Evidence that the Central Pattern Generator for Swimming in Tritonia Arose from a Non-Rhythmic Neuromodulatory Arousal System: Implications for the Evolution of Specialized Behavior1

Abstract

Comparisons of the nervous systems of closely related invertebrate species show that identified neurons tend to be highly conserved even though the behaviors in which they participate vary. All opisthobranch molluscs examined have a similar set of serotonin-immunoreactive neurons located medially in the cerebral ganglion. In a small number of species, these neurons have been physiologically and morphologically identified. In the nudibranch, Tritonia diomedea, three of the neurons (the dorsal swim interneurons, DSIs) have been shown to be members of the central pattern generator (CPG) underlying dorsal/ventral swimming. The DSIs act as intrinsic neuromodulators, altering cellular and synaptic properties within the swim CPG circuit. Putative homologues of the DSIs have been identified in a number of other opisthobranchs. In the notaspid, Pleurobranchaea californica, the apparent DSI homologues (As1–3) play a similar role in the escape swim and they also have widespread actions on other systems such as feeding and ciliary locomotion. In the gymnosomatid, Clione limacina, the presumed homologous neurons (Cr-SP) are not part of the swimming pattern generator, which is located in the pedal ganglia, but act as extrinsic modulators, responding to noxious stimuli and increasing the frequency of the swim motor program. Putative homologous neurons are also present in non-swimming species such as the anaspid, Aplysia californica, where at least one of the cerebral serotonergic neurons, CC3 (CB-1), evokes neuromodulatory actions in response to noxious stimuli. Thus, the CPG circuit in Tritonia appears to have evolved from the interconnections of neurons that are common to other opisthobranchs where they participate in arousal to noxious stimuli but are not rhythmically active.