1. The ionic conductances underlying some of the electrophysiological properties of multiply innervated or tonic fibres of rat extraocular muscles were examined in vitro with double-barrelled micro-electrodes.2. Exposure of the muscle to a Cl-free saline did not change the effective resistance (R(eff)) of tonic fibres which was 5.14 +/- 0.45 MOmega (n = 7) in control saline and 4.78 +/- 0.45 MOmega (n = 12) in Cl-free saline (P > 0.1). In contrast, in singly innervated or twitch fibres Cl removal increased R(eff) from 1.77 +/- 0.21 MOmega (n = 19) to 2.69 +/- 0.12 MOmega (n = 22) (P < 0.001).3. Tonic fibres with membrane potentials restored to - 80 mV by injecting current responded to intracellular depolarizing pulses with a brief, slow response (slow peak potential) which added to the rising phase of the electrotonic potential. The slow peak potential began at a membrane potential of - 40 to - 35 mV and was graded. Increasing depolarizations evoked faster and larger responses which did not over-shoot the zero level of membrane potential.4. The slow peak potential was not blocked by 10 muM-D-600 hydrochloride but was markedly reduced by the absence of Na and by 10 muM-tetrodotoxin. The response was broadened about five times by 25 mM-tetraethylammonium.5. Raising bath temperature from 21-25 degrees C to 37 degrees C reversibly depressed and shortened the slow peak potential but did not transform it into an action potential.6. It is concluded that the characteristic high R(eff) of tonic fibres results from a lack of a membrane conductance to Cl and that the slow peak potential involves the transient activation of Na and K channels which are pharmacologically similar to the respective channels of twitch fibres.