EEG-triggered TMS reveals stronger brain state-dependent modulation of motor evoked potentials at weaker stimulation intensities

Schaworonkow, Natalie; Triesch, Jochen; Ziemann, Ulf; Zrenner, Christoph

doi:10.1016/j.brs.2018.09.009

Cited by 109 publications

(72 citation statements)

References 39 publications

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“…In each of the three µ-phase conditions, we administered 100 stimuli at the intensities suggested by the threshold-tracking algorithm. In accord with previous work 3,6 , the administration of 100 stimuli per µ-phase condition was chosen to ensure an adequate number of trials (i.e., after trial removal during the EEG and EMG preprocessing stages) to achieve sufficient statistical power for differentiating phase-specific stimulation effects. The stimulation order was pseudorandomized so that blocks of three consecutive stimuli contained one stimulus targeting each µ-phase condition.…”

Section: Scientific Reports |mentioning

confidence: 99%

Interhemispheric symmetry of µ-rhythm phase-dependency of corticospinal excitability

Stefanou

Galevska

Zrenner

et al. 2020

Sci Rep

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oscillatory activity in the µ-frequency band (8-13 Hz) determines excitability in sensorimotor cortex. In humans, the primary motor cortex (M1) in the two hemispheres shows significant anatomical, connectional, and electrophysiological differences associated with motor dominance. It is currently unclear whether the µ-oscillation phase effects on corticospinal excitability demonstrated previously for the motordominant M1 are also different between motor-dominant and motor-non-dominant M1 or, alternatively, are similar to reflect a ubiquitous physiological trait of the motor system at rest. Here, we applied singlepulse transcranial magnetic stimulation to the hand representations of the motor-dominant and the motornon-dominant M1 of 51 healthy right-handed volunteers when electroencephalography indicated a certain µ-oscillation phase (positive peak, negative peak, or random). We determined resting motor threshold (RMT) as a marker of corticospinal excitability in the three µ-phase conditions. RMT differed significantly depending on the pre-stimulus phase of the µ-oscillation in both M1, with highest RMT in the positive-peak condition, and lowest RMT in the negative-peak condition. µ-phase-dependency of RMt correlated directly between the two M1, and interhemispheric differences in µ-phase-dependency were absent. In conclusion, µ-phase-dependency of corticospinal excitability appears to be a ubiquitous physiological trait of the motor system at rest, without hemispheric dominance.The hypothesis that µ-oscillatory activity modulates cortical excitability in the sensorimotor cortex has recently received growing experimental support from electrophysiological studies in primates 1 and humans 2-6 . The ongoing oscillations of motor networks at rest have been shown to resonate at the µ-frequency band (8-13 Hz) 7 , while the phase of the µ-rhythm has been related to a periodical transition between high-and low-excitability states in neurons of sensorimotor cortex 1 . In a study based on local field potential (LFP) recordings in the right monkey primary motor cortex (M1), neuronal firing rate was highest during the trough of the µ-oscillation, and lowest during its peak 1 .The development of real-time electroencephalography (EEG)-triggered transcranial magnetic stimulation (TMS) has recently enabled a deterministic probing of the effects of the phase of a pre-stimulus oscillation on corticospinal excitability, as indexed by the motor evoked potential (MEP) amplitude, in the human M1. Using real-time brain-state-dependent TMS, we have shown that the EEG negative peak of the µ-oscillation represents a high-excitability state of corticospinal neurons (i.e., larger MEP amplitudes are elicited when TMS is triggered at the EEG negative peak of the µ-oscillation compared to the EEG positive peak) 2-5 . This effect has been demonstrated separately for the M1 of the motor-dominant 2,3 and the motor-non-dominant 4 hemisphere of right-handed subjects.Although µ-oscillations are ubiquitously present in the sensorimotor cortex at rest 7...

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Section: Scientific Reports |mentioning

confidence: 99%

Interhemispheric symmetry of µ-rhythm phase-dependency of corticospinal excitability

Stefanou

Galevska

Zrenner

et al. 2020

Sci Rep

Self Cite

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“…Rhythmic oscillatory brain activity at rest is associated with high versus low neuronal responsiveness, or ‘excitability’ of a region (Jensen and Mazaheri, 2010; Jensen et al, 2011). Measuring these momentary fluctuations of neural activity via electro- or magnetoencephalography (EEG/MEG) over human primary motor cortex (M1), it has been demonstrated that frequency, amplitude and phase of the ongoing oscillation cycle systematically modulate responses evoked by transcranial magnetic stimulation (TMS) (Zarkowski et al, 2006; Sauseng et al, 2009; Schaworonkow et al, 2018; Kelly et al, 2009; Mazaheri et al, 2009; Schubert et al, 2006). In particular, it has been shown that corticomotor excitability is significantly higher when the power (amplitude) of sensorimotor rhythms in the alpha band (8–14 Hz, also called the ‘mu’-rhythm), or beta band (15–30 Hz) are low, or when M1 is stimulated during the trough of the oscillatory cycle of these rhythms (Zaehle et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Neural activity related to volitional regulation of cortical excitability

Ruddy

Balsters

Mantini

et al. 2018

eLife

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To date there exists no reliable method to non-invasively upregulate or downregulate the state of the resting human motor system over a large dynamic range. Here we show that an operant conditioning paradigm which provides neurofeedback of the size of motor evoked potentials (MEPs) in response to transcranial magnetic stimulation (TMS), enables participants to self-modulate their own brain state. Following training, participants were able to robustly increase (by 83.8%) and decrease (by 30.6%) their MEP amplitudes. This volitional up-versus down-regulation of corticomotor excitability caused an increase of late-cortical disinhibition (LCD), a TMS derived read-out of presynaptic GABAB disinhibition, which was accompanied by an increase of gamma and a decrease of alpha oscillations in the trained hemisphere. This approach paves the way for future investigations into how altered brain state influences motor neurophysiology and recovery of function in a neurorehabilitation context.

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“…One way to potentially minimize this variability in TMS measurement is by delivering real time electroencephalogram (EEG) triggered TMS. Synchronizing each TMS pulse with specific sensorimotor oscillatory phases in alpha bands of EEG signals enables consistency in the delivery of the stimulus, and in turn reduces variability in trial to trial MEPs (Zrenner et al, 2018; Schaworonkow et al, 2019). This method may provide a more comprehensive understanding of the effect of the intervention on CME.…”

Section: Discussionmentioning

confidence: 99%

A Systematic Review of Paired Associative Stimulation (PAS) to Modulate Lower Limb Corticomotor Excitability: Implications for Stimulation Parameter Selection and Experimental Design

Alder¹,

Signal²,

Olsen³

et al. 2019

Front. Neurosci.

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Non-invasive neuromodulatory interventions have the potential to influence neural plasticity and augment motor rehabilitation in people with stroke. Paired associative stimulation (PAS) involves the repeated pairing of single pulses of electrical stimulation to a peripheral nerve and single pulses of transcranial magnetic stimulation over the contralateral primary motor cortex. Efficacy of PAS in the lower limb of healthy and stroke populations has not been systematically appraised. Optimal protocols including stimulation parameter settings have yet to be determined. This systematic review (a) examines the efficacy of PAS on lower limb corticomotor excitability in healthy and stroke populations and (b) evaluates the stimulation parameters employed. Five databases were searched for randomized, non-randomized, and pre-post experimental studies evaluating lower limb PAS in healthy and stroke populations. Two independent reviewers identified eligible studies and assessed methodological quality using a modified Downs and Blacks Tool and the TMS Checklist. Intervention stimulation parameters and TMS measurement details were also extracted and compared. Twelve articles, comprising 24 experiments, met the inclusion criteria. Four articles evaluated PAS in people with stroke. Following a single session of PAS, 21 experiments reported modulation of corticomotor excitability, lasting up to 60 min; however, the research lacked methodological rigor. Intervention stimulation parameters were highly variable across experiments, and whilst these appeared to influence efficacy, variations in the intervention and outcome assessment methods hindered the ability to draw conclusions about optimal parameters. Lower limb PAS research requires further investigation before considering its translation into clinical practice. Eight key recommendations serve as guide for enhancing future research in the field.

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EEG-triggered TMS reveals stronger brain state-dependent modulation of motor evoked potentials at weaker stimulation intensities

Cited by 109 publications

References 39 publications

Interhemispheric symmetry of µ-rhythm phase-dependency of corticospinal excitability

Interhemispheric symmetry of µ-rhythm phase-dependency of corticospinal excitability

Neural activity related to volitional regulation of cortical excitability

A Systematic Review of Paired Associative Stimulation (PAS) to Modulate Lower Limb Corticomotor Excitability: Implications for Stimulation Parameter Selection and Experimental Design

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