Ionic basis of learning-correlated excitability changes in Hermissenda type A photoreceptors

Repeated pairings of light and rotation (conditioning) result in persistent changes in excitability of Hermissenda type B and A photoreceptors, which are correlated with pairing-specific reductions in phototactic behavior. Although considerable attention has been devoted to characterization of conditioning-produced neurophysiological changes that occur in type B cells, less information is available concerning the changes produced in type A cells. Here we recorded from identified, synaptically isolated lateral and medial type A photoreceptors from conditioned, random-control, or untrained animals on retention days following conditioning. Type A photoreceptors from conditioned animals responded to light with a receptor potential that was significantly smaller than those of random-control or untrained animals, which did not differ. The phototactic suppression and type A cell light response magnitudes were negatively correlated for individual conditioned animals. Animals exhibiting strong phototactic suppression also showed small light responses. Expression of the training-associated light response difference was a calcium-dependent phenomenon: reducing extracellular calcium to < 1 microM enhanced the generator potential of A cells, regardless of conditioning history, and greatly reduced the differences in generator potential amplitude attributable to training. Voltage-clamp studies revealed that conditioning resulted in a two- to threefold increase in the amplitude of a voltage-dependent, sustained outward K+ current (I(Delayed)). I(Delayed) magnitudes were positively correlated with phototactic suppression for individual conditioned animals: type A cells of animals exhibiting strong phototactic suppression expressed large values of I(Delayed). I(Delayed) is a composite current, consisting of at least three separable components: 1) residual A current (I(A)); 2) slow, tetraethylammonium-sensitive calcium-activated K+ current (I(K-Ca)); and 3) a delayed-rectifier-type, voltage-dependent K+ current (I(K,v)). Analysis of these currents failed to reveal significant training-associated changes in I(A) or I(K-Ca). But I(K,v) was enhanced by approximately 60-150% in both lateral and medial cells and thus contributes to the conditioning-associated increase in I(Delayed).