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

Abstract

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.speech production | speech comprehension | intersubject correlation | brain-to-brain coupling S uccessful 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. The extent of brain areas involved in the production of real-world speech in a speaker's brain during naturalistic communication is largely unknown. As a result, the degree of overlap between the production and comprehension systems, and the ways in which they interact, remain controversial. This study pursues three aims: (i) to map all areas (including but not limited to sensory, motoric, linguistic, and extralinguistic) that are reliably activated during the production of complex, real-world narrative; (ii) to map the overlap between areas that respond reliably during the production and the comprehension of real-world narrative; and (iii) to assess the coupling between activity in the speaker's brain during naturalistic production and activity in the listener's brain during comprehension of the same narrative. We discuss each challenge in turn.The functional-anatomic architecture underlying the production of speech in an ecological context is incompletely characterized. Studies investigating production-based brain activity have been mainly restricted to the production of single phonemes (1-5), words (6-8), or short phrases in decontextualized, isolated environments (9-13) (see refs. 14...

Cues, quantification, and agreement in language comprehension

“…Finally, given the divergence between the effects of plural quantification observed here and the lack of effects observed in production research, our results provide an important caveat to recent proposals highlighting the overlap between comprehension and production processes at representational, cognitive, and neural levels (e.g., Dell & Chang, 2014;Gennari & MacDonald, 2009;MacDonald, 2013;Pickering & Garrod, 2013;Segaert, Menenti, Weber, Petersson, & Hagoort, 2012;Silbert, Honey, Simony, Poeppel, & Hasson, 2014). Although it is clear that language comprehension and production share many underlying mechanisms, and that the systems supporting the two tasks interact very strongly, our present results support Tanner et al's (2014) proposal that there are some nontrivial divergences in the cues used during the two tasks.…”

Prediction of psychosis across protocols and risk cohorts using automated language analysis

“…Of note, the premise that processes underlying normal language production and comprehension are relatively homogeneous is supported by a body of work by Hasson, showing alignment of brain activation time courses across normal individuals (intersubject coherence) during both listening and speaking 35 . Our finding of strong correlations between automated and manual linguistic variables provides evidence of concurrent validity for the natural language processing approach.…”

Neural integration of language production and comprehension

“…Second, researchers assume that the linguistic mechanisms are lateralized, with production processes (e.g., lexical selection, articulation) and, to some extent, comprehension processes primarily occurring in the left hemisphere. Silbert et al (2) report a neuroimaging study based on the production and comprehension of naturalistic narrative that challenges these two assumptions.…”

“…Using a novel "time-warping" technique, Silbert et al (2) analyzed the correlation between blood-oxygen level-dependent (BOLD) responses as three participants repeatedly produced and other participants subsequently comprehended a single 15-min narrative. Silbert et al's approach contrasts with almost all neuroimaging studies of language processing, which depend on event-related designs and averaging of the neural responses, and which make use of very limited stimuli or responses (e.g., single phonemes, words, or decontextualized sentences).…”