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Motoneurons regulate the central pattern generator during drug-induced locomotor-like activity in the neonatal mouse.

ABSTRACT: Motoneurons are traditionally viewed as the output of the spinal cord that do not influence locomotor rhythmogenesis. We assessed the role of motoneuron firing during ongoing locomotor-like activity in neonatal mice expressing archaerhopsin-3 (Arch), halorhodopsin (eNpHR), or channelrhodopsin-2 (ChR2) in Choline acetyltransferase neurons (ChAT⁺) or Arch in LIM-homeodomain transcription factor Isl1⁺ neurons. Illumination of the lumbar cord in mice expressing eNpHR or Arch in ChAT⁺ or Isl1⁺ neurons, depressed motoneuron discharge, transiently decreased the frequency, and perturbed the phasing of the locomotor-like rhythm. When the light was turned off motoneuron firing and locomotor frequency both transiently increased. These effects were not due to cholinergic neurotransmission, persisted during partial blockade of gap junctions and were mediated, in part, by AMPAergic transmission. In spinal cords expressing ChR2, illumination increased motoneuron discharge and transiently accelerated the rhythm. We conclude that motoneurons provide feedback to the central pattern generator (CPG) during drug-induced locomotor-like activity.

SUBMITTER: Falgairolle M

PROVIDER: S-EPMC5550280 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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Motoneurons regulate the central pattern generator during drug-induced locomotor-like activity in the neonatal mouse.

Falgairolle Melanie M Puhl Joshua G JG Pujala Avinash A Liu Wenfang W O'Donovan Michael J MJ

eLife 20170703

Motoneurons are traditionally viewed as the output of the spinal cord that do not influence locomotor rhythmogenesis. We assessed the role of motoneuron firing during ongoing locomotor-like activity in neonatal mice expressing archaerhopsin-3 (Arch), halorhodopsin (eNpHR), or channelrhodopsin-2 (ChR2) in Choline acetyltransferase neurons (ChAT+) or Arch in LIM-homeodomain transcription factor Isl1+ neurons. Illumination of the lumbar cord in mice expressing eNpHR or ...[more]

PMID: 28671548

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Project description:A fundamental question in comparative neuroethology is the extent to which synaptic wiring determines behavior vs. the extent to which it is constrained by phylogeny. We investigated this by examining the connectivity and activity of homologous neurons in different species. Melibe leonina and Dendronotus iris (Mollusca, Gastropoda, Nudibranchia) have homologous neurons and exhibit homologous swimming behaviors consisting of alternating left-right (LR) whole body flexions. Yet, a homologous interneuron (Si1) differs between the two species in its participation in the swim motor pattern (SMP) and synaptic connectivity. In this study we examined Si1 homologs in two additional nudibranchs: Flabellina iodinea, which evolved LR swimming independently of Melibe and Dendronotus, and Tritonia diomedea, which swims with dorsal-ventral (DV) body flexions. In Flabellina, the contralateral Si1s exhibit alternating rhythmic bursting activity during the SMP and are members of the swim central pattern generator (CPG), as in Melibe The Si1 homologs in Tritonia do not burst rhythmically during the DV SMP but are inhibited and receive bilaterally synchronous synaptic input. In both Flabellina and Tritonia, the Si1 homologs exhibit reciprocal inhibition, as in Melibe However, in Flabellina the inhibition is polysynaptic, whereas in Tritonia it is monosynaptic, as in Melibe In all species, the contralateral Si1s are electrically coupled. These results suggest that Flabellina and Melibe convergently evolved a swim CPG that contains Si1; however, they differ in monosynaptic connections. Connectivity is more similar between Tritonia and Melibe, which exhibit different swimming behaviors. Thus connectivity between homologous neurons varies independently of both behavior and phylogeny.NEW & NOTEWORTHY This research shows that the synaptic connectivity between homologous neurons exhibits species-specific variations on a basic theme. The neurons vary in the extent of electrical coupling and reciprocal inhibition. They also exhibit different patterns of activity during rhythmic motor behaviors that are not predicted by their circuitry. The circuitry does not map onto the phylogeny in a predictable fashion either. Thus neither neuronal homology nor species behavior is predictive of neural circuit connectivity.

Dataset Information

Motoneurons regulate the central pattern generator during drug-induced locomotor-like activity in the neonatal mouse.

Publications

Motoneurons regulate the central pattern generator during drug-induced locomotor-like activity in the neonatal mouse.

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