Corticospinal and reciprocal inhibition actions on human soleus motoneuron activity during standing and walking

Abstract

Reciprocal Ia inhibition constitutes a key segmental neuronal pathway for coordination of antagonist muscles. In this study, we investigated the soleus H-reflex and reciprocal inhibition exerted from flexor group Ia afferents on soleus motoneurons during standing and walking in 15 healthy subjects following transcranial magnetic stimulation (TMS). The effects of separate TMS or deep peroneal nerve (DPN) stimulation and the effects of combined (TMS + DPN) stimuli on the soleus H-reflex were assessed during standing and at mid- and late stance phases of walking. Subthreshold TMS induced short-latency facilitation on the soleus H-reflex that was present during standing and at midstance but not at late stance of walking. Reciprocal inhibition was increased during standing and at late stance but not at the midstance phase of walking. The effects of combined TMS and DPN stimuli on the soleus H-reflex significantly changed between tasks, resulting in an extra facilitation of the soleus H-reflex during standing and not during walking. Our findings indicate that corticospinal inputs and Ia inhibitory interneurons interact at the spinal level in a task-dependent manner, and that corticospinal modulation of reciprocal Ia inhibition is stronger during standing than during walking.

Keywords: Humans; Ia interneurons; TMS; motor control; soleus H‐reflex.

Figure 1

Experimental design. (A) Experimental position and conditioning-test (C-T) interval between posterior tibial (PTN, test stimuli) and deep peroneal (DPN, conditioning stimuli) nerves used to establish reciprocal inhibition of the soleus H-reflex with subjects seated. (B) Experimental position and C-T intervals between conditioning transcranial magnetic stimulation (TMS) and reciprocal inhibition on soleus H-reflex (triple stimulation paradigm).

Figure 2

Background EMG activity. Mean rectified EMG activity in soleus (upper traces) and TA (lower traces) muscles during walking (A) and during standing (B) in one subject. Abscissa was expressed as a percentage of the total duration of the step cycle in A and in msec in B. Vertical arrows indicate when stimuli were delivered at mid- and late stance phases of walking.

Figure 3

Reciprocal Ia inhibition at rest. (A) Nonrectified waveform averages (N = 20) of the control (green line) and conditioned (black line) H-reflexes from one representative subject during seated. Conditioning stimuli were applied to the deep peroneal nerve (DPN) at 1–1.5 × MT at a conditioning-test (C-T) interval of 2 msec. (B) Difference between conditioned and mean control H-reflex (% the mean control H-reflex) in the same subject as in A, plotted against the C-T interval between DPN and PTN stimuli. Vertical bars are ±1 SEM. *P < 0.05.

Figure 4

Reciprocal inhibition during standing and walking. (A) Nonrectified waveform averages (N = 20) of the control (green lines) and conditioned (black lines) soleus H-reflexes from one subject at midstance (upper traces) and late stance (middle traces) phases of walking, and during standing (lower traces). Conditioning stimuli were applied to the deep peroneal nerve (DPN) at 1–1.2 × MT and at a conditioning-test interval of 2 msec. (B) Overall mean difference between conditioned and mean control H-reflex (% the mean control H-reflex) for each task from all subjects. **P < 0.01 and ***P < 0.001. Vertical bars are ±1 SEM.

Figure 5

Effects of subthreshold TMS on soleus H-reflex during standing and walking. (A) Nonrectified waveform averages (N = 20) of the control (green lines) and conditioned (black lines) soleus H-reflexes from one subject at midstance (upper traces) and late stance (middle traces) phases of walking, and during standing (lower traces). TMS conditioning stimuli were set at 0.95 × AMT and the conditioning-test (C-T) interval was −2 msec. (B) Overall mean difference between conditioned and control H-reflex (% of the mean control H-reflex) plotted against the C-T interval between the TMS and PTN stimuli, at midstance (black line and filled circles), late stance (thin line and open circles) and during standing (interrupted line and open circles) from all subjects tested. Vertical bars are ±1 SEM. **P < 0.01.

Figure 6

(A) Comparison between the net and combined stimuli effects. Difference between conditioned and control H-reflex (% of the mean control H-reflex) during walking (mid- and late stance phases) and standing from all 15 subjects tested. White columns illustrate the algebraic sum of the effects of separate stimuli, and black columns illustrate the effect of combined stimuli. Asterisks show statistically significant differences between the effect of combined stimuli and the net effect as well as across tasks. (B) Overall amplitude of the combined effects having subtracted the net effects is plotted against the conditioning-test interval between TMS and PTN for three subjects during standing. Vertical bars are ±1 SEM. *P < 0.05 and ***P < 0.01.

Figure 7

Corticospinal projections on soleus motoneurons, Ia and presynaptic interneurons. Schematic diagram showing the descending inputs from motor cortex onto soleus motoneurons (open circle with Sol inside), Ia inhibitory interneurons (in green) receiving group Ia afferents from TA (in blue), and primary afferent depolarization interneurons mediating presynaptic inhibition of Ia afferents projecting on soleus motoneurons (in red) or on Ia afferents from TA projecting on Ia inhibitory interneurons (in blue). INs = interneurons.