Predicting “When” in Discourse Engages the Human Dorsal Auditory Stream: An fMRI Study Using Naturalistic Stories

The hierarchical organization of human cortical circuits integrates information across different timescales via temporal receptive windows, which increase in length from lower to higher levels of the cortical hierarchy (Hasson et al., 2015). A recent neurobiological model of higher-order language processing (Bornkessel-Schlesewsky et al., 2015) posits that temporal receptive windows in the dorsal auditory stream provide the basis for a hierarchically organized predictive coding architecture (Friston and Kiebel, 2009). In this stream, a nested set of internal models generates time-based (“when”) predictions for upcoming input at different linguistic levels (sounds, words, sentences, discourse). Here, we used naturalistic stories to test the hypothesis that multi-sentence, discourse-level predictions are processed in the dorsal auditory stream, yielding attenuated BOLD responses for highly predicted versus less strongly predicted language input. The results were as hypothesized: discourse-related cues, such as passive voice, which effect a higher predictability of remention for a character at a later point within a story, led to attenuated BOLD responses for auditory input of high versus low predictability within the dorsal auditory stream, specifically in the inferior parietal lobule, middle frontal gyrus, and dorsal parts of the inferior frontal gyrus, among other areas. Additionally, we found effects of content-related (“what”) predictions in ventral regions. These findings provide novel evidence that hierarchical predictive coding extends to discourse-level processing in natural language. Importantly, they ground language processing on a hierarchically organized predictive network, as a common underlying neurobiological basis shared with other brain functions. SIGNIFICANCE STATEMENT Language is the most powerful communicative medium available to humans. Nevertheless, we lack an understanding of the neurobiological basis of language processing in natural contexts: it is not clear how the human brain processes linguistic input within the rich contextual environments of our everyday language experience. This fMRI study provides the first demonstration that, in natural stories, predictions concerning the probability of remention of a protagonist at a later point are processed in the dorsal auditory stream. Results are congruent with a hierarchical predictive coding architecture assuming temporal receptive windows of increasing length from auditory to higher-order cortices. Accordingly, language processing in rich contextual settings can be explained via domain-general, neurobiological mechanisms of information processing in the human brain.