External loops of human premotor spinal oscillators identified by simultaneous measurements of interspike intervals and phase relations.
Single nerve-fibre action potentials (APs) were recorded extracellularly from alpha and gamma-motoneurons and secondary muscle spindle afferents from a ventral S4 nerve root (some afferents are contained in lower sacral motor roots) in an individual with traumatic spinal cord lesion sub TH1. Simultaneous interspike intervals (IIs) of, and phases between, the APs of 5 nerve fibres were measured, and distributions were constructed. The II distributions were of a broad peak type. Phase distributions showed 1 to 3 peaks interpreted as phase relations between the firings of the nerve fibres. Under certain phase relations, the rhythmic firing of alpha and gamma-motoneurons is further interpreted as an interaction of oscillatory firing neuronal subnetworks driving alpha and gamma-motoneurons. Following repetitive touch and pin-prick stimulation in- and outside the anal reflex area, the II distributions of alpha and gamma-motoneurons and of secondary spindle afferents assimilated partly or fully, while preserving their phase relations. This coordinated firing is interpreted as the oscillatory firing of alpha neuronal networks building up an external loop to the periphery via the gamma-loop. Upon touch, pin-prick, and anal reflex stimulation, and anal and bladder catheter pulling, the values and the number of the phase relations changed. Mostly two phase relations per oscillation cycle were observed. Two phase relations probably represent the physiologic case for the somatic nervous system. Only one phase relation was found when full synchronization of all units occurred. Three phase relations were found when the parasympathetic nervous system division interacted with the somatic one. Based on data obtained from brain-dead individuals it is discussed that the increased synchronization and instability in the number and the values of phase relations suggested pathologic functioning of the caudal functionally disconnected spinal cord in patients with spinal cord lesions: Oscillatory firing neuronal networks, which lost their specific properties, interacted more easily and unspecifically with other oscillatory firing networks. Further, it is discussed that physiologic tremor is caused by chance synchronization of oscillatory firing neuronal networks and therefore originates in the central nervous system (CNS). Since spinal oscillators build up external loops to the periphery, it is suggested that in patients with incomplete spinal cord lesions it should be possible to re-preformate oscillatory firing neuronal networks by a rhythm training, to reduce spasticity and to re-train useful movements, especially locomotion.
Schalow
G
G
Department of Clinical Research, Swiss Paraplegic Centre Nottwil, Switzerland.
Zäch
G A
GA
D000344:Afferent Pathways / Q000503:physiopathology; D001003:Anal Canal / Q000294:innervation; D001926:Brain Death; D006801:Humans; D008959:Models, Neurological; D009046:Motor Neurons / Q000502:physiology*; D009130:Muscle, Smooth / Q000294:innervation; D009412:Nerve Fibers / Q000502:physiology*; D012018:Reflex; D013116:Spinal Cord / Q000503:physiopathology; D013119:Spinal Cord Injuries / Q000503:physiopathology*; D013126:Spinal Nerve Roots / Q000503:physiopathology; D013997:Time Factors; D001743:Urinary Bladder / Q000294:innervation