Necessary, Sufficient and Permissive: A Single Locomotor Command Neuron Important for Intersegmental Coordination

Abstract

In this report we posed the over-arching 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.

Command or Obey? Homologous Neurons Differ in Hierarchical Position for the Generation of Homologous Behaviors

“…For example, brainstem neurons provide commands to locomotor central pattern generators (CPGs) in the spinal cord (Dubuc et al, 2008;Roberts et al, 2008;Kiehn, 2016). Similarly, in invertebrates, commands for locomotion and feeding come from neurons outside of the CPG and often in other ganglia (Gillette et al, 1982;Gamkrelidze et al, 1995;Panchin et al, 1995;Frost and Katz, 1996;Stein, 2009;Puhl et al, 2012). Here, we show that the hierarchical position of a neuron differs in two species even though the neuron is involved in the production of the same behavior in those species.…”

Multiplexed modulation of behavioral choice

“…Filled circles indicate inhibitory interactions; filled arrowheads with plus signs indicate excitatory interactions. DA indicates bath-application of dopamine; the X indicates that DA inhibits the pathway to the swim CPG; the DA also activates the crawl CPG (Puhl et al, 2012). Modified from Esch et al has no impact on the CS (an effect not shown in Fig.…”

“…Caenorhabditis elegans also uses dopamine and serotonin to set the balance between these two locomotory behaviors (Vidal-Gadea et al, 2011). Recently it has been discovered that, in the leech, systemically applied dopamine induces R3b1 to burst in a manner consistent with crawling and constrains the entire central nervous system to crawl only (never swim) when R3b1 is electrically stimulated (Puhl et al, 2012). A strategy of employing neuromodulators to encode an environmental context that would naturally be relatively unchanging, such as water depth, would be consistent with our observation [also seen by Esch et al ] that leeches poke their heads above water when first introduced to a new environment (and only occasionally after that).…”

“…They are 'command-like' neurons for locomotion Puhl et al, 2012) that respond in a distinctly location-specific manner: stimulating the posterior of the leech (which gives rise to swimming or crawling) activates them and anterior stimulation (which gives rise to shortening) inhibits them. The effect of activating R3b1 cells is influenced by the animal's environment: stimulating an R3b1 cell usually elicits crawling rather than swimming when a nearly intact leech is in shallow water, but the same R3b1 cell activation elicits mostly swimming when the leech is in deep water Puhl and Mesce, 2010).…”

Some recent advances in spider sensory physiology

“…Biogenic amine modulators like dopamine and serotonin, which act at both the segmental and cephalic levels, predictably influenced the type of locomotion expressed in isolated CNS preparations. Finally, signaling from a multifunctional identified descending cephalic neuron onto cells housed in the segmental ganglia (named R3b-1) is both necessary and sufficient for crawling but only activates and modulates swimming (it is not necessary for swimming; Puhl et al 2012). These results and others like them have inspired new projects where investigators are probing how higher-order, decision-making cephalic neurons interact with segmental locomotor circuits as well as how neuromodulators influence their interactions.…”