Changes in the Spinal Neural Circuits are Dependent on the Movement Speed of the Visuomotor Task

Abstract

Previous studies have shown that spinal neural circuits are modulated by motor skill training. However, the effects of task movement speed on changes in spinal neural circuits have not been clarified. The aim of this research was to investigate whether spinal neural circuits were affected by task movement speed. Thirty-eight healthy subjects participated in this study. In experiment 1, the effects of task movement speed on the spinal neural circuits were examined. Eighteen subjects performed a visuomotor task involving ankle muscle slow (nine subjects) or fast (nine subjects) movement speed. Another nine subjects performed a non-visuomotor task (controls) in fast movement speed. The motor task training lasted for 20 min. The amounts of D1 inhibition and reciprocal Ia inhibition were measured using H-relfex condition-test paradigm and recorded before, and at 5, 15, and 30 min after the training session. In experiment 2, using transcranial magnetic stimulation (TMS), the effects of corticospinal descending inputs on the presynaptic inhibitory pathway were examined before and after performing either a visuomotor (eight subjects) or a control task (eight subjects). All measurements were taken under resting conditions. The amount of D1 inhibition increased after the visuomotor task irrespective of movement speed (P < 0.01). The amount of reciprocal Ia inhibition increased with fast movement speed conditioning (P < 0.01), but was unchanged by slow movement speed conditioning. These changes lasted up to 15 min in D1 inhibition and 5 min in reciprocal Ia inhibition after the training session. The control task did not induce changes in D1 inhibition and reciprocal Ia inhibition. The TMS conditioned inhibitory effects of presynaptic inhibitory pathways decreased following visuomotor tasks (P < 0.01). The size of test H-reflex was almost the same size throughout experiments. The results suggest that supraspinal descending inputs for controlling joint movement are responsible for changes in the spinal neural circuits, and that task movement speed is one of the critical factors for inducing plastic changes in reciprocal Ia inhibition.

Keywords: movement speed; presynaptic inhibition; reciprocal Ia inhibition; spinal plasticity; visuomotor task.

Figure 1

Schematic of the motor tasks. (A) Experimental set-up. (B) Example of raw EMG activity of tibialis anterior (TA) muscle and soleus (SOL) muscles during isometric maximum voluntary contraction (MVC) and each motor task. (C) Example of the angle joint movement during each motor task, which corresponded to electromyography (EMG) activity of TA and SOL muscles.

Figure 2

The changes in the motor performance in slow-speed, fast-speed, and control groups. The graph shows the time course of the changes in the motor performance in the slow, fast, and control groups. The ordinate shows mean error values normalized by the value of the first block. The abscissa shows each block. The dagger (†) represents significant difference (P < 0.05) between the first block and fifth block, and the double dagger (‡) represent significant difference (P < 0.01) between the first block and six block in the slow-speed group. The asterisks (*) represents significant difference (P < 0.05) between the first block and fourth and fifth blocks, and the double asterisks (**) represent significant difference (P < 0.01) between the first block and sixth block in the fast-speed group. Error bar indicates SEM.

Figure 3

Effects of the movement speed of visuomotor task on the D1 inhibition and reciprocal Ia inhibition. The graphs show the mean values of the D1 inhibition (A) and reciprocal Ia inhibition (B) in the slow- and fast-speed groups. The ordinate indicates the conditioned H-reflex amplitude expressed as a percentage of the test H-reflex amplitude. The abscissa shows the times at which measurements were taken [before (pre), 5 min after (post 5), 15 min after (post 15), and 30 min after (post 30) the visuomotor task]. Open circles represent the slow-speed group and closed circles represent the fast-speed group. Values below 100% indicate inhibition and values above 100% indicate facilitation. The asterisks (*) and the double asterisks (**) represent significant differences (*P < 0.05) and (**P < 0.01), respectively. The section marked (§) represents a significant difference (P < 0.05) between slow- and fast-speed group in the post 5 time period. Error bar indicates SEM.

Figure 4

Effects of the control task on the D1 inhibition and reciprocal Ia inhibition. The graphs show the mean values of the D1 inhibition (A) and reciprocal Ia inhibition (B) in the control group. The ordinate shows the conditioned H-reflex amplitude expressed as a percentage of the test H-reflex amplitude. The abscissa shows the time at which measurements were taken [before (pre), 5 min after (post 5), 15 min after (post 15), and 30 min after (post 30) the visuomotor task]. Values below 100% indicate inhibition and values above 100% indicate facilitation. Error bar indicates SEM.

Figure 5

The effect of visuomotor task and control task on the transcranial magnetic stimulation (TMS) conditioned inhibitory effects on the presynaptic inhibitory pathways. (A) Typical averaged waveforms of H-reflexes (n = 10) in each stimulus condition were recorded from two representative subjects who performed a visuomotor task (left) or a control task (right). (B–E) The graphs show the mean values of the D1 inhibition (B), TMS conditioned D1 inhibition (C), TMS conditioned test H-reflex amplitude (D), and the net difference in the amount of D1 inhibition (E), in the visuomotor and non-visuomotor group. In (B–D), the ordinate shows the conditioned H-reflex amplitude expressed as a percentage of the test H-reflex amplitude. The dashed line indicates the test H-reflex amplitude (100%). Values below 100% indicate inhibition and values above 100% indicate facilitation. In (E), the ordinate shows the degree of changes in the D1 inhibition which is calculated by subtracting the minor facilitation effect of TMS conditioned test H-reflex amplitude (mean conditioned H-reflex—test H-reflex) from the changing amount of D1 inhibition in the absence and presence of TMS (difference between graph B and C, expressed as a percentage of the test H-reflex amplitude). Open and closed bars represent the time at which measurements were taken before (pre) and after (post) the motor task, respectively. The double asterisks (**) represent significant difference (**P < 0.01). Error bar indicates SEM.

Figure 6

The effect of visuomotor task and control task on the transcranial magnetic stimulation (TMS) conditioned H-reflex at short latency facilitation phase. (A) Typical averaged waveforms of H-reflexes (n = 10) in each stimulus condition were recorded from two representative subjects who performed a visuomotor task (left) or a control task (right). The arrows indicate the artifact of TMS stimulation. The conditioning stimulation of TMS was applied after the test H-reflex stimulation. (B) The graphs show the mean values of the TMS conditioned H-reflex amplitude at short latency facilitation phase in the visuomotor and non-visuomotor group. The ordinate shows the conditioned H-reflex amplitude expressed as a percentage of the test H-reflex amplitude. Values below 100% indicate inhibition and values above 100% indicate facilitation. Open and closed bars represent the time at which measurements were taken before (pre) and after (post) the motor task, respectively. The daggers (†) represent significant differences (^†P < 0.05) between conditioned H-reflex and baseline test H-reflex, which is shown by the dashed line. Error bar indicates SEM.