Probabilistic mapping of language networks from high frequency activity induced by direct electrical stimulation

Abstract

Direct electrical stimulation (DES) at 50 Hz is used as a gold standard to map cognitive functions but little is known about its ability to map large‐scale networks and specific subnetwork. In the present study, we aim to propose a new methodological approach to evaluate the specific hypothesis suggesting that language errors/dysfunction induced by DES are the result of large‐scale network modification rather than of a single cortical region, which explains that similar language symptoms may be observed after stimulation of different cortical regions belonging to this network. We retrospectively examined 29 patients suffering from focal drug‐resistant epilepsy who benefitted from stereo‐electroencephalographic (SEEG) exploration and exhibited language symptoms during a naming task following 50 Hz DES. We assessed the large‐scale language network correlated with behavioral DES‐induced responses (naming errors) by quantifying DES‐induced changes in high frequency activity (HFA, 70–150 Hz) outside the stimulated cortical region. We developed a probabilistic approach to report the spatial pattern of HFA modulations during DES‐induced language errors. Similarly, we mapped the pattern of after‐discharges (3–35 Hz) occurring after DES. HFA modulations concurrent to language symptoms revealed a brain network similar to our current knowledge of language gathered from standard brain mapping. In addition, specific subnetworks could be identified within the global language network, related to different language processes, generally described in relation to the classical language regions. Spatial patterns of after‐discharges were similar to HFA induced during DES. Our results suggest that this new methodological DES‐HFA mapping is a relevant approach to map functional networks during SEEG explorations, which would allow to shift from “local” to “network” perspectives.

Language Mapping Using Stereo Electroencephalography: A Review and Expert Opinion

“…However, no correlation was performed with post-operative outcome according to the resection status of these eloquent sites. Perrone-Bertolotti et al (2020) similarly reported in 29 patients bilateral, left predominant, widespread positive language sites in the frontal, temporal and parietal lobes using a naming task. No correlation was performed with post-operative outcome.…”

“…These structural and functional evidences suggest that the BLTA could be strongly structurally and functionally connected to both the ventral and the dorsal streams of the perisylvian language network ( Duffau et al, 2014 ). In a recent study ( Perrone-Bertolotti et al, 2020 ) assessed large-scale language network correlated with ECS induced naming errors by quantifying ECS induced HFA changes outside the stimulated cortical region. The authors found long distance HFA modification contemporary to ECS naming impairments suggesting distant effect of ECS.…”

Electrical Stimulation Mapping of Brain Function: A Comparison of Subdural Electrodes and Stereo-EEG

“…However, there is some evidence for functional responses evoked by activation of remote regions, with the stimulation site perhaps serving as an input into the larger functional network (David et al, 2010 ). Differences in ESM-induced power modulations in high-frequency (70–150 Hz) SEEG spectra at remote sites, during ESM trials with/without speech/language responses provide support for network effects of local stimulation, and supplement the CCEPs data (Perrone-Bertolotti et al, 2020 ). Therefore, the functional consequences of transient local current delivery to brain tissue during ESM may be relatively widespread.…”

Intracerebral electrical stimulation to understand the neural basis of human face identity recognition

“…For instance, besides their highly face-selectivity, they may have a higher pattern of connectivity compared to noncritical FIR regions, which provides these nodes to be input gates into a larger network supporting FIR (Mandonnet et al, 2010). This hypothesis is supported by DES studies revealing that critical cortical sites for language-related functions are highly connected within the language-related network and show stronger connectivity than noncritical sites (Perrone-Bertolotti et al, 2020;Rolston & Chang, 2018). According to this hypothesis, thanks to their high connectivity, stimulating critical FIR nodes will lead to the stimulation current physiologically propagating to the whole (or a large part at least) of the FIR network, inducing a behavioral effect.…”