Prediction of Naming Outcome With fMRI Language Lateralization in Left Temporal Epilepsy Surgery

Abstract

Background and objectives: Naming decline after left temporal lobe epilepsy (TLE) surgery is common and difficult to predict. Preoperative language fMRI may predict naming decline, but this application is still lacking evidence. We performed a large multicenter cohort study of the effectiveness of fMRI in predicting naming deficits after left TLE surgery.

Methods: At 10 US epilepsy centers, 81 patients with left TLE were prospectively recruited and given the Boston Naming Test (BNT) before and ≈7 months after anterior temporal lobectomy. An fMRI language laterality index (LI) was measured with an auditory semantic decision-tone decision task contrast. Correlations and a multiple regression model were built with a priori chosen predictors.

Results: Naming decline occurred in 56% of patients and correlated with fMRI LI (r = -0.41, p < 0.001), age at epilepsy onset (r = -0.30, p = 0.006), age at surgery (r = -0.23, p = 0.039), and years of education (r = 0.24, p = 0.032). Preoperative BNT score and duration of epilepsy were not correlated with naming decline. The regression model explained 31% of the variance, with fMRI contributing 14%, with a 96% sensitivity and 44% specificity for predicting meaningful naming decline. Cross-validation resulted in an average prediction error of 6 points.

Discussion: An fMRI-based regression model predicted naming outcome after left TLE surgery in a large, prospective multicenter sample, with fMRI as the strongest predictor. These results provide evidence supporting the use of preoperative language fMRI to predict language outcome in patients undergoing left TLE surgery.

Classification of evidence: This study provides Class I evidence that fMRI language lateralization can help in predicting naming decline after left TLE surgery.

Figure 1. Typical Extent of fMRI Activation to the SD-TD Task Contrast

(A) Frequency of activations across individual patient maps. Voxels that contained significant activation in <25% of patients are shown in purple; voxels active in 25% to 50% of patients, in red; and voxels active in >50% of patients, in yellow. Activation tended to be left-lateralized in most patients and included areas known to be involved in language and semantic processing. (B) Example activation patterns in 3 individual patients taken from the prediction analysis: the most right and left-lateralized patients in our sample and a patient with representative symmetric activation. Of note, patients with atypical lateralization tend to activate homologous contralateral regions. LI = laterality index; SD-TD = semantic decision–tone decision.

Figure 2. Scatterplot of Individual Patient BNT Score Change by fMRI LI

Positive fMRI laterality indices (LIs) correspond to left-lateralized patients. Reliable change index (RCI) calculated from the right temporal lobe epilepsy cohort is shown as a dashed line, denoting a reliable decline. All but 1 of the declining patients had left-lateralized fMRI LIs. BNT = Boston Naming Test.

Figure 3. Scatterplot of Predicted vs Actual Change in BNT Scores

Red dotted lines indicate the reliable change index (RCI). Patients in the lower right quadrant were not predicted to have decline based on the regression model but experienced a postoperative decline, as defined by the RCI. BNT = Boston Naming Test.

Figure 4. Bootstrap Distribution of Average Prediction Error of the Complete Regression Model

Each model was fitted with 90% of the patients and error measured with the held back 10%. Bootstrap distribution was created by repeating this using random resampling for 10,000 iterations. Mean error is shown as the dashed line, with the range denoting the 10% and 90% quantiles. BNT = Boston Naming Test.