Cyclic Guanosine Monophosphate Modulates Locomotor Acceleration Induced by Nitric Oxide but not Serotonin in Clione limacina Central Pattern Generator Swim Interneurons

Typically, the marine mollusk, Clione limacina, exhibits a slow, hovering locomotor gait to maintain its position in the water column. However, the animal exhibits behaviorally relevant locomotor swim acceleration during escape response and feeding behavior. Both nitric oxide and serotonin mediate this behavioral swim acceleration. In this study, we examine the role that the second messenger, cGMP, plays in mediating nitric oxide and serotonin-induced swim acceleration. We observed that the application of an analog of cGMP or an activator of soluble guanylyl cyclase increased fictive locomotor speed recorded from Pd-7 interneurons of the animal’s locomotor central pattern generator. Moreover, inhibition of soluble guanylyl cyclase decreased fictive locomotor speed. These results suggest that basal levels of cGMP are important for slow swimming and that increased production of cGMP mediates swim acceleration in Clione. Because nitric oxide has its effect through cGMP signaling and because we show herein that cGMP produces cellular changes in Clione swim interneurons that are consistent with cellular changes produced by serotonin application, we hypothesize that both nitric oxide and serotonin function via a common signal transduction pathway that involves cGMP. Our results show that cGMP mediates nitric oxide-induced but not serotonin-induced swim acceleration in Clione.

The Swimming Circuit in the Pteropod Mollusk Clione limacina

The pelagic marine mollusk Clione limacina (class Gastropoda, subclass Opisthobranchaea, order Pteropoda), 3–5 cm in length, swims by rhythmically moving (1–2-Hz) two winglike appendages. Each swim cycle consists of two phases—the dorsal (D) and ventral (V) wing flexions. The nervous system of Clione consists of five pairs of ganglia. The wing movements are controlled by the pedal ganglia giving rise to the wing nerves. The neuronal circuit of the swim central pattern generator (CPG) is located in the pedal ganglia, which is able to generate the basic pattern of rhythmic activity after isolation from the organism (fictive swimming). Approximately 120 pedal neurons exhibit rhythmic activity during fictive swimming. According to their morphology, rhythmic neurons are divided into motoneurons (MNs), with axons exiting via the wing nerves to wing muscles, and interneurons (INs), with axons projecting to the contralateral ganglion.