Predictive and reactive behaviors represent two mutually exclusive strategies in a sensorimotor task. Predictive behavior consists in internally estimating timing and features of a target stimulus and relies on a cortical medial frontal system (superior frontal gyrus - SFG). Reactive behavior consists in waiting for actual perception of the target stimulus and relies on the lateral frontal cortex (inferior frontal gyrus - IFG). We investigated whether SFG-IFG connections by the frontal aslant tract (FAT) can mediate predictive/reactive interactions. In 19 healthy human volunteers, we applied online transcranial magnetic stimulation (TMS) to 6 spots along the medial and lateral terminations of the FAT, during the set period of a delayed reaction task. Such scenario can be solved using either predictive or reactive strategies. TMS increased the propensity towards reactive behavior if applied to a specific portion of the SFG and increased predictive behavior when applied to a specific IFG spot. The two active spots in the SFG and IFG were directly connected by a sub-bundle of FAT fibers as indicated by DWI-tractography. Since FAT connectivity identifies two distant cortical nodes with opposite functions, we propose that the FAT mediates mutually inhibitory interactions between SFG and IFG to implement a "winner takes all" decisional process. We hypothesize such role of the FAT to be domain-general, whenever competition occurs between internal predictive and external reactive behaviors. Finally, we also show that anatomical connectivity is a powerful factor to explain and predict the spatial distribution of brain stimulation effects.Significance StatementWe interact with sensory cues adopting two main mutually-exclusive strategies: a) trying to anticipate the occurrence of the cue or b) waiting for the GO-signal to be manifest and react to it. 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 mediates the direct competition and exclusiveness between predictive and reactive strategies. More generally, implementing anatomical connectivity in TMS studies strongly reduces spatial noise.

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

Giampiccolo, Davide;
2023-01-01

Abstract

Predictive and reactive behaviors represent two mutually exclusive strategies in a sensorimotor task. Predictive behavior consists in internally estimating timing and features of a target stimulus and relies on a cortical medial frontal system (superior frontal gyrus - SFG). Reactive behavior consists in waiting for actual perception of the target stimulus and relies on the lateral frontal cortex (inferior frontal gyrus - IFG). We investigated whether SFG-IFG connections by the frontal aslant tract (FAT) can mediate predictive/reactive interactions. In 19 healthy human volunteers, we applied online transcranial magnetic stimulation (TMS) to 6 spots along the medial and lateral terminations of the FAT, during the set period of a delayed reaction task. Such scenario can be solved using either predictive or reactive strategies. TMS increased the propensity towards reactive behavior if applied to a specific portion of the SFG and increased predictive behavior when applied to a specific IFG spot. The two active spots in the SFG and IFG were directly connected by a sub-bundle of FAT fibers as indicated by DWI-tractography. Since FAT connectivity identifies two distant cortical nodes with opposite functions, we propose that the FAT mediates mutually inhibitory interactions between SFG and IFG to implement a "winner takes all" decisional process. We hypothesize such role of the FAT to be domain-general, whenever competition occurs between internal predictive and external reactive behaviors. Finally, we also show that anatomical connectivity is a powerful factor to explain and predict the spatial distribution of brain stimulation effects.Significance StatementWe interact with sensory cues adopting two main mutually-exclusive strategies: a) trying to anticipate the occurrence of the cue or b) waiting for the GO-signal to be manifest and react to it. 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 mediates the direct competition and exclusiveness between predictive and reactive strategies. More generally, implementing anatomical connectivity in TMS studies strongly reduces spatial noise.
2023
brain stimulation, frontal aslant tract, motor control, predictive proactive, reactive, tractography
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Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/11562/1110046
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