Distinct Neural Circuits Control Rhythm Inhibition and Spitting by the Myogenic Pharynx of C. elegans
Author(s)
Bhatla, Nikhil; Droste, Rita; Sando, Steven Robert; Huang, Anne; Horvitz, Howard Robert
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Neural circuits have long been known to modulate myogenic muscles such as the heart, yet a mechanistic understanding at the cellular and molecular levels remains limited. We studied how light inhibits pumping of the Caenorhabditis elegans pharynx, a myogenic muscular pump for feeding, and found three neural circuits that alter pumping. First, light inhibits pumping via the I2 neuron monosynaptic circuit. Our electron microscopic reconstruction of the anterior pharynx revealed evidence for synapses from I2 onto muscle that were missing from the published connectome, and we show that these “missed synapses” are likely functional. Second, light inhibits pumping through the RIP-I1-MC neuron polysynaptic circuit, in which an inhibitory signal is likely transmitted from outside the pharynx into the pharynx in a manner analogous to how the mammalian autonomic nervous system controls the heart. Third, light causes a novel pharyngeal behavior, reversal of flow or “spitting,” which is induced by the M1 neuron. These three neural circuits show that neurons can control a myogenic muscle organ not only by changing the contraction rate but also by altering the functional consequences of the contraction itself, transforming swallowing into spitting. Our observations also illustrate why connectome builders and users should be cognizant that functional synaptic connections might exist despite the absence of a declared synapse in the connectome.
Date issued
2015-07Department
Massachusetts Institute of Technology. Department of Biology; Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences; McGovern Institute for Brain Research at MITJournal
Current Biology
Publisher
Elsevier
Citation
Bhatla, Nikhil; Droste, Rita; Sando, Steven R.; Huang, Anne and Horvitz, H. Robert. “Distinct Neural Circuits Control Rhythm Inhibition and Spitting by the Myogenic Pharynx of C. Elegans.” Current Biology 25, no. 16 (August 2015): 2075–2089. © 2015 Elsevier Ltd
Version: Author's final manuscript
ISSN
0960-9822
1879-0445