Presurgical language fMRI: Mapping of six critical regions

Abstract

Language mapping is a key goal in neurosurgical planning. fMRI mapping typically proceeds with a focus on Broca's and Wernicke's areas, although multiple other language-critical areas are now well-known. We evaluated whether clinicians could use a novel approach, including clinician-driven individualized thresholding, to reliably identify six language regions, including Broca's Area, Wernicke's Area (inferior, superior), Exner's Area, Supplementary Speech Area, Angular Gyrus, and Basal Temporal Language Area. We studied 22 epilepsy and tumor patients who received Wada and fMRI (age 36.4[12.5]; Wada language left/right/mixed in 18/3/1). fMRI tasks (two × three tasks) were analyzed by two clinical neuropsychologists who flexibly thresholded and combined these to identify the six regions. The resulting maps were compared to fixed threshold maps. Clinicians generated maps that overlapped significantly, and were highly consistent, when at least one task came from the same set. Cases diverged when clinicians prioritized different language regions or addressed noise differently. Language laterality closely mirrored Wada data (85% accuracy). Activation consistent with all six language regions was consistently identified. In blind review, three external, independent clinicians rated the individualized fMRI language maps as superior to fixed threshold maps; identified the majority of regions significantly more frequently; and judged language laterality to mirror Wada lateralization more often. These data provide initial validation of a novel, clinician-based approach to localizing language cortex. They also demonstrate clinical fMRI is superior when analyzed by an experienced clinician and that when fMRI data is of low quality judgments of laterality are unreliable and should be withheld. Hum Brain Mapp 38:4239-4255, 2017. © 2017 Wiley Periodicals, Inc.

Keywords: epilepsy; fMRI; language; neurology; neuropsychology; surgery.

Figure 1

Historic (left) and current (right) models of the language system. Left: “Speech areas: Evidence from stimulation,” modified from Penfield & Roberts, 1959. Right: A model reflecting more recent knowledge (circles are approximate). (1) Broca's Area, in the posterior third of the inferior frontal gyrus. (2) Exner's Area, in the posterior middle frontal gyrus. (3) Supplementary motor area. (4) Angular gyrus. (5) Wernicke's area, inferior (mid to anterior STG) and superior (posterior STG and supramarginal gyrus) components. (6) Basal temporal language areas. Note that anterior temporal cortex also appears critically involved in auditory naming (not highlighted). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Overview of clinical imaging protocol. An MPRAGE and other images were also acquired. Two sets of task‐related T2* images were typically acquired with each set including ON; VRN; and ARN. ON, object naming; VRN, verbal responsive naming; ARN, auditory responsive naming. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Example map, Case V. Conjunction of ON, visual responsive naming and ARN language maps. ON, object naming; ARN, auditory responsive naming. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Example divergent case with significant noise (Case E) showing maps generated by clinician 1 (red) and two (yellow), and the overlap (orange). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 5

Example divergent case where clinicians prioritized representations of different language regions (case O). Clinician 1 prioritized SMA (left, red) while clinician 2 better emphasized basal temporal language areas (right, yellow). Clinically this frequently occurs when the clinical question relates to different anatomical regions (e.g., frontal tumor vs. anterior temporal lobectomy). In this instance, the fixed threshold approach identified minimal temporal activation. [Color figure can be viewed at http://wileyonlinelibrary.com]