Changes of oscillatory brain activity induced by repetitive transcranial magnetic stimulation of the left dorsolateral prefrontal cortex in healthy subjects
Introduction
Transcranial magnetic stimulation (TMS) uses a brief electric current passing through a magnetic coil positioned on the scalp to create a transient high-intensity magnetic field that focuses on the cortex and induces neuronal responses (Di Lazzaro et al., 2011, Hallett, 2007). The application of many pulses (repetitive TMS, rTMS) can modulate brain's activity during periods that outlast the stimulation time and is thus of potential interest for therapeutic applications, such as depression (Dell'Osso et al., 2009, George, 2010, Richieri et al., 2011), schizophrenia with auditory hallucinations (Hasan et al., 2013, Homan et al., 2012), migraines (Brigo et al., 2012, Magis et al., 2012) or stroke (Hummel et al., 2008, Jung et al., 2012).
It is supposed that the inhibitory and excitatory properties of rTMS protocols depend on the stimulation parameters, particularly the frequency of stimulation and the temporal structure of the paradigm, i.e. whether the series of pulses are applied continuously or not (Classen and Stefan, 2008). Those properties can be efficiently estimated when stimulating the motor cortex by recording motor evoked potentials (MEPs) on peripheral muscles. From such electromyographic (EMG) recordings, it has been shown that low-frequency stimulation (≤ 1 Hz) usually produces lasting decrease in motor cortex excitability, whereas high-frequency stimulation (≥ 5 Hz) induces facilitatory effects (Di Lazzaro et al., 2011, Hayashi et al., 2004, Houdayer et al., 2008, Noh et al., 2012, Romero et al., 2002). Similarly, theta burst stimulation (TBS, burst of three 50 Hz pulses repeated every 200 ms) is supposed to produce opposite neuronal after-effects depending whether bursts are applied continuously (cTBS, inhibitory) or intermittently (iTBS, excitatory) (Hoogendam et al., 2010, Huang et al., 2005). When stimulating outside the motor cortex, electroencephalographic (EEG) signals during or just following single pulse TMS provide similar valuable information about the changes in cortical activity, either locally or at remote locations from the site of stimulation (Ilmoniemi et al., 1997, Rosanova et al., 2009). Concerning rTMS, a recent review and meta-analysis of EEG/rTMS studies pointed out that it exists a certain degree of inter-study variability in the observed EEG after-effects (Thut and Pascual-Leone, 2010). In addition, the classical dichotomy between low vs. high frequency rTMS and inhibition vs. excitation has been challenged by a series of studies of EEG power changes following rTMS at different frequencies (1 Hz, 5 Hz, 20 Hz) that all showed increases of cortical motor oscillations in alpha and beta bands (Brignani et al., 2008, Fuggetta et al., 2008, Veniero et al., 2011). However, EEG oscillatory activity is only an indirect measure of inhibitory and excitatory properties of underlying neuronal networks. Still, from recordings in anesthetised animals combining extracellular and EEG recordings (Contreras and Steriade, 1995), it has been shown a direct correlation between low frequencies of EEG and hyperpolarisation waves, suggesting that amplitude of low frequency EEG positively correlate with large-scale neuronal inhibition. Importantly, it has also been shown that in the range of beta–gamma bands (20–80 Hz), oscillatory power was positively correlated with inhibitory transmission of fast-spiking cells (Cardin et al., 2009), making this band an indirect marker of local inhibition (see (Buzsáki and Wang, 2012) for a recent review on the mechanisms of gamma oscillations).
Whereas rTMS of dorsolateral prefrontal cortex (DLPFC) is commonly used for treating depression (Avery et al., 2006, Fitzgerald et al., 2003, George, 2010, George et al., 1995, Pascual-Leone et al., 1996), only a limited number of studies performed in healthy subjects described brain's responses to this type of stimulation (Graf et al., 2001, Griskova et al., 2007, Grossheinrich et al., 2009, Okamura et al., 2001). While the responses to motor cortex rTMS are relatively consistent across studies in healthy controls, it is not the case for DLPFC rTMS because of the heterogeneity of the population samples and of the experimental design. The main experimental factors that introduced variability in reported rTMS effects are the pulse parameters (Arai et al., 2005, Classen and Stefan, 2008, Taylor and Loo, 2007), the different ways of targeting the DLPFC between experimenters and the different anatomy of the underlying gyri between subjects (Thielscher et al., 2010).
In this study, we overcome these potential confounds by studying the EEG after-effects of five rTMS protocols (sham, 1 Hz, 10 Hz, iTBS, cTBS) of the left DLPFC performed on the same subjects by the same experimenter (A. W.-K.). In contrast to the previous studies where only one or two active protocols were compared to sham, the same subject underwent here all five protocols. From such repeated measures, we wanted to evaluate which rTMS protocol induces the most significant after-effects and whether patterns of cortical responses differ between rTMS protocols. To that end, statistical results on modifications of EEG oscillatory activity by rTMS are presented below at the group level.
Section snippets
Participants
The study was approved by the regional ethical committee of Grenoble University Hospital (CPP Sud-Est I, ID RCB: 2011-A00114-37) and a written informed consent to participate in the study was obtained from all participants. Twenty healthy volunteers (10 males, 10 females), aged 21 to 60 (mean 31.2 ± 10.3 years) were enrolled for five rTMS sessions with concurrent EEG recordings. Two successive experimental sessions in the same subject were separated by at least 1 week and up to 10 days. All sessions
Experimental events
Three out of 20 subjects had to be excluded from the entire analysis because of very bad quality of EEG signals or because of drowsiness. One additional subject had to also be removed from 10 Hz and 1 Hz analyses because of too short artefact free periods. Additionally, the coil position was slightly adapted in 3 subjects who experienced pain in the left eye or in the trigeminal nerve when stimulated on the target defined a priori. Two subjects reported headache after 10 Hz rTMS and one subject
Discussion
The aim of this research was to investigate the EEG after-effects of different rTMS protocols of the left DLPFC in healthy controls maintained at rest and awake. From scalp and source localisation analyses, the largest responses were identified around the anatomical target of rTMS, but also distant responses could be observed, particularly in the homologous region in high frequency bands.
To our knowledge, only five studies of EEG changes after DLPFC rTMS were performed in healthy subjects (Graf
Acknowledgments
This study was funded by a research grant from Région Rhônes Alpes. Agata Woźniak-Kwaśniewska is a PhD student sponsored by a Région Rhône-Alpes scholarship. Olivier David is funded by Inserm. The authors also thank Pr. Christian Marendaz for sharing the TMS research facility, Mr. Sylvain Harquel for technical assistance in EEG recordings and Dr. Marjorie Villien and Dr. Manik Bhattacharjee for MRI acquisitions.
References (58)
- et al.
Comparison between short train, monophasic and biphasic repetitive transcranial magnetic stimulation (rTMS) of the human motor cortex
Clin. Neurophysiol.
(2005) - et al.
Differences in after-effect between monophasic and biphasic high-frequency rTMS of the human motor cortex
Clin. Neurophysiol.
(2007) - et al.
A controlled study of repetitive transcranial magnetic stimulation in medication-resistant major depression
Biol. Psychiatry
(2006) - et al.
EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis
J. Neurosci. Methods
(2004) - et al.
A study of the effectiveness of high-frequency left prefrontal cortex transcranial magnetic stimulation in major depression in patients who have not responded to right-sided stimulation
Psychiatry Res.
(2009) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence
Trends Cogn. Sci.
(2005)- et al.
Multiple sparse priors for the M/EEG inverse problem
NeuroImage
(2008) - et al.
Development of the EEG of school-age children and adolescents. I. Analysis of band power
Electroencephalogr. Clin. Neurophysiol.
(1988) - et al.
High frequency repetitive transcranial magnetic stimulation (rTMS) of the left dorsolateral cortex: EEG topography during waking and subsequent sleep
Psychiatry Res.
(2001) - et al.
The effects of 10 Hz repetitive transcranial magnetic stimulation on resting EEG power spectrum in healthy subjects
Neurosci. Lett.
(2007)
Theta burst stimulation of the prefrontal cortex: safety and impact on cognition, mood, and resting electroencephalogram
Biol. Psychiatry
Transcranial magnetic stimulation: a primer
Neuron
Transcranial magnetic stimulation in therapy studies: examination of the reliability of “standard” coil positioning by neuronavigation
Biol. Psychiatry
Physiology of repetitive transcranial magnetic stimulation of the human brain
Brain Stimul.
Theta burst stimulation of the human motor cortex
Neuron
Controversy: Noninvasive and invasive cortical stimulation show efficacy in treating stroke patients
Brain Stimul.
Electromagnetic source reconstruction for group studies
NeuroImage
The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
Imaging human EEG dynamics using independent component analysis
Neurosci. Biobehav. Rev.
Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression
Lancet
Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex
Clin. Neurophysiol.
Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research
Stimulus waveform influences the efficacy of repetitive transcranial magnetic stimulation
J. Affect. Disord.
Schizophrenia as failure of left hemispheric dominance for the phonological component of language
PLoS ONE
Theta-burst transcranial magnetic stimulation alters cortical inhibition
J. Neurosci.
A neuronal network model for simulating the effects of repetitive transcranial magnetic stimulation on local field potential power spectra
PLoS ONE
Modulation of cortical oscillatory activity during transcranial magnetic stimulation
Hum. Brain Mapp.
Transcranial magnetic stimulation of visual cortex in migraine patients: a systematic review with meta-analysis
J. Headache Pain
Rhythms of the Brain
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