Connectivity by the Frontal Aslant Tract (FAT) explains local functional specialization of the superior and inferior frontal gyri in humans while choosing predictive over reactive strategies: a tractography-guided TMS study

Abstract

Predictive and reactive behaviors represent two mutually exclusive strategies for successfully completing a sensorimotor task. It is thought that predictive actions are based on the medial premotor system, in the superior frontal gyrus (SFG) and reactive stimulus-response behaviors rely on a lateral premotor system, in the inferior frontal gyrus (IFG). The frontal aslant tract (FAT), a white matter tract connecting SFG and IFG, is a possible neural substrate of the predictive/reactive interactions. We used diffusion-weighted imaging (DWI) of 17 male and female healthy human volunteers, to dissect 3 sub-bundles of fibers belonging to the left FAT (bundles 1, 2 and 3), arising ventrally from 1) the ventral precentral gyrus, 2) midway between the PCG and pars opercularis (POp) and 3) the POp and terminating dorsally in 3 different parts of the SFG, in a caudal-rostral order. We applied online transcranial magnetic stimulation (TMS) to 6 spots, corresponding to the medial and lateral terminations of bundles 1-3 during the fixed-duration set period of a delayed reaction task, that can be solved using a predictive (anticipatory) strategy or with a reactive strategy. Results showed that TMS changed the frequency of predictive/reactive strategies only when applied over 2 spots, the SFG and IFG terminations of bundle 2. Importantly, the effects of TMS were opposite when applied to the SFG or to the IFG. Our data show that the SFG and the IFG have opposite roles in producing predictive or reactive behavior and that reciprocal integration or competition is probably mediated by the FAT. Significance StatementAs is well-known by athletes at starting blocks, interaction with the world can occur with a predictive strategy (anticipating a GO-signal) or a reactive strategy (waiting for the GO-signal to be manifest) and they are mutually exclusive. Here we showed, by using non-invasive brain stimulation (TMS), that two specific cortical regions in the superior frontal gyrus (SFG) and the inferior frontal gyrus (IFG) have opposite roles in facilitating a predictive or a reactive strategy. Importantly these two very distant regions but with highly interconnected functions are specifically connected by a small white matter bundle, which probably mediates the competition between predictive and reactive strategies. More generally, we show that the implementing anatomical connectivity in TMS studies strongly reduces spatial noise.