Electromyographic identification of spinal oscillator patterns and recouplings in a patient with incomplete spinal cord lesion: oscillator formation training as a method to improve motor activities

A patient with a strongly lesioned spinal cord, sub C5, relearned running, besides improving other movements, by an oscillator formation training (rhythmic, dynamic, stereotyped exercise). After 45 days of jumping on a springboard and other rhythm trainings, the patient was able to run 90 m in 41 s (7.9 km/h) (even 9.3 km/h 3 years after the lesion) besides marching (5.7 km/h), cycling, playing tennis and skiing. FF-type (alpha 1) (f = 8.3-11.4 Hz) and FR-type (alpha 2) (f = 6.7 Hz) motor unit firings were identified by electromyography (EMG) with surface electrodes by their oscillatory firing patterns in this patient. In EMG literature, the alpha 2-oscillatory firing is called "myokymic discharging". Alternating long and short oscillation periods were measured in FF-type motor units, with changing focus (change from long/short to short/long oscillation periods). The alternating mean period durations differed by approximately 10 ms. Transient synchronization of oscillatory firing FF-type motor units was observed with up to two phase relations per oscillation cycle. In recumbent position, the phase change in synchronization of two oscillatory firing motor units in the soleus muscle of one leg correlated with the change from alternating to symmetrical oscillatory firing of a third motor unit in the soleus muscle of the other leg. This measurement indicates that the alternating oscillatory firing of premotor neuronal networks is correlated with synchronization of oscillatory firing neuronal subnetworks, i.e., with coupling changes of oscillators, and is not due to reciprocal inhibition of half-centre oscillators as suggested by the change from alternating to symmetrical oscillatory firing. Coupling changes of oscillatory firing subnetworks to generate macroscopic (integrative) network functions are therefore a general organization form of the central nervous system (CNS), and are not related to rhythmic movements like walking or running only. It is proposed that synchronization of spinal oscillators, phase changes in synchronization, changes from alternating to symmetrical firing and backwards, and changes in the focus of alternating oscillatory firing are, among others, physiologic coupling rules of the human CNS to generate, by ongoing coupling changes of oscillatory firing subnetworks, integrative functions such as rhythmic and non-rhythmic movements. One phase relation between two oscillatory firing alpha 1-motor units was preserved from one volitional leg muscle activation (isometric contraction) to the subsequent one. Since running times improved upon successive runs for 90 m, the spinal cord seems to be able to store pattern organization for seconds up to minutes. Controlled and uncontrolled oscillatory firing of alpha 1-motor units in volitionally activated leg muscles were observed in this patient, which indicated that there still were pathologic recruitments of subnetworks after re-learning running and other movements. During walking, running, and jumping on a springboard, the activation patterns of the vastus lateralis, hamstrings, tibialis anterior, peronaeus longus, peronaeus brevis and soleus muscles were recorded (surface electromyography) to be still pathologic in accordance with partly still pathologic joint rotation angles measured kinematically. Especially upon running, the left knee joint flexion was reduced in swing by a rather permanent activity of the rectus femoris combined with an extra burst of the vastus lateralis in mid-swing. The recorded abnormalities are due to modification of the motor program rather than to muscle weakness per se. A further improvement of the movements of the patient seems possible by improving the motor program, i.e., by improving the functioning of the spinal pattern generators.(ABSTRACT TRUNCATED)