Mapping anterior temporal lobe language areas with fMRI: a multicenter normative study

Abstract

Removal of the anterior temporal lobe (ATL) is an effective surgical treatment for intractable temporal lobe epilepsy but carries a risk of language and verbal memory deficits. Preoperative localization of functional zones in the ATL might help reduce these risks, yet fMRI protocols in current widespread use produce very little activation in this region. Based on recent evidence suggesting a role for the ATL in semantic integration, we designed an fMRI protocol comparing comprehension of brief narratives (Story task) with a semantically shallow control task involving serial arithmetic (Math task). The Story > Math contrast elicited strong activation throughout the ATL, lateral temporal lobe, and medial temporal lobe bilaterally in an initial cohort of 18 healthy participants. The task protocol was then implemented at 6 other imaging centers using identical methods. Data from a second cohort of participants scanned at these centers closely replicated the results from the initial cohort. The Story-Math protocol provides a reliable method for activation of surgical regions of interest in the ATL. The bilateral activation supports previous claims that conceptual processing involves both temporal lobes. Used in combination with language lateralization measures, reliable ATL activation maps may be useful for predicting cognitive outcome in ATL surgery, though the validity of this approach needs to be established in a prospective surgical series.

Figure 1

Anterior temporal subregions used to quantify activation extent and reliability of activation across individual participants. Red = superior temporal pole, cyan = inferior temporal pole, light blue = anterior lateral, dark blue = posterior lateral, dark green = anterior ventral, light green = posterior ventral, orange = anterior medial, yellow = posterior medial. See Methods for anatomical definitions of each subregion.

Figure 2

Areas of greater activation for the Story condition relative to the Math condition in the MCW cohort (thresholded at whole-brain corrected p < .05), shown in serial sagittal sections through the left (top row) and right (middle row) hemisphere, and in serial coronal sections covering the temporal lobes (bottom row). Colors indicate voxel-wise thresholds at p < .005 (red), p< .0005 (orange), and p < .00005 (yellow). Stereotaxic locations are given in the upper left corner of each slice.

Figure 3

Overlap between activated areas for three fMRI language paradigms and regions typically resected in left anterior temporal lobe surgery (see Methods). Blue indicates temporal lobe regions activated with each paradigm (all thresholded at whole-brain corrected p < .05) that do not fall within the typical resection zone (see (Binder et al., 2008b) for a description of the Semantic Decision vs. Rest and the Semantic Decision vs. Tone Decision studies). Green indicates activated regions that overlap with the typical resection zone.

Figure 4

Areas of greater activation for the Story condition relative to the Math condition in the Multicenter cohort, shown in serial sagittal sections through the left (top row) and right (middle row) hemisphere, and coronal sections through the temporal lobes. Formatting as in Figure 2.

Figure 5

Representative individual subject activation maps (one subject from each center), shown in serial sagittal sections through the left hemisphere after stereotaxic normalization. Colors indicate areas of greater activation for the Story condition relative to the Math condition, thresholded at whole-brain corrected p< .05.

Figure 6

ATL areas showing consistent signal loss across participants. Green indicates overlap in at least 50%, red in 75%, and yellow in 90% of participants.