Modulation of presynaptic action potential kinetics underlies synaptic facilitation of type B photoreceptors after associative conditioning in Hermissenda

Descriptions of conditioned response generation in Hermissenda stipulate th at the synaptic interaction between type B and A photoreceptors should be e nhanced after associative pairings of light and rotation. Although evidence from several laboratories has confirmed this assumption, the mechanism und erlying this synaptic facilitation has not been elucidated. Here we report that in vitro conditioning (i.e., light paired with stimulation of vestibul ar hair cells) modifies the kinetics of presynaptic action potentials in th e B photoreceptor in a manner sufficient to account for this synaptic facil itation. After paired training, we observed an increase in the duration of evoked action potentials and a decrease in the amplitude of the spike after hyperpolarization in the B-cell. As previously reported, paired training al so enhanced the excitability (i.e., input resistance and evoked spike rate) of the B photoreceptor. In a second experiment, simultaneous recordings we re made in type B and A photoreceptors, and paired training was found to pr oduce an increase in the amplitude of the IPSP in the A photoreceptor in re sponse to an evoked spike in the B-cell. Importantly, there was no change i n the initial slope of the postsynaptic IPSP in the A photoreceptor, sugges ting that spike duration-independent mechanisms of neurotransmitter exocyto sis or postsynaptic receptor sensitivity did not contribute to the observed synaptic facilitation. Perfusion of 4-aminopyridine (4-AP) mimicked a know n effect of behavioral conditioning in that it specifically reduced the amp litude of the transient voltage-dependent K+ current (I-A) in the B-cell, b ut in addition, produced action potential broadening and synaptic facilitat ion that was analogous to that observed after in vitro conditioning. Finall y, the effect of 4-AP on B-cell action potentials and on the postsynaptic I PSP in the A-cell was occluded by previous paired (but not unpaired) traini ng, suggesting that the prolongation of the B-cell action potential by a re duction of I-A was sufficient to account for the observed synaptic facilita tion. The occlusion of the effects of 4-AP by paired training was not attri butable to a saturation of the capacity of the B-cell for transmitter exocy tosis, because it was observed that tetraethylammonium (TEA)-induced inhibi tion of the delayed voltage-dependent K+ current induced both spike broaden ing and synaptic facilitation regardless of training history. Collectively, these results demonstrate that training-induced facilitation at B-cell syn apses is attributable to the effects of a reduction of a presynaptic K+ con ductance on action potential kinetics and suggest another critical similari ty between the cellular basis for learning in Hermissenda and other inverte brate systems.