Table 2.
Quantified EEG changes after repeated TMS pulses
| Authors | Subjects | TMS-parameters | EEG-measures | Timing of EEG | Aftereffects | Duration of aftereffects |
|---|---|---|---|---|---|---|
| Urushihara et al. (2006) | N = 9 healthy | 0.2 Hz/21 min of monophasic M1,PM,SMA/85%rMT/250p | SEP-amplitude | Before and after TMS | Yes: ~55% facilitation after PM-stim | Not assessed |
| Hosono et al. (2008) | N = 13 healthy | 0.2 Hz/20 min/mono- vs. biphasic PM,sham/85%rMT/250p | SEP-amplitude | Before and after TMS | Yes: ~30–40% facilitation for mono-but no effect for bi-phasic | At least 10 min but recovered after 30 min |
| Van Der Werf and Paus (2006) | N = 12 | 0.6 Hz/15 min M1,PM/90%rMT/540p | TMS-induced response | Before and after TMS | Yes: ~60% amplitude decrease, reduction in induced activity (theta) | At least 40 min not studied longer |
| Satow et al. (2003) | N = 8 healthy | 0.9 Hz/16.6 min S1/90%rMT/900p | SEP-amplitude | Before and after rTMS | No | n.a. |
| Rollnik et al. (2004) | N = 11 healty | 0.9 Hz/15–20 × 60 s trains frontal/90%MT | Error-related negativity | After TMS | Yes: attenuation of ERN | At least 3 min not studied longer |
| Chen et al. (2003) | N = 8 healthy | 0.9 Hz/15 min PM/90%aMT/818p | Movement-related power/coherence (task) | Before and after TMS | Yes: less task-related alpha/beta decrease coherence increase (alpha) | Up to 15 min recovered after 30 min |
| Enomoto et al. (2001) | N = 7 healthy | 1 Hz/3.3 min PM, M1,S1/110%aMT/200p | SEP-amplitude | Before and after rTMS | Yes: ~40% suppression with M1 but not PM or S1 | Up to 60 min recovered after 70 min |
| Restuccia et al. (2007) | N = 8 healthy | 1 Hz/20 min S1/sham/80%MT/1200p | Early/late HF-SEPs | Before and after TMS | Yes: ~18/26% facilit./suppress. after S1 relative to sham | Up to 15 min recovered after 20 min |
| Bohotin et al. (2002) | N = 24 healthy | 1 Hz/15 min occipital/100%PT/900p | VEP-amplitude & habituation | Before and after TMS | Yes: ~15% suppression in controls | Up to 15–30 min |
| Fumal et al. (2003) | N = 24 healthy | 1 Hz/15 min occipital/100%PT/900p | VEP-amplitude & habituation | Before and after TMS | Yes: ~15% suppression | Up to 33 min recovery after 40 min |
| Schutter and van Honk (2003) | N = 8 healthy | 1 Hz/20 min occipital/110%MT/1200p | VEP-amplitude | After TMS and sham | Yes: ~55% suppression | Not assessed |
| Thut et al. (2003) | N = 6 healthy | 1 Hz/10 min Occipital/110%PT/600p | VEP-amplitude alpha-changes | Before and after TMS | Yes: ~40% suppression of desynchronization (alpha) | At least 8 min recovered after 20 min |
| Evers et al. (2001) | N = 14 healthy | 1 Hz/2 min DLPFC/95%MT/120p | Visual P300 | Before and after TMS | No | n.a. |
| Hansenne et al. (2004) | N = 17 healthy | 1 Hz/10 and 15 min DLPFC/100%MT/600–900p | Auditory P300 | Before and after TMS | Yes/No: latency increase after 15 min but not 10 min rTMS | Not assessed |
| Rossi et al. (2000) | N = 5 healthy | 1 Hz/15 min M1/110%MT/900p | Readiness potential | After TMS and Sham | Yes: ~30% focal amplitude decrease | Not assessed |
| Strens et al. (2002) | N = 15 healthy | 1 Hz/25 min M1/90%aMT/1500p | Spectral power coherence (rest and task) | Before and after TMS | Yes: ~15% focal increase in coherence (alpha) | Up to 25 min recovered after 30 min |
| Tamura et al. (2005) | N = 12 healthy | 1 Hz/10 min M1/95%rMT/600p | Movement-related oscillations | Control and after TMS | Yes: ~10% decrease in synchronization (beta) | Not assessed |
| Brignani et al. (2008) | N = 6 healthy | 1 Hz/10 min M1/110%MT/600p | EEG power (rest) | During TMS | Yes: max 82% focal, cumulative increase in power (alpha) | Not assessed |
| Pastor et al. (2006) | N = 6 healthy | 1 Hz/10 min Cerebellum/60%max/600p | Steady-state potentials | Before and after TMS | Yes: change in prefrontal oscillations (gamma) | At least 7.5 min not studied longer |
| Schutter et al. (2001) | N = 12 healthy | 1 Hz/20 min DLPFC/130%MT/1200p | Spectral power (rest) | After TMS and sham | Yes: increase in prefrontal power (theta) | At least 1 h not studied longer |
| Ragert et al. (2004) | N = 13 healthy | 5 Hz/5 × 5 × 10 s: 5 s ITI S1/90%MT1250p | Paired pulse SEP-inhibition | Before and after TMS | Yes: suppression of inhibition with ipsil-vs. contralateral S1 | At least 1h not studied longer |
| Holler et al. (2006) | N = 8 healthy | 5 Hz/5 × 60 s train: 60 s ITI M1/90%rMT/1500p | Anticipatory CNV | Before and after TMS/sham | Yes: focal amplitude increase | Not assessed |
| Oliviero et al. (2003) | N = 16 healthy | 5 Hz/10 s single train M1/100%aMT/50p | Spectral power coherence (rest and task) | Before and after TMS | Yes: ~25% focal coherence decrease (alpha) | Immediately after TMS recovered after 25 min |
| Fuggetta et al. (2008) | N = 11 healthy | 5 Hz/20 × 4 s trains: 30 s ITI M1/80–100%MT/400p | EEG power and coherence (rest) | During TMS | Yes: ~30–40% focal incr/decr in alpha and beta power/coherence | Not assessed |
| Huber et al. (2007) | N = 10 healthy | 5 Hz/5 × 6 × 10 s train: 5 s ITI M1/90%rMT/1500p | Sleep EEG | After TMS and sham | Yes: ~40% local increase in slow wave activity | Up to 30 min of nREM recovered after 31 min |
| Esser et al. (2006) | N = 7 healthy | 5 Hz/5 × 6 × 10 s train: 5 s ITI M1/90%rMT/1500p | TMS-induced response | Before and after rTMS | Yes: ~60% amplitude increase | At least 10 min not studied longer |
| Restuccia et al. (2007) | N = 8 healthy | 10 Hz/12 × 10 s trains: 20 s ITI S1/sham/80%MT/1200p | Early/late HF-SEPs | Before and after TMS | Yes: ~–/14% –/facilit. after S1 relative to sham | At least 20 min |
| Bohotin et al. (2002) | N = 30 Migraine | 10 Hz/18 × 5 s trains: 10 s ITI occipital/100%PT/900p | VEP-amplitude & habituation | Before and after TMS | Yes: ~15% facilitation in migraineurs | Up to 9–30 min |
| Jing et al. (2001b) | N = 15 healthy | 10 Hz/2 × 3 s train: 5 min ITI DLPFC/100%MT/60p | Auditory P300 | Before and after TMS | Yes: ~15–25% decrease in N100-amplitude, changes in P200/P300-latencies | Not assessed |
| Jing et al. (2001a) | N = 29 healthy | 10 Hz/2 × 3 s train: 5 min ITI DLPFC/100%MT/60p | Auditory P300 | Before and after TMS | Yes: latency-increase | Not assessed |
| Griskova et al. (2007) | N = 18 healthy | 10 Hz/100 × 2 s train: 10 s ITI DLPFC/110%MT/2000p | Spectral power (rest) | Before and after TMS | Yes: ~400% increase in delta-power | At least 10 min, not studied longer |
| Okamura et al. (2001) | N = 32 healthy | 10 Hz/2 × 3 s train: 300 s ITI Frontal/100%MT/60p | Spectral power (rest) | Before and after TMS | Yes: change in peak frequency and power (~10%, many frequencies) | At least 5 min not studied longer |
| Jing and Takigawa (2000) | N = 19 healthy | 10 Hz/2 × 3 s train: 5 min ITI DLPFC/100%MT/60p | Coherence (rest) | Before and after TMS | Yes: max 32% focal directed coherence increase (alpha) | At least 5 min not studied longer |
| Klimesch et al. (2003) | N = 16 healthy | High frequency/IAF-20 Hz 1.2–4.8 s trains: >12 s ITI parietal,frontal/110%MT/24p | Band power and event-related desynchronization | Before and after TMS | Yes: ~40% increase of desynchronization (alpha) | Not assessed |
| Evers et al. (2001) | N = 14 healthy | 20 Hz/3 × 5 s train: 1 min ITI DLPFC/95%MT/300p | Visual P300 | Before and after TMS | Yes: latency-decrease | Not assessed |
| Graf et al. (2001) | N = 8 healthy | 20 Hz/40 × 2 s train: 28 s ITI DLPFC/90%MT/1600p | Sleep EEG | Before and after TMS | Yes: minor reduction in sleep stage 1 | Not assessed |
| Cohrs et al. (1998) | N = 13 healthy | 20 Hz/160 × 0.25 s: 8 s ITI DLPFC/120%rMT/800p | Sleep EEG | After TMS and sham | Yes: delay in REM-latency prolonged nREM-REM cycle | Not assessed |
| Schutter et al. (2003) | N = 5 healthy | 25 Hz/80 × 10 s train: 5 s ITI Cerebellum/80%MT/2000p | Spectral power (rest) | Before and after TMS | Yes: change in prefrontal asymmetry (gamma) | At least 15 min not studied longer |
| Ishikawa et al. (2007) | N = 12 healthy | cThetaBS/40 s M1,S1/80%aMT/600p | SEP-amplitude | Before and after TMS | Yes: ~20% suppression with S1 vs. ~50% facilitation with M1 | Up to 53 min recovered after 60 min |
| Sağlam et al. (2008) | N = 8 healthy | cThetaBS/40 s M1,S1/80%aMT/600p | EEG-EMG-coherence | Before and after TMS | Yes: ~50% suppression with M1 but not S1 | Up to 30–60 min recovered after 90 min |
| Schindler et al. (2008) | N = 4 healthy | cThetaBS/33 s right FEF/80%rMT/600p | Spectral analysis (rest) | Before and after TMS | Yes: ~enhanced synchronization in stimulated hemisphere | At least 60 min not studied longer |
| Ortu et al. (2009) | N = 7 healthy | cThetaBS/40 s M1,PM/80%aMT/600p | Readiness potential | Before and after TMS | Yes: ~30–50% suppression with left M1 but nor right M1 nor PM | At least 30 min not studied longer |
| Grossheinrich et al. (2009) | N = 12 healthy | cThetaBS/40 s DLPFC,mPFC/80%rMT/600p imThetaBS as sham | Spectral analysis (rest) | Before and after TMS | No | n.a. |
| iThetaBS/20 × 2 s: 8 s ITI imThetaBS as sham | Spectral analysis | Before and after TMS | Yes: alpha-power enhancement after DLPFC | Up to 50 min not studied longer | ||
| Poreisz et al. (2008) | N = 12 healthy | cThetaBS/40 s S1,Sham/80%aMT/600p | Laser-evoked potential | Before and after TMS | Yes: ~15% suppression of N2 | Up to 8–10 min not studied longer |
| iThetaBS/20 × 2 s: 8 s ITI S1,Sham/80%aMT/600p | Laser-evoked potential | Before and after TMS | Yes: ~20% suppression of N2 | Up to 8–10 min not studied longer | ||
| imThetaBS/8 × 5 s: 10 s ITI S1,Sham/80%aMT/600p | Laser-evoked potential | Before and after TMS | Yes: ~25% suppression of N2 | Up to 8–10 min not studied longer | ||
| Katayama and Rothwell (2007) | N = 11 healthy | iThetaBS/19 × 2 s: 8 s ITI M1,S1/80%aMT/600p | SEP-amplitude | Before and after TMS | Yes: ~10–20% facilitation with S1 but not M1 | Up to 30 min not studied longer |
| Tsuji and Rothwell (2002) | N = 9 healthy | PAS, 30 min M1/105%rMT/180p | SEP-amplitude | Before and after TMS | Yes: ~40–60% facilitation | Up to 10 min recovered after 20 min |
| Wolters et al. (2005) | N = 64 healthy | PAS, 30 min M1,S1/150%rMT/180p | SEP-amplitude | Before and after TMS | Yes: ~15–20% facilitation with S1 but not M1 | Up to 30 min recovered after 60 min |
| Huber et al. (2008) | N = 19 healthy | PAS, 22.5 min M1/130%rMT/90p | TMS-induced response | Before and after TMS | Yes: ~10% facilitation or 10% inhibition depending on ISI | At least 2 min not studied longer |
| Slow wave activity (sleep) | After TMS | Yes: correlation with change in TMS-induced response | At least 90 min not studied longer |
Studies ordered according to protocols and EEG-measure
TMS-parameters: iThetaBS: intermittent Theta Burst Stimulation; cThetaBS: continuous Theta Burst Stimulation, PAS: repeated paired associative stimulation; ITI: inter-train interval; aMT: active motor threshold; rMT: resting motor threshold; PT: phosphene threshold; p: pulses; IAF: individual alpha frequency; Stimulation sites DLPFC: dorsolateral prefrontal cortex, PM: premotor; EEG-measures SEP: somatosensory evoked potential; HF-SEP: high-frequency SEPs