Actor or Director? Homologous Neurons Differ in Hierarchical Position for the Generation of Homologous Behaviors

Abstract

Nervous systems are hierarchically organized; higher order neurons provide commands to central pattern generators (CPGs), which autonomously produce rhythmic motor patterns. Such hierarchies are generally thought to be inherent in the structure of nervous systems. Here, however, we report that a neuron that is a CPG member in one species acts as a higher order neuron in another species in the production of a homologous motor behavior. In the nudibranch mollusc, Melibe leonina, swim interneuron 1 (Si1) is in the CPG underlying swimming, firing bursts in phase with the motor pattern. In contrast, its homolog in another nudibranch, Dendronotus iris, serves as a neuromodulatory command neuron for the CPG of a homologous swimming behavior. In Dendronotus, Si1 fired irregularly throughout the swim motor pattern. The burst and firing frequencies of Dendronotus swim CPG neurons correlated with the firing frequency of Si1. Si1 activity was both necessary and sufficient for the initiation and maintenance of the swim motor pattern. Each Si1 was electrically coupled to all of the CPG neurons and made monosynaptic excitatory synapses with both Si3s. Si1 also potentiated the excitatory synapses from Si3 to Si2. Artificial synaptic enhancement of the Si3‐to‐Si2 synapses using dynamic clamp combined with depolarization of Si3s mimicked the effects of Si1 stimulation on the swim motor pattern. Thus, in Dendronotus, Si1 is a command neuron that turns on, maintains, and accelerates the motor pattern through synaptic and neuromodulatory actions, thereby differing from its homolog in Melibe in its hierarchical position in the motor system.