Functional alterations in cortical processing of speech in glioma-infiltrated cortex

Abstract

Recent developments in the biology of malignant gliomas have demonstrated that glioma cells interact with neurons through both paracrine signaling and electrochemical synapses. Glioma-neuron interactions consequently modulate the excitability of local neuronal circuits, and it is unclear the extent to which glioma-infiltrated cortex can meaningfully participate in neural computations. For example, gliomas may result in a local disorganization of activity that impedes the transient synchronization of neural oscillations. Alternatively, glioma-infiltrated cortex may retain the ability to engage in synchronized activity, in a manner similar to normal-appearing cortex, but exhibit other altered spatiotemporal patterns of activity with subsequent impact on cognitive processing. Here, we use subdural electrocorticography to sample both normal-appearing and glioma-infiltrated cortex during speech. We find that glioma-infiltrated cortex engages in synchronous activity during task performance in a manner similar to normal-appearing cortex, but recruits a diffuse spatial network. On a temporal scale, we show that glioma-infiltrated cortex has lower capacity for information encoding when performing nuanced tasks such as speech production of monosyllabic versus polysyllabic words. As a result, temporal decoding strategies for distinguishing monosyllabic from polysyllabic words were feasible for signals arising from normal-appearing cortex, but not from glioma-infiltrated cortex. These findings inform our understanding of cognitive processing in chronic disease states and have implications for neuromodulation and prosthetics in patients with malignant gliomas.

Large-scale brain networks and intra-axial tumor surgery: a narrative review of functional mapping techniques, critical needs, and scientific opportunities

“…Likewise, high-gamma activity is increased in the inferior frontal gyrus and temporal lobe during speech production and auditory processing (Chang et al, 2013). Because of the task-specific nature, regional specificity, and temporal scale, ECoG has been used as the source of brain-machine interface decoding in several applications (Krucoff et al, 2016;Flint et al, 2017;Aabedi et al, 2021). For example, motor cortex gamma power has been shown to account for ∼30-40% of the variance for finger force output and ∼12% of variance of precise finger movements (Flint et al, 2014(Flint et al, , 2017, both of which increase when other features are included.…”

Involvement of White Matter Language Tracts in Glioma: Clinical Implications, Operative Management, and Functional Recovery After Injury

“…Recent evidence demonstrating that gliomas integrate within functional neuronal networks and proliferate in response to synaptic activity carries significant clinical and therapeutic implications for disease control and post-treatment recovery ( Venkatesh et al, 2019 ; Young et al, 2020a ; Aabedi et al, 2021c ; Krishna et al, 2021a ). For instance, hyper-excitable networks can be targeted with stimulation or other forms of neuromodulation, which may have an impact on tumor progression, though work in this arena is still in its infancy ( Sprugnoli et al, 2021a , b ).…”