Differential neuropeptide modulation of premotor and motor neurons in the lobster cardiac ganglion

Authors: OLEISKY, EMILY - Bowdoin College; STANHOPE, MEREDITH - Bowdoin College; Hull, Joe; CHRISTIE, ANDREW - University Of Hawaii; DICKINSON, PATSY - Bowdoin College

Submitted to: Journal of Clinical Neurophysiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/4/2020
Publication Date: 10/23/2020
Citation: Oleisky, E., Stanhope, M., Hull, J.J., Christie, A., Dickinson, P. 2020. Differential neuropeptide modulation of premotor and motor neurons in the lobster cardiac ganglion. Journal of Clinical Neurophysiology. 124:1241-1256. https://doi.org/10.1152/jn.00089.2020.
DOI: https://doi.org/10.1152/jn.00089.2020

Interpretive Summary: The crustacean cardiac neuromuscular system has been developed as a model system for understanding the modulatory control of rhythmic motor behavior (e.g. walking, running, breathing, etc). An example of a central pattern generator-effector system in crustaceans is cardiac ganglion (pattern generator) activation of heart musculature (effector). The cardiac ganglion in the American lobster consists of nine neurons: four small premotor neurons and five larger motor neurons. The two types of cells are typically linked both electrically and chemically. However, when they are unlinked, application of the cardioactive peptide, myosuppressin, triggers different activities in the two cell types. The results suggest that the motor neurons influence activity frequency, whereas the premotor neurons affect the duration of activity. Although multiple myosuppressin receptors were identified in various lobster tissues, there appeared to be differential expression in the premotor and motor neurons for three of the receptors. This selective expression may account for the different activity patterns generated in the two cell types by application of the same peptide (i.e. myosuppressin). These findings provide potential insights into the development of rhythmic motor behavior and can be used to guide future studies into the physiological roles of myosuppressin.

Technical Abstract: The American lobster, Homarus americanus, cardiac neuromuscular system is controlled by the cardiac ganglion (CG), a central pattern generator consisting of four premotor and five motor neurons. Here, we show that the premotor and motor neurons can establish independent bursting patterns when decoupled by a physical ligature. We also show that mRNA encoding myosuppressin, a cardioactive neuropeptide, is produced within the CG. We thus asked whether myosuppressin modulates the decoupled premotor and motor neurons, and if so, how this modulation might underlie the role(s) that these neurons play in myosuppressin’s effects on ganglionic output. Although myosuppressin exerted dose-dependent effects on burst frequency and duration in both premotor and motor neurons in the intact CG, its effects on the ligatured ganglion were more complex, with different effects and thresholds on the two types of neurons. These data suggest that the motor neurons are more important in determining the changes in frequency of the CG elicited by low concentrations of myosuppressin, whereas the premotor neurons have a greater impact on changes elicited in burst duration. A single putative myosuppressin receptor (MSR-I) was previously described from the Homarus nervous system. We identified four additional putative MSRs (MSR-II–V) and investigated their individual distributions in the CG premotor and motor neurons using RT-PCR. Transcripts for only three receptors (MSR-II–IV) were amplified from the CG. Potential differential distributions of the receptors were observed between the premotor and motor neurons; these differences may contribute to the distinct physiological responses of the two neuron types to myosuppressin.