Diverse frontoparietal connectivity supports semantic prediction and integration in sentence comprehension.

Abstract

Predictive processing in parietal, temporal, frontal, and sensory cortex allows us to anticipate future meanings to maximize the efficiency of language comprehension, with the temporoparietal junction (TPJ) and inferior frontal gyrus (IFG) thought to be situated towards the top of a predictive hierarchy. Although the regions underpinning this fundamental brain function are well-documented, it remains unclear how they interact to achieve efficient comprehension. To this end we recorded functional magnetic resonance imaging (fMRI) in 22 participants (11 males) while they comprehended sentences presented part-by-part, in which we manipulated the constraint provided by sentential contexts on upcoming semantic information. Using this paradigm, we examined the connectivity patterns of bilateral TPJ and IFG during anticipatory phases (i.e., before the onset of targets) and integration phases (i.e., after the onset of targets). When upcoming semantic content was highly predictable in strong-constraint contexts, both left TPJ and bilateral IFG showed stronger visual coupling, while right TPJ showed stronger connectivity with regions within control, default mode, and visual networks, including IFG, parahippocampal gyrus, posterior cingulate, and fusiform gyrus. These connectivity patterns were weaker when predicted semantic content appeared, in line with predictive coding theory. Conversely, for less predictable content, these connectivity patterns were stronger during the integration phase. Overall, these results suggest that both top-down semantic prediction and bottom-up integration during predictive processing are supported by flexible coupling of frontoparietal regions with control, memory, and sensory systems.Significance Statement Recent work has revealed the neural basis of predictive language comprehension. However, it remains unclear how brain regions change their connectivity in a dynamic fashion to support comprehension in highly predictive and less predictive contexts. Here, we show that stronger frontoparietal connectivity with cognitive control, memory, and sensory areas supports top-down prediction generation in strong-constraint contexts; these connectivity patterns are reduced when the anticipated information appears. This pattern is reversed when upcoming sensory input is unpredictable; connectivity is stronger after word inputs have been presented, allowing semantic integration with preceding low-constraint context. Our findings suggest that both top-down semantic prediction and bottom-up semantic integration in language comprehension rely upon diverse functional coupling of higher-order frontoparietal regions with other brain systems.