High frequency oscillations are associated with cognitive processing in human recognition memory

Michal T. Kucewicz, Jan Cimbalnik, Joseph Y. Matsumoto, Benjamin Brinkmann, Mark R. Bower, Vincent Vasoli, Vlastimil Sulc, Fred Meyer, W. R. Marsh, Squire Matthew Stead, Gregory Alan Worrell

Research output: Contribution to journalArticle

61 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)2231-2244
Number of pages14
JournalBrain
Volume137
Issue number8
DOIs
StatePublished - 2014

Fingerprint

Nonparametric Statistics
Brain
Cognition
Amygdala
Hippocampus
Electrodes
Biomarkers
Recognition (Psychology)
Recognition Memory
Oscillation
Cognitive Processing
Learning
Encoding

Keywords

  • cognitive processing
  • gamma oscillations
  • high frequency oscillations
  • memory
  • neural networks

ASJC Scopus subject areas

  • Clinical Neurology
  • Arts and Humanities (miscellaneous)

Cite this

High frequency oscillations are associated with cognitive processing in human recognition memory. / Kucewicz, Michal T.; Cimbalnik, Jan; Matsumoto, Joseph Y.; Brinkmann, Benjamin; Bower, Mark R.; Vasoli, Vincent; Sulc, Vlastimil; Meyer, Fred; Marsh, W. R.; Stead, Squire Matthew; Worrell, Gregory Alan.

In: Brain, Vol. 137, No. 8, 2014, p. 2231-2244.

Research output: Contribution to journalArticle

Kucewicz, MT, Cimbalnik, J, Matsumoto, JY, Brinkmann, B, Bower, MR, Vasoli, V, Sulc, V, Meyer, F, Marsh, WR, Stead, SM & Worrell, GA 2014, 'High frequency oscillations are associated with cognitive processing in human recognition memory', Brain, vol. 137, no. 8, pp. 2231-2244. https://doi.org/10.1093/brain/awu149
Kucewicz, Michal T. ; Cimbalnik, Jan ; Matsumoto, Joseph Y. ; Brinkmann, Benjamin ; Bower, Mark R. ; Vasoli, Vincent ; Sulc, Vlastimil ; Meyer, Fred ; Marsh, W. R. ; Stead, Squire Matthew ; Worrell, Gregory Alan. / High frequency oscillations are associated with cognitive processing in human recognition memory. In: Brain. 2014 ; Vol. 137, No. 8. pp. 2231-2244.
@article{3dd3b26f16aa4cfab377f7a9ae1029d5,
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.",
keywords = "cognitive processing, gamma oscillations, high frequency oscillations, memory, neural networks",
author = "Kucewicz, {Michal T.} and Jan Cimbalnik and Matsumoto, {Joseph Y.} and Benjamin Brinkmann and Bower, {Mark R.} and Vincent Vasoli and Vlastimil Sulc and Fred Meyer and Marsh, {W. R.} and Stead, {Squire Matthew} and Worrell, {Gregory Alan}",
year = "2014",
doi = "10.1093/brain/awu149",
language = "English (US)",
volume = "137",
pages = "2231--2244",
journal = "Brain",
issn = "0006-8950",
publisher = "Oxford University Press",
number = "8",

}

TY - JOUR

T1 - High frequency oscillations are associated with cognitive processing in human recognition memory

AU - Kucewicz, Michal T.

AU - Cimbalnik, Jan

AU - Matsumoto, Joseph Y.

AU - Brinkmann, Benjamin

AU - Bower, Mark R.

AU - Vasoli, Vincent

AU - Sulc, Vlastimil

AU - Meyer, Fred

AU - Marsh, W. R.

AU - Stead, Squire Matthew

AU - Worrell, Gregory Alan

PY - 2014

Y1 - 2014

N2 - 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.

AB - 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.

KW - cognitive processing

KW - gamma oscillations

KW - high frequency oscillations

KW - memory

KW - neural networks

UR - http://www.scopus.com/inward/record.url?scp=84904967933&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84904967933&partnerID=8YFLogxK

U2 - 10.1093/brain/awu149

DO - 10.1093/brain/awu149

M3 - Article

C2 - 24919972

AN - SCOPUS:84904967933

VL - 137

SP - 2231

EP - 2244

JO - Brain

JF - Brain

SN - 0006-8950

IS - 8

ER -