Event Abstract

Probing preparatory inhibition bilaterally with double-coil TMS

  • 1 Institut de Neuroscience, Université Catholique de Louvain, Belgium

Excitability of the corticospinal pathway can be investigated non-invasively in humans by applying transcranial magnetic stimulation (TMS) over the primary motor cortex (M1), eliciting motor-evoked potentials (MEPs) in targeted contralateral muscles. The amplitude of MEPs elicited in muscles of the contralateral limb (often the hand) is a precious indicator of corticospinal excitability (CSE) at the time of stimulation (Duque et al., 2017). Comparing MEP amplitudes in different conditions have helped to characterize the corticospinal correlates of various neural processes (Klein et al., 2012; Cos et al., 2014; Derosiere et al., 2015, 2017a, 2017b; Derosière et al., 2015; Zénon et al., 2015; Algoet et al., 2018) including those underlying action preparation (Duque et al., 2010, 2012, 2013, 2014, 2016, Klein et al., 2014, 2016; Quoilin and Derosiere, 2015; Wilhelm et al., 2016; Quoilin et al., 2016, 2018; Vassiliadis et al., 2018). During action preparation recent TMS studies have revealed that the motor output pathway shows profound inhibitory changes, even during the planning of simple finger movements (Bestmann & Duque, 2016; Duque, Greenhouse, Labruna, & Ivry, 2017). As such, MEPs are strongly supressed preceding motor responses, indicating that the excitability of the corticospinal pathway is largely inhibited when the motor system prepares a behavior (Duque, et al., 2017). To date, these studies have exploited a classical single-coil TMS protocol, stimulating one hemisphere (e.g. the right hemisphere) and registering MEPs in the contralateral hand (e.g. the left hand). Hence, in most experiments, the MEP data have only provided researchers with half of the story, increasing the probability of seeing data being misinterpreted. This occurs because applying TMS over both M1 in separate blocks doubles the duration of the experiment, making it impossible to fit all the conditions in a single session. Thus, so far, it has been assumed that differences in the strength of preparatory inhibition between conditions in which the target muscle (e.g. left index agonist) is either selected (e.g. left index response) or non-selected (e.g. right index response) for the forthcoming movement are due to the distinct function of the left index finger muscle in these two situations (Duque et al., 2010, 2014; Labruna et al., 2014). Yet, there is a substantial confound here because besides the function (selected vs. non-selected), conditions also differ in regard to the hand being cued for the response (left or right). Hence, left MEP differences in preparatory inhibition between left and right hand movement trials may be due to the use of the non-dominant vs dominant hand and not to the distinct function of the targeted muscle in these trials. We recently showed that, in the resting state, double-coil stimulation of the two M1 with a 1 ms inter-pulse interval (double-coil1ms TMS) elicits MEPs in both hands that are comparable to MEPs obtained using single-coil TMS (Grandjean et al., 2017a, 2017b, 2018). In the present study (Vassiliadis et al., 2018), we intended to evaluate whether MEPs elicited with double-coil1ms TMS are equivalent to single-coil MEPs when elicited during action preparation in an instructed-delay choice reaction time task where subjects have to inhibit a cued response until an imperative signal is displayed. We thus aimed at assessing if the inhibitory mechanisms extensively described in this type of task (Duque et al., 2017) are faithfully reproduced when using a double-coil1ms protocol. To do so, we compared the amplitude as well as the coefficient of variation (CV) of MEPs produced by double-coil1ms or single-coil TMS during action preparation. We observed that MEPs were suppressed (smaller amplitude) and often less variable (smaller CV) during the delay period compared to baseline as previously reported (Klein-Flügge et al., 2013; Duque et al., 2017). Importantly, these effects were equivalent whether single-coil or double-coil1ms TMS was used. This result supports the absence of any neural interactions between the two corticospinal volleys with the double-coil1ms method and suggests that double-coil1ms TMS is a reliable tool to assess CSE, not only when subjects are at rest, but also when they are involved in a task. The advantages of double-coil1ms TMS are manifold. First, the number of MEPs that can be collected in a given amount of time is doubled. This is a crucial aspect as it gives the opportunity to test more conditions within the same duration than could be done with a regular single-coil method. Second, MEPs are elicited in both hands at a near simultaneous time, meaning that CSE excitability can be probed bilaterally on each trial. Hence, dominant and non-dominant hand MEPs are elicited in the exact same conditions during the task (Duque et al., 2013). This obviously increases the signal to noise ratio in a significant way. Third, the acquisition of MEPs in both hands allows researchers to make direct comparisons between bilateral MEPs on a single-trial basis and to develop new measures such as indexes reflecting the ratio between CSE changes occurring in the two hands. In fact, one may be interested in studying the impact of various task parameters (e.g. instruction, presence of reward, sensory evidence, level of urgency, effort required etc.) on the relationship between bilateral MEP amplitudes and CVs. Hence, the present technique opens new horizons in the study of how both hemispheres interact in various task settings (Verleger et al., 2009; Klein et al., 2016).

References

Algoet M, Duque J, Iannetti GD, Mouraux A (2018) Temporal Profile and Limb-specificity of Phasic Pain-Evoked Changes in Motor Excitability. Neuroscience 386:240–255 Available at: https://linkinghub.elsevier.com/retrieve/pii/S0306452218304573. Cos I, Duque J, Cisek P (2014) Rapid prediction of biomechanical costs during action decisions. J Neurophysiol 112:1256–1266 Available at: http://jn.physiology.org/cgi/doi/10.1152/jn.00147.2014. Derosière G, Billot M, Ward ET, Perrey S (2015) Adaptations of motor neural structures’ activity to lapses in attention. Cereb Cortex 25:66–74. Derosiere G, Vassiliadis P, Demaret S, Zenon A, Duque J (2015) Disentangling the involvement of primary motor cortex in value-based reinforcement learning and value-based decision making. Soc Neurosci 2015 2015:2015–2017 Available at: http://dial.uclouvain.be/handle/boreal:172088. Derosiere G, Vassiliadis P, Demaret S, Zénon A, Duque J (2017a) Learning stage-dependent effect of M1 disruption on value-based motor decisions. Neuroimage Available at: http://linkinghub.elsevier.com/retrieve/pii/S1053811917307164. Derosiere G, Zénon A, Alamia A, Duque J (2017b) Primary motor cortex contributes to the implementation of implicit value-based rules during motor decisions. Neuroimage 146:1115–1127 Available at: http://dx.doi.org/10.1016/j.neuroimage.2016.10.010. Duque J, Greenhouse I, Labruna L, Ivry RB (2017) Physiological Markers of Motor Inhibition during Human Behavior. Trends Neurosci 40:219–236 Available at: http://dx.doi.org/10.1016/j.tins.2017.02.006. Duque J, Labruna L, Cazares C, Ivry RB (2014) Dissociating the influence of response selection and task anticipation on corticospinal suppression during response preparation. Neuropsychologia 65:287–296 Available at: http://dx.doi.org/10.1016/j.neuropsychologia.2014.08.006. Duque J, Labruna L, Verset S, Olivier E, Ivry RB (2012) Dissociating the role of prefrontal and premotor cortices in controlling inhibitory mechanisms during motor preparation. J Neurosci 32:806–816. Duque J, Lew D, Mazzocchio R, Olivier E, Richard B (2010) Evidence for two concurrent inhibitory mechanisms during response preparation. J Neurosci 30:3793–3802. Duque J, Olivier E, Rushworth M (2013) Top–Down Inhibitory Control Exerted by the Medial Frontal Cortex during Action Selection under Conflict. J Cogn Neurosci 25:1634–1648 Available at: http://www.mitpressjournals.org/doi/10.1162/jocn_a_00421. Duque J, Petitjean C, Swinnen SP (2016) Effect of aging on motor inhibition during action preparation under sensory conflict. Front Aging Neurosci 8:1–14. Grandjean J, Derosiere G, Vassiliadis P, Quemener L, de Wilde Y, Duque J (2017a) Validation of a double-coil TMS method to assess corticospinal excitability. Brain Stimul 10:507 Available at: http://linkinghub.elsevier.com/retrieve/pii/S1935861X17304801. Grandjean J, Derosiere G, Vassiliadis P, Quemener L, Wilde Y de, Duque J (2018) Towards assessing corticospinal excitability bilaterally: Validation of a double-coil TMS method. J Neurosci Methods 293:162–168 Available at: http://linkinghub.elsevier.com/retrieve/pii/S016502701730345X. Grandjean J, Vassiliadis P, Derosiere G, de Wilde Y, Quemener L, Duque J (2017b) A New Double-Coil TMS Method to Assess Corticospinal Excitability Bilaterally. Front Neurosci Available at: http://www.frontiersin.org/neuroscience/10.3389/conf.fnins.2017.94.00118/full. Klein-Flügge MC, Nobbs D, Pitcher JB, Bestmann S (2013) Variability of human corticospinal excitability tracks the state of action preparation. J Neurosci 33:5564–5572 Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3736101&tool=pmcentrez&rendertype=abstract. Klein P-A, Olivier E, Duque J (2012) Influence of Reward on Corticospinal Excitability during Movement Preparation. J Neurosci 32:18124–18136. Klein PA, Duque J, Labruna L, Ivry RB (2016) Comparison of the two cerebral hemispheres in inhibitory processes operative during movement preparation. Neuroimage 125:220–232 Available at: http://dx.doi.org/10.1016/j.neuroimage.2015.10.007. Klein PA, Petitjean C, Olivier E, Duque J (2014) Top-down suppression of incompatible motor activations during response selection under conflict. Neuroimage 86:138–149 Available at: http://dx.doi.org/10.1016/j.neuroimage.2013.08.005. Labruna L, Lebon F, Duque J, Klein P-A, Cazares C, Ivry RB (2014) Generic Inhibition of the Selected Movement and Constrained Inhibition of Nonselected Movements during Response Preparation. J Cogn Neurosci 26:269–278. Quoilin C, Derosiere G (2015) Global and Specific Motor Inhibitory Mechanisms during Action Preparation. J Neurosci 35:16297–16299 Available at: http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.3664-15.2015 [Accessed August 2, 2017]. Quoilin C, Lambert J, Jacob B, Klein PA, Duque J (2016) Comparison of motor inhibition in variants of the instructed-delay choice reaction time task. PLoS One 11:1–16. Quoilin C, Wilhelm E, Maurage P, Timary P De, Duque J (2018) Deficient inhibition in alcohol-dependence : let’s consider the role of the motor system ! Neuropsychopharmacology:0–8 Available at: http://dx.doi.org/10.1038/s41386-018-0074-0. Vassiliadis P, Grandjean J, Derosiere G, Wilde Y De (2018) Using a Double-Coil TMS Protocol to Assess Preparatory Inhibition Bilaterally. 12:1–14. Verleger R, Kuniecki M, Möller F, Fritzmannova M, Siebner HR (2009) On how the motor cortices resolve an inter-hemispheric response conflict: An event-related EEG potential-guided TMS study of the flankers task. Eur J Neurosci 30:318–326. Wilhelm E, Quoilin C, Petitjean C, Duque J (2016) A Double-Coil TMS Method to Assess Corticospinal Excitability Changes at a Near-Simultaneous Time in the Two Hands during Movement Preparation. Front Hum Neurosci 10:1–11 Available at: http://journal.frontiersin.org/article/10.3389/fnhum.2016.00088. Zénon A, Klein PA, Alamia A, Boursoit F, Wilhelm E, Duque J (2015) Increased reliance on value-based decision processes following motor cortex disruption. Brain Stimul 8:957–964 Available at: http://dx.doi.org/10.1016/j.brs.2015.05.007.

Keywords: Transcramial magnetic stimulation, Motor-evoked potential (MEP), Primary motor cortex (M1), corticospinal excitability, Coefficient of variation (C.V.), action preparation, inhibition

Conference: Belgian Brain Congress 2018 — Belgian Brain Council, LIEGE, Belgium, 19 Oct - 19 Oct, 2018.

Presentation Type: e-posters

Topic: NOVEL STRATEGIES FOR NEUROLOGICAL AND MENTAL DISORDERS: SCIENTIFIC BASIS AND VALUE FOR PATIENT-CENTERED CARE

Citation: Vassiliadis P, Grandjean J, Derosiere G, De Wilde Y, Quemener L and Duque J (2019). Probing preparatory inhibition bilaterally with double-coil TMS. Front. Neurosci. Conference Abstract: Belgian Brain Congress 2018 — Belgian Brain Council. doi: 10.3389/conf.fnins.2018.95.00029

Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters.

The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated.

Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed.

For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions.

Received: 11 Aug 2018; Published Online: 17 Jan 2019.

* Correspondence: Dr. Pierre Vassiliadis, Institut de Neuroscience, Université Catholique de Louvain, Brussels, Belgium, pierre.vassiliadis@epfl.ch