Necessary, sufficient and permissive: A single locomotor command neuron important for intersegmental coordination

In this report we posed the overarching question: What multiple contributions can a single neuron have on controlling the behavior of an animal, especially within a given context? To address this timely question, we studied the neuron R3b-1 in the medicinal leech. This bilaterally paired neuron descends from the cephalic ganglion and projects uninterrupted through the segmental ganglia comprising the nerve cord; its terminal arbors invade each hemi-ganglion. We discovered that a single R3b-1 neuron functions as a command neuron in the strictest sense, as it was both necessary and sufficient for fictive crawling behavior. Aside from these command-related properties, we determined that R3b-1 modulates the cycle period of crawl motor activity. R3b-1 has previously been shown to activate swimming behavior, but when the CNS was exposed to dopamine (DA), crawling became the exclusive locomotor pattern produced by R3b-1. DA exposure also led to bursting in R3b-1 that matched periods observed during fictive crawling, even when potential ascending inputs from crawl oscillators were removed. Although the above attributes render R3b-1 an intriguing cell, it is its ability to permit the coordination of the segmentally distributed crawl oscillators that makes this multifunctional neuron so notable. To our knowledge, this cell provides the first biological example of a single command neuron that is also vital for the intersegmental coordination of a locomotor behavior. Furthermore, our study highlights the importance of DA as an internal contextual cue that can integrate functional layers of the nervous system for adaptive behavior.