The selectivity and functional connectivity of the anterior temporal lobes

Abstract

One influential account asserts that the anterior temporal lobe (ATL) is a domain-general hub for semantic memory. Other evidence indicates it is part of a domain-specific social cognition system. Arbitrating these accounts using functional magnetic resonance imaging has previously been difficult because of magnetic susceptibility artifacts in the region. The present study used parameters optimized for imaging the ATL, and had subjects encode facts about unfamiliar people, buildings, and hammers. Using both conjunction and region of interest analyses, person-selective responses were observed in both the left and right ATL. Neither building-selective, hammer-selective nor domain-general responses were observed in the ATLs, although they were observed in other brain regions. These findings were supported by "resting-state" functional connectivity analyses using independent datasets from the same subjects. Person-selective ATL clusters were functionally connected with the brain's wider social cognition network. Rather than serving as a domain-general semantic hub, the ATLs work in unison with the social cognition system to support learning facts about others.

Figure 1.

Temporal signal-to-noise ratio (TSNR) maps showing EPI image quality over the anterior temporal lobes. The color gradient indicates the TSNR of the smoothed EPI time course data overlaid on the AFNI Talairach N27 atlas brain. TSNR was calculated by dividing the mean signal intensity at a voxel by the standard deviation of its signal time course. The color map is thresholded at a TSNR of 40, with all areas in red indicating a TSNR of at least 200. Simulations indicate that a TSNR of 40 (indicated in the map by light blue) is the minimum to reliably detect effects between conditions in fMRI data (Murphy et al. 2007). Note that virtually all of the anterior temporal lobes far exceed this threshold, with many anterior temporal regions exceeding a TSNR of 200.

Figure 2.

Person-selective responses in the anterior temporal lobes. (A) person-selective clusters in the anterior temporal lobes identified using conjunction analyses. The rendered surfaces show the person-selective clusters in the left and right hemispheres where person > building AND person > hammer with P < 0.05 and cluster-size corrected for the volume of the anterior temporal lobes. (B) Activity in the anterior temporal lobe ROIs. The rendered surfaces show the extent of the anterior temporal ROIs in the left and right hemispheres. The bar graphs demonstrate the average percent signal change across subjects in the left and right anterior temporal ROIs relative to the nonconceptual (riser detection) control task. In both ROIs, the responses to person-fact encoding were reliably greater than the responses to building- or hammer-fact encoding. Responses during building- and hammer-fact encoding were not different from each other. Error bars on bar charts in both panels indicate ±1 standard error of the subject means.

Figure 3.

Domain-specific and domain-general responses outside the anterior temporal lobes indentified using conjunction analyses. Domain-general responses (shown in gold) were observed in various regions outside the anterior temporal lobes, including the left inferior and superior frontal gyri, the left middle temporal gyrus, and the hippocampus. A hammer-selective cluster (shown in blue) was observed in the left middle temporal gyrus (L pMTG) immediately posterior to a domain-general cluster. More medially, building-selective clusters (shown in green) were observed in left and right middle occipital gyri. Person-selective clusters (shown in red) were observed along the midline in the medial PFC and the precuneus, among other regions. All clusters are corrected for multiple comparisons.

Figure 4.

The person-selective clusters in the anterior temporal lobes are functionally connected with the wider social cognition network. Color overlays indicate clusters of functional connectivity with the anterior temporal seed voxels measured in the independent Vigilance Task scanning run. The left and right anterior temporal seed voxels were identified as those voxels in each hemisphere with the highest average t-value for the person > building and person > hammer t-maps in the Fact-Learning Task scanning runs. The depicted functional connectivity t-maps were obtained as follows. First, for each subject a Pearson correlation map was constructed showing correlation between each voxel and an anterior temporal seed voxel. Second, these r-maps were converted to Z score maps. Finally, these Z-maps were included in a random effects, one-sample t-test to identify voxels whose means differed from zero with P < 0.0005 and cluster-size corrected for multiple comparisons across the whole brain at P < 0.05.