Age-related influence of vision and proprioception on Ia presynaptic inhibition in soleus muscle during upright stance

Abstract

This study investigated the modulation of Ia afferent input in young and elderly adults during quiet upright stance in normal and modified visual and proprioceptive conditions. The surface EMG of leg muscles, recruitment curve of the soleus (SOL) Hoffmann (H) reflex and presynaptic inhibition of Ia afferents from SOL, assessed with the D1 inhibition and single motor unit methods, were recorded when young and elderly adults stood with eyes open or closed on two surfaces (rigid vs. foam) placed over a force platform. The results showed that elderly adults had a longer path length for the centre of pressure and larger antero-posterior body sway across balance conditions (P < 0.05). Muscle EMG activities were greater in elderly compared with young adults (P < 0.05), whereas the H(max) expressed as a percentage of the H(max) was lower (P = 0.048) in elderly (38 ± 16%) than young adults (58 ± 16%). The conditioned H reflex/test H reflex ratio (D1 inhibition method) increased with eye closure and when standing on foam (P < 0.05), with greater increases for elderly adults (P = 0.019). These changes were accompanied by a reduced peak motor unit discharge probability when standing on rigid and foam surfaces (P 0.001), with a greater effect for elderly adults (P = 0.026). Based on these latter results, the increased conditioned H reflex/test H reflex ratio in similar sensory conditions is likely to reflect occlusion at the level of presynaptic inhibitory interneurones. Together, these findings indicate that elderly adults exhibit greater modulation of Ia presynaptic inhibition than young adults with variation in the sensory conditions during upright standing.

Figure 1. Maximal amplitude of centre of pressure (CoP) displacement in antero-posterior direction during upright stance

The A-P_max for young (open bars) and elderly adults (filled bars) with eyes open on a rigid surface (REO) and a foam mat (FEO) and with eyes closed on a rigid surface (REC) and a soft mat (FEC). The displacements are greater for elderly adults than for young adults (age main effect, P < 0.05). † Significant differences between supports, P < 0.05. ‡ Significant differences between vision conditions, P < 0.05.

Figure 2. Electromyographic activity for leg muscles during upright stance

The rectified and averaged EMG (aEMG) for the soleus (SOL), gastrocnemii medialis (GM) and lateralis (GL) and tibialis anterior (TA) muscles are shown for both vision and surface conditions for young (open bars) and elderly adults (filled bars). The aEMG is greater for elderly adults than for young adults (age main effect, P < 0.05). † Significant differences between support surfaces, P < 0.05. ‡ Significant differences between vision conditions, P < 0.05.

Figure 3. Relation between the H_max/M_max ratio and the background soleus aEMG

The H_max/M_max ratio was plotted against the rectified and averaged EMG activity of the SOL in young (open circles; r² = 0.29; P < 0.001) and elderly adults (filled circles; r² = 0.32; P < 0.001). Data from all balances conditions are plotted.

Figure 4. Recordings of the test H reflex and conditioned H reflex

Representative traces of test H reflex and conditioned (cond) H reflex (averaged over 20 responses) for one young subject and one elderly subject with eyes open on a rigid surface (REO) and a foam mat (FEO) and with eyes closed on a rigid surface (REC) and a foam mat (FEC).

Figure 5. Relations between D1 inhibition, CoP and co-contraction level

A, relations between the ratio of the conditioned H reflex relative to the test H reflex and the maximal amplitude of the CoP in the antero-posterior direction (A-P_max). B, relations between the H-reflex ratio and the co-contraction level. C, relations between the co-contraction level and A-P_max. All the relations are statistically significant for elderly adults (P < 0.001), but not for young adults.

Figure 6. Post-stimulus time histograms (PSTHs) derived from single motor unit recordings

A and B, post-stimulus time histogram (see Methods) for one young (A) and one elderly adult (B) in the two vision conditions when standing on a rigid surface. Motor unit discharge probability is expressed as discharge/impulse for 0.5 ms bins. The arrows indicate the onset of the peak of motor unit discharge in response to tibial nerve stimulation and dashed lines underline the changes in the first 0.5 ms bin of the peak between the two vision conditions. C and D, discharge probability of motor units within the first 0.5 ms bin of the peak of the PSTH during upright stance on a rigid (n = 18; C) and a foam surface (n = 13; D) with eyes open and closed in young (blue dots) and elderly adults (red dots). The thick black line represents the mean values of discharge probability when data from young and elderly adults are pooled together. E, changes in discharge probability within the first 0.5 ms bin of the peak of the PSTH with eye closure (expressed as a percentage of discharge probability for the eyes open condition) in young (blue bar) and elderly adults (red bar) for data collapsed across surface conditions. * Significant differences between age groups, P < 0.05. ‡ Significant differences between vision conditions, P < 0.05.