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Traveling waves and trial averaging : The nature of single-trial and averaged brain responses in large-scale cortical signals

Alexander, David M. ; Jurica, Peter ; Trengove, Chris ; Nikolaev, Andrey R. LU orcid ; Gepshtein, Sergei ; Zvyagintsev, Mikhail ; Mathiak, Klaus ; Schulze-Bonhage, Andreas ; Ruescher, Johanna and Ball, Tonio , et al. (2013) In NeuroImage 73. p.95-112
Abstract

Analyzing single trial brain activity remains a challenging problem in the neurosciences. We gain purchase on this problem by focusing on globally synchronous fields in within-trial evoked brain activity, rather than on localized peaks in the trial-averaged evoked response (ER). We analyzed data from three measurement modalities, each with different spatial resolutions: magnetoencephalogram (MEG), electroencephalogram (EEG) and electrocorticogram (ECoG). We first characterized the ER in terms of summation of phase and amplitude components over trials. Both contributed to the ER, as expected, but the ER topography was dominated by the phase component. This means the observed topography of cross-trial phase will not necessarily reflect... (More)

Analyzing single trial brain activity remains a challenging problem in the neurosciences. We gain purchase on this problem by focusing on globally synchronous fields in within-trial evoked brain activity, rather than on localized peaks in the trial-averaged evoked response (ER). We analyzed data from three measurement modalities, each with different spatial resolutions: magnetoencephalogram (MEG), electroencephalogram (EEG) and electrocorticogram (ECoG). We first characterized the ER in terms of summation of phase and amplitude components over trials. Both contributed to the ER, as expected, but the ER topography was dominated by the phase component. This means the observed topography of cross-trial phase will not necessarily reflect the phase topography within trials. Hence the observed topography of cross-trial phase will not accurately reflect the phase topography within trials. To assess the organization of within-trial phase, traveling wave (TW) components were quantified by computing the phase gradient. TWs were intermittent but ubiquitous in the within-trial evoked brain activity. At most task-relevant times and frequencies, the within-trial phase topography was described better by a TW than by the trial-average of phase. The trial-average of the TW components also reproduced the topography of the ER; we suggest that the ER topography arises, in large part, as an average over TW behaviors. These findings were consistent across the three measurement modalities. We conclude that, while phase is critical to understanding the topography of event-related activity, the preliminary step of collating cortical signals across trials can obscure the TW components in brain activity and lead to an underestimation of the coherent motion of cortical fields.

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publishing date
type
Contribution to journal
publication status
published
subject
keywords
Cortical topography, Evoked response, Phase, Traveling waves
in
NeuroImage
volume
73
pages
18 pages
publisher
Elsevier
external identifiers
  • scopus:84874379051
  • pmid:23353031
ISSN
1053-8119
DOI
10.1016/j.neuroimage.2013.01.016
language
English
LU publication?
no
id
365071c3-5fcb-473d-baf5-66c93b557c5d
date added to LUP
2020-03-31 19:50:23
date last changed
2024-04-03 05:10:42
@article{365071c3-5fcb-473d-baf5-66c93b557c5d,
  abstract     = {{<p>Analyzing single trial brain activity remains a challenging problem in the neurosciences. We gain purchase on this problem by focusing on globally synchronous fields in within-trial evoked brain activity, rather than on localized peaks in the trial-averaged evoked response (ER). We analyzed data from three measurement modalities, each with different spatial resolutions: magnetoencephalogram (MEG), electroencephalogram (EEG) and electrocorticogram (ECoG). We first characterized the ER in terms of summation of phase and amplitude components over trials. Both contributed to the ER, as expected, but the ER topography was dominated by the phase component. This means the observed topography of cross-trial phase will not necessarily reflect the phase topography within trials. Hence the observed topography of cross-trial phase will not accurately reflect the phase topography within trials. To assess the organization of within-trial phase, traveling wave (TW) components were quantified by computing the phase gradient. TWs were intermittent but ubiquitous in the within-trial evoked brain activity. At most task-relevant times and frequencies, the within-trial phase topography was described better by a TW than by the trial-average of phase. The trial-average of the TW components also reproduced the topography of the ER; we suggest that the ER topography arises, in large part, as an average over TW behaviors. These findings were consistent across the three measurement modalities. We conclude that, while phase is critical to understanding the topography of event-related activity, the preliminary step of collating cortical signals across trials can obscure the TW components in brain activity and lead to an underestimation of the coherent motion of cortical fields.</p>}},
  author       = {{Alexander, David M. and Jurica, Peter and Trengove, Chris and Nikolaev, Andrey R. and Gepshtein, Sergei and Zvyagintsev, Mikhail and Mathiak, Klaus and Schulze-Bonhage, Andreas and Ruescher, Johanna and Ball, Tonio and van Leeuwen, Cees}},
  issn         = {{1053-8119}},
  keywords     = {{Cortical topography; Evoked response; Phase; Traveling waves}},
  language     = {{eng}},
  month        = {{06}},
  pages        = {{95--112}},
  publisher    = {{Elsevier}},
  series       = {{NeuroImage}},
  title        = {{Traveling waves and trial averaging : The nature of single-trial and averaged brain responses in large-scale cortical signals}},
  url          = {{http://dx.doi.org/10.1016/j.neuroimage.2013.01.016}},
  doi          = {{10.1016/j.neuroimage.2013.01.016}},
  volume       = {{73}},
  year         = {{2013}},
}