Spinal plasticity with motor imagery practice

Abstract

Key points: While a consensus has now been reached on the effect of motor imagery (MI) - the mental simulation of an action - on motor cortical areas, less is known about its impact on spinal structures. The current study, using H-reflex conditioning paradigms, examined the effect of a 20 min MI practice on several spinal mechanisms of the plantar flexor muscles. We observed modulations of spinal presynaptic circuitry while imagining, which was even more pronounced following an acute session of MI practice. We suggested that the small cortical output generated during MI may reach specific spinal circuits and that repeating MI may increase the sensitivity of the spinal cord to its effects. The short-term plasticity induced by MI practice may include spinal network modulation in addition to cortical reorganization.

Abstract: Kinesthetic motor imagery (MI) is the mental simulation of a movement with its sensory consequences but without its concomitant execution. While the effect of MI practice on cortical areas is well known, its influence on spinal circuitry remains unclear. Here, we assessed plastic changes in spinal structures following an acute MI practice. Thirteen young healthy participants accomplished two experimental sessions: a 20 min MI training consisting of four blocks of 25 imagined maximal isometric plantar flexions, and a 20 min rest (control session). The level of spinal presynaptic inhibition was assessed by conditioning the triceps surae spinal H-reflex with two methods: (i) the stimulation of the common peroneal nerve that induced D1 presynaptic inhibition (H_PSI response), and (ii) the stimulation of the femoral nerve that induced heteronymous Ia facilitation (H_FAC response). We then compared the effects of MI on unconditioned (H_TEST ) and conditioned (H_PSI and H_FAC ) responses before, immediately after and 10 min after the 20 min session. After resting for 20 min, no changes were observed on the recorded parameters. After MI practice, the amplitude of rest H_TEST was unchanged, while H_PSI and H_FAC significantly increased, showing a reduction of presynaptic inhibition with no impact on the afferent-motoneuronal synapse. The current results revealed the acute effect of MI practice on baseline spinal presynaptic inhibition, increasing the sensitivity of the spinal circuitry to MI. These findings will help in understanding the mechanisms of neural plasticity following chronic practice.

Keywords: D1 presynaptic inhibition; H-reflex; heteronymous Ia facilitation; soleus; triceps surae.

Figure 1. Overview of the experimental protocol and illustrations of the inhibitory and facilitatory pathways of the soleus H‐reflex

A, the main experiment (experiment A) was designed to assess (i) the online effect of MI in comparison to rest and (ii) the acute effects of a single MI training session. The second experiment (experiment B) was designed as a control condition that aimed at recording the responses before (PRE) and immediately after (POST0) a rest period of similar duration with MI training session. H_FAC, H‐reflex conditioned by facilitatory pathway; H_PSI, H‐reflex conditioned by presynaptic inhibitory pathway; H_TEST, H‐reflex test; M_MAX, maximal M‐wave. B, depiction of the neural networks inducing D1 presynaptic inhibition. The soleus unconditioned H reflex, labelled TEST H‐Reflex (H_TEST), is elicited by electrical stimulation of the tibial nerve (TEST STIM). A prior conditioning stimulus (Condi stim) applied to the common peroneal nerve reduces the amplitude of the soleus H‐reflex (Conditioned reflex). The Ia afferent of the tibialis muscle connects to inhibitory interneurons that inhibit the Ia terminals of the soleus muscle. C, depiction of the neural networks inducing heteronymous Ia facilitation. A prior conditioning stimulus (Condi stim) applied to the femoral nerve increases the amplitude of the test H‐reflex. This facilitation is monosynaptic between the quadriceps Ia afferents (Ia quadri) and the motoneuronal pool of the soleus (MTN soleus). In B and C, graphs below illustrations depict plots of conditioned responses (as percentage unconditioned H_TEST) as a function of the inter‐stimulus intervals for one representative participant. Each point represents an average value of 5 trials. Positive intervals represent conditioned stimulation evoked before the TEST STIM and negative intervals the conditioned stimulation evoked after the TEST STIM.

Figure 2. Initial effect of motor imagery (MI) on test and conditioned responses

H‐reflexes of soleus (SOL) and gastrocnemius medialis (GM) are depicted at rest (open bars) and during MI (filled bars), normalized by the corresponding maximal M‐wave (M_MAX). A and B, the effect of MI on D1 presynaptic inhibition (H_PSI) in SOL and GM, respectively. C and D, the effect of MI on heteronymous Ia facilitation (H_FAC) in SOL and GM, respectively. E and F, the relationships between the increase of H_PSI and H_FAC during MI for SOL and GM, respectively. Increases of H_PSI and H_FAC amplitude induced by MI are expressed as a percentage of the responses at rest (% REST). ^*Significant difference at P < 0.05. G, EMG signals of soleus responses in one representative participant.

Figure 3. Effect of MI on test reflexes

Normalized test H‐reflexes (H_TEST/M_MAX) of soleus (A, SOL) and gastrocnemius medialis (B, GM) were recorded at rest (open bars) and during MI (filled bars) before (PRE), immediately after (POST0) and 10 min after (POST10) the training session. ^*Significant difference between MI and rest H_TEST/M_MAX (P < 0.05).

Figure 4. H‐reflexes test (H_TEST), conditioned with presynaptic inhibition (H_PSI) and with heteronymous Ia facilitation (H_FAC) before and after the MI training session

Responses of soleus (SOL) and gastrocnemius medialis (GM) are depicted in A and B, respectively, before (PRE), immediately after (POST0) and 10 min after (POST 10) MI session. TEST responses depict unconditioned reflexes (open bars), while H_PSI depicts H‐reflexes conditioned by prior common peroneal nerve (presynaptic inhibition conditioning) and H_FAC represents H‐reflexes conditioned by prior femoral nerve stimulation (Heteronymous Ia facilitation) (filled bars for each conditioned responses). Each response (TEST, H_PSI and H_FAC) is normalized by the corresponding maximal M‐wave (M_MAX). ^*, ^** and ^***: significant difference with the corresponding TEST response at the same time point (conditioning effect: H_TEST vs. H_PSI or H_FAC), at P < 0.05, P < 0.01 and P < 0.001, respectively. ^§ and ^§§: significant difference with the corresponding H response at PRE (time effect: PRE vs. POST0 or POST 10) at P < 0.05 and P < 0.01, respectively.

Figure 5. Test (H_TEST) and conditioned reflexes with presynaptic inhibition (H_PSI) before and after the control condition

Normalized H_TEST (open bars) and H_PSI (filled bars) of soleus (A) and gastrocnemius medialis (B) before and after the rest period of 20 min. ^*Significant difference (P < 0.05) between H_TEST and H_PSI.

Figure 6

Potential neural mechanisms involved in spinal excitability modulation following MI practice