Dataset Information

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.

SUBMITTER: Silbert LJ

PROVIDER: S-EPMC4217461 | biostudies-literature | 2014 Oct

REPOSITORIES: biostudies-literature

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

Silbert Lauren J LJ Honey Christopher J CJ Simony Erez E Poeppel David D Hasson Uri U

Proceedings of the National Academy of Sciences of the United States of America 20140929 43

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-m ...[more]

PMID: 25267658

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Project description:Narrative comprehension involves a constant interplay of the accumulation of incoming events and their integration into a coherent structure. This study characterizes cognitive states during narrative comprehension and the network-level reconfiguration occurring dynamically in the functional brain. We presented movie clips of temporally scrambled sequences to human participants (male and female), eliciting fluctuations in the subjective feeling of comprehension. Comprehension occurred when processing events that were highly causally related to the previous events, suggesting that comprehension entails the integration of narratives into a causally coherent structure. The functional neuroimaging results demonstrated that the integrated and efficient brain state emerged during the moments of narrative integration with the increased level of activation and across-modular connections in the default mode network. Underlying brain states were synchronized across individuals when comprehending novel narratives, with increased occurrences of the default mode network state, integrated with sensory processing network, during narrative integration. A model based on time-resolved functional brain connectivity predicted changing cognitive states related to comprehension that are general across narratives. Together, these results support adaptive reconfiguration and interaction of the functional brain networks on causal integration of the narratives.SIGNIFICANCE STATEMENT The human brain can integrate temporally disconnected pieces of information into coherent narratives. However, the underlying cognitive and neural mechanisms of how the brain builds a narrative representation remain largely unknown. We showed that comprehension occurs as the causally related events are integrated to form a coherent situational model. Using fMRI, we revealed that the large-scale brain states and interaction between brain regions dynamically reconfigure as comprehension evolves, with the default mode network playing a central role during moments of narrative integration. Overall, the study demonstrates that narrative comprehension occurs through a dynamic process of information accumulation and causal integration, supported by the time-varying reconfiguration and brain network interaction.

Project description:Speech comprehension is a complex human skill, the performance of which requires the perceiver to combine information from several sources - e.g. voice, face, gesture, linguistic context - to achieve an intelligible and interpretable percept. We describe a functional imaging investigation of how auditory, visual and linguistic information interact to facilitate comprehension. Our specific aims were to investigate the neural responses to these different information sources, alone and in interaction, and further to use behavioural speech comprehension scores to address sites of intelligibility-related activation in multifactorial speech comprehension. In fMRI, participants passively watched videos of spoken sentences, in which we varied Auditory Clarity (with noise-vocoding), Visual Clarity (with Gaussian blurring) and Linguistic Predictability. Main effects of enhanced signal with increased auditory and visual clarity were observed in overlapping regions of posterior STS. Two-way interactions of the factors (auditory × visual, auditory × predictability) in the neural data were observed outside temporal cortex, where positive signal change in response to clearer facial information and greater semantic predictability was greatest at intermediate levels of auditory clarity. Overall changes in stimulus intelligibility by condition (as determined using an independent behavioural experiment) were reflected in the neural data by increased activation predominantly in bilateral dorsolateral temporal cortex, as well as inferior frontal cortex and left fusiform gyrus. Specific investigation of intelligibility changes at intermediate auditory clarity revealed a set of regions, including posterior STS and fusiform gyrus, showing enhanced responses to both visual and linguistic information. Finally, an individual differences analysis showed that greater comprehension performance in the scanning participants (measured in a post-scan behavioural test) were associated with increased activation in left inferior frontal gyrus and left posterior STS. The current multimodal speech comprehension paradigm demonstrates recruitment of a wide comprehension network in the brain, in which posterior STS and fusiform gyrus form sites for convergence of auditory, visual and linguistic information, while left-dominant sites in temporal and frontal cortex support successful comprehension.

Dataset Information

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

Publications

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

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