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Journal of Experimental Biology partnership with Dryad

Coordination of distinct but interacting rhythmic motor programs by a modulatory projection neuron using different co-transmitters in different ganglia
Molly A. Kwiatkowski, Emily R. Gabranski, Kristen E. Huber, M. Christine Chapline, Andrew E. Christie, Patsy S. Dickinson

SUMMARY

While many neurons are known to contain multiple neurotransmitters, the specific roles played by each co-transmitter within a neuron are often poorly understood. Here, we investigated the roles of the co-transmitters of the pyloric suppressor (PS) neurons, which are located in the stomatogastric nervous system (STNS) of the lobster Homarus americanus. The PS neurons are known to contain histamine; using RT-PCR, we identified a second co-transmitter as the FMRFamide-like peptide crustacean myosuppressin (Crust-MS). The modulatory effects of Crust-MS application on the gastric mill and pyloric patterns, generated in the stomatogastric ganglion (STG), closely resembled those recorded following extracellular PS neuron stimulation. To determine whether histamine plays a role in mediating the effects of the PS neurons in the STG, we bath-applied histamine receptor antagonists to the ganglion. In the presence of the antagonists, the histamine response was blocked, but Crust-MS application and PS stimulation continued to modulate the gastric and pyloric patterns, suggesting that PS effects in the STG are mediated largely by Crust-MS. PS neuron stimulation also excited the oesophageal rhythm, produced in the commissural ganglia (CoGs) of the STNS. Application of histamine, but not Crust-MS, to the CoGs mimicked this effect. Histamine receptor antagonists blocked the ability of both histamine and PS stimulation to excite the oesophageal rhythm, providing strong evidence that the PS neurons use histamine in the CoGs to exert their effects. Overall, our data suggest that the PS neurons differentially utilize their co-transmitters in spatially distinct locations to coordinate the activity of three independent networks.

FOOTNOTES

  • AUTHOR CONTRIBUTIONS

    M.A.K., E.R.G., K.E.H., M.C.C., A.E.C. and P.S.D. were involved in the conception, design and execution of the study and the interpretation of findings. M.A.K., A.E.C. and P.S.D. drafted and revised the article.

  • COMPETING INTERESTS

    No competing interests declared.

  • FUNDING

    This project was supported by a grant from the Arnold and Mabel Beckman Foundation, by National Science Foundation award 1121973 from the division of Integrative Organismal Systems, by the National Center for Research Resources (award 5P20RR016463-12) and the National Institute of General Medical Sciences (award 8 P20 GM103423-12) from the National Institutes of Health, and by the Cades Foundation of Honolulu, Hawaii. Deposited in PMC for release after 12 months.

  • LIST OF ABBREVIATIONS

    CG
    cardiac ganglion
    CoG
    commissural ganglion
    CPG
    central pattern generator
    dlvn
    dorsal lateral ventricular nerve
    GM
    gastric mill neuron
    HA
    histamine
    ion
    inferior oesophageal nerve
    ivn
    inferior ventricular nerve
    LG
    lateral gastric neuron
    LP
    lateral pyloric neuron
    MPN
    modulatory proctolin neuron
    mvn
    medial ventricular nerve
    OD1
    oesophageal dilator 1 neuron
    OG
    oesophageal ganglion
    PD
    pyloric dilator neuron
    PS
    pyloric suppressor neuron
    PY
    pyloric neuron
    pyn
    pyloric nerve
    RT-PCR
    reverse transcriptase-polymerase chain reaction
    son
    superior oesophageal nerve
    STG
    stomatogastric ganglion
    stn
    stomatogastric nerve
    STNS
    stomatogastric nervous system
    VD
    ventral dilator neuron
    vlvn
    ventral lateral ventricular nerve
    vpdn
    ventral pyloric dilator nerve
    vpon
    ventral posterior oesophageal nerve
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