Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours

Abstract

Closely related species can exhibit different behaviours despite homologous neural substrates. The nudibranch molluscsTritonia diomedeaandMelibe leoninaswim differently, yet their nervous systems contain homologous serotonergic neurons. InTritonia, the dorsal swim interneurons (DSIs) are members of the swim central pattern generator (CPG) and their neurotransmitter serotonin is both necessary and sufficient to elicit a swim motor pattern. Here it is shown that the DSI homologues inMelibe, the cerebral serotonergic posterior-A neurons (CeSP-As), are extrinsic to the swim CPG, and that neither theCeSP-As nor their neurotransmitter serotonin is necessary for swim motor pattern initiation, which occurred when theCeSP-As were inactive. Furthermore, the serotonin antagonist methysergide blocked the effects of both the serotonin andCeSP-As but did not prevent the production of a swim motor pattern. However, theCeSP-As and serotonin could influence theMelibeswim circuit; depolarization of a cerebral serotonergic posterior-A was sufficient to initiate a swim motor pattern and hyperpolarization of aCeSP-A temporarily halted an ongoing swim motor pattern. Serotonin itself was sufficient to initiate a swim motor pattern or make an ongoing swim motor pattern more regular. Thus, evolution of species-specific behaviour involved alterations in the functions of identified homologous neurons and their neurotransmitter.