A comparison of five fMRI protocols for mapping speech comprehension systems

Abstract

Aims: Many fMRI protocols for localizing speech comprehension have been described, but there has been little quantitative comparison of these methods. We compared five such protocols in terms of areas activated, extent of activation, and lateralization.

Methods: fMRI BOLD signals were measured in 26 healthy adults during passive listening and active tasks using words and tones. Contrasts were designed to identify speech perception and semantic processing systems. Activation extent and lateralization were quantified by counting activated voxels in each hemisphere for each participant.

Results: Passive listening to words produced bilateral superior temporal activation. After controlling for prelinguistic auditory processing, only a small area in the left superior temporal sulcus responded selectively to speech. Active tasks engaged an extensive, bilateral attention, and executive processing network. Optimal results (consistent activation and strongly lateralized pattern) were obtained by contrasting an active semantic decision task with a tone decision task. There was striking similarity between the network of brain regions activated by the semantic task and the network of brain regions that showed task-induced deactivation, suggesting that semantic processing occurs during the resting state.

Conclusions: fMRI protocols for mapping speech comprehension systems differ dramatically in pattern, extent, and lateralization of activation. Brain regions involved in semantic processing were identified only when an active, nonlinguistic task was used as a baseline, supporting the notion that semantic processing occurs whenever attentional resources are not controlled. Identification of these lexical-semantic regions is particularly important for predicting language outcome in patients undergoing temporal lobe surgery.

Figure 1

Group fMRI activation maps from three passive listening experiments. Top: Passive listening to words relative to resting. Middle: Passive listening to tones relative to resting. Bottom: Passive listening to words relative to tones. Data are displayed as serial sagittal sections through the brain at 9-mm intervals. X-axis locations for each slice are given in the top panel. Green lines indicate the stereotaxic Y and Z origin planes. Hot colors (red-yellow) indicate positive activations and cold colors (blue-cyan) negative activations for each contrast. All maps are thresholded at a whole-brain corrected P < 0.05 using voxel-wise P < 0.0001 and cluster extent > 200 mm³. The three steps in each color continuum represent voxel-wise P thresholds of 10⁻⁴, 10⁻⁵, and 10⁻⁶.

Figure 2

Group fMRI activation maps from three active listening experiments. Top: Semantic Decision relative to resting. Middle: Tone Decision relative to resting. Bottom: Semantic Decision relative to Tone Decision. Display conventions as described for Figure 1.

Figure 3

Group fMRI activation map from the Semantic Decision – Phoneme Decision contrast.

Figure 4

A comparison of left hemisphere areas activated by the Semantic Decision task relative to the Phoneme Decision task (top) and areas active during Rest relative to the Tone Decision task (bottom).

Figure 5

Overlap of the Semantic Decision – Rest and Semantic Decision – Tone Decision activations with a map of left anterior temporal lobe (ATL) resections in 23 epilepsy patients. ATL resection volumes were mapped in each patient by registration and subtraction of pre- and post-operative structural MRI scans. These resection volumes were then combined in stereotaxic space to produce a map showing the probability of resection at each voxel. The probability map was thresholded to identify voxels resected in at least 5 of 23 patients (colored areas). Yellow indicates overlap of the ATL resection map with the Semantic Decision – Rest activation. Green indicates overlap of the ATL resection map with the Semantic Decision – Tone Decision activation. Blue indicates overlap of the ATL resection map with both of the fMRI maps.