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The spatiotemporal dynamics of semantic integration in the human brain.

ABSTRACT: Language depends critically on the integration of lexical information across multiple words to derive semantic concepts. Limitations of spatiotemporal resolution have previously rendered it difficult to isolate processes involved in semantic integration. We utilized intracranial recordings in epilepsy patients (n = 58) who read written word definitions. Descriptions were either referential or non-referential to a common object. Semantically referential sentences enabled high frequency broadband gamma activation (70-150 Hz) of the inferior frontal sulcus (IFS), medial parietal cortex, orbitofrontal cortex (OFC) and medial temporal lobe in the left, language-dominant hemisphere. IFS, OFC and posterior middle temporal gyrus activity was modulated by the semantic coherence of non-referential sentences, exposing semantic effects that were independent of task-based referential status. Components of this network, alongside posterior superior temporal sulcus, were engaged for referential sentences that did not clearly reduce the lexical search space by the final word. These results indicate the existence of complementary cortical mosaics for semantic integration in posterior temporal and inferior frontal cortex.

SUBMITTER: Murphy E

PROVIDER: S-EPMC10598228 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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The spatiotemporal dynamics of semantic integration in the human brain.

Murphy Elliot E Forseth Kiefer J KJ Donos Cristian C Snyder Kathryn M KM Rollo Patrick S PS Tandon Nitin N

Nature communications 20231024 1

Language depends critically on the integration of lexical information across multiple words to derive semantic concepts. Limitations of spatiotemporal resolution have previously rendered it difficult to isolate processes involved in semantic integration. We utilized intracranial recordings in epilepsy patients (n = 58) who read written word definitions. Descriptions were either referential or non-referential to a common object. Semantically referential sentences enabled high frequency broadband ...[more]

PMID: 37875526

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Project description:The ability to integrate semantic information into the context of a sentence is essential for human communication. Several studies have shown that the predictability of a final keyword based on the sentence context influences semantic integration on the behavioral, neurophysiological, and neural level. However, the architecture of the underlying network interactions for semantic integration across the lifespan remains unclear. In this study, 32 healthy participants (30-75 years) performed an auditory cloze probability task during functional magnetic resonance imaging (fMRI), requiring lexical decisions on the sentence's final words. Semantic integration demands were implicitly modulated by presenting sentences with expected, unexpected, anomalous, or pseudoword endings. To elucidate network interactions supporting semantic integration, we combined univariate task-based fMRI analyses with seed-based connectivity and between-network connectivity analyses. Behavioral data revealed typical semantic integration effects, with increased integration demands being associated with longer response latencies and reduced accuracy. Univariate results demonstrated increased left frontal and temporal brain activity for sentences with higher integration demands. Between-network interactions highlighted the role of task-positive and default mode networks for sentence processing with increased semantic integration demands. Furthermore, increasing integration demands led to a higher number of behaviorally relevant network interactions, suggesting that the increased between-network coupling becomes more relevant for successful task performance as integration demands increase. Our findings elucidate the complex network interactions underlying semantic integration across the aging continuum. Stronger interactions between various task-positive and default mode networks correlated with more efficient processing of sentences with increased semantic integration demands. These results may inform future studies with healthy old and clinical populations.

Dataset Information

The spatiotemporal dynamics of semantic integration in the human brain.

Publications

The spatiotemporal dynamics of semantic integration in the human brain.

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