The frontal aslant white matter tract (FAT) and semantic selection in word production

Abstract

The frontal aslant tract (FAT) is a white matter structure joining the anterior supplementary and pre-supplementary motor area (SMA and pre-SMA) to the inferior and middle frontal gyri. FAT shows leftward asymmetry (Catani et al., 2012), which suggests its role in language processing. Although previous studies showed the contribution of FAT in speech motor control (Kinoshita at al., 2015; Kemerdere et al., 2016), the exact character of FAT as a functional connection remains poorly understood. In our previous work (Sierpowska et al., 2015), we reported that direct electrical stimulation applied at the level of the left FAT during brain surgery provoked overregularization errors in a verb generation task. This case study motivated us to examine the relationship between the microstructural properties of FAT and performance in a demanding verb generation task in healthy individuals and to test whether it follows a left-lateralization pattern.
50 healthy subjects (mean age= 43.7 ± 21.6) were scanned with high-resolution diffusion-weighted imaging (DWI) and underwent behavioral testing using a verb generation task (dataset shared by Janssen et al., in prep). Stimuli consisted of 100 high-frequency concrete Dutch nouns (e.g. “hond” [dog]). Verbs could not be formed by morphological derivation of the noun. Based on the responses given by the 50 participants, we sorted the items into high and low selection demands (Thompson-Schill et al., 1998). The FAT connection was obtained using two regions of interest (ROI) and one exclusion mask. The ROIs were defined within the MNI space according to the following neuroanatomical landmarks: (1) the SMA and pre-SMA, conjoined and (2) the pars triangularis and opercularis of the inferior frontal gyrus (IFG, conjoined). The exclusion mask was defined around the midline on a sagittal section. Subsequently, the masks were transferred to each individual’s diffusion space and their corresponding white matter circuitry was calculated using a probabilistic approach (FSL probtrackx). All individual results were then binarized and used as masks to derive fractional anisotropy (FA) values, further used for comparison with behavioral data with Spearman correlations.
FA values of the left FAT correlated with accuracy in verb generation, but only for the high selection condition (r(49) = .278; P = .025). Additionally, strong correlations were found between the right FAT FA values and accuracy for both high (r(49)= .611; P < .001) and low selection conditions (r(49) = .459; P < .001).
This study confirms that the previously found relationship between the left FAT and performance on verb generation is also apparent in a healthy population. Additionally, the fact that this relationship only holds for items with high selection demands suggests that semantic control mechanisms underlie the left FAT’s role in language. Finally, the newly observed relationship between verb generation and the same tract in the right hemisphere, typically non-dominant for language, opens a new direction for further studies. In the neurosurgical context, these results aid in further establishing language monitoring protocols for protecting white matter connectivity in surgeries for removal of tumors subjacent to both left and right (pre)SMA.