Induction of action potentials by denervation of tonic fibres in rat extraocular muscles

Abstract

The effects of denervation by nerve section on the electrical properties of tonic and twitch fibres of rat extraocular muscles were examined. Normally innervated tonic fibres lack action potentials. Upon direct stimulation they generate graded, voltage-dependent responses or slow peak potentials (s.p.p.s). However, one week after denervation the s.p.p.s are transformed into action potentials which are slower and broader than those of twitch fibres. The action potentials are Na dependent and partially resistant to blockade with 10(-5) M-tetrodotoxin and 10(-6) M-saxitoxin. Changing the holding potential of the fibres from -80 mV to more negative levels increases the maximal rate of rise of the action potential. This effect is not observed on the s.p.p.s of normally innervated fibres. Following denervation the resting potential of tonic and twitch fibres becomes about 10-15 mV less negative. In denervated muscles stimulation with pulses of hyperpolarizing current evokes graded responses in tonic fibres and action potentials in twitch fibres. In normally innervated muscles, these anodal break responses are never observed in tonic fibres and are very rare in twitch fibres. By two weeks after nerve section, reinnervation is present. The action potentials of tonic fibres are still present but stronger stimulation is needed to evoke anodal break responses. By three weeks, direct stimulation of tonic fibres evokes normal s.p.p.s in about 25% of the studied fibres and action potentials in the rest. By four weeks, most tonic fibres have lost the action potential but small anodal break responses can be evoked in most. It is suggested that following denervation a new population of Na channels appears in tonic fibres. The properties of these channels are different from those of the channels normally present in innervated tonic fibres but they are in some ways similar to those of the channels which appear in twitch fibres following denervation.