Effects of neurochemically excited group III-IV muscle afferents on motoneuron afterhyperpolarization.

When humans voluntarily and maximally contract a muscle under isometric conditions, the average firing rate of motor units decreases from an initially high value over several tens of seconds. The mechanisms underlying the rate reduction are probably manifold. One mechanism could involve changes in the motoneuron afterhyperpolarization, another reflex effects of group III-IV muscle afferents that are excited during developing muscle fatigue. It appears possible that changes in motoneuron afterhyperpolarization are mediated by these afferent inputs. We therefore studied effects on motoneuron afterhyperpolarization of small-diameter muscle afferents excited by intra-arterially injected metabolites such as bradykinin and serotonin. In decerebrate and mostly spinalized cats, lumbosacral alpha-motoneurons were recorded intracellularly. Current pulses were injected to test for input resistance and elicit action potentials and afterhyperpolarizations. Afterhyperpolarizations were averaged from c. 10 successive stimulus repetitions. Measurements were taken of afterhyperpolarization amplitude, half-width and area; and exponential functions were fitted to the afterhyperpolarization decay phase to determine afterhyperpolarization decay time-constants. In selected cases, the entire afterhyperpolarization trajectory was fitted with a sum of two exponentials to assess more precisely changes in afterhyperpolarization trajectory. Small catheters were inserted into side-branches of the sural artery and the accompanying vein to apply substances like bradykinin, serotonin and KCl to the calf muscles. Concentrations were in the range of those used by other workers. Intra-arterial injection of bradykinin and serotonin usually decreased blood pressure, which may at times have affected mean motoneuron membrane potentials. Afterhyperpolarization amplitude usually changed with membrane potential in a way expected from ensuing changes in driving potential. Whenever excitation of group III-IV muscle afferents caused moderate to strong increases in motoneuron synaptic noise, afterhyperpolarization amplitudes were reduced, usually in parallel to decreases in input resistance. Afterhyperpolarization half-widths were mostly unaffected, but occasionally decreased. There was a significant trend for afterhyperpolarization decay time-constants to increase during increased synaptic noise, this increase being inversely correlated with the reduction in afterhyperpolarization amplitude. The reduction in input resistance was associated with a decrease in the membrane time-constant, which could therefore not account for the prolongation of the afterhyperpolarization decay time-constant. The afterhyperpolarization area decreased, indicating that the reduction of afterhyperpolarization amplitude outweighed the prolongation of afterhyperpolarization decay time-constant. During a prolonged fatiguing muscle contraction group III-IV afferents become increasingly excited, produce augmenting synaptic inputs in motoneurons, and will change afterhyperpolarization properties. On average, these changes per se tend to diminish the effect of afterhyperpolarization on motoneuron discharge.