Canonical Response Parameterization: Quantifying the structure of responses to single-pulse intracranial electrical brain stimulation

Single-pulse electrical stimulation in the nervous system, often called cortico-cortical evoked potential (CCEP) measurement, is an important technique to understand how brain regions interact with one another. Voltages are measured from implanted electrodes in one brain area while stimulating anoth...

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Published inPLoS computational biology Vol. 19; no. 5; p. e1011105
Main Authors Miller, Kai J., Müller, Klaus-Robert, Valencia, Gabriela Ojeda, Huang, Harvey, Gregg, Nicholas M., Worrell, Gregory A., Hermes, Dora
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.05.2023
Public Library of Science (PLoS)
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ISSN1553-7358
1553-734X
1553-7358
DOI10.1371/journal.pcbi.1011105

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Abstract Single-pulse electrical stimulation in the nervous system, often called cortico-cortical evoked potential (CCEP) measurement, is an important technique to understand how brain regions interact with one another. Voltages are measured from implanted electrodes in one brain area while stimulating another with brief current impulses separated by several seconds. Historically, researchers have tried to understand the significance of evoked voltage polyphasic deflections by visual inspection, but no general-purpose tool has emerged to understand their shapes or describe them mathematically. We describe and illustrate a new technique to parameterize brain stimulation data, where voltage response traces are projected into one another using a semi-normalized dot product. The length of timepoints from stimulation included in the dot product is varied to obtain a temporal profile of structural significance, and the peak of the profile uniquely identifies the duration of the response. Using linear kernel PCA, a canonical response shape is obtained over this duration, and then single-trial traces are parameterized as a projection of this canonical shape with a residual term. Such parameterization allows for dissimilar trace shapes from different brain areas to be directly compared by quantifying cross-projection magnitudes, response duration, canonical shape projection amplitudes, signal-to-noise ratios, explained variance, and statistical significance. Artifactual trials are automatically identified by outliers in sub-distributions of cross-projection magnitude, and rejected. This technique, which we call “Canonical Response Parameterization” (CRP) dramatically simplifies the study of CCEP shapes, and may also be applied in a wide range of other settings involving event-triggered data.
AbstractList Single-pulse electrical stimulation in the nervous system, often called cortico-cortical evoked potential (CCEP) measurement, is an important technique to understand how brain regions interact with one another. Voltages are measured from implanted electrodes in one brain area while stimulating another with brief current impulses separated by several seconds. Historically, researchers have tried to understand the significance of evoked voltage polyphasic deflections by visual inspection, but no general-purpose tool has emerged to understand their shapes or describe them mathematically. We describe and illustrate a new technique to parameterize brain stimulation data, where voltage response traces are projected into one another using a semi-normalized dot product. The length of timepoints from stimulation included in the dot product is varied to obtain a temporal profile of structural significance, and the peak of the profile uniquely identifies the duration of the response. Using linear kernel PCA, a canonical response shape is obtained over this duration, and then single-trial traces are parameterized as a projection of this canonical shape with a residual term. Such parameterization allows for dissimilar trace shapes from different brain areas to be directly compared by quantifying cross-projection magnitudes, response duration, canonical shape projection amplitudes, signal-to-noise ratios, explained variance, and statistical significance. Artifactual trials are automatically identified by outliers in sub-distributions of cross-projection magnitude, and rejected. This technique, which we call "Canonical Response Parameterization" (CRP) dramatically simplifies the study of CCEP shapes, and may also be applied in a wide range of other settings involving event-triggered data.Single-pulse electrical stimulation in the nervous system, often called cortico-cortical evoked potential (CCEP) measurement, is an important technique to understand how brain regions interact with one another. Voltages are measured from implanted electrodes in one brain area while stimulating another with brief current impulses separated by several seconds. Historically, researchers have tried to understand the significance of evoked voltage polyphasic deflections by visual inspection, but no general-purpose tool has emerged to understand their shapes or describe them mathematically. We describe and illustrate a new technique to parameterize brain stimulation data, where voltage response traces are projected into one another using a semi-normalized dot product. The length of timepoints from stimulation included in the dot product is varied to obtain a temporal profile of structural significance, and the peak of the profile uniquely identifies the duration of the response. Using linear kernel PCA, a canonical response shape is obtained over this duration, and then single-trial traces are parameterized as a projection of this canonical shape with a residual term. Such parameterization allows for dissimilar trace shapes from different brain areas to be directly compared by quantifying cross-projection magnitudes, response duration, canonical shape projection amplitudes, signal-to-noise ratios, explained variance, and statistical significance. Artifactual trials are automatically identified by outliers in sub-distributions of cross-projection magnitude, and rejected. This technique, which we call "Canonical Response Parameterization" (CRP) dramatically simplifies the study of CCEP shapes, and may also be applied in a wide range of other settings involving event-triggered data.
Single-pulse electrical stimulation in the nervous system, often called cortico-cortical evoked potential (CCEP) measurement, is an important technique to understand how brain regions interact with one another. Voltages are measured from implanted electrodes in one brain area while stimulating another with brief current impulses separated by several seconds. Historically, researchers have tried to understand the significance of evoked voltage polyphasic deflections by visual inspection, but no general-purpose tool has emerged to understand their shapes or describe them mathematically. We describe and illustrate a new technique to parameterize brain stimulation data, where voltage response traces are projected into one another using a semi-normalized dot product. The length of timepoints from stimulation included in the dot product is varied to obtain a temporal profile of structural significance, and the peak of the profile uniquely identifies the duration of the response. Using linear kernel PCA, a canonical response shape is obtained over this duration, and then single-trial traces are parameterized as a projection of this canonical shape with a residual term. Such parameterization allows for dissimilar trace shapes from different brain areas to be directly compared by quantifying cross-projection magnitudes, response duration, canonical shape projection amplitudes, signal-to-noise ratios, explained variance, and statistical significance. Artifactual trials are automatically identified by outliers in sub-distributions of cross-projection magnitude, and rejected. This technique, which we call “Canonical Response Parameterization” (CRP) dramatically simplifies the study of CCEP shapes, and may also be applied in a wide range of other settings involving event-triggered data.
Single-pulse electrical stimulation in the nervous system, often called cortico-cortical evoked potential (CCEP) measurement, is an important technique to understand how brain regions interact with one another. Voltages are measured from implanted electrodes in one brain area while stimulating another with brief current impulses separated by several seconds. Historically, researchers have tried to understand the significance of evoked voltage polyphasic deflections by visual inspection, but no general-purpose tool has emerged to understand their shapes or describe them mathematically. We describe and illustrate a new technique to parameterize brain stimulation data, where voltage response traces are projected into one another using a semi-normalized dot product. The length of timepoints from stimulation included in the dot product is varied to obtain a temporal profile of structural significance, and the peak of the profile uniquely identifies the duration of the response. Using linear kernel PCA, a canonical response shape is obtained over this duration, and then single-trial traces are parameterized as a projection of this canonical shape with a residual term. Such parameterization allows for dissimilar trace shapes from different brain areas to be directly compared by quantifying cross-projection magnitudes, response duration, canonical shape projection amplitudes, signal-to-noise ratios, explained variance, and statistical significance. Artifactual trials are automatically identified by outliers in sub-distributions of cross-projection magnitude, and rejected. This technique, which we call “Canonical Response Parameterization” (CRP) dramatically simplifies the study of CCEP shapes, and may also be applied in a wide range of other settings involving event-triggered data. We introduce a new machine learning technique for quantifying the structure of responses to single-pulse intracranial electrical brain stimulation. This approach allows voltage response traces of very different shape to be compared with one another. A tool like this has been needed to replace the status quo, where researchers may understand their data in terms of discovered structure rather than in terms of a pre-assigned, hand-picked, feature. The method compares single-trial responses pairwise to understand if there is a reproducible shape and how long it lasts. When significant structure is identified, the shape underlying it is isolated and each trial is parameterized in terms of this shape. This simple parameterization enables quantification of statistical significance, signal-to-noise ratio, explained variance, and average voltage of the response. Differently-shaped voltage traces from any setting can be compared with any other in a succinct mathematical framework. This versatile tool to quantify single-pulse stimulation data should facilitate a blossoming in the study of brain connectivity using implanted electrodes.
Audience Academic
Author Hermes, Dora
Valencia, Gabriela Ojeda
Worrell, Gregory A.
Müller, Klaus-Robert
Gregg, Nicholas M.
Miller, Kai J.
Huang, Harvey
AuthorAffiliation 5 Dept of Artificial Intelligence, Korea University, Seoul, Republic of Korea
7 Medical Scientist Training Program, Mayo Clinic, Rochester, Minnesota, United States of America
University of Oxford, UNITED KINGDOM
1 Dept of Neurological Surgery, Mayo Clinic, Rochester, Minnesota, United States of America
8 Dept of Neurology, Mayo Clinic, Rochester, Minnesota, United States of America
2 Dept of Biomedical Engineering & Physiology, Mayo Clinic, Rochester, Minnesota, United States of America
6 Max Planck Institute for Informatics, Saarbrücken, Germany
4 Machine Learning Group, Department of Computer Science, Berlin Institute of Technology, Berlin, Germany
3 Google Research, Brain Team, Berlin, Germany
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37228169$$D View this record in MEDLINE/PubMed
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License Copyright: © 2023 Miller et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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The authors have declared that no competing interests exist.
ORCID 0000-0002-3861-7685
0000-0002-6687-6422
0000-0002-6151-043X
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Snippet Single-pulse electrical stimulation in the nervous system, often called cortico-cortical evoked potential (CCEP) measurement, is an important technique to...
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StartPage e1011105
SubjectTerms Biology and Life Sciences
Brain
Brain Mapping - methods
Brain stimulation
Convulsions & seizures
Current impulses
Electric potential
Electric Stimulation - methods
Electrical stimulation of the brain
Electrical stimuli
Electrodes
Electrodes, Implanted
Engineering and Technology
ESB
Evoked potentials (Electrophysiology)
Evoked Potentials - physiology
Health aspects
Hypotheses
Implanted electrodes (biology)
Inspection
Measurement
Medicine and Health Sciences
Methods
Nervous system
Outliers (statistics)
Parameterization
Patient outcomes
Patients
Physical Sciences
Research and Analysis Methods
Social Sciences
Stimulation
Voltage
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Title Canonical Response Parameterization: Quantifying the structure of responses to single-pulse intracranial electrical brain stimulation
URI https://www.ncbi.nlm.nih.gov/pubmed/37228169
https://www.proquest.com/docview/2826805206
https://www.proquest.com/docview/2820030304
https://pubmed.ncbi.nlm.nih.gov/PMC10246848
https://doaj.org/article/bda98805033a4659b25ad36ef7353f39
http://dx.doi.org/10.1371/journal.pcbi.1011105
Volume 19
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