Phase matters when there is power: Phasic modulation of corticospinal excitability occurs at high amplitude sensorimotor mu-oscillations
Prior studies have suggested that oscillatory activity in cortical networks can modulate stimulus-evoked responses through time-varying fluctuations in neural excitation-inhibition dynamics. Studies combining transcranial magnetic stimulation (TMS) with electromyography (EMG) and electroencephalogra...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-12-01
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| Series: | Neuroimage: Reports |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2666956022000563 |
| _version_ | 1811208878527873024 |
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| author | Recep A. Ozdemir Sofia Kirkman Justine R. Magnuson Peter J. Fried Alvaro Pascual-Leone Mouhsin M. Shafi |
| author_facet | Recep A. Ozdemir Sofia Kirkman Justine R. Magnuson Peter J. Fried Alvaro Pascual-Leone Mouhsin M. Shafi |
| author_sort | Recep A. Ozdemir |
| collection | DOAJ |
| description | Prior studies have suggested that oscillatory activity in cortical networks can modulate stimulus-evoked responses through time-varying fluctuations in neural excitation-inhibition dynamics. Studies combining transcranial magnetic stimulation (TMS) with electromyography (EMG) and electroencephalography (EEG) can provide direct measurements to examine how instantaneous fluctuations in cortical oscillations contribute to variability in TMS-induced corticospinal responses. However, the results of these studies have been conflicting, as some reports showed consistent phase effects of sensorimotor mu-rhythms with increased excitability at the negative mu peaks, while others failed to replicate these findings or reported unspecific mu-phase effects across subjects. Given the lack of consistent results, we systematically examined the modulatory effects of instantaneous and pre-stimulus sensorimotor mu-rhythms on corticospinal responses with offline EEG-based motor evoked potential (MEP) classification analyses across five identical visits. Instantaneous sensorimotor mu-phase or pre-stimulus mu-power alone did not significantly modulate MEP responses. Instantaneous mu-power analyses showed weak effects with larger MEPs during high-power trials at the overall group level analyses, but this trend was not reproducible across visits. However, TMS delivered at the negative peak of high magnitude mu-oscillations generated the largest MEPs across all visits, with significant differences compared to other peak-phase combinations. High power effects on MEPs were only observed at the trough phase of ongoing mu oscillations originating from the stimulated region, indicating site and phase specificity, respectively. More importantly, such phase-dependent power effects on corticospinal excitability were reproducible across multiple visits. We provide further evidence that fluctuations in corticospinal excitability indexed by MEP amplitudes are partially driven by dynamic interactions between the magnitude and the phase of ongoing sensorimotor mu oscillations at the time of TMS, and suggest promising insights for (re)designing neuromodulatory TMS protocols targeted to specific cortical oscillatory states. |
| first_indexed | 2024-04-12T04:29:24Z |
| format | Article |
| id | doaj.art-aa7aed989bf54d02af1f70e6e6a48100 |
| institution | Directory Open Access Journal |
| issn | 2666-9560 |
| language | English |
| last_indexed | 2024-04-12T04:29:24Z |
| publishDate | 2022-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neuroimage: Reports |
| spelling | doaj.art-aa7aed989bf54d02af1f70e6e6a481002022-12-22T03:47:59ZengElsevierNeuroimage: Reports2666-95602022-12-0124100132Phase matters when there is power: Phasic modulation of corticospinal excitability occurs at high amplitude sensorimotor mu-oscillationsRecep A. Ozdemir0Sofia Kirkman1Justine R. Magnuson2Peter J. Fried3Alvaro Pascual-Leone4Mouhsin M. Shafi5Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Boston, MA, USA; Department of Neurology, Harvard Medical School, Boston, MA, USA; Corresponding author. Mouhsin Shafi Berenson-Allen Center for Non-Invasive Brain Stimulation, Beth Israel Medical Center, Harvard Medical School, Boston, MA, USA.Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Boston, MA, USABerenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Boston, MA, USA; Department of Neurology, Harvard Medical School, Boston, MA, USABerenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Boston, MA, USA; Department of Neurology, Harvard Medical School, Boston, MA, USADepartment of Neurology, Harvard Medical School, Boston, MA, USA; Hinda and Arthur Marcus Institute for Aging Research and Deanne and Sidney Wolk Center for Memory Health, Hebrew Senior Life, Boston, MA, USA; Guttmann Brain Health Institute, Institut Guttmann de Neurorehabilitació, Universitat Autonoma de Barcelona, Badalona, SpainBerenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Boston, MA, USA; Department of Neurology, Harvard Medical School, Boston, MA, USA; Corresponding author. Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Boston, MA, USA.Prior studies have suggested that oscillatory activity in cortical networks can modulate stimulus-evoked responses through time-varying fluctuations in neural excitation-inhibition dynamics. Studies combining transcranial magnetic stimulation (TMS) with electromyography (EMG) and electroencephalography (EEG) can provide direct measurements to examine how instantaneous fluctuations in cortical oscillations contribute to variability in TMS-induced corticospinal responses. However, the results of these studies have been conflicting, as some reports showed consistent phase effects of sensorimotor mu-rhythms with increased excitability at the negative mu peaks, while others failed to replicate these findings or reported unspecific mu-phase effects across subjects. Given the lack of consistent results, we systematically examined the modulatory effects of instantaneous and pre-stimulus sensorimotor mu-rhythms on corticospinal responses with offline EEG-based motor evoked potential (MEP) classification analyses across five identical visits. Instantaneous sensorimotor mu-phase or pre-stimulus mu-power alone did not significantly modulate MEP responses. Instantaneous mu-power analyses showed weak effects with larger MEPs during high-power trials at the overall group level analyses, but this trend was not reproducible across visits. However, TMS delivered at the negative peak of high magnitude mu-oscillations generated the largest MEPs across all visits, with significant differences compared to other peak-phase combinations. High power effects on MEPs were only observed at the trough phase of ongoing mu oscillations originating from the stimulated region, indicating site and phase specificity, respectively. More importantly, such phase-dependent power effects on corticospinal excitability were reproducible across multiple visits. We provide further evidence that fluctuations in corticospinal excitability indexed by MEP amplitudes are partially driven by dynamic interactions between the magnitude and the phase of ongoing sensorimotor mu oscillations at the time of TMS, and suggest promising insights for (re)designing neuromodulatory TMS protocols targeted to specific cortical oscillatory states.http://www.sciencedirect.com/science/article/pii/S2666956022000563 |
| spellingShingle | Recep A. Ozdemir Sofia Kirkman Justine R. Magnuson Peter J. Fried Alvaro Pascual-Leone Mouhsin M. Shafi Phase matters when there is power: Phasic modulation of corticospinal excitability occurs at high amplitude sensorimotor mu-oscillations Neuroimage: Reports |
| title | Phase matters when there is power: Phasic modulation of corticospinal excitability occurs at high amplitude sensorimotor mu-oscillations |
| title_full | Phase matters when there is power: Phasic modulation of corticospinal excitability occurs at high amplitude sensorimotor mu-oscillations |
| title_fullStr | Phase matters when there is power: Phasic modulation of corticospinal excitability occurs at high amplitude sensorimotor mu-oscillations |
| title_full_unstemmed | Phase matters when there is power: Phasic modulation of corticospinal excitability occurs at high amplitude sensorimotor mu-oscillations |
| title_short | Phase matters when there is power: Phasic modulation of corticospinal excitability occurs at high amplitude sensorimotor mu-oscillations |
| title_sort | phase matters when there is power phasic modulation of corticospinal excitability occurs at high amplitude sensorimotor mu oscillations |
| url | http://www.sciencedirect.com/science/article/pii/S2666956022000563 |
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