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Coupled neural systems underlie the production and comprehension of naturalistic narrative speech

Significance Successful verbal communication requires the finely orchestrated interaction between production-based processes in the speaker’s brain and comprehension-based processes in the listener’s brain. Here we first develop a time-warping tool that enables us to map all brain areas reliably activated during the production of real-world speech. The results indicate that speech production is not localized to the left hemisphere but recruits an extensive bilateral network of linguistic and extralinguistic brain areas. We then directly compare the neural responses during speech production and comprehension and find that the two systems respond in similar ways. Our results argue that a shared neural mechanism supporting both production and comprehension facilitates communication and underline the importance of studying comprehension and production within unified frameworks. Neuroimaging studies of language have typically focused on either production or comprehension of single speech utterances such as syllables, words, or sentences. In this study we used a new approach to functional MRI acquisition and analysis to characterize the neural responses during production and comprehension of complex real-life speech. First, using a time-warp based intrasubject correlation method, we identified all areas that are reliably activated in the brains of speakers telling a 15-min-long narrative. Next, we identified areas that are reliably activated in the brains of listeners as they comprehended that same narrative. This allowed us to identify networks of brain regions specific to production and comprehension, as well as those that are shared between the two processes. The results indicate that production of a real-life narrative is not localized to the left hemisphere but recruits an extensive bilateral network, which overlaps extensively with the comprehension system. Moreover, by directly comparing the neural activity time courses during production and comprehension of the same narrative we were able to identify not only the spatial overlap of activity but also areas in which the neural activity is coupled across the speaker’s and listener’s brains during production and comprehension of the same narrative. We demonstrate widespread bilateral coupling between production- and comprehension-related processing within both linguistic and nonlinguistic areas, exposing the surprising extent of shared processes across the two systems.