Tumour-infiltrated cortex participates in large-scale cognitive circuits

Abstract:

The extent to which tumour-infiltrated brain tissue contributes to cognitive function remains unclear. While prior studies have suggested involvement of tumour-infiltrated tissue in local circuits associated with language and motor function, it is unknown whether such tissue participates in distributed networks important for higher-order cognitive abilities like executive function. In this study, we tested the hypothesis that cortical tissue infiltrated by diffuse low-grade gliomas participates in large-scale cognitive circuits using a unique combination of intracranial electrocorticography (ECoG) and resting-state functional magnetic resonance (fMRI) imaging in four patients. We observed significant task-related high gamma (70-250 Hz) power modulations in tumour-infiltrated cortex in response to increased cognitive effort, implying preserved functionality of neoplastic tissue for complex tasks. Strikingly, we found that tumour locations corresponding to task-responsive electrodes exhibited functional connectivity patterns that significantly co-localised with canonical brain networks implicated in executive function. Finally, we discovered that tumour regions with larger task-related high gamma power elevations tended to be more functionally connected to the dorsal attention network, further demonstrating the participation of tumour-infiltrated cortex in large-scale brain networks that support executive function in health. Overall, this study contributes convergent fMRI-ECoG evidence that tumour-infiltrated cortex participates in large-scale neurocognitive circuits, reflecting preserved functionality of neoplastic brain tissue relevant to clinical management. Significance statement Gliomas interact with healthy neural circuits as they grow in the brain. Understanding these interactions is crucial for planning surgeries to remove gliomas without inducing long-term cognitive deficits. While prior studies have shown that glioma-infiltrated tissue can integrate within local functional circuits, it is unknown whether such tissue participates in large-scale whole-brain networks. Using electrocorticography, we show that glioma-infiltrated tissue responds significantly to tasks of increasing cognitive demand, reflecting its involvement in executive function processes. Using pre-operative functional neuroimaging, we found that tumour regions responsive to complex tasks were also functionally connected to large-scale networks implicated in executive function. These findings imply that gliomas participate within large-scale cognitive circuits, possibly reflecting preserved functionality relevant to clinical management.