Relation of resting potential of rat gastrocnemius and soleus muscles to innervation, activity, and the Na‐K pump

Abstract

The effect of nerve on resting membrane potential of rat muscle was studied. Denervation produces a decline from 83.5mV in gastrocnemius and from 68.8 mV in soleus to a range of 60 mV. The rate of decline is more rapid with distal than with proximal nerve section. With reinnervation, potential returns to normal. Immobilization, posterior rhizotomy or spinal section produces a decline in gastrocnemius membrane potential to about 70 mV indicating that integrity of ventral root does not prevent a fall. Independence of resting potential and muscle fiber size is indicated by work hypertrophy, by near and distant section of nerve and by variation in resting potential for the same degree of atrophy produced by disuse or denervation.Existence of a plateau below which resting potential does not decline following denervation is compatible with the concept of two fractions of normal resting potential maintained by different mechanisms. The higher and more vulnerable is less in soleus than in gastrocnemius. It responds to direct and indirect tetanus with a decline, the low point of which is similar to that which follows nerve section. Direct tetanization o f denervated gastrocnemius muscle affects only the residual of the upper fraction of membrane potential not yet reduced by denervation.Topical or intravenous administration of ouabain produces a decline of resting potential to the range of 60 mV. Following nerve section only the residual portion of "upper fraction" is vulnerable to ouabain. At no time does administration of ouabain produce a fall of mean resting potential below the level achieved by long term nerve section alone.Shortly after the introduction of microelectrode techniques into neurophysiology, evidence was adduced for the existence of two fractions of muscle membrane potential in the sartorius of the frog (Ling and Gerard, '49). The upper or A potential, from 55 to 80 mV, was described as sensitive to tetanus and supported by rnetabolism while the B potential from 0 to 55 mV was 'less directly so." With the advent of better understanding of ionic fluxes and the contribution of the sodium pump to the resting potential, the original observations assume new pertinence. The relation of the fractions of membrane potential to passive ionic distribution across the muscle membrane, to the sodium pump and to innervation warrants further analysis. Denervation is known to cause a decline in resting potential of mammalian muscle (Ware, Bennett and MacIntyre, '54; Lullman and Pracht, '57; Thesleff, '63; Lenman, '65). The mechanism by which this fall is produced remains obscure. Whether it relates to inactivity, muscle fiber size, a J. EXP. ZOOL., 166: 377-386."trophic" Muence of the lower motor neuron, or to the sodium pump has not been evaluated. The current studies were undertaken in the hope of obtaining better inferential information about these relations. METHODSThe gastrocnemius and soleus muscles of the male albino rat were explored by means of 3M-KC1 filled glass micropipettes. Tips of 3 to 20 MQ resista...

Increased sodium pump activity following repetitive stimulation of rat soleus muscles.

“…Earlier experiments had revealed a difficulty in that intraperitoneal injection of this drug in an effective dose caused a progressive depolarization of muscle fibres (cf. Locke & Solomon, 1967) and eventually a loss of excitability. Under these conditions repetitive stimulation would have had uncertain effects on the muscle since an increasing proportion of the fibres would have become unresponsive.…”

“…One explanation for this early enhancement of the M-wave would be that the resting and action potentials of individual muscle fibres increase during muscle activity but this suggestion has not been supported by the results of previous studies in animal muscles. Thus, it has been a general finding that the resting and action potentials of mammalian skeletal muscle fibres decrease following repetitive A. HICKS AND A. J. McCOMAS stimulation (for example, Locke & Solomon, 1967;Hanson, 1974;Juel, 1986), presumably as a result of the rise in interstitial [K+] associated with impulse activity (Hnik, Holas, Krekule, Kriz, Mejsnar, Smiesko, Ujec & Vyskocil, 1976;Juel, 1986). These results are not conclusive, however, since most of the animal experiments have been conducted in vitro, using bathing media likely to cause partial depolarization of muscle fibres with a concomitant rise in intracellular tNa+] (Creese & Northover, 1961;Kernan, 1963).…”

“…Even in in vivo experiments, stimulus-induced depolarization has been reported by Locke & Solomon (1967). In those experiments it is probable that the impulse-MUSCLE SODIUM PUMP mediated K+ efflux caused a fall in EK which could not be compensated for by the electrogenic sodium pump (see below).…”

Modulation of cholinergic proteins and RNA by ouabain in chick muscle cultures

“…Denervation of skeletal muscle increases ACHR levels and sensitivity to acetylcl~oline in all species studied 1231, ACHE levels in at least the chicken and rabbit [24,25] and RNA synthesis in the frog [26]. Ouabain depolarizes skeletal muscle to the same extent as denervation [27] and does not produce any further depolarization of denervated muscle [28,29].…”

The Effect of Sodium Pump Blockade and Denervation on the Steady‐state Sodium Permeability of Mouse Skeletal Muscle Fibres

“…Clausen & Flatman, 1977;Marunaka, 1986). A decrease in the contribution of this rheogenic pump to the resting potential has been suggested as an explanation for the 15-20 mV depolarization of muscle fibres seen after surgical denervation (Locke & Solomon, 1967;Bray, Hawken, Hubbard, Pockett & Wilson, 1976). On theoretical grounds alone (Thomas, 1972), it is most unlikely that an electrogenic pump current could account for 20 mV of an Em (membrane potential) of -80 mV.…”