title: High frequency oscillations are associated with cognitive processing in human recognition memory.
abstract: High frequency oscillations are associated with normal brain function, but also increasingly recognized as potential biomarkers of the epileptogenic brain. Their role in human cognition has been predominantly studied in classical gamma frequencies (30-100 Hz), which reflect neuronal network coordination involved in attention, learning and memory. Invasive brain recordings in animals and humans demonstrate that physiological oscillations extend beyond the gamma frequency range, but their function in human cognitive processing has not been fully elucidated. Here we investigate high frequency oscillations spanning the high gamma (50-125 Hz), ripple (125-250 Hz) and fast ripple (250-500 Hz) frequency bands using intracranial recordings from 12 patients (five males and seven females, age 21-63 years) during memory encoding and recall of a series of affectively charged images. Presentation of the images induced high frequency oscillations in all three studied bands within the primary visual, limbic and higher order cortical regions in a sequence consistent with the visual processing stream. These induced oscillations were detected on individual electrodes localized in the amygdala, hippocampus and specific neocortical areas, revealing discrete oscillations of characteristic frequency, duration and latency from image presentation. Memory encoding and recall significantly modulated the number of induced high gamma, ripple and fast ripple detections in the studied structures, which was greater in the primary sensory areas during the encoding (Wilcoxon rank sum test, P = 0.002) and in the higher-order cortical association areas during the recall (Wilcoxon rank sum test, P = 0.001) of memorized images. Furthermore, the induced high gamma, ripple and fast ripple responses discriminated the encoded and the affectively charged images. In summary, our results show that high frequency oscillations, spanning a wide range of frequencies, are associated with memory processing and generated along distributed cortical and limbic brain regions. These findings support an important role for fast network synchronization in human cognition and extend our understanding of normal physiological brain activity during memory processing.
authors.affiliation: 1 Department of Neurology, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA.
authors.forename: Michal T
authors.initials: MT
authors.lastname: Kucewicz
authors.affiliation: 1 Department of Neurology, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA2 International Clinical Research Center, St. Anne's University Hospital, Pekarska 53, Brno 656 91, Czech Republic.
authors.forename: Jan
authors.initials: J
authors.lastname: Cimbalnik
authors.affiliation: 1 Department of Neurology, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA.
authors.forename: Joseph Y
authors.initials: JY
authors.lastname: Matsumoto
authors.affiliation: 1 Department of Neurology, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA.
authors.forename: Benjamin H
authors.initials: BH
authors.lastname: Brinkmann
authors.affiliation: 1 Department of Neurology, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA.
authors.forename: Mark R
authors.initials: MR
authors.lastname: Bower
authors.affiliation: 1 Department of Neurology, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA.
authors.forename: Vincent
authors.initials: V
authors.lastname: Vasoli
authors.affiliation: 1 Department of Neurology, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA2 International Clinical Research Center, St. Anne's University Hospital, Pekarska 53, Brno 656 91, Czech Republic.
authors.forename: Vlastimil
authors.initials: V
authors.lastname: Sulc
authors.affiliation: 3 Department of Neurosurgery, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA.
authors.forename: Fred
authors.initials: F
authors.lastname: Meyer
authors.affiliation: 3 Department of Neurosurgery, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA.
authors.forename: W R
authors.initials: WR
authors.lastname: Marsh
authors.affiliation: 1 Department of Neurology, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA.
authors.forename: S M
authors.initials: SM
authors.lastname: Stead
authors.affiliation: 1 Department of Neurology, Mayo Clinic, 200 First St SW, Rochester MN, 55905, USA worrell.gregory@mayo.edu.
authors.forename: Gregory A
authors.initials: GA
authors.lastname: Worrell
mesh_terms: D000328:Adult; D000339:Affect / Q000502:physiology; D000679:Amygdala / Q000502:physiology / Q000601:surgery; D058256:Brain Waves / Q000502:physiology*; D002540:Cerebral Cortex / Q000502:physiology; D054022:Cerebrum / Q000502:physiology*; D004567:Electrodes, Implanted; D004569:Electroencephalography / Q000295:instrumentation / Q000379:methods*; D005260:Female; D059907:Functional Neuroimaging; D006624:Hippocampus / Q000502:physiology / Q000601:surgery; D006801:Humans; D008297:Male; D008568:Memory / Q000502:physiology*; D011939:Mental Recall / Q000502:physiology; D008875:Middle Aged; D009415:Nerve Net / Q000502:physiology*; D021641:Recognition, Psychology / Q000502:physiology; D013003:Somatosensory Cortex / Q000502:physiology; D014796:Visual Perception / Q000502:physiology; D055815:Young Adult
keywords: cognitive processing; gamma oscillations; high frequency oscillations; memory; neural networks