Cortico-hippocampal dynamics of hierarchical syntactic planning in natural speech production

Abstract

The human brain must rapidly construct hierarchical structures to organize complex sequential behavior, yet the neural dynamics supporting this process during natural behavior remain poorly understood. Spoken language provides a powerful model system for investigating this computation, requiring rapid transformation of conceptual intent into structured sequential output. Using rare intracranial stereo-electroencephalography (SEEG) recordings from patients producing extended spontaneous speech, we examined how syntactic planning unfolds over time using measures of constituency, dependency structure, and probabilistic syntactic categories. We identified a hierarchical planning architecture in which global sentence structure and core syntactic categories (nouns and verbs) were specified before more local planning operations. Neural representations of these categories emerged up to 1 s before articulation and persisted throughout the planning period, whereas optional modifiers, including adjectives and adverbs, were recruited only closer to speech onset. These observations support a model of hierarchical incremental planning in which abstract sentence structure precedes the incremental specification of individual sentence elements. While core syntactic categories engaged a broader fronto-temporo-parietal network than other word classes, syntactic-depth-related activity emerged in parallel across cortical regions and the hippocampus, suggesting that hippocampal relational representations contribute to sentence structure building. Together, these findings support a cortico-hippocampal model of speech production in which hierarchical sentence structure and core syntactic categories are planned before secondary syntactic elements are incrementally incorporated into the evolving sentence plan. These results provide a neural account of how abstract linguistic structure is transformed into fluent speech.