Intracellular autogenetic and synergistic effects of muscular contraction on flexor motoneurones

Abstract

Intracellular records were taken from cat motoneurons innervating flexor muscles of the hind limb. Contractions of the ankle flexors tibialis anterior and extensor digitorum longus were elicited by stimulation of the peripheral end of the cut L 7 ventral root and the reflex effects of these contractions were recorded in silent and repetitively firing motoneurons. Contraction usually produces a hyperpolarizing response inside flexor motoneurons. This hyperpolarization is tension-sensitive in the sense that when, at constant muscle extension, the strength of the contraction is increased, the magnitude of the inhibitory response is augmented. Increasing the resting length of the muscles, while using a stimulus of constant strength to the ventral root, causes this inhibitory response to increase in some cells. More often, however, the hyperpolarization caused by contraction is gradually reduced in duration and/or amplitude as the muscles are extended. Even with the muscles slackened, so that they develop no tension at their ends, contraction usually produces prominent hyperpolarization of the motoneurons. By passing polarizing currents or injecting chloride ions through the intracellular micro-electrode, the hyperpolarizing potentials produced by contraction of the slack and extended muscles are shown to be, at least in part, genuinely post-synaptic inhibitory events. When the neuron is fired repetitively by injected current, the "silent period" in contraction corresponds to the hyperpolarization of the postsynaptic membrane. Monosynaptic testing of the flexor motoneuron pool was used to confirm the essential features of the intracellularly recorded activity. Acutely spinalizing the animal increases the magnitude of the inhibitory responses caused by contraction. Recordings from dorsal root fibers show that Golgi tendon organs of the ankle flexors are very sensitive to contraction and are indeed often activated by the internal forces developed in a contracting slack muscle. A number of muscle spindles of the ankle flexors are activated by stimulation of the ventral root at a strength submaximal or just maximal for the [alpha] -motor fibers, despite the simultaneous unloading effect of the contracting extrafusal fibers. This spindle activation, which occurs mainly during the phase of tension development in contraction, is favored by an increased extension of the muscle. Attempts were made to establish whether it is due to [alpha]-motor innervation of the receptors or to some mechanical interaction between the intra- and extrafusal muscle fibers. The possible central and peripheral causes of the changes in motoneuron excitability produced by flexor muscle contraction are discussed. Tendon organs of flexor muscles strongly inhibit flexor motoneurons and that [alpha]-motor innervation of muscle spindles is likely to play a more prominent role in flexors than in extensor muscles.