Distinct neural signatures of phonemic and semantic verbal fluency: a double dissociation in cortical activation and functional connectivity revealed by fNIRS

Significance: The verbal fluency task (VFT) is a widely used paradigm in neuroimaging, yet its phonemic (pVFT) and semantic (sVFT) variants are frequently treated interchangeably despite limited understanding of their distinct neural substrates. Aim: We aim to systematically characterize the differences in cortical activation and functional connectivity (FC) patterns between pVFT and sVFT and to test the stability of these differences against individual variations in behavior and executive function, thereby providing actionable guidance for neuroscience research and clinical practice. Approach: We employed a within-subject design using functional near-infrared spectroscopy to compare cortical activation and FC during pVFT and sVFT. In-task behavioral performance and executive function measures were quantified to test whether individual differences could account for the neural dissociation. Results: We identified dissociated neural signatures between the two tasks. At the activation level, we observed that pVFT elicited significantly stronger activation across the prefrontal cortex (PFC), including the bilateral inferior frontal gyrus, dorsolateral prefrontal cortex, and orbitofrontal cortex. By contrast, sVFT was associated with greater activation in the bilateral supramarginal gyrus. At the network level, pVFT induced a state of higher global functional integration, characterized by enhanced long-range FC between PFC and posterior temporo-parietal regions. Critically, these neural dissociation patterns were not significantly modulated by variations in VFT behavioral performance or general executive function. Conclusions: pVFT and sVFT are subserved by partially nonoverlapping and stable neurocognitive systems. This has significant methodological implications, underscoring that the choice of VFT variant in future neuroscience research should be judiciously guided by the specific neural circuitry under investigation.