Transcranial Magnetic Stimulation (TMS): Applications in Clinical and Basic Neuroscience

A special issue of Brain Sciences (ISSN 2076-3425). This special issue belongs to the section "Neural Engineering, Neuroergonomics and Neurorobotics".

Deadline for manuscript submissions: closed (1 February 2021) | Viewed by 25829

Special Issue Editor

Discipline of Physiology, Adelaide Medical School, The University of Adelaide, Adelaide, Australia
Interests: transcranial magnetic brain stimulation; electroencephalography; motor control; motor learning; neuroplasticity; intracortical function; ageing; concussion

Special Issue Information

Dear Colleagues,

TMS represents one of the few techniques able to non-invasively assess and modulate neurophysiological function in human participants. While this technique was established within the motor domain, coregistration with other neuroimaging modalities (e.g., electroencephalography, functional magnetic resonance imaging, etc.) now means that TMS is utilised within broad, multidisciplinary areas of both basic and clinical neuroscience. Consequently, TMS methodology and technology is continuously evolving, resulting in an ever-growing potential for applications with functional relevance. The aim of this Special Issue is therefore to highlight novel and developing areas of TMS application in both health and disease. Research focused on neuroplasticity and intracortical circuitry are particularly encouraged. Studies aiming to better understand the neurophysiological processes underpinning both conventional and emerging methodologies are also appreciated. We invite contributions in the form of review articles and original research pieces.

Dr. George Opie
Guest Editor

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Keywords

  • transcranial magnetic stimulation
  • TMS
  • clinical and basic neuroscience
  • non-invasive
  • motor
  • neuroimaging
  • electroencephalography
  • fMRI
  • neuroplasticity
  • intracortical circuitry

Published Papers (9 papers)

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Research

13 pages, 1502 KiB  
Article
Influence of Brain-Derived Neurotrophic Factor Genotype on Short-Latency Afferent Inhibition and Motor Cortex Metabolites
by Ryoki Sasaki, Naofumi Otsuru, Shota Miyaguchi, Sho Kojima, Hiraku Watanabe, Ken Ohno, Noriko Sakurai, Naoki Kodama, Daisuke Sato and Hideaki Onishi
Brain Sci. 2021, 11(3), 395; https://doi.org/10.3390/brainsci11030395 - 20 Mar 2021
Cited by 10 | Viewed by 2246
Abstract
The Met allele of the brain-derived neurotrophic factor (BDNF) gene confers reduced cortical BDNF expression and associated neurobehavioral changes. BDNF signaling influences the survival, development, and synaptic function of cortical networks. Here, we compared gamma-aminobutyric acid (GABA)ergic network activity in the human primary [...] Read more.
The Met allele of the brain-derived neurotrophic factor (BDNF) gene confers reduced cortical BDNF expression and associated neurobehavioral changes. BDNF signaling influences the survival, development, and synaptic function of cortical networks. Here, we compared gamma-aminobutyric acid (GABA)ergic network activity in the human primary motor cortex (M1) between the Met (Val/Met and Met/Met) and non-Met (Val/Val) genotype groups. Short- and long-interval intracortical inhibition, short-latency afferent inhibition (SAI), and long-latency afferent inhibition were measured using transcranial magnetic stimulation (TMS) as indices of GABAergic activity. Furthermore, the considerable inter-individual variability in inhibitory network activity typically measured by TMS may be affected not only by GABA but also by other pathways, including glutamatergic and cholinergic activities; therefore, we used 3-T magnetic resonance spectroscopy (MRS) to measure the dynamics of glutamate plus glutamine (Glx) and choline concentrations in the left M1, left somatosensory cortex, and right cerebellum. All inhibitory TMS conditions produced significantly smaller motor-evoked potentials than single-pulses. SAI was significantly stronger in the Met group than in the Val/Val group. Only the M1 Glx concentration was significantly lower in the Met group, while the BDNF genotype did not affect choline concentration in any region. Further, a positive correlation was observed between SAI and Glx concentrations only in M1. Our findings provide evidence that the BDNF genotype regulates both the inhibitory and excitatory circuits in human M1. In addition, lower Glx concentration in the M1 of Met carriers may alter specific inhibitory network on M1, thereby influencing the cortical signal processing required for neurobehavioral functions. Full article
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12 pages, 1888 KiB  
Article
Cortical Plasticity and Interneuron Recruitment in Adolescents Born to Women with Gestational Diabetes Mellitus
by Jago M. Van Dam, Mitchell R. Goldsworthy, William M. Hague, Suzette Coat and Julia B. Pitcher
Brain Sci. 2021, 11(3), 388; https://doi.org/10.3390/brainsci11030388 - 19 Mar 2021
Cited by 3 | Viewed by 1992
Abstract
Exposure to gestational diabetes mellitus (GDM) in utero is associated with a range of adverse cognitive and neurological outcomes. Previously, we reported altered neuroplastic responses to continuous theta burst stimulation (cTBS) in GDM-exposed adolescents. Recent research suggests that the relative excitability of complex [...] Read more.
Exposure to gestational diabetes mellitus (GDM) in utero is associated with a range of adverse cognitive and neurological outcomes. Previously, we reported altered neuroplastic responses to continuous theta burst stimulation (cTBS) in GDM-exposed adolescents. Recent research suggests that the relative excitability of complex oligosynaptic circuits (late I-wave circuits) can predict these responses. We aimed to determine if altered I-wave recruitment was associated with neuroplastic responses in adolescents born to women with GDM. A total of 20 GDM-exposed adolescents and 10 controls (aged 13.1 ± 1.0 years) participated. cTBS was used to induce neuroplasticity. I-wave recruitment was assessed by comparing motor-evoked potential latencies using different TMS coil directions. Recruitment of late I-waves was associated with stronger LTD-like neuroplastic responses to cTBS (p = < 0.001, R2 = 0.36). There were no differences between groups in mean neuroplasticity (p = 0.37), I-wave recruitment (p = 0.87), or the association between these variables (p = 0.41). The relationship between I-wave recruitment and the response to cTBS previously observed in adults is also present in adolescents and does not appear to be altered significantly by in utero GDM exposure. Exposure to GDM does not appear to significantly impair LTD-like synaptic plasticity or interneuron recruitment. Full article
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13 pages, 2969 KiB  
Article
Preconditioning Stimulus Intensity Alters Paired-Pulse TMS Evoked Potentials
by Vishal Rawji, Isabella Kaczmarczyk, Lorenzo Rocchi, Po-Yu Fong, John C. Rothwell and Nikhil Sharma
Brain Sci. 2021, 11(3), 326; https://doi.org/10.3390/brainsci11030326 - 04 Mar 2021
Cited by 14 | Viewed by 3624
Abstract
Motor cortex (M1) paired-pulse TMS (ppTMS) probes excitatory and inhibitory intracortical dynamics by measurement of motor-evoked potentials (MEPs). However, MEPs reflect cortical and spinal excitabilities and therefore cannot isolate cortical function. Concurrent TMS-EEG has the ability to measure cortical function, while limiting peripheral [...] Read more.
Motor cortex (M1) paired-pulse TMS (ppTMS) probes excitatory and inhibitory intracortical dynamics by measurement of motor-evoked potentials (MEPs). However, MEPs reflect cortical and spinal excitabilities and therefore cannot isolate cortical function. Concurrent TMS-EEG has the ability to measure cortical function, while limiting peripheral confounds; TMS stimulates M1, whilst EEG acts as the readout: the TMS-evoked potential (TEP). Whilst varying preconditioning stimulus intensity influences intracortical inhibition measured by MEPs, the effects on TEPs is undefined. TMS was delivered to the left M1 using single-pulse and three, ppTMS paradigms, each using a different preconditioning stimulus: 70%, 80% or 90% of resting motor threshold. Corticospinal inhibition was present in all three ppTMS conditions. ppTMS TEP peaks were reduced predominantly under the ppTMS 70 protocol but less so for ppTMS 80 and not at all for ppTMS 90. There was a significant negative correlation between MEPs and N45 TEP peak for ppTMS 70 reaching statistical trends for ppTMS 80 and 90. Whilst ppTMS MEPs show inhibition across a range of preconditioning stimulus intensities, ppTMS TEPs do not. TEPs after M1 ppTMS vary as a function of preconditioning stimulus intensity: smaller preconditioning stimulus intensities result in better discriminability between conditioned and unconditioned TEPs. We recommend that preconditioning stimulus intensity should be minimized when using ppTMS to probe intracortical inhibition. Full article
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14 pages, 2005 KiB  
Article
Modulation of Motor Cortex Plasticity by Repetitive Paired-Pulse TMS at Late I-Wave Intervals Is Influenced by Intracortical Excitability
by George M. Opie, Ryoki Sasaki, Brodie J. Hand and John G. Semmler
Brain Sci. 2021, 11(1), 121; https://doi.org/10.3390/brainsci11010121 - 18 Jan 2021
Cited by 8 | Viewed by 2519
Abstract
The late indirect (I)-waves recruited by transcranial magnetic stimulation (TMS) over primary motor cortex (M1) can be modulated using I-wave periodicity repetitive TMS (iTMS). The purpose of this study was to determine if the response to iTMS is influenced by different interstimulus intervals [...] Read more.
The late indirect (I)-waves recruited by transcranial magnetic stimulation (TMS) over primary motor cortex (M1) can be modulated using I-wave periodicity repetitive TMS (iTMS). The purpose of this study was to determine if the response to iTMS is influenced by different interstimulus intervals (ISIs) targeting late I-waves, and whether these responses were associated with individual variations in intracortical excitability. Seventeen young (27.2 ± 6.4 years, 12 females) healthy adults received iTMS at late I-wave intervals (4.0, 4.5, and 5.0 ms) in three separate sessions. Changes due to each intervention were examined with motor evoked potential (MEP) amplitudes and short-interval intracortical facilitation (SICF) using both posterior-anterior (PA) and anterior-posterior (AP) TMS current directions. Changes in MEP amplitude and SICF were influenced by iTMS ISI, with the greatest facilitation for ISIs at 4 and 5 ms with PA TMS, and 4 ms with AP TMS. Maximum SICF at baseline (irrespective of ISI) was associated with increased iTMS response, but only for PA stimulation. These results suggest that modifying iTMS parameters targeting late I-waves can influence M1 plasticity. They also suggest that maximum SICF may be a means by which responders to iTMS targeting the late I-waves could be identified. Full article
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15 pages, 904 KiB  
Article
TMS Correlates of Pyramidal Tract Signs and Clinical Motor Status in Patients with Cervical Spondylotic Myelopathy
by Giuseppe Lanza, Valentina Puglisi, Luisa Vinciguerra, Francesco Fisicaro, Carla Vagli, Mariagiovanna Cantone, Giovanni Pennisi, Manuela Pennisi and Rita Bella
Brain Sci. 2020, 10(11), 806; https://doi.org/10.3390/brainsci10110806 - 31 Oct 2020
Cited by 16 | Viewed by 1870
Abstract
Background: While the association between motor-evoked potential (MEP) abnormalities and motor deficit is well established, few studies have reported the correlation between MEPs and signs of pyramidal tract dysfunction without motor weakness. We assessed MEPs in patients with pyramidal signs, including motor deficits, [...] Read more.
Background: While the association between motor-evoked potential (MEP) abnormalities and motor deficit is well established, few studies have reported the correlation between MEPs and signs of pyramidal tract dysfunction without motor weakness. We assessed MEPs in patients with pyramidal signs, including motor deficits, compared to patients with pyramidal signs but without weakness. Methods: Forty-three patients with cervical spondylotic myelopathy (CSM) were dichotomized into 21 with pyramidal signs including motor deficit (Group 1) and 22 with pyramidal signs and normal strength (Group 2), and both groups were compared to 33 healthy controls (Group 0). MEPs were bilaterally recorded from the first dorsal interosseous and tibialis anterior muscle. The central motor conduction time (CMCT) was estimated as the difference between MEP latency and peripheral latency by magnetic stimulation. Peak-to-peak MEP amplitude and right-to-left differences were also measured. Results: Participants were age-, sex-, and height-matched. MEP latency in four limbs and CMCT in the lower limbs were prolonged, and MEP amplitude in the lower limbs decreased in Group 1 compared to the others. Unlike motor deficit, pyramidal signs were not associated with MEP measures, even when considering age, sex, and height as confounding factors. Conclusions: In CSM, isolated pyramidal signs may not be associated, at this stage, with MEP changes. Full article
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38 pages, 2039 KiB  
Article
Whole-Language and Item-Specific Inhibition in Bilingual Language Switching: The Role of Domain–General Inhibitory Control
by Judy D. Zhu and Paul F. Sowman
Brain Sci. 2020, 10(8), 517; https://doi.org/10.3390/brainsci10080517 - 05 Aug 2020
Cited by 6 | Viewed by 3557
Abstract
A prominent theory of bilingual speech production holds that appropriate language selection is achieved via inhibitory control. Such inhibition may operate on the whole-language and/or item-specific level. In this study, we examined these two levels of control in parallel, by introducing a novel [...] Read more.
A prominent theory of bilingual speech production holds that appropriate language selection is achieved via inhibitory control. Such inhibition may operate on the whole-language and/or item-specific level. In this study, we examined these two levels of control in parallel, by introducing a novel element into the traditional cued language switching paradigm: half of the stimuli were univalent (each required naming in the same language every time it appeared), and the other half were bivalent (each required naming in different languages on different trials). Contrasting switch and stay trials provided an index for whole-language inhibition, while contrasting bivalent and univalent stimuli provided an index for item-specific inhibition. We then investigated the involvement of domain-general brain mechanisms in these two levels of language control. Neuroimaging studies report activation of the pre-supplementary motor area (pre-SMA), a key region in the executive control brain network, during language switching tasks. However, it is unclear whether or not the pre-SMA plays a causal role in language control, and at which level it exerts control. Using repetitive transcranial magnetic stimulation (TMS) to transiently disrupt the pre-SMA, we observed an essential role of this brain region in general speech execution, while evidence for its specific involvement in each level of inhibition remains inconclusive. Full article
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16 pages, 2318 KiB  
Article
Influence of Voluntary Contraction Level, Test Stimulus Intensity and Normalization Procedures on the Evaluation of Short-Interval Intracortical Inhibition
by Cécilia Neige, Sidney Grosprêtre, Alain Martin and Florent Lebon
Brain Sci. 2020, 10(7), 433; https://doi.org/10.3390/brainsci10070433 - 08 Jul 2020
Cited by 7 | Viewed by 2668
Abstract
Short-interval intracortical inhibition (SICI) represents an inhibitory phenomenon acting at the cortical level. However, SICI estimation is based on the amplitude of a motor-evoked potential (MEP), which depends on the discharge of spinal motoneurones and the generation of compound muscle action potential (M-wave). [...] Read more.
Short-interval intracortical inhibition (SICI) represents an inhibitory phenomenon acting at the cortical level. However, SICI estimation is based on the amplitude of a motor-evoked potential (MEP), which depends on the discharge of spinal motoneurones and the generation of compound muscle action potential (M-wave). In this study, we underpin the importance of taking into account the proportion of spinal motoneurones that are activated or not when investigating the SICI of the right flexor carpi radialis (normalization with maximal M-wave (Mmax) and MEPtest, respectively), in 15 healthy subjects. We probed SICI changes according to various MEPtest amplitudes that were modulated actively (four levels of muscle contraction: rest, 10%, 20% and 30% of maximal voluntary contraction (MVC)) and passively (two intensities of test transcranial magnetic stimulation (TMS): 120 and 130% of motor thresholds). When normalized to MEPtest, SICI remained unchanged by stimulation intensity and only decreased at 30% of MVC when compared with rest. However, when normalized to Mmax, we provided the first evidence of a strong individual relationship between SICI and MEPtest, which was ultimately independent from experimental conditions (muscle states and TMS intensities). Under similar experimental conditions, it is thus possible to predict SICI individually from a specific level of corticospinal excitability in healthy subjects. Full article
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16 pages, 946 KiB  
Article
The Left Posterior Parietal Cortex Contributes to the Selection Process for the Initial Swing Leg in Gait Initiation
by Koichi Hiraoka, Shintaro Gonno and Ryota Inomoto
Brain Sci. 2020, 10(5), 317; https://doi.org/10.3390/brainsci10050317 - 22 May 2020
Cited by 2 | Viewed by 2309
Abstract
The present study examined whether the left posterior parietal cortex contributes to the selection process for the initial swing leg in gait initiation. Healthy humans initiated the gait in response to an auditory start cue. Transcranial magnetic stimulation (TMS) was given over P3, [...] Read more.
The present study examined whether the left posterior parietal cortex contributes to the selection process for the initial swing leg in gait initiation. Healthy humans initiated the gait in response to an auditory start cue. Transcranial magnetic stimulation (TMS) was given over P3, P4, F3 or F4 simultaneously, with the auditory start cue, in the on-TMS condition. A coil was placed over one of the four TMS sites, but TMS was not given in the off-TMS condition. The probability of right leg selection in the on-TMS condition was significantly lower than in the off-TMS condition when the coil was placed over P3, indicating that the left posterior parietal cortex contributes to the selection process of the initial swing leg of gait initiation. The latency of the anticipatory postural adjustment for gait initiation with the left leg was shortened by TMS over F4 or P4, but with the right leg was shortened by TMS over P3 or P4. Thus, the cortical process affecting the time taken to execute the motor process of gait initiation with the right leg may be related to the selection process of the initial swing leg of gait initiation. Full article
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19 pages, 3122 KiB  
Article
Site-Specific Effects of Online rTMS during a Working Memory Task in Healthy Older Adults
by Lysianne Beynel, Simon W. Davis, Courtney A. Crowell, Moritz Dannhauer, Wesley Lim, Hannah Palmer, Susan A. Hilbig, Alexandra Brito, Connor Hile, Bruce Luber, Sarah H. Lisanby, Angel V. Peterchev, Roberto Cabeza and Lawrence G. Appelbaum
Brain Sci. 2020, 10(5), 255; https://doi.org/10.3390/brainsci10050255 - 27 Apr 2020
Cited by 19 | Viewed by 3953
Abstract
The process of manipulating information within working memory is central to many cognitive functions, but also declines rapidly in old age. Improving this process could markedly enhance the health-span in older adults. The current pre-registered, randomized and placebo-controlled study tested the potential of [...] Read more.
The process of manipulating information within working memory is central to many cognitive functions, but also declines rapidly in old age. Improving this process could markedly enhance the health-span in older adults. The current pre-registered, randomized and placebo-controlled study tested the potential of online repetitive transcranial magnetic stimulation (rTMS) applied at 5 Hz over the left lateral parietal cortex to enhance working memory manipulation in healthy elderly adults. rTMS was applied, while participants performed a delayed-response alphabetization task with two individually titrated levels of difficulty. Coil placement and stimulation amplitude were calculated from fMRI activation maps combined with electric field modeling on an individual-subject basis in order to standardize dosing at the targeted cortical location. Contrary to the a priori hypothesis, active rTMS significantly decreased accuracy relative to sham, and only in the hardest difficulty level. When compared to the results from our previous study, in which rTMS was applied over the left prefrontal cortex, we found equivalent effect sizes but opposite directionality suggesting a site-specific effect of rTMS. These results demonstrate engagement of cortical working memory processing using a novel TMS targeting approach, while also providing prescriptions for future studies seeking to enhance memory through rTMS. Full article
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