Oscillatory Corticospinal Activity during Static Contraction of Ankle Muscles Is Reduced in Healthy Old versus Young Adults

Abstract

Aging is accompanied by impaired motor function, but age-related changes in neural networks responsible for generating movement are not well understood. We aimed to investigate the functional oscillatory coupling between activity in the sensorimotor cortex and ankle muscles during static contraction. Fifteen young (20-26 yr) and fifteen older (65-73 yr) subjects were instructed to match a target force by performing static ankle dorsi- or plantar flexion, while electroencephalographic (EEG) activity was recorded from the cortex and electromyographic (EMG) activity was recorded from dorsi- (proximal and distal anterior tibia) and plantar (soleus and medial gastrocnemius) flexor muscles. EEG-EMG and EMG-EMG beta band (15-35 Hz) coherence was analyzed as an index of corticospinal activity. Our results demonstrated that beta cortico-, intra-, and intermuscular coherence was reduced in old versus young subjects during static contractions. Old subjects demonstrated significantly greater error than young subjects while matching target forces, but force precision was not related to beta coherence. We interpret this as an age-related decrease in effective oscillatory corticospinal activity during steady-state motor output. Additionally, our data indicate a potential effect of alpha coherence and tremor on performance. These results may be instrumental in developing new interventions to strengthen sensorimotor control in elderly subjects.

Figure 1

Experimental setup and static contractions. Subjects sat in a chair with their left foot fastened to a force pedal and maintained a force level of 10% of their maximal voluntary contraction (MVC) for 2 min, first for dorsiflexion (DF) and subsequently for plantar flexion (PF). The target force level was projected onto the wall as a horizontal line that subjects were asked to follow as precisely as possible with a yellow force trace showing online force production. During contractions, electroencephalographic (EEG) and electromyographic (EMG) signals from the proximal and distal ends of the anterior tibial muscle (TA_prox and TA_dist), soleus (SOL), and medial gastrocnemius (GM) were recorded.

Figure 2

Coherence head plots. Spatial localization of summed beta band (15–35 Hz) corticomuscular coherence for single young (a, c) and old (b, d) subjects during static dorsiflexion (a, b; EEG-TA_prox coherence) and plantar flexion (c, d; EEG-SOL coherence).

Figure 3

Raw EEG and EMG traces, autospectra, and coherence results from a single young subject. EEG from Cz (a), EMG from proximal (b), and distal (c) ends of the anterior tibial muscle (TA_prox and TA_dist, resp.); autospectra for Cz (d), TA_prox (e), TA_dist (f); and coherence for Cz-TA_prox (g), Cz-TA_dist (h), and TA_prox-TA_dist (i) during static dorsiflexion. Dashed lines on coherence plots indicate upper 95% confidence interval limits.

Figure 4

EMG power. Summed EMG power in alpha (5–15 Hz) and beta (15–35 Hz) bands for young and old subjects during dorsiflexion (white background) and plantar flexion (grey background). Significant differences between young and old groups are indicated by ^∗p < 0.05; ^∗∗p < 0.01. TA_prox: proximal end of anterior tibial; TA_dist: distal end of anterior tibial; SOL: soleus; GM: medial gastrocnemius.

Figure 5

Pooled coherence during dorsiflexion. Pooled coherence estimates for young (black areas) and old (light grey areas) groups during static dorsiflexion (a, c, e) and χ² test statistics as a function of frequency (b, d, f) illustrating frequencies at which group means differed. Shaded boxes in b, d, and f mark the beta band (15–35 Hz). Dashed lines indicate upper 95% confidence interval limits. TA_prox: proximal end of anterior tibial muscle; TA_dist: distal end of anterior tibial muscle.

Figure 6

Coherence area estimates. Logarithmic coherence area in alpha (5–15 Hz), beta (15–35 Hz), low (15–25 Hz), and high (25–35 Hz) beta during static dorsiflexion (a) and plantar flexion (b) for young and old subjects. Significant differences between young and old groups are indicated by ^∗p < 0.05; ^∗∗p < 0.01; ^∗∗∗p < 0.001; ^#p < 0.1. TA_prox: proximal end of anterior tibial; TA_dist: distal end of anterior tibial; SOL: soleus; GM: medial gastrocnemius.

Figure 7

Pooled coherence during plantar flexion. Pooled coherence estimates for young (black areas) and old (light grey areas) groups during static plantar flexion (a, c, e) and χ² test statistics as a function of frequency (b, d, f) illustrating frequencies at which group means differed. Shaded boxes in b, d, and f mark the beta band (15–35 Hz). Dashed lines indicate upper 95% confidence interval limits. SOL: soleus; GM: medial gastrocnemius.

Figure 8

Performance during static contractions. Group differences in force precision during submaximal dorsiflexion (a) and plantar flexion (b). Significant differences between young and old groups are indicated by ^∗p < 0.05, ^∗∗p < 0.01. RMS: root mean square.