Conductance changes, an electrogenic pump and the hyperpolarization of leech neurones following impulses

Abstract

Following trains of impulses, sensory neurones in the C.N.S. of the leech show a prolonged hyperpolarization, which lasts for seconds or minutes. In the present investigation the mechanisms that underly this hyperpolarization have been studied by recording intracellularly. Two factors have been found to be responsible. One is the activity of an electrogenic pump (see Baylor & Nicholls, 1969b); the other is a long-lasting change in K conductance. 1. Additional evidence that an electrogenic pump contributes to a slow after-hyperpolarization of leech sensory neurones is provided by the effects of injecting Na intracellularly. This leads to an increase in membrane potential that is blocked by the cardiac glycoside strophanthidin. Furthermore, after a train of impulses, reducing the K concentration in the external fluid characteristically reduces the hyperpolarizing action of the pump. 2. The hyperpolarization following impulses is associated with a reduction of the cell membrane resistance that can persist for several minutes. 3. Several lines of evidence suggest that the reduction in input resistance during the hyperpolarization is mainly due to an increased permeability to K. Thus, when the K concentration in Ringer fluid is reduced, the peak amplitude of the hyperpolarization following a train becomes larger. Furthermore, the conductance dependent part of the after-hyperpolarization has a reversal potential close to the equilibrium potential for K (E_K). Substitution of Cl by SO₄ has little effect either on the after-hyperpolarization or on the conductance change following a train. 4. Increased external Ca concentrations lead to a marked increase in the hyperpolarization that follows impulse activity. The enhanced hyperpolarization in high Ca is associated with a corresponding reduction in input resistance. The amplitude and duration of the hyperpolarization following a brief train of impulses can be increased by a factor of 5 or more in Ringer fluid containing 10 mM-Ca instead of the usual 1·8 mM. The hyperpolarization and resistance changes still occur in solutions containing 20 mM-Mg. 5. To augment the hyperpolarization the increased concentration of Ca must be present during the train of impulses. 6. The relative contributions of the K conductance increase and of the electrogenic pump for generating the hyperpolarization after impulse activity are different in the three types of sensory cell responding to touch, pressure and noxious stimulation.