Changes in cortically related intermuscular coherence accompanying improvements in locomotor skills in incomplete spinal cord injury

Abstract

In human spinal cord injury, the neuronal mechanisms mediating the improvement of locomotor function in response to intensive treadmill training are not well understood. In this study, we examined if such recovery is mediated, in part, by increases in residual corticospinal drive to muscles of the leg during walking. To do this, we measured the coherence of electromyogram (EMG) activity between two antagonist muscles (intermuscular coherence), specifically at frequencies between 24 and 40 Hz, which is thought to indicate common drive to two muscles from corticospinal inputs. In 12 subjects with incomplete spinal cord injury, intermuscular coherence was measured between hamstrings and vastus lateralis EMG that was activated during walking on a motorized treadmill. Before training, appreciable coherence in the 24-40 Hz frequency band was only present in subjects with moderate volitional motor strength in their leg muscles (n = 8 subjects) compared with subjects with little or no leg muscle strength (n = 4 subjects), reconfirming that 24-40 Hz frequency coherence is likely mediated by common supraspinal inputs. After training, increases in 24-40 Hz coherence only occurred in the eight subjects with moderate leg muscle strength who also exhibited improvements in locomotor recovery as assessed by the 21 point WISCI II scale (termed responders). In contrast, development of intermuscular coherence in the 24-40 Hz frequency band did not occur in the four subjects with absent or weak muscle strength. These subjects also did not improve in their locomotor ability as reflected in unchanging WISCI II scores (termed nonresponders). Lower-frequency coherence (5-18 Hz), which is thought to contain common drive from spinal inputs, did not change in either group. In a subset of subjects that were previously assessed with transcranial magnetic stimulation (TMS) before and after training (n = 5 responders and 3 nonresponders), there was a significant and positive relationship between increases in 24-40 Hz coherence and increases in evoked muscle responses to TMS of the primary motor cortex. Taken together, increases in higher-frequency EMG coherence in subjects with residual voluntary muscle strength and its parallel relation to changes in TMS-evoked responses provides further evidence that improvements in locomotor function from treadmill training are mediated, in part, by increases in corticospinal drive to muscles of the leg during walking.