Elsevier

Progress in Neurobiology

Volume 98, Issue 3, September 2012, Pages 279-301
Progress in Neurobiology

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

https://doi.org/10.1016/j.pneurobio.2012.06.008Get rights and content

Abstract

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.

Highlights

► 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.

Section snippets

Intracranial EEG and human cognition

In the last few years, an increasing number of research groups have turned to intracranial EEG (iEEG) recordings to study the neural bases of human cognition. iEEG itself is an old technique that dates back to the early pioneers of electrophysiological recordings (Jasper and Carmichael, 1935), soon after Berger's first application of the EEG to humans. Because of its invasive nature, its use in humans has mainly been restricted to the clinical circumstances of patients undergoing resective

Tell us something new: what can we learn from iEEG HFA about the functional dynamics of the human brain?

We argue that studying HFA with iEEG is relevant for two reasons: first, because it may serve to provide a link between animal research on the cellular mechanisms supporting cognitive functions and the non-invasive investigation of complex cognitive processes in humans. Second, because it allows one to test specific neuroscientific models of human cognitive processes, which often make predictions at a level of spatial and temporal precision that cannot be tested using other methods. These

iEEG and cognitive HFA: guidelines for experimental research

If, as we hope, the previous examples are convincing evidence that iEEG research on HFA can provide unique information about the human brain at work, we expect the number of contributors to this field to increase at a fast pace, as it has already started to do in the last few years. This review is a unique opportunity to combine the experience of five research groups with long-standing expertise in iEEG research, and to provide some guidelines for experimental research on HFA. Human

Use of HFA to anticipate and prevent post-operative cognitive deficits

The objective of presurgical iEEG monitoring is not only to define the epileptogenic network as a surgical target, but also to identify cortical regions that support critical sensory, motor or cognitive functions and should be spared from surgery. The best way to anticipate post-operative deficits is to test the ‘functional integrity’ (Chelune, 1995) of the candidate cortical target for surgical resection. This integrity is usually evaluated by combining neuropsychological testing, functional

Expected conceptual, methodological and technological evolution of iEEG research on cognitive HFA

As more and more research groups use iEEG to probe the fine spatio-temporal dynamics of the human brain, their scientific questions become increasingly sophisticated and require finer and broader means of investigation. iEEG itself can be used more efficiently, through faster and better analysis techniques, but it can also be improved to provide a truly multi-modal and multi-scale perspective on the large-scale neural networks supporting cognition. In this final section, we discuss several

Acknowledgments

J.P.L. was supported by two grants from the French National Research Agency (ANR: OpenVibe2 and MLA). NA was supported by an Emmy Noether grant from the Deutsche Forschungsgemeinschaft. F.M. was supported by grant MO930/4-1 from the DFG. N.E.C. was supported by NINDS R01-40596. EH was supported by the US NIH (NS18741) and by INSERM. We thank all the patients who participated in the studies cited in this review. N.E.C. thanks Anna Korzeniewska, Ph.D. for Fig. 6. J.P.L. thanks Tomas Ossandon for

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