ELECTROMYOGRAPHIC IDENTIFICATION OF SPINAL OSCILLATOR PATTERNS AND RECOUPLINGS IN A PATIENT WITH INCOMPLETE SPINAL-CORD LESION - OSCILLATORFORMATION TRAINING AS A METHOD TO IMPROVE MOTOR ACTIVITIES

Citation
G. Schalow et al., ELECTROMYOGRAPHIC IDENTIFICATION OF SPINAL OSCILLATOR PATTERNS AND RECOUPLINGS IN A PATIENT WITH INCOMPLETE SPINAL-CORD LESION - OSCILLATORFORMATION TRAINING AS A METHOD TO IMPROVE MOTOR ACTIVITIES, General physiology and biophysics, 15, 1996, pp. 121-220
Citations number
129
Categorie Soggetti
Physiology,Biophysics
ISSN journal
02315882
Volume
15
Year of publication
1996
Supplement
1
Pages
121 - 220
Database
ISI
SICI code
0231-5882(1996)15:<121:EIOSOP>2.0.ZU;2-#
Abstract
A patient with a strongly lesioned spinal cord, sub C5, relearned runn ing, besides improving other movements, by an oscillator formation tra ining (rhythmic, dynamic, stereotyped exercise). After 45 days of jump ing on a springboard and other rhythm trainings, the patient was able to run 90 m in 4ls (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-t ype (alpha(1)) (f = 8.3-11.4 Hz) and FR-type (alpha(2)) (f = 6.7 Hz) m otor unit firings were identified by electromyography (EMG) with surfa ce 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 meas ured in FF-type motor units, with changing focus (change from long/sho rt to short/long oscillation periods). The alternating mean period dur ations differred by approximately 10 ms. Transient synchronization of oscillatory firing FF-type motor units was observed with up to two pha se relations per oscillation cycle. In recumbent position, the phase c hange in synchronization of two oscillatory firing motor units in the soleus muscle of one leg correlated with the change from alternating t o symmetrical oscillatory firing of a third motor unit in the soleus m uscle of the other leg. This measurement indicates that the alternatin g 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 inhibiti on of half-centre oscillators as suggested by the change from alternat ing to symmetrical oscillatory firing. Coupling changes of oscillatory firing subnetworks to generate macroscopic (integrative) network func tions 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 oscilla tors, phase changes in synchronization, changes from alternating to sy mmetrical firing and backwards, and changes in the focus of alternatin g 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-rhy thmic movements. One phase relation between two oscillatory firing alp ha(1)-motor units was preserved from one volitional leg muscle activat ion (isometric contraction) to the subsequent one. Since running times improved upon successive runs for 90 m, the spinal cord seems to be a ble to store pattern organization for seconds up to minutes. Controlle d and uncontrolled oscillatory firing of alpha(1)-motor units in volit ionally activated leg muscles were observed in this patient, which ind icated that there still were pathologic recruitments of subnetworks af ter re-learning running and other movements. During walking, running, and jumping on a springboard, the activation patterns of the vastus la teralis, hamstrings, tibialis anterior, peronaeus longus, peronaeus br evis and soleus muscles were recorded (surface electromyography) to be still pathologic in accordance with partly still pathologic joint rot ation angles measured kinematically. Especially upon running, the left knee joint flexion was reduced in swine by a rather permanent activit y of the rectus femoris combined with an extra burst of the vastus lat eralis in mid-swing. The recorded abnormalities are due to modificatio n of the motor program rather than to muscle weakness per se. A furthe r improvement of the movements of the patient seems possible by improv ing the motor program, i.e. by improving the functioning of the spinal pattern generators. By comparing the phasic EMG activity upon walking , running and jumping on a springboard, the motor program turned out t o be best for jumping and running, at least with respect to the activi ty of the left peronaeus longus muscle. This indicates that during the more rhythmic, dynamic, stereotyped movements (like jumping or runnin g) more physiologic spinal motor programs were activated by the remain ing supraspinal drive. Jumping on a springboard generated the most phy siologic movement pattern, probably by ''Mitbewegung'' (co-movement) a ctivated by the synchronization of both legs once per jumping cycle, w hich induced stronger synchronization of right and left movement patte rn generators by a shared afferent input and cycle resettings of oscil latory firing subnetworks of the left and right pattern generators. It is proposed that at least partly, the spinal cord generates stereotyp ed movements by coupling changes of oscillatory firing subnetworks. Th e main cause for the movement disorders (and spasticity) occurring fol lowing spinal cord lesion is the pathologic organization of the functi onally deteriorated neuronal subunits below the lesion (because of non use as one reason) in combination with a lesion- and degeneration-indu ced unbalanced supraspinal and afferent drive, respectively for self-o rganization of spinal networks. On the basis of our successful therapy trial and measurements on normal, brain-dead, completely (paraplegic) and incompletely spinal cord lesioned (tetraparetic) individuals, it is proposed that the training-induced plasticity of the human CNS to r e-preformate neuronal networks for up to minutes and permanently has b een underestimated. The oscillator formation training was successful, since the rhythm training fitted the rhythmic organization of the CNS (at least with respect to the premotor alpha(1), alpha(2) alpha(3)-osc illators), as the rhythmic, stereotyped, dynamic leg movements are mai nly located in the lumbosacral enlargement of the cord, which was not lesioned in this patient (lesion sub C5), and could be activated by th e little remaining supraspinal drive, and since co-movement (''Mitbewe gung'') was induced once per jumping cycle by the simultaneous afferen t input. This improvement in movements was made possible by re-preform ation of spinal neuronal networks for improved self-organization by rh ythmic movement-induced afferent input, and by rebalanced lesion-adapt ed drive of supraspinal networks (by lesion-adapted reorganization). T he type-related single motor axon firing patterns were partly verified by telemetrically obtained rhythmic EMG patterns. The self-organizati on of spinal oscillators, including coupling rules between o