Cortical responses to noninvasive perturbations enable individual brain fingerprinting

Ozdemir, Recep A.; Tadayon, Ehsan; Boucher, Pierre; Sun, Haoqi; Momi, Davide; Ganglberger, Wolfgang; Westover, M. Brandon; Pascual‐Leone, Álvaro; Santarnecchi, Emiliano; Shafi, Mouhsin M.

doi:10.1016/j.brs.2021.02.005

Cited by 49 publications

(43 citation statements)

References 29 publications

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“…TMS-evoked 8 and induced changes in endogenous oscillatory activity 9 can be observed using electroencephalography (EEG) 10 , 11 . An averaged TMS-evoked EEG potential (TEP) is used to describe local and network effects of focal single pulse TMS 8 , 10 , 12 , 13 . However, the TEP waveform contains all activity within several hundred milliseconds of the pulse.…”

Section: Introductionmentioning

confidence: 99%

A structured ICA-based process for removing auditory evoked potentials

Ross

Ozdemir

Lian

et al. 2022

Sci Rep

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Transcranial magnetic stimulation (TMS)-evoked potentials (TEPs), recorded using electroencephalography (EEG), reflect a combination of TMS-induced cortical activity and multi-sensory responses to TMS. The auditory evoked potential (AEP) is a high-amplitude sensory potential—evoked by the “click” sound produced by every TMS pulse—that can dominate the TEP and obscure observation of other neural components. The AEP is peripherally evoked and therefore should not be stimulation site specific. We address the problem of disentangling the peripherally evoked AEP of the TEP from components evoked by cortical stimulation and ask whether removal of AEP enables more accurate isolation of TEP. We hypothesized that isolation of the AEP using Independent Components Analysis (ICA) would reveal features that are stimulation site specific and unique individual features. In order to improve the effectiveness of ICA for removal of AEP from the TEP, and thus more clearly separate the transcranial-evoked and non-specific TMS-modulated potentials, we merged sham and active TMS datasets representing multiple stimulation conditions, removed the resulting AEP component, and evaluated performance across different sham protocols and clinical populations using reduction in Global and Local Mean Field Power (GMFP/LMFP) and cosine similarity analysis. We show that removing AEPs significantly reduced GMFP and LMFP in the post-stimulation TEP (14 to 400 ms), driven by time windows consistent with the N100 and P200 temporal characteristics of AEPs. Cosine similarity analysis supports that removing AEPs reduces TEP similarity between subjects and reduces TEP similarity between stimulation conditions. Similarity is reduced most in a mid-latency window consistent with the N100 time-course, but nevertheless remains high in this time window. Residual TEP in this window has a time-course and topography unique from AEPs, which follow-up exploratory analyses suggest could be a modulation in the alpha band that is not stimulation site specific but is unique to individual subject. We show, using two datasets and two implementations of sham, evidence in cortical topography, TEP time-course, GMFP/LMFP and cosine similarity analyses that this procedure is effective and conservative in removing the AEP from TEP, and may thus better isolate TMS-evoked activity. We show TEP remaining in early, mid and late latencies. The early response is site and subject specific. Later response may be consistent with TMS-modulated alpha activity that is not site specific but is unique to the individual. TEP remaining after removal of AEP is unique and can provide insight into TMS-evoked potentials and other modulated oscillatory dynamics.

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Section: Introductionmentioning

confidence: 99%

A structured ICA-based process for removing auditory evoked potentials

Ross

Ozdemir

Lian

et al. 2022

Sci Rep

Self Cite

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“…TMS-EEG experiments performed without controlling for the auditory component result in TEPs that are contaminated by auditory potentials (Massimini et al, 2005;Nikouline et al, 1999;Rocchi et al, 2021;Rogasch et al, 2014;ter Braack et al, 2015). Controlling for the auditory confounding can be challenging, so that merely increasing the loudness of the masking noises has proved to be not always effective in previous TMS-EEG studies (Conde et al, 2019;Ozdemir et al, 2021;ter Braack et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

TAAC - TMS Adaptable Auditory Control: a universal tool to mask TMS click

Russo

Puglisi

Palù

et al. 2021

Preprint

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Background Coupling transcranial magnetic stimulation with electroencephalography (TMS-EEG) allows recording the EEG response to a direct, non-invasive cortical perturbation. However, obtaining a genuine TMS-evoked EEG potential requires controlling for several confounds, among which a main source is represented by the auditory evoked potentials (AEPs) associated to the TMS discharge noise (TMS click). This contaminating factor can be in principle prevented by playing a masking noise through earphones. New method Here we release TMS Adaptable Auditory Control (TAAC), a highly flexible, open-source, Matlab-based interface that generates in real-time customized masking noises. TAAC creates noises starting from the stimulator-specific TMS click and tailors them to fit the individual, subject-specific click perception by mixing and manipulating the standard noises in both time and frequency domains. Results We showed that TAAC allows us to provide standard as well as customized noises able to effectively and safely mask the TMS click. Comparison with existing methods Here, we showcased two customized noises by comparing them to two standard noises previously used in the TMS literature (i.e., a white noise and a noise generated from the stimulator-specific TMS click only). For each, we quantified the Sound Pressure Level (SPL; measured by a Head and Torso Simulator - HATS) required to mask the TMS click in a population of 20 healthy subjects. Both customized noises were effective at safe (according to OSHA and NIOSH safety guidelines), lower SPLs with respect to standard noises. Conclusions At odds with previous methods, TAAC allows creating effective and safe masking noises specifically tailored on each TMS device and subject. The combination of TAAC with tools for the real-time visualization of TEPs can help control the influence of auditory confounds also in non-compliant patients. Finally, TAAC is a highly flexible and open-source tool, so it can be further extended to meet different experimental requirements.

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“…Similarity between TEPs across site and between subjects at each site, pre and post AEP removal, was quanti ed in vector space using the cosine similarity index [12,20]. We rst generated a TEP matrix for each subject (from averaged responses) with a xed window size (385ms) covering EEG responses from 14 to 400ms.…”

Section: Similarity Indexmentioning

confidence: 99%

“…An averaged TMS-evoked EEG potential (TEP) is used to describe local and network effects of focal single pulse TMS [8,[11][12]. However, the TEP waveform contains all activity within several hundred milliseconds of the pulse.…”

Section: Introductionmentioning

confidence: 99%

“…The TEP re ects TMS-evoked brain activation [18][19] that can be speci c to stimulation site [9,12,[20][21][22], and reproducible [12,20,23], particularly at earlier latencies. However, the speci city of longer latency responses is a matter of debate [15,[24][25] due to high correlation between TEPs and sensory responses to TMS by 60-80 ms [16-17,20] and high correlation between active and sham stimulation starting as early as 58 ms [15,17].…”

Section: Introductionmentioning

confidence: 99%

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A Structured ICA-based Process for Removing Auditory Evoked Potentials Reveals TMS-evoked Potentials and TMS-modulated Oscillations

Ross

Ozdemir

Lian³

et al. 2021

Preprint

Self Cite

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Background: Transcranial magnetic stimulation (TMS)-evoked potentials (TEPs), recorded using electroencephalography (EEG), reflect a combination of TMS-induced cortical activity and multi-sensory responses to TMS. The auditory evoked potential (AEP) is a high-amplitude sensory potential—evoked by the “click” sound produced by every TMS pulse—that can dominate the TEP and obscure observation of other neural components. The AEP is peripherally evoked and therefore should not be stimulation site specificObjectives/Methods: We address the problem of disentangling the peripherally evoked AEP of the TEP from components evoked by cortical stimulation and ask whether removal of AEP enables more accurate isolation of TEP. We hypothesized that isolation of the AEP using Independent Components Analysis (ICA) would reveal features that are stimulation site specific and unique individual features. In order to improve the effectiveness of ICA for removal of AEP from the TEP, and thus more clearly separate the transcranial-evoked and non-specific TMS-modulated potentials, we merged sham and active TMS datasets representing multiple stimulation conditions, removed the resulting AEP component, and evaluated performance across different sham protocols and clinical populations using reduction in Global and Local Mean Field Potentials (GMFA/LMFA) and cosine similarity analysis.Results: We show that removing AEPs significantly reduced GMFA and LMFA in the post-stimulation TEP (14 to 400 ms), driven by time windows consistent with the N100 and P200 temporal characteristics of AEPs. Cosine similarity analysis supports that removing AEPs reduces TEP similarity between subjects and reduces TEP similarity between stimulation conditions. Similarity is reduced most in a mid-latency window consistent with the N100 time-course, but nevertheless remains high in this time window. Residual TEP in this window has a time-course and topography unique from AEPs, which follow-up analyses suggest could be a modulation in the alpha band that is not stimulation site specific but is unique to individual subject.Conclusion(s): We show, using two datasets and two implementations of sham, evidence in cortical topography, TEP time-course, GMFA/LMFA and cosine similarity analyses that this procedure is effective and conservative in removing the AEP from TEP, and thereby reveals better defined TMS-evoked activity. We show TEP remaining in early, mid and late latencies. The early response is site and subject specific. Later responses are consistent with TMS-modulated alpha activity that is not site specific but is unique to the individual. TEP remaining after removal of AEP is unique and can provide insight into TMS-evoked potentials and other modulated oscillatory dynamics.

show abstract

Cortical responses to noninvasive perturbations enable individual brain fingerprinting

Cited by 49 publications

References 29 publications

A structured ICA-based process for removing auditory evoked potentials

A structured ICA-based process for removing auditory evoked potentials

TAAC - TMS Adaptable Auditory Control: a universal tool to mask TMS click

A Structured ICA-based Process for Removing Auditory Evoked Potentials Reveals TMS-evoked Potentials and TMS-modulated Oscillations

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