Nicolas Gueugneau

Motor cortical plasticity induced by motor learning through mental practice.

Several investigations suggest that actual and mental actions trigger similar neural substrates. Motor learning via physical practice results in long-term potentiation (LTP)-like plasticity processes, namely potentiation of M1 and a temporary occlusion of additional LTP-like plasticity. However, whether this neuroplasticity process contributes to improve motor performance through mental practice remains to be determined. Here, we tested skill learning-dependent changes in primary motor cortex (M1) excitability and plasticity by means of transcranial magnetic stimulation (TMS) in subjects trained to physically execute or mentally perform a sequence of finger opposition movements. Before and after physical practice and motor-imagery practice, M1 excitability was evaluated by measuring the input-output (IO) curve of motor evoked potentials. M1 LTP and long-term depression (LTD)-like plasticity was assessed with paired-associative stimulation (PAS) of the median nerve and motor cortex using an interstimulus interval of 25 ms (PAS25) or 10 ms (PAS10), respectively. We found that even if after both practice sessions subjects significantly improved their movement speed, M1 excitability and plasticity were differentially influenced by the two practice sessions. First, we observed an increase in the slope of IO curve after physical but not after MI practice. Second, there was a reversal of the PAS25 effect from LTP-like plasticity to LTD-like plasticity following physical and MI practice. Third, LTD-like plasticity (PAS10 protocol) increased after physical practice, whilst it was occluded after MI practice. In conclusion, we demonstrated that MI practice lead to the development of neuroplasticity, as it affected the PAS25- and PAS10- induced plasticity in M1. These results, expanding the current knowledge on how MI training shapes M1 plasticity, might have a potential impact in rehabilitation.

Interhemispheric inhibition during mental actions of different complexity.

Several investigations suggest that actual and mental actions trigger similar neural substrates. Yet, neurophysiological evidences on the nature of interhemispheric interactions during mental movements are still meagre. Here, we asked whether the content of mental images, investigated by task complexity, is finely represented in the inhibitory interactions between the two primary motor cortices (M1s). Subjects’ left M1 was stimulated by means of transcranial magnetic stimulation (TMS) while they were performing actual or mental movements of increasing complexity with their right hand and exerting a maximum isometric force with their left thumb and index. Thus, we simultaneously assessed the corticospinal excitability in the right opponent pollicis muscle (OP) and the ipsilateral silent period (iSP) in the left OP during actual and mental movements. Corticospinal excitability in right OP increased during actual and mental movements, but task complexity-dependent changes were only observed during actual movements. Interhemispheric motor inhibition in the left OP was similarly modulated by task complexity in both mental and actual movements. Precisely, the duration and the area of the iSP increased with task complexity in both movement conditions. Our findings suggest that mental and actual movements share similar inhibitory neural circuits between the two homologous primary motor cortex areas.

Dominant vs. nondominant arm advantage in mentally simulated actions in right handers

Although plentiful data are available regarding mental states involving the dominant-right arm, the evidence for the nondominant-left arm is sparse. Here, we investigated whether right-handers can generate accurate predictions with either the right or the left arm. Fifteen adults carried out actual and mental arm movements in two directions with varying inertial resistance (inertial anisotropy phenomenon). We recorded actual and mental movement times and used the degree of their similarity as an indicator for the accuracy of motor imagery/prediction process. We found timing correspondences (isochrony) between actual and mental right arm movements in both rightward (low inertia resistance) and leftward (high inertia resistance) directions. Timing similarities between actual and mental left arm movements existed for the leftward direction (low inertia resistance) but not for the rightward direction (high inertia resistance). We found similar results when participants reaching towards the midline of the workspace, a result that excludes a hemispace effect. Electromyographic analysis during mental movements showed that arm muscles remained inactivate, thus eliminating a muscle activation strategy that could explain intermanual differences. Furthermore, motor-evoked potentials enhancement in both right and left biceps brachii during mental actions indicated that subjects were actively engaged in mental movement simulation and that the disadvantage of the left arm cannot be attributed to the nonactivation of the right motor cortex. Our findings suggest that predictive mechanisms are more robust for the right than the left arm in right-handers. We discussed these findings from the perspective of the internal models theory and the dynamic-dominance hypothesis of laterality.

Daily update of motor predictions by physical activity

Motor prediction, i.e., the ability to predict the sensory consequences of motor commands, is critical for adapted motor behavior. Like speed or force, the accuracy of motor prediction varies in a 24-hour basis. Although the prevailing view is that basic biological markers regulate this circadian modulation, behavioral factors such as physical activity, itself modulated by the alternation of night and day, can also regulate motor prediction. Here, we propose that physical activity updates motor prediction on a daily basis. We tested our hypothesis by up- and down-regulating physical activity via arm-immobilization and high-intensity training, respectively. Motor prediction was assessed by measuring the timing differences between actual and mental arm movements. Results show that although mental movement time was modulated during the day when the arm was unconstrained, it remained constant when the arm was immobilized. Additionally, increase of physical activity, via release from immobilization or intense bout of training, significantly reduced mental movement time. Finally, mental and actual times were similar in the afternoon in the unconstrained condition, indicating that predicted and actual movements match after sufficient amount of physical activity. Our study supports the view that physical activity calibrates motor predictions on a daily basis.

High-frequency neuromuscular electrical stimulation modulates interhemispheric inhibition in healthy Humans.

High-frequency neuromuscular electrical stimulation (HF NMES) induces muscular contractions through neural mechanisms that partially match physiological motor control. Indeed, a portion of the contraction arises from central mechanisms, whereby spinal motoneurons are recruited through the evoked sensory volley. However, the involvement of supraspinal centers of motor control during such stimulation remains poorly understood. Therefore, we tested whether a single HF NMES session applied to the upper limb influences interhemispheric inhibition (IHI) from left to right motor cortex (M1). Using noninvasive electrophysiology and transcranial magnetic stimulation, we evaluated the effects of a 10-min HF NMES session applied to a right wrist flexor on spinal and corticospinal excitability of both arms, as well as IHI, in healthy subjects. HF NMES induced a rapid decline in spinal excitability on the right stimulated side that closely matched the modulation of evoked force during the protocol. More importantly, IHI was significantly increased by HF NMES, and this increase was correlated to the electromyographic activity within the contralateral homologous muscle. Our study highlights a new neurophysiological mechanism, suggesting that HF NMES has an effect on the excitability of the transcallosal pathway probably to regulate the lateralization of the motor output. The data suggest that HF NMES can modify the hemispheric balance between both M1 areas. These findings provide important novel perspectives for the implementation of HF NMES in sport training and neurorehabilitation. NEW & NOTEWORTHY High-frequency neuromuscular electrical stimulation (HF NMES) induces muscular contractions that partially match physiological motor control. Here, we tested whether HF NMES applied to the upper limb influences interhemispheric inhibition. Our results show that interhemispheric inhibition was increased after HF NMES and that this increase was correlated to the electromyographic activity within the contralateral homologous muscle. This opens up original perspectives for the implementation of HF NMES in sport training and neurorehabilitation.

Presynaptic inhibition mechanisms may subserve the spinal excitability modulation induced by neuromuscular electrical stimulation

This study aimed at deciphering the origins of spinal excitability modulation that follows neuromuscular electrical stimulation (NMES). Ten participants (age: 24.6 ± 4.2 years) performed 2 randomized NMES sessions on plantar flexors with frequencies of stimulations of 20 or 100 Hz (pulse width: 1 ms) at 20% of maximal voluntary contraction (MVC). Before and after each session, the posterior tibial nerve was stimulated to record H-reflex of soleus (SOL), gastrocnemius medialis (GM) and gastrocnemius lateralis (GL). D1 presynaptic inhibition was assessed by conditioning H reflex with prior common peroneal nerve stimulation. Resting H-reflex of SOL decreased after both protocols, but in a greater extent following the 100 Hz session (100 Hz: -34.6 ± 7.3%, 20 Hz: -17.1 ± 3.8%; P = 0.002), accompanied by an increase of presynaptic inhibition (+22 ± 5.8% at 100 Hz vs. +8 ± 3.7% at 20 Hz, P < 0.001). GM and GL spinal excitability and presynaptic inhibition were also altered after NMES, but in a similarly extent after 20 Hz and 100 Hz protocols. Neuromuscular fatigue following a single session of NMES involves spinal presynaptic circuitry, even at low stimulation frequency. The spinal sensitivity to NMES seems also muscle dependent.