Brain State-dependent Brain Stimulation with Real-time Electroencephalography-Triggered Transcranial Magnetic Stimulation

Stefanou, Maria‐Ioanna; Baur, Dirk G.; Belardinelli, Paolo; Bergmann, Til Ole; Blum, Corinna; Gordon, Pedro Caldana; Nieminen, Jaakko O.; Zrenner, Brigitte; Ziemann, Ulf; Zrenner, Christoph

doi:10.3791/59711

Cited by 23 publications

(23 citation statements)

References 26 publications

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“…Similarly, TMS may be more effective when delivered during specific phases of oscillatory brain activity, a phenomenon we first described as phase-dependent plasticity (151). Innovative closed-loop systems have now been developed that enable this phenomenon to be harnessed and personalized by triggering stimulus bursts during specific phases of brain activity determined using electroencephalography (152)(153)(154)(155). This approach is now being trialed in individuals with depression (155).…”

Section: Relationship To Other Disorders and Stimulation Modalities Imentioning

confidence: 99%

Using Brain Imaging to Improve Spatial Targeting of Transcranial Magnetic Stimulation for Depression

Cash

Weigand

Zalesky

et al. 2021

Biological Psychiatry

225

184

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Transcranial magnetic stimulation (TMS) is an effective treatment for depression but is limited in that the optimal therapeutic target remains unknown. Early TMS trials lacked a focal target and thus positioned the TMS coil over the prefrontal cortex using scalp measurements. Over time, it became clear that this method leads to variation in the stimulation site and that this could contribute to heterogeneity in antidepressant response. Newer methods allow for precise positioning of the TMS coil over a specific brain location, but leveraging these precise methods requires a more precise therapeutic target. We review how neuroimaging is being used to identify a more focal therapeutic target for depression. We highlight recent studies showing that more effective TMS targets in the frontal cortex are functionally connected to deep limbic regions such as the subgenual cingulate cortex. We review how connectivity might be used to identify an optimal TMS target for use in all patients and potentially even a personalized target for each individual patient. We address the clinical implications of this emerging field and highlight critical questions for future research.

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Section: Relationship To Other Disorders and Stimulation Modalities Imentioning

confidence: 99%

Using Brain Imaging to Improve Spatial Targeting of Transcranial Magnetic Stimulation for Depression

Cash

Weigand

Zalesky

et al. 2021

Biological Psychiatry

225

184

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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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“…Evidence suggests that tACS can entrain specific frequency oscillations in the cortex (Helfrich et al., 2014; Pogosyan et al., 2009). Therefore, we examined whether the phase‐dependent modulation of cortical excitability that has previously been shown during endogenous alpha oscillations (Bergmann et al., 2019; Desideri et al., 2019; Schaworonkow et al., 2019; Stefanou et al., 2019) was also evident during tACS‐imposed alpha oscillations. We found no difference in MEP amplitude or SICI on the up‐going and down‐going phase of the tACS‐imposed alpha frequency oscillation: the current results provide no evidence for differences in corticospinal excitability or GABAergic inhibition when targeting the up‐going (peak) and down‐going (trough) phase of the tACS‐imposed oscillation.…”

Section: Discussionmentioning

confidence: 97%

“…To date, there are reports of phase‐dependent effects of tACS applied at beta frequencies on MEP amplitude (Battaglini et al., 2020; Berger et al., 2018; Guerra et al., 2016; Khademi et al., 2019; Nakazono et al., 2016; Schilberg et al., 2018) but not tACS applied at alpha frequencies, despite reports of phase‐dependent modulation of MEP amplitude with endogenous alpha oscillations (Bergmann et al., 2019; Desideri et al., 2019; Schaworonkow et al., 2019; Stefanou et al., 2019). Two studies have investigated phase‐dependent effects of tACS‐induced alpha oscillation on MEP amplitude.…”

Section: Introductionmentioning

confidence: 99%

“…First, in non-human primates, greater pyramidal cell firing has been observed on the down-going phase of the alpha oscillation and it was suggested that this phasic enhancement in firing rate was due to a phasic reduction in inhibitory tone (Haegens et al, 2011). Second, in humans, recent studies have shown an alpha phase-dependent modulation of corticospinal excitability, with greater excitability on the down-going phase than the up-going phase of the endogenous alpha oscillation ( (Bergmann et al, 2019;Desideri et al, 2019;Schaworonkow et al, 2019;Stefanou et al, 2019), but also see (Madsen et al, 2019)).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Examining motor evoked potential amplitude and short‐interval intracortical inhibition on the up‐going and down‐going phases of a transcranial alternating current stimulation (tacs) imposed alpha oscillation

Vallence

Dansie

Goldsworthy

et al. 2021

Eur J of Neuroscience

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Many brain regions exhibit rhythmical activity thought to reflect the summed behaviour of large populations of neurons. The endogenous alpha rhythm has been associated with phase‐dependent modulation of corticospinal excitability. However, whether exogenous alpha rhythm, induced using transcranial alternating current stimulation (tACS) also has a phase‐dependent effect on corticospinal excitability remains unknown. Here, we triggered transcranial magnetic stimuli (TMS) on the up‐ or down‐going phase of a tACS‐imposed alpha oscillation and measured motor evoked potential (MEP) amplitude and short‐interval intracortical inhibition (SICI). There was no significant difference in MEP amplitude or SICI when TMS was triggered on the up‐ or down‐going phase of the tACS‐imposed alpha oscillation. The current study provides no evidence of differences in corticospinal excitability or GABAergic inhibition when targeting the up‐going (peak) and down‐going (trough) phase of the tACS‐imposed oscillation.

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Brain State-dependent Brain Stimulation with Real-time Electroencephalography-Triggered Transcranial Magnetic Stimulation

Cited by 23 publications

References 26 publications

Using Brain Imaging to Improve Spatial Targeting of Transcranial Magnetic Stimulation for Depression

Using Brain Imaging to Improve Spatial Targeting of Transcranial Magnetic Stimulation for Depression

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

Examining motor evoked potential amplitude and short‐interval intracortical inhibition on the up‐going and down‐going phases of a transcranial alternating current stimulation (tacs) imposed alpha oscillation

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