High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research
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
References (260)
- et al.
Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks
Clinical Neurophysiology
(1999) - et al.
Intracranial EEG correlates of expectancy and memory formation in the human hippocampus and nucleus accumbens
Neuron
(2010) - et al.
Memory formation by neuronal synchronization
Brain Research Reviews
(2006) - et al.
Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease
Lancet Neurology
(2009) - et al.
Operational principles of neurocognitive networks
International Journal of Psychophysiology
(2006) - et al.
In vivo animation of auditory-language-induced gamma-oscillations in children with intractable focal epilepsy
Neuroimage
(2008) - et al.
A practical procedure for real-time functional mapping of eloquent cortex using electrocorticographic signals in humans
Epilepsy & Behavior
(2009) Two-stage model of memory trace formation: a role for “noisy” brain states
Neuroscience
(1989)Theta oscillations in the hippocampus
Neuron
(2002)- et al.
The functional role of cross-frequency coupling
Trends in Cognitive Sciences
(2010)
Feasibility of simultaneous intracranial EEG-fMRI in humans: a safety study
Neuroimage
Depth electrographic study of a fast rhythm evoked from the human calcarine region by steady illumination
Electroencephalography and Clinical Neurophysiology
Hippocampal adequacy versus functional reserve: predicting memory functions following temporal lobectomy
Archives of Clinical Neuropsychology
Induced electrocorticographic gamma activity during auditory perception
Clinical Neurophysiology
Cortical gamma responses: searching high and low
International Journal of Psychophysiology
Simultaneous MEG and intracranial EEG recordings during attentive reading
Neuroimage
Dynamic statistical parametric mapping: combining fMRI and MEG for high-resolution imaging of cortical activity
Neuron
Category-related activation for written words in the posterior fusiform is task specific
Neuropsychologia
Deep brain stimulation in obsessive–compulsive disorder
Progress in Brain Research
Spatiotemporal imaging of cortical activation during verb generation and picture naming
Neuroimage
The fMRI BOLD signal tracks electrophysiological spectral perturbations, not event-related potentials
Neuroimage
Phase-locking within human mediotemporal lobe predicts memory formation
Neuroimage
Sub-centimeter language organization in the human temporal lobe
Brain and Language
Reduced spike-timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus
Neuron
A mechanism for cognitive dynamics: neuronal communication through neuronal coherence
Trends in Cognitive Sciences
Dynamic causal modelling
Neuroimage
Endogenous electric fields may guide neocortical network activity
Neuron
Theta-coupled periodic replay in working memory
Current Biology
Parallel versus serial processing dependencies in the perisylvian speech network: a Granger analysis of intracranial EEG data
Brain and Language
Short and long term biocompatibility of NeuroProbes silicon probes
Journal of Neuroscience Methods
Neurons in the human basolateral amygdala and hippocampal formation do not respond to odors
Neuroscience Letters
Activity of human hippocampal formation and amygdala neurons during memory testing
Electroencephalography and Clinical Neurophysiology
Spatio-temporal stages in face and word processing. 2. Depth-recorded potentials in the human frontal and Rolandic cortices
Journal of Physiology, Paris
Spatio-temporal stages in face and word processing. I. Depth-recorded potentials in the human occipital, temporal and parietal lobes [corrected]
Journal of Physiology, Paris
Generators of the late cognitive potentials in auditory and visual oddball tasks
Electroencephalography and Clinical Neurophysiology
Human extrastriate visual cortex and the perception of faces, words, numbers, and colors
Cerebral Cortex
Ephaptic coupling of cortical neurons
Nature Neuroscience
Ripples in the medial temporal lobe are relevant for human memory consolidation
Brain
Sustained neural activity patterns during working memory in the human medial temporal lobe
Journal of Neuroscience
Cross-frequency coupling supports multi-item working memory in the human hippocampus
Proceedings of the National Academy of Sciences of the United States of America
Working Memory
Unitary inhibitory field potentials in the CA3 region of rat hippocampus
Journal of Physiology
Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks
Nature Neuroscience
Electrophysiological studies of face perception in humans
Journal of Cognitive Neuroscience
ERP manifestations of processing printed words at different psycholinguistic levels: time course and scalp distribution
Journal of Cognitive Neuroscience
Data mining neocortical high-frequency oscillations in epilepsy and controls
Brain
High-frequency oscillations in human brain
Hippocampus
Hippocampal and entorhinal cortex high-frequency oscillations (100–500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures
Epilepsia
The electrical activity in the motor cortex that accompanies voluntary movement
Journal of Physiology
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