Shared Cortical Language Networks with Convergent Hierarchical Network Dynamics for Lexicosemantic Processing in Comprehension and Naming

Introduction: Lexicosemantic processing is a fundamental component of language that describes the mapping between concepts and sensorimotor forms. Prominent psycholinguistic models suggest that spoken and written language engage a shared lexicosemantic processing network in both speech perception and production, yet convergent neural mechanisms are unclear. Here, we used electrocorticography to identify the spatiotemporal dynamics of lexicosemantic processing in comprehension and naming.

Methods: 74 patients underwent invasive electrocorticography and completed auditory (AN) and orthographic (ON) naming. We analyzed gamma activity (65-115Hz) using surface-based mixed-effects multilevel analyses to identify lexicosemantic processing networks and autoregressive hidden Markov models (ARHMM) to isolate time-varying network dynamics. Lastly, direct cortical stimulation (DCS) was used to attribute causality to critical nodes.

Results: At speech onset, activation of superior temporal gyrus (pSTG) was followed by middle temporal gyrus (pMTG), and posterior middle frontal gyrus (pMFG). For each written word, visual cortex activity was followed by activation of lexical and phonological reading routes (fusiform gyrus, mFus; pSTG; pMTG; intraparietal sulcus, IPS; pMFG; inferior frontal gyrus; IFG). Both modalities engaged pMTG and pMFG for comprehension, and activity was correlated with linguistic composition (p < 0.001). The last word activated a shared network (pMTG;mFus;IPS;IFG) for naming. ARHMM isolated 5 states for AN and 6 for ON with 3 convergent states. The first convergent state occurring at stimulus offset was characterized by outflow from pMTG, mFus, IPS, and IFG, and state duration was correlated with reaction time for both tasks (p < 0.001) implicating it in multimodal lexical access. Regions where DCS disrupted both AN and ON included pMTG, mFus, IFG, and pMFG.

Conclusion : Juxtaposing network dynamics of multimodal lexicosemantic processing in speech perception and production informs our understanding of normal language function, which provides important insights that could help minimize postoperative language deficits and facilitate designs of neural prosthetics for language disorders.