189 citation statements)

References 46 publications

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“…An approach approximating the approach validated by Binder et al (Sabsevitz et al, 2003), which uses a semantic decision task paired with an active control and uses a laterality index in analysis (whole‐brain or regional), was reported by up to 7% of programs. A similar approach to that used by Bonelli et al (2012), lateralizing language by completing both verbal fluency and noun–verb generation, using a crosshair control and region of interest analysis, was reported by up to 5% of programs.…”

Section: Resultsmentioning

confidence: 96%

“…Conversely, it is also frequently seen as opposing standardization, objectivity, and the research method. Note, however, that the best validation studies to date do actually use a highly standardized approach (Bonelli et al, 2012; Janecek et al, 2013; Szaflarski et al, 2017). As in a more comprehensive survey of clinicians' experience of clinical language fMRI (Benjamin et al, 2018), analysts frequently (46%) report that language laterality judged by fMRI has disagreed with that yielded by other methods in at least some instances.…”

Section: Discussionmentioning

confidence: 99%

“…It is our view that recommending a single paradigm for clinical use is not yet possible; head to head comparison of the existing protocols that have to date been validated for a range of purposes, in a range of populations, remains a priority. Note that teams can obtain and become familiar with many of the best‐studied protocols free of charge by emailing the relevant authors (Bonelli et al, 2012; Janecek et al, 2013). Versions of key tasks are also freely available at cogneuro.net/omfmri.…”

Section: Discussionmentioning

confidence: 99%

“…Language functional magnetic resonance imaging (fMRI) is an imaging method and neurocognitive assessment validated for predicting language decline after temporal lobe surgery (Bonelli et al, 2012; Sabsevitz et al, 2003). The demonstration of its equivalence or superiority to the Wada test (Intracarotid Amobarbital Testing; IAT) with certain protocols (Janecek et al, 2013), and its noninvasive nature, has led to its widespread adoption in neurosurgical planning.…”

Section: Introductionmentioning

confidence: 99%

“…For example, software packages often implement different solutions in key analysis steps, and fMRI validation studies have used a range of packages such as AFNI (Sabsevitz et al, 2003), SPM (Bonelli et al, 2012), and custom software (Benjamin et al, 2017). Each step in data preprocessing alters the output; and the literature validating fMRI preprocessing may or may not include explicit realignment of echo‐planar imaging (EPI) data, or involvement of explicit smoothing of 2 mm, 10 mm, or an unspecified amount (Benjamin et al, 2017; Bonelli et al, 2012; Janecek et al, 2013). The approach to identification of task‐related signal also varies, with both general linear modeling and correlation coefficients in use.…”

Section: Introductionmentioning

confidence: 99%

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Presurgical language fMRI: Technical practices in epilepsy surgical planning

Benjamin¹,

Dhingra²,

et al. 2018

Human Brain Mapping

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Little is known about how language functional MRI (fMRI) is executed in clinical practice in spite of its widespread use. Here we comprehensively documented its execution in surgical planning in epilepsy. A questionnaire focusing on cognitive design, image acquisition, analysis and interpretation, and practical considerations was developed. Individuals responsible for collecting, analyzing, and interpreting clinical language fMRI data at 63 epilepsy surgical programs responded. The central finding was of marked heterogeneity in all aspects of fMRI. Most programs use multiple tasks, with a fifth routinely using 2, 3, 4, or 5 tasks with a modal run duration of 5 min. Variants of over 15 protocols are in routine use with forms of noun–verb generation, verbal fluency, and semantic decision‐making used most often. Nearly all aspects of data acquisition and analysis vary markedly. Neither of the two best‐validated protocols was used by more than 10% of respondents. Preprocessing steps are broadly consistent across sites, language‐related blood flow is most often identified using general linear modeling (76% of respondents), and statistical thresholding typically varies by patient (79%). The software SPM is most often used. fMRI programs inconsistently include input from experts with all required skills (imaging, cognitive assessment, MR physics, statistical analysis, and brain–behavior relationships). These data highlight marked gaps between the evidence supporting fMRI and its clinical application. Teams performing language fMRI may benefit from evaluating practice with reference to the best‐validated protocols to date and ensuring individuals trained in all aspects of fMRI are involved to optimize patient care.

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Section: Resultsmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Presurgical language fMRI: Technical practices in epilepsy surgical planning

Benjamin¹,

Dhingra²,

et al. 2018

Human Brain Mapping

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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

Berl

Zimmaro

Khan

et al. 2014

Annals of Neurology

140

177

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Objective Functional magnetic resonance imaging is sensitive to the variation in language network patterns. Large populations are needed to rigorously assess atypical patterns, which, even in neurological populations, are a minority. Methods We studied 220 patients with focal epilepsy and 118 healthy volunteers who performed an auditory description decision task. We compared a data-driven hierarchical clustering approach to the commonly used a priori laterality index (LI) threshold (LI < 0.20 as atypical) to classify language patterns within frontal and temporal regions of interest. We explored (n = 128) whether IQ varied with different language activation patterns. Results The rate of atypical language among healthy volunteers (2.5%) and patients (24.5%) agreed with previous studies; however, we found 6 patterns of atypical language: a symmetrically bilateral, 2 unilaterally crossed, and 3 right dominant patterns. There was high agreement between classification methods, yet the cluster analysis revealed novel correlations with clinical features. Beyond the established association of left-handedness, early seizure onset, and vascular pathology with atypical language, cluster analysis identified an association of handedness with frontal lateralization, early seizure onset with temporal lateralization, and left hemisphere focus with a unilateral right pattern. Intelligence quotient was not significantly different among patterns. Interpretation Language dominance is a continuum; however, our results demonstrate meaningful thresholds in classifying laterality. Atypical language patterns are less frequent but more variable than typical language patterns, posing challenges for accurate presurgical planning. Language dominance should be assessed on a regional rather than hemispheric basis, and clinical characteristics should inform evaluation of atypical language dominance. Reorganization of language is not uniformly detrimental to language functioning.

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Imaging language networks before and after anterior temporal lobe resection: Results of a longitudinal fMRI study

Cited by 149 publications

References 46 publications

Presurgical language fMRI: Technical practices in epilepsy surgical planning

Presurgical language fMRI: Technical practices in epilepsy surgical planning

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

Characterization of atypical language activation patterns in focal epilepsy

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