The Journal of Neurophysiology Vol. 77 No. 4 April 1997, pp. 1861-1888
Copyright ©1997 The American Physiological Society

Ionic Basis of Learning-Correlated Excitability Changes in Hermissenda Type A Photoreceptors

Joseph Farley and Yunru Han

Programs in Neural Science and Biochemistry, Indiana University, Bloomington, Indiana 47405

Farley, Joseph and Yunru Han. Ionic basis of learning-correlated excitability changes in Hermissenda type A photoreceptors. J. Neurophysiol. 77: 1861-1888, 1997. 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 µM 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 ~60-150% in both lateral and medial cells and thus contributes to the conditioning-associated increase in I_Delayed.

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