Dissecting gamma frequency activity during human memory processing.
Gamma frequency activity (30-150 Hz) is induced in cognitive tasks and is thought to reflect underlying neural processes. Gamma frequency activity can be recorded directly from the human brain using intracranial electrodes implanted in patients undergoing treatment for drug-resistant epilepsy. Previous studies have independently explored narrowband oscillations in the local field potential and broadband power increases. It is not clear, however, which processes contribute to human brain gamma frequency activity, or their dynamics and roles during memory processing. Here a large dataset of intracranial recordings obtained during encoding of words from 101 patients was used to detect, characterize and compare induced gamma frequency activity events. Individual bursts of gamma frequency activity were isolated in the time-frequency domain to determine their spectral features, including peak frequency, amplitude, frequency span, and duration. We found two distinct types of gamma frequency activity events that showed either narrowband or broadband frequency spans revealing characteristic spectral properties. Narrowband events, the predominant type, were induced by word presentations following an initial induction of broadband events, which were temporally separated and selectively correlated with evoked response potentials, suggesting that they reflect different neural activities and play different roles during memory encoding. The two gamma frequency activity types were differentially modulated during encoding of subsequently recalled and forgotten words. In conclusion, we found evidence for two distinct activity types induced in the gamma frequency range during cognitive processing. Separating these two gamma frequency activity components contributes to the current understanding of electrophysiological biomarkers, and may prove useful for emerging neurotechnologies targeting, mapping and modulating distinct neurophysiological processes in normal and epileptogenic brain.
Mayo Clinic, Department of Neurology, Mayo Systems Electrophysiology Laboratory (MSEL), Rochester MN, USA.|Mayo Clinic, Department of Physiology and Biomedical Engineering, Rochester MN, USA.
Michal T
MT
Kucewicz
Mayo Clinic, Department of Neurology, Mayo Systems Electrophysiology Laboratory (MSEL), Rochester MN, USA.|Mayo Clinic, Department of Physiology and Biomedical Engineering, Rochester MN, USA.
Brent M
BM
Berry
Mayo Clinic, Department of Neurology, Mayo Systems Electrophysiology Laboratory (MSEL), Rochester MN, USA.|Mayo Clinic, Department of Physiology and Biomedical Engineering, Rochester MN, USA.|Czech Institute of Informatics, Robotics and Cybernetics, Czech Technical University in Prague, Czech Republic.
Vaclav
V
Kremen
Mayo Clinic, Department of Neurology, Mayo Systems Electrophysiology Laboratory (MSEL), Rochester MN, USA.|Mayo Clinic, Department of Physiology and Biomedical Engineering, Rochester MN, USA.
Benjamin H
BH
Brinkmann
Thomas Jefferson University Hospital, Department of Neurology, Philadelphia PN, USA.
Michael R
MR
Sperling
Dartmouth-Hitchcock Medical Center, Department of Neurology, Lebanon NH, USA.
Barbara C
BC
Jobst
Emory University, Department of Neurosurgery, Atlanta GA, USA.
Robert E
RE
Gross
University of Texas Southwestern Medical Center, Department of Neurosurgery, Dallas TX, USA.
Bradley
B
Lega
Columbia University, Department of Neurology, New York NY, USA.
Sameer A
SA
Sheth
University of Pennsylvania Hospital, Department of Radiology, Philadelphia PN, USA.
Joel M
JM
Stein
Mayo Clinic, Department of Neurology, Mayo Systems Electrophysiology Laboratory (MSEL), Rochester MN, USA.
Sandthitsu R
SR
Das
Thomas Jefferson University Hospital, Department of Radiology, Philadelphia PN, USA.
Richard
R
Gorniak
Mayo Clinic, Department of Neurology, Mayo Systems Electrophysiology Laboratory (MSEL), Rochester MN, USA.|Mayo Clinic, Department of Physiology and Biomedical Engineering, Rochester MN, USA.
S Matthew
SM
Stead
University of Pennsylvania, Department of Psychology, Philadelphia PN, USA.
Daniel S
DS
Rizzuto
University of Pennsylvania, Department of Psychology, Philadelphia PN, USA.
Michael J
MJ
Kahana
Mayo Clinic, Department of Neurology, Mayo Systems Electrophysiology Laboratory (MSEL), Rochester MN, USA.|Mayo Clinic, Department of Physiology and Biomedical Engineering, Rochester MN, USA.
Gregory A
GA
Worrell
D001921:Brain / Q000502:physiology; D000069279:Drug Resistant Epilepsy / Q000503:physiopathology; D004567:Electrodes, Implanted; D005074:Evoked Potentials, Visual / Q000502:physiology; D065818:Gamma Rhythm / Q000502:physiology*; D006801:Humans; D008568:Memory / Q000502:physiology*
ECoG; evoked response potential; gamma oscillations; intracranial EEG; neuronal ensembles