Syntactic structure building in the anterior temporal lobe during natural story listening

Abstract

The neural basis of syntax is a matter of substantial debate. In particular, the inferior frontal gyrus (IFG), or Broca's area, has been prominently linked to syntactic processing, but the anterior temporal lobe has been reported to be activated instead of IFG when manipulating the presence of syntactic structure. These findings are difficult to reconcile because they rely on different laboratory tasks which tap into distinct computations, and may only indirectly relate to natural sentence processing. Here we assessed neural correlates of syntactic structure building in natural language comprehension, free from artificial task demands. Subjects passively listened to Alice in Wonderland during functional magnetic resonance imaging and we correlated brain activity with a word-by-word measure of the amount syntactic structure analyzed. Syntactic structure building correlated with activity in the left anterior temporal lobe, but there was no evidence for a correlation between syntactic structure building and activity in inferior frontal areas. Our results suggest that the anterior temporal lobe computes syntactic structure under natural conditions.

Figure 1

A sentence fragment from the story. The numbers indicate the NodeCnt measure associated with each word. NodeCnt provided an estimate of the amount of structure built word-by-word (see Methods). Node labels follow the conventions of the Treebank 2 scheme (Marcus et al., 1994).

Figure 2

Illustration of how predictors were generated. (A) A 15-second epoch of the sound signal illustrating how word boundaries were identified and annotated with lexical frequency and node count information. (B) We assigned a node count and lexical frequency value (shown) to each time point when a word was presented during the time course of the 12 minute story segment. (C) We convolved each predictor (e.g. lexical frequency, shown) with a function describing the estimated hemodynamic response (Boynton et al., 1996) and re-sampled at .5hz to match the characteristics of the recorded fMRI data. Note the lexical frequency time course in panel B includes low frequency components evident as fluctuations in panel C. NodeCnt, number of syntactic nodes; LexFreq, lexical frequency.

Figure 3

Regions of interest (ROIs). Regions exhibiting significant correlation between subjects using ISC (orange; r > .21) and regions correlated with the sound power (red). Dark lines indicate anatomically and functionally-based sub-divisions of the ROIs (see Methods). Numbers for each ROI correspond to Table 1. (A) Lateral view. Red, sound power was correlated with activity bilaterally in a portion of the STG including Heschl s Gyrus. Orange, activity was correlated across subjects in a large portion of the temporal lobe bilaterally, as well as IFG and MFG. (B) Medial view. Activity was correlated across subjects in a portion of the parietal lobe (precuneus and cuneus) extending into the lingual gyrus.

Figure 4

The estimated responses evoked by syntactic structure building (NodeCnt) in aTL (grey bars) and IFG (white bars) across hemispheres. The correlation between NodeCnt and activity in aTL was significantly greater than that in the IFG; the effect was also significantly greater in the left hemisphere than in the right (see text for details). Error bars indicate standard error of the mean.

Figure 5

Regions where activity correlated with (A) Syntactic structure-building, or (B) Lexical frequency. Activation is shown on the brain of a single representative subject thresholded at p < .05 (corrected for multiple comparisons). Structure building correlated with activity in the left aTL. Lexical frequency is correlated activity in the left and right MFG and the precuneus bilaterally. Correction for multiple comparisons followed the same procedure used in the soundwave power analysis in the main text (see Methods).