The Mechanism of Dual Responsiveness in Muscle Fibers of the Grasshopper Romalea microptera

Abstract

Dually innervated Romalea muscle fibers which respond differently to stimulation of their fast and slow axons are excited by intracellularly applied depolarizing stimuli. The responses, though spike-like in appearance, are graded in amplitude depending upon the strength of the stimuli and do not exceed about 30 my. in height. In other respects, however, these graded responses possess properties that are characteristic of electrically excitable activity: vanishingly brief latency; refractoriness; a post-spike undershoofi They are blocked by hyperpolarizing the fiber membrane; respond repetitively to prolonged depolarization, and are subject to depolarizing inactivation. As graded activity, these responses propagate decrementally.The fast and slow axons of the dually responsive muscle fibers initiate respectively large and small postsynaptic potentials (p.s.p.'s) in the muscle fiber. These responses possess properties that characterize electrically inexcitable depolarizing activity. They are augmented by hyperpolarization and diminished by depolarization. Their latency is independent of the membrane potential. They have no refractory period, thus being capable of summation. The fast p.s.p, evokes a considerable or maximal electrically excitable response. The combination, which resembles a spike, leads to a twitch-like contraction of the muscle fiber. The individual slow p.s.p.'s elicit no or only little electrically excitable responses, and they evoke slower smaller contractile responses. The functional aspects of dual responsiveness and the several aspects of the theoretical importance of the gradedly responsive, electrically excitable component are discussed.

The Membrane Components of Crustacean Neuromuscular Systems.

“…The effects of such anatomical complexity on the responses of e.p.s.p. 's during intracellular applied currents have been noted in the diffusely innervated muscle fibers of frog (Burke and Ginsborg, 1956) and grasshopper (Cerf et al, 1959), and might perhaps play a role in other cases (cf. Smith et al, 1965).…”

The Membrane Components of Crustacean Neuromuscular Systems

“…In response to the excitatory postsynaptic potentials (e.p.s.p. 's) or to depolarization by an intracellularly applied current the fibers normally develop only a relatively small graded depolarizing electrogenesis (Fatt and Ginsborg, 1958;, as is also the case in many other arthropod muscles (Cerf et al, 1959;Hagiwara et al, 1964). However, spikes can be elicited after treating the cells with a variety of agents (Fatt and Katz, 1953;Fatt and Ginsborg, 1958;Reuben and Grundfest, 1960 b;Bel ton and Grundfest, 1961 a;Hagiwara and Naka, 1964).…”

“…The methods of dissection and precautions to avoid damage to the preparations have been described earlier (Grundfest et al, 1959;Girardier et al, 1963). The standard bathing media were those of Cole (1941) for lobster and of van Harreveld (1936) for crayfish preparations.…”

“…Inhibitory Synapses Applications of GABA, in concentrations which activate the inhibitory synapses maximally, decrease the membrane resistance of arthropod muscle fibers (Boistel and Fatt, 1958;Grundfest et al, 1959;Usherwood and Grundfest, 1965). In the crayfish muscle fiber the emf of the CI battery, which is involved in the inhibitory electrogenesis, is usually depolarizing with respect to the resting potential.…”

“…The fibers of the walking leg muscles of crayfish and lobster that were used in the present study are each innervated by an excitatory and an inhibitory motor axon (Boistel and Fatt, 1958;Grundfest et al, 1959). Thus, the fibers have two electrogenically and pharmacologically distinctive components of electrically inexcitable, postsynaptic membrane (Grundfest, 1957.…”