Network Controllability in the Inferior Frontal Gyrus Relates to Controlled Language Variability and Susceptibility to TMS

Abstract

In language production, humans are confronted with considerable word selection demands. Often, we must select a word from among similar, acceptable, and competing alternative words to construct a sentence that conveys an intended meaning. In recent years, the left inferior frontal gyrus (LIFG) has been identified as being critical to this ability. Despite a recent emphasis on network approaches to understanding language, how the LIFG interacts with the brain's complex networks to facilitate controlled language performance remains unknown. Here, we take a novel approach to understanding word selection as a network control process in the brain. Using an anatomical brain network derived from high-resolution diffusion spectrum imaging, we computed network controllability underlying the site of transcranial magnetic stimulation (TMS) in the LIFG between administrations of language tasks that vary in response (cognitive control) demands: open-response tasks (word generation) versus closed response tasks (number naming). We found that a statistic that quantifies the LIFG's theoretically predicted control of communication across modules in the human connectome explains TMS-induced changes in open-response language task performance only. Moreover, we found that a statistic that quantifies the LIFG's theoretically predicted control of difficult-to-reach states explains vulnerability to TMS in the closed-ended (but not open-ended) response task. These findings establish a link among network controllability, cognitive function, and TMS effects.SIGNIFICANCE STATEMENT This work illustrates that network control statistics applied to anatomical connectivity data demonstrate relationships with cognitive variability during controlled language tasks and TMS effects.

Keywords: TMS; cognitive control; connectomics; diffusion imaging; neural networks; neuroimaging.