High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research

Human intracranial EEG (iEEG) recordings are primarily performed in epileptic patients for presurgical mapping. When patients perform cognitive tasks, iEEG signals reveal high-frequency neural activities (HFAs, between around 40 Hz and 150 Hz) with exquisite anatomical, functional and temporal specificity. Such HFAs were originally interpreted in the context of perceptual or motor binding, in line with animal studies on gamma-band (‘40 Hz’) neural synchronization. Today, our understanding of HFA has evolved into a more general index of cortical processing: task-induced HFA reveals, with excellent spatial and time resolution, the participation of local neural ensembles in the task-at-hand, and perhaps the neural communication mechanisms allowing them to do so. This review promotes the claim that studying HFA with iEEG provides insights into the neural bases of cognition that cannot be derived as easily from other approaches, such as fMRI. We provide a series of examples supporting that claim, drawn from studies on memory, language and default-mode networks, and successful attempts of real-time functional mapping. These examples are followed by several guidelines for HFA research, intended for new groups interested by this approach. Overall, iEEG research on HFA should play an increasing role in cognitive neuroscience in humans, because it can be explicitly linked to basic research in animals. We conclude by discussing the future evolution of this field, which might expand that role even further, for instance through the use of multi-scale electrodes and the fusion of iEEG with MEG and fMRI.

► High-frequency activity in intracranial EEG reveals human functional network dynamics.
► Intracranial EEG bridges human functional neuroimaging and animal electrophysiology.
► Intracranial EEG can provide key tests of brain-based models of human cognition.
► Guidelines proposed for the analysis of intracranial EEG data during cognitive tasks.