Elsevier

Brain Stimulation

Volume 8, Issue 6, November–December 2015, Pages 1010-1020
Brain Stimulation

Review
Measuring Brain Stimulation Induced Changes in Cortical Properties Using TMS-EEG

https://doi.org/10.1016/j.brs.2015.07.029Get rights and content

Highlights

  • A review of measuring the effects of neuromodulation using TMS-EEG.

  • TMS-EEG provides direct information on cortical reactivity and connectivity.

  • Distinctive changes in TEPs before and after brain stimulation have been highlighted.

  • Understanding the mechanisms involved in neuroplasticity.

Abstract

Neuromodulatory brain stimulation can induce plastic reorganization of cortical circuits that persist beyond the period of stimulation. Most of our current knowledge about the physiological properties has been derived from the motor cortex. The integration of transcranial magnetic stimulation (TMS) and electroencephalography (EEG) is a valuable method for directly probing excitability, connectivity and oscillatory dynamics of regions throughout the brain. Offering in depth measurement of cortical reactivity, TMS-EEG allows the evaluation of TMS-evoked components that may act as a marker for cortical excitation and inhibition. A growing body of research is using concurrent TMS and EEG (TMS-EEG) to explore the effects of different neuromodulatory techniques such as repetitive TMS and transcranial direct current stimulation on cortical function, particularly in non-motor regions. In this review, we outline studies examining TMS-evoked potentials and oscillations before and after, or during a single session of brain stimulation. Investigating these studies will aid in our understanding of mechanisms involved in the modulation of excitability and inhibition by neuroplasticity following different stimulation paradigms.

Introduction

Neuromodulatory brain stimulation can induce plastic reorganization of cortical circuits which persist beyond the period of stimulation [1]. A variety of neuromodulation techniques are currently used to modulate brain activity, the most common of which are repetitive Transcranial Magnetic Stimulation (rTMS) and transcranial Direct Current Stimulation (tDCS). Traditionally measuring the cortical effect of these techniques has been restricted to the motor cortex, namely due to the easily measureable output of motor evoked potentials (MEPs) which occurs in response to single and paired pulse TMS. As such there is a large body of existing work which has used this non-repetitive TMS over the motor cortex to track changes in cortical activity resulting from neuromodulatory brain stimulation paradigms, specifically looking at corticomotor excitability and cortical inhibition [2], [3], [4], [5]. To expand the brain regions and range of variables that can be measured before and after neuromodulation, researchers have increasingly combined this single and paired pulse TMS with electroencephalogram (EEG). Concurrent use of TMS and EEG (TMS-EEG) allows a method for probing varied superficial cortical brain regions to study intracortical neural circuits [6]. Furthermore, TMS-EEG captures additional cortical properties such as the generation of oscillatory brain activity and the propagation of signals to other cortical regions [7]. In this review, we summarize the impact of the most commonly applied neuromodulatory techniques on motor cortical excitability determined using MEPs. We then examine the cortical properties that can be assessed using TMS-EEG and explore how these measures compliment and extend information gained from MEPs. Finally, we outline the studies that have used this approach to assess changes in cortical properties resulting from neuromodulatory paradigms in both motor and non-motor regions, particularly looking at TMS-evoked potentials (TEPs) and oscillations before and after, or during one single session of brain stimulation.

Section snippets

Effects of neuromodulatory brain stimulation on brain function

Neuromodulatory paradigms can influence neural activity in humans in different ways, either increasing or decreasing cortical excitability depending on the stimulation parameters [8], [9], [10], [11]. This unique ability to safely modulate cortical activity has led to many experimental and therapeutic applications using these techniques. However, inter-individual variability and state-dependency of neuromodulatory brain stimulation approaches need to be taken into account when efficacy and

Combining TMS and EEG to measure cortical properties

Despite the wealth of information gained from motor cortex studies on neuromodulatory brain stimulation, recordings of TMS-induced physiological effects (e.g. muscle twitch and MEPs) have not traditionally been accessible in non-motor cortical regions. In brain regions other than motor cortex, other measurable effects such as the perception of phosphenes with TMS [46] and behavioral outcome (task performance) have been investigated although these effects can be limited by either subjectivity or

Probing brain stimulation-induced changes in cortical properties using TMS-EEG

As described above, TMS-EEG provides additional information on cortical properties than studies of only motor cortex output. Cortical reactivity can also be explored in depth by investigating changes in latency, amplitude, distribution and waveforms of TEPs, which can act as quantifiable markers in a similar manner to MEPs, allowing study of cortical properties outside of the motor cortex. The plasticity inducing properties of non-invasive brain stimulation allows temporary modification of

Conclusion

TMS-EEG studies of different neuromodulatory techniques have shown that there are distinctive changes in TEPs before and after brain stimulation. In particularly, peaks occurring approximately at 30 ms, 45 ms and 100 ms following motor cortex stimulation seem more frequently affected by neuromodulation, and change in alpha and theta frequencies are most prevalent in the studies investigated. Even though peaks occurring at different time points and changes in various frequency bands have been

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    Disclosures and conflict of interests: NCR is supported by an NHMRC Early Career Fellowship (1072057). KEH is supported by an NHMRC Career Development Fellowship (1082894). PBF is supported by an NHMRC Practitioner Fellowship (606907). PBF has received equipment for research from MagVenture A/S, Medtronic Ltd, Cervel Neurotech and Brainsway Ltd and funding for research from Cervel Neurotech. There are no other conflicts. PBF has received consultancy fees as a scientific advisor for Bionomics.

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