Unravelling the modulation of intracortical inhibition during motor imagery: An adaptive threshold-hunting study

AbstractMotor imagery (MI) is the mental simulation of an action without any apparent muscular contraction. By means of transcranial magnetic stimulation, few studies revealed a decrease of short-interval intracortical inhibition (SICI) within the primary motor cortex. However, this decrease is ambiguous, as one would expect greater inhibition during MI to prevent overt motor output. The current study investigated the extent of SICI modulation during MI through a methodological and a conceptual reconsideration of i) the importance of parameters to assess SICI (Exp.1) and ii) the inhibitory process within the primary motor cortex as an inherent feature of MI (Exp.2). Participants performed two tasks: 1) rest and 2) imagery of isometric abduction of the right index finger. Using transcranial magnetic stimulation, motor evoked potentials were elicited in the right first dorsal interosseous muscle. An adaptive threshold-hunting paradigm was used, where the stimulus intensity required to maintain a fixed motor evoked potential amplitude was quantified. To test SICI, we conditioned the test stimulus with a conditioning stimulus (CS) of different intensities. Results revealed an Intensity by Task interaction showing that SICI decreased during MI as compared to rest only for the higher CS intensity (Exp.1). At the lowest CS intensities, a Task main effect revealed that SICI increased during MI (Exp.2). SICI modulation during MI depends critically on the CS intensity. By optimising CS intensity, we have shown that SICI circuits may increase during MI, revealing a potential mechanism to prevent the production of a movement while the motor system is activated.HighlightsExcitatory and inhibitory neural processes interact during motor imagery, as the motor regions are activated but no movement is produced.The current study investigated the extent of short interval intracortical inhibition modulation (SICI) during motor imagery.When using optimal settings, SICI increased during motor imagery, likely to prevent the production of an overt movement.

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Short-interval intracortical inhibition in human primary motor cortex: A multi-locus transcranial magnetic stimulation study

NeuroImage ◽

10.1016/j.neuroimage.2019.116194 ◽

2019 ◽

Vol 203 ◽

pp. 116194 ◽

Cited By ~ 2

Author(s):

Jaakko O. Nieminen ◽

Lari M. Koponen ◽

Niko Mäkelä ◽

Victor Hugo Souza ◽

Matti Stenroos ◽

...

Keyword(s):

Transcranial Magnetic Stimulation ◽

Motor Cortex ◽

Magnetic Stimulation ◽

Primary Motor Cortex ◽

Short Interval ◽

Intracortical Inhibition

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Interhemispheric interactions between the right angular gyrus and the left motor cortex: a transcranial magnetic stimulation study

Journal of Neurophysiology ◽

10.1152/jn.00642.2020 ◽

2021 ◽

Author(s):

Julianne Baarbé ◽

Michael Vesia ◽

Matt Brown ◽

Karlo J. Lizarraga ◽

Carolyn A Gunraj ◽

...

Keyword(s):

Transcranial Magnetic Stimulation ◽

Motor Cortex ◽

Magnetic Stimulation ◽

Posterior Parietal Cortex ◽

Short Interval ◽

Intracortical Inhibition ◽

Angular Gyrus ◽

Posterior Parietal ◽

The Right ◽

Left Angular Gyrus

The interconnection of the angular gyrus of right posterior parietal cortex (PPC) and the left motor cortex (LM1) is essential for goal-directed hand movements. Previous work with transcranial magnetic stimulation (TMS) showed that right PPC stimulation increases LM1 excitability but right PPC followed by left PPC-LM1 stimulation (LPPC-LM1) inhibits LM1 corticospinal output compared to LPPC-LM1 alone. It is not clear if right PPC-mediated inhibition of LPPC-LM1 is due to inhibition of left PPC or to combined effects of right and left PPC stimulation on LM1 excitability. We used paired-pulse TMS to study the extent to which combined right and left PPC stimulation, targeting the angular gyri, influences LM1 excitability. We tested 16 healthy subjects in five paired-pulsed TMS experiments using MRI-guided neuronavigation to target the angular gyri within PPC. We tested the effects of different right angular gyrus (RAG) and LM1 stimulation intensities on the influence of RAG on LM1 and on influence of left angular gyrus (LAG) on LM1 (LAG-LM1). We then tested the effects of RAG and LAG stimulation on LM1 short-interval intracortical facilitation(SICF), short-interval intracortical inhibition(SICI) and long-interval intracortical inhibition(LICI). The results revealed that RAG facilitated LM1, inhibited SICF and inhibited LAG-LM1. Combined RAG-LAG stimulation did not affect SICI but increased LICI. These experiments suggest that RAG-mediated inhibition of LAG-LM1 is related to inhibition of early I-wave activity and enhancement of GABAB receptor-mediated inhibition in LM1. The influence of RAG on LM1 likely involves ipsilateral connections from LAG to LM1 and heterotopic connections from RAG to LM1.

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Task-related changes in intracortical inhibition assessed with paired- and triple-pulse transcranial magnetic stimulation

Journal of Neurophysiology ◽

10.1152/jn.00651.2014 ◽

2015 ◽

Vol 113 (5) ◽

pp. 1470-1479 ◽

Cited By ~ 12

Author(s):

George M. Opie ◽

Michael C. Ridding ◽

John G. Semmler

Keyword(s):

Transcranial Magnetic Stimulation ◽

Motor Cortex ◽

Magnetic Stimulation ◽

Muscle Activation ◽

Primary Motor Cortex ◽

Index Finger ◽

Precision Grip ◽

Intracortical Inhibition ◽

Presynaptic Mechanisms ◽

First Dorsal Interosseous Muscle

Recent research has demonstrated a task-related modulation of postsynaptic intracortical inhibition within primary motor cortex for tasks requiring isolated (abduction) or synergistic (precision grip) muscle activation. The current study sought to investigate task-related changes in pre- and postsynaptic intracortical inhibition in motor cortex. In 13 young adults (22.5 ± 3.5 yr), paired-pulse transcranial magnetic stimulation (TMS) was used to measure short (SICI)- and long-interval intracortical inhibition (LICI) (i.e., postsynaptic motor cortex inhibition) in first dorsal interosseous muscle, and triple-pulse TMS was used to investigate changes in SICI-LICI interactions (i.e., presynaptic motor cortex inhibition). These measurements were obtained at rest and during muscle activation involving isolated abduction of the index finger and during a precision grip using the index finger and thumb. SICI was reduced during abduction and precision grip compared with rest, with greater reductions during precision grip. The modulation of LICI during muscle activation depended on the interstimulus interval (ISI; 100 and 150 ms) but was not different between abduction and precision grip. For triple-pulse TMS, SICI was reduced in the presence of LICI at both ISIs in resting muscle (reflecting presynaptic motor cortex inhibition) but was only modulated at the 150-ms ISI during index finger abduction. Results suggest that synergistic contractions are accompanied by greater reductions in postsynaptic motor cortex inhibition than isolated contractions, but the contribution of presynaptic mechanisms to this disinhibition is limited. Furthermore, timing-dependent variations in LICI provide additional evidence that measurements using different ISIs may not represent activation of the same cortical process.

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Event-related desynchronization reflects downregulation of intracortical inhibition in human primary motor cortex

Journal of Neurophysiology ◽

10.1152/jn.01092.2012 ◽

2013 ◽

Vol 110 (5) ◽

pp. 1158-1166 ◽

Cited By ~ 108

Author(s):

Mitsuaki Takemi ◽

Yoshihisa Masakado ◽

Meigen Liu ◽

Junichi Ushiba

Keyword(s):

Motor Cortex ◽

Motor Imagery ◽

Sensorimotor Cortex ◽

Primary Motor Cortex ◽

Motor Evoked Potentials ◽

Short Interval ◽

Hand Movement ◽

Intracortical Inhibition ◽

Imagery Task ◽

Event Related Desynchronization

There is increasing interest in electroencephalogram (EEG)-based brain-computer interface (BCI) as a tool for rehabilitation of upper limb motor functions in hemiplegic stroke patients. This type of BCI often exploits mu and beta oscillations in EEG recorded over the sensorimotor areas, and their event-related desynchronization (ERD) following motor imagery is believed to represent increased sensorimotor cortex excitability. However, it remains unclear whether the sensorimotor cortex excitability is actually correlated with ERD. Thus we assessed the association of ERD with primary motor cortex (M1) excitability during motor imagery of right wrist movement. M1 excitability was tested by motor evoked potentials (MEPs), short-interval intracortical inhibition (SICI), and intracortical facilitation (ICF) with transcranial magnetic stimulation (TMS). Twenty healthy participants were recruited. The participants performed 7 s of rest followed by 5 s of motor imagery and received online visual feedback of the ERD magnitude of the contralateral hand M1 while performing the motor imagery task. TMS was applied to the right hand M1 when ERD exceeded predetermined thresholds during motor imagery. MEP amplitudes, SICI, and ICF were recorded from the agonist muscle of the imagined hand movement. Results showed that the large ERD during wrist motor imagery was associated with significantly increased MEP amplitudes and reduced SICI but no significant changes in ICF. Thus ERD magnitude during wrist motor imagery represents M1 excitability. This study provides electrophysiological evidence that a motor imagery task involving ERD may induce changes in corticospinal excitability similar to changes accompanying actual movements.

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Late Cortical Disinhibition in Human Motor Cortex: A Triple-Pulse Transcranial Magnetic Stimulation Study

Journal of Neurophysiology ◽

10.1152/jn.00782.2009 ◽

2010 ◽

Vol 103 (1) ◽

pp. 511-518 ◽

Cited By ~ 60

Author(s):

R. F. H. Cash ◽

U. Ziemann ◽

K. Murray ◽

G. W. Thickbroom

Keyword(s):

Transcranial Magnetic Stimulation ◽

Motor Cortex ◽

Magnetic Stimulation ◽

Short Interval ◽

Motor Evoked Potential ◽

Silent Period ◽

Intracortical Inhibition ◽

Human Motor Cortex ◽

Acid Type ◽

Human Motor

In human motor cortex transcranial magnetic stimulation (TMS) has been used to identify short-interval intracortical inhibition (SICI) corresponding to γ-aminobutyric acid type A (GABAA) effects and long-interval intracortical inhibition (LICI) and the cortical silent period (SP) corresponding to postsynaptic GABAB effects. Presynaptic GABAB effects, corresponding to disinhibition, can also be identified with TMS and have been shown to be acting during LICI by measuring SICI after a suprathreshold priming stimulus (PS). The duration of disinhibition is not certain and, guided by studies in experimental preparations, we hypothesized that it may be longer-lasting than postsynaptic inhibition, leading to a period of late cortical disinhibition and consequently a net increase in corticospinal excitability. We tested this first by measuring the motor-evoked potential (MEP) to a test stimulus (TS), delivered after a PS at interpulse intervals (IPIs) ≤300 ms that encompassed the period of PS-induced LICI and its aftermath. MEP amplitude was initially decreased, but then increased at IPIs of 190–210 ms, reaching 160 ± 17% of baseline 200 ms after PS ( P < 0.05). SP duration was 181 ± 5 ms. A second experiment established that the onset of the later period of increased excitability correlated with PS intensity ( r2 = 0.99) and with the duration of the SP ( r2 = 0.99). The third and main experiment demonstrated that SICI was significantly reduced in strength at all IPIs ≤220 ms after PS. We conclude that TMS-induced LICI is associated with a period of disinhibition that is at first masked by LICI, but that outlasts LICI and gives rise to a period during which disinhibition predominates and net excitability is raised. Identification of this late period of disinhibition in human motor cortex may provide an opportunity to explore or modulate the behavior of excitatory networks at a time when inhibitory effects are restrained.

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Differences between motor execution and motor imagery of grasping movements in the motor cortical excitatory circuit

PeerJ ◽

10.7717/peerj.5588 ◽

2018 ◽

Vol 6 ◽

pp. e5588 ◽

Cited By ~ 2

Author(s):

Hai-Jiang Meng ◽

Yan-Ling Pi ◽

Ke Liu ◽

Na Cao ◽

Yan-Qiu Wang ◽

...

Keyword(s):

Motor Cortex ◽

Motor Imagery ◽

Primary Motor Cortex ◽

Cortical Excitability ◽

Short Interval ◽

Corticospinal Excitability ◽

Motor Execution ◽

Human Motor Cortex ◽

Motor Cortical ◽

The Right

Background Both motor imagery (MI) and motor execution (ME) can facilitate motor cortical excitability. Although cortical excitability is modulated by intracortical inhibitory and excitatory circuits in the human primary motor cortex, it is not clear which intracortical circuits determine the differences in corticospinal excitability between ME and MI. Methods We recruited 10 young healthy subjects aged 18−28 years (mean age: 22.1 ± 3.14 years; five women and five men) for this study. The experiment consisted of two sets of tasks involving grasp actions of the right hand: imagining and executing them. Corticospinal excitability and short-interval intracortical inhibition (SICI) were measured before the interventional protocol using transcranial magnetic stimulation (baseline), as well as at 0, 20, and 40 min (T0, T20, and T40) thereafter. Results Facilitation of corticospinal excitability was significantly greater after ME than after MI in the right abductor pollicis brevis (APB) at T0 and T20 (p < 0.01 for T0, and p < 0.05 for T20), but not in the first dorsal interosseous (FDI) muscle. On the other hand, no significant differences in SICI between ME and MI were found in the APB and FDI muscles. The facilitation of corticospinal excitability at T20 after MI correlated with the Movement Imagery Questionnaire (MIQ) scores for kinesthetic items (Rho = −0.646, p = 0.044) but did not correlate with the MIQ scores for visual items (Rho = −0.265, p = 0.458). Discussion The present results revealed significant differences between ME and MI on intracortical excitatory circuits of the human motor cortex, suggesting that cortical excitability differences between ME and MI may be attributed to the activation differences of the excitatory circuits in the primary motor cortex.

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Differential Influence of the Dorsal Premotor and Primary Somatosensory Cortex on Corticospinal Excitability during Kinesthetic and Visual Motor Imagery: A Low-Frequency Repetitive Transcranial Magnetic Stimulation Study

Brain Sciences ◽

10.3390/brainsci11091196 ◽

2021 ◽

Vol 11 (9) ◽

pp. 1196

Author(s):

Viola Oldrati ◽

Alessandra Finisguerra ◽

Alessio Avenanti ◽

Salvatore Maria Aglioti ◽

Cosimo Urgesi

Keyword(s):

Transcranial Magnetic Stimulation ◽

Somatosensory Cortex ◽

Motor Imagery ◽

Magnetic Stimulation ◽

Primary Motor Cortex ◽

Repetitive Transcranial Magnetic Stimulation ◽

Premotor Cortex ◽

Mental Simulation ◽

Primary Somatosensory Cortex ◽

Visual Motor

Consistent evidence suggests that motor imagery involves the activation of several sensorimotor areas also involved during action execution, including the dorsal premotor cortex (dPMC) and the primary somatosensory cortex (S1). However, it is still unclear whether their involvement is specific for either kinesthetic or visual imagery or whether they contribute to motor activation for both modalities. Although sensorial experience during motor imagery is often multimodal, identifying the modality exerting greater facilitation of the motor system may allow optimizing the functional outcomes of rehabilitation interventions. In a sample of healthy adults, we combined 1 Hz repetitive transcranial magnetic stimulation (rTMS) to suppress neural activity of the dPMC, S1, and primary motor cortex (M1) with single-pulse TMS over M1 for measuring cortico-spinal excitability (CSE) during kinesthetic and visual motor imagery of finger movements as compared to static imagery conditions. We found that rTMS over both dPMC and S1, but not over M1, modulates the muscle-specific facilitation of CSE during kinesthetic but not during visual motor imagery. Furthermore, dPMC rTMS suppressed the facilitation of CSE, whereas S1 rTMS boosted it. The results highlight the differential pattern of cortico-cortical connectivity within the sensorimotor system during the mental simulation of the kinesthetic and visual consequences of actions.

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Modulation of motor cortex inhibition during motor imagery

Journal of Neurophysiology ◽

10.1152/jn.00549.2016 ◽

2017 ◽

Vol 117 (4) ◽

pp. 1776-1784 ◽

Cited By ~ 12

Author(s):

Benjamin W. X. Chong ◽

Cathy M. Stinear

Keyword(s):

Motor Cortex ◽

Motor Imagery ◽

Primary Motor Cortex ◽

Muscle Relaxation ◽

Short Interval ◽

Motor Evoked Potential ◽

Intracortical Inhibition ◽

Abductor Pollicis Brevis ◽

Voluntary Muscle ◽

Abductor Digiti Minimi

Motor imagery (MI) is similar to overt movement, engaging common neural substrates and facilitating the corticomotor pathway; however, it does not result in excitatory descending motor output. Transcranial magnetic stimulation (TMS) can be used to assess inhibitory networks in the primary motor cortex via measures of 1-ms short-interval intracortical inhibition (SICI), long-interval intracortical inhibition (LICI), and late cortical disinhibition (LCD). These measures are thought to reflect extrasynaptic GABAA tonic inhibition, postsynaptic GABAB inhibition, and presynaptic GABAB disinhibition, respectively. The behavior of 1-ms SICI, LICI, and LCD during MI has not yet been explored. This study aimed to investigate how 1-ms SICI, LICI, and LCD are modulated during MI and voluntary relaxation (VR) of a target muscle. Twenty-five healthy young adults participated. TMS was used to assess nonconditioned motor evoked potential (MEP) amplitude, 1-ms SICI, 100- (LICI100) and 150-ms LICI, and LCD in the right abductor pollicis brevis (APB) and right abductor digiti minimi during rest, MI, and VR of the hand. Compared with rest, MEP amplitudes were facilitated in APB during MI. SICI was not affected by task or muscle. LICI100 decreased in both muscles during VR but not MI, whereas LCD was recruited in both muscles during both tasks. This indicates that VR modulates postsynaptic GABAB inhibition, whereas both tasks modulate presynaptic GABAB inhibition in a non-muscle-specific way. This study highlights further neurophysiological parallels between actual and imagined movement, which may extend to voluntary relaxation. NEW & NOTEWORTHY This is the first study to investigate how 1-ms short-interval intracortical inhibition, long-interval intracortical inhibition, and late cortical disinhibition are modulated during motor imagery and voluntary muscle relaxation. We present novel findings of decreased 100-ms long-interval intracortical inhibition during voluntary muscle relaxation and increased late cortical disinhibition during both motor imagery and voluntary muscle relaxation.

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Modulation of Effects of Intermittent Theta Burst Stimulation Applied Over Primary Motor Cortex (M1) by Conditioning Stimulation of the Opposite M1

Journal of Neurophysiology ◽

10.1152/jn.00274.2009 ◽

2009 ◽

Vol 102 (2) ◽

pp. 766-773 ◽

Cited By ~ 24

Author(s):

Patrick Ragert ◽

Mickael Camus ◽

Yves Vandermeeren ◽

Michael A. Dimyan ◽

Leonardo G. Cohen

Keyword(s):

Transcranial Magnetic Stimulation ◽

Motor Cortex ◽

Magnetic Stimulation ◽

Primary Motor Cortex ◽

Corticospinal Excitability ◽

Homeostatic Plasticity ◽

Theta Burst Stimulation ◽

Burst Stimulation ◽

The Right ◽

Theta Burst

The excitability of the human primary motor cortex (M1) as tested with transcranial magnetic stimulation (TMS) depends on its previous history of neural activity. Homeostatic plasticity might be one important physiological mechanism for the regulation of corticospinal excitability and synaptic plasticity. Although homeostatic plasticity has been demonstrated locally within M1, it is not known whether priming M1 could result in similar homeostatic effects in the homologous M1 of the opposite hemisphere. Here, we sought to determine whether down-regulating excitability (priming) in the right (R) M1 with 1-Hz repetitive transcranial magnetic stimulation (rTMS) changes the excitability-enhancing effect of intermittent theta burst stimulation (iTBS) applied over the homologous left (L) M1. Subjects were randomly allocated to one of four experimental groups in a sham-controlled parallel design with real or sham R M1 1-Hz TMS stimulation always preceding L M1 iTBS or sham by about 10 min. The primary outcome measure was corticospinal excitability in the L M1, as measured by recruitment curves (RCs). Secondary outcome measures included pinch force, simple reaction time, and tapping speed assessed in the right hand. The main finding of this study was that preconditioning R M1 with 1-Hz rTMS significantly decreased the excitability-enhancing effects of subsequent L M1 iTBS on RCs. Application of 1-Hz rTMS over R M1 alone and iTBS over L M1 alone resulted in increased RC in L M1 relative to sham interventions. The present findings are consistent with the hypothesis that homeostatic mechanisms operating across hemispheric boundaries contribute to regulate motor cortical function in the primary motor cortex.

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Magnifying the View of the Hand Changes Its Cortical Representation. A Transcranial Magnetic Stimulation Study

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01266 ◽

2018 ◽

Vol 30 (8) ◽

pp. 1098-1107 ◽

Cited By ~ 1

Author(s):

Elisabetta Ambron ◽

Nicole White ◽

Olufunsho Faseyitan ◽

Sudha K. Kessler ◽

Jared Medina ◽

...

Keyword(s):

Transcranial Magnetic Stimulation ◽

Motor Cortex ◽

Magnetic Stimulation ◽

Motor Evoked Potentials ◽

Hot Spot ◽

Short Interval ◽

Body Part ◽

Intracortical Inhibition ◽

Cortical Representation ◽

Motor Cortex Excitability

Changes in the perceived size of a body part using magnifying lenses influence tactile perception and pain. We investigated whether the visual magnification of one's hand also influences the motor system, as indexed by transcranial magnetic stimulation (TMS)-induced motor evoked potentials (MEPs). In Experiment 1, MEPs were measured while participants gazed at their hand with and without magnification of the hand. MEPs were significantly larger when participants gazed at a magnified image of their hand. In Experiment 2, we demonstrated that this effect is specific to the hand that is visually magnified. TMS of the left motor cortex did not induce an increase of MEPs when participants looked at their magnified left hand. Experiment 3 was performed to determine if magnification altered the topography of the cortical representation of the hand. To that end, a 3 × 5 grid centered on the cortical hot spot (cortical location at which a motor threshold is obtained with the lowest level of stimulation) was overlaid on the participant's MRI image, and all 15 sites in the grid were stimulated with and without magnification of the hand. We confirmed the increase in the MEPs at the hot spot with magnification and demonstrated that MEPs significantly increased with magnification at sites up to 16.5 mm from the cortical hot spot. In Experiment 4, we used paired-pulse TMS to measure short-interval intracortical inhibition and intracortical facilitation. Magnification was associated with an increase in short-interval intracortical inhibition. These experiments demonstrate that the visual magnification of one's hand induces changes in motor cortex excitability and generates a rapid remapping of the cortical representation of the hand that may, at least in part, be mediated by changes in short-interval intracortical inhibition.

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