Related neuropeptides use different balances of unitary mechanisms to modulate the cardiac neuromuscular system in the American lobster,Homarus americanus

Abstract

To produce flexible outputs, neural networks controlling rhythmic motor behaviors can be modulated at multiple levels, including the pattern generator itself, sensory feedback, and the response of the muscle to a given pattern of motor output. We examined the role of two related neuropeptides, GYSDRNYLRFamide (GYS) and SGRNFLRFamide (SGRN), in modulating the neurogenic lobster heartbeat, which is controlled by the cardiac ganglion (CG). When perfused though an isolated whole heart at low concentrations, both peptides elicited increases in contraction amplitude and frequency. At higher concentrations, both peptides continued to elicit increases in contraction amplitude, but GYS caused a decrease in contraction frequency, while SGRN did not alter frequency. To determine the sites at which these peptides induce their effects, we examined the effects of the peptides on the periphery and on the isolated CG. When we removed the CG and stimulated the motor nerve with constant bursts of stimuli, both GYS and SGRN increased contraction amplitude, indicating that each peptide modulates the muscle or the neuromuscular junction. When applied to the isolated CG, neither peptide altered burst frequency at low peptide concentrations; at higher concentrations, SGRN decreased burst frequency, whereas GYS continued to have no effect on frequency. Together, these data suggest that the two peptides elicit some of their effects using different mechanisms; in particular, given the known feedback pathways within this system, the importance of the negative (nitric oxide) relative to the positive (stretch) feedback pathways may differ in the presence of the two peptides. cardiac ganglion; FMRFamide-like peptide; feedback ADAPTIVE RHYTHMIC BEHAVIOR is determined not only by the output of the nervous system, but also by the interactions of the nervous system with the periphery. Output from the nervous system is transformed into movement at the level of the muscles by way of the neuromuscular transform (Brezina et al. 2000a(Brezina et al. , 2000bBrezina and Weiss 2000;Williams et al. 2013); the resulting movements determine the level and nature of feedback from the periphery, which can in turn affect the output of the nervous system. Thus the generation of rhythmic movements is determined by the integration of activity, inputs, and interactions of multiple components of the multilayered neuromuscular system: the central pattern generator (CPG) and motor neurons, the neuromuscular junctions (NMJs) and muscles, and feedback systems.

Forces generated during stretch in the heart of the lobsterHomarus americanusare anisotropic and are altered by neuromodulators

“…The signals from the force transducers were amplified by a Model 44 Brownlee Precision Instrumentation amplifier and recorded with a Cambridge Electronic Design (CED) Micro 1401 digitizer paired with Spike2 version 7.03 software (CED, Cambridge, UK). The output of the force transducer is reported in grams rather than Newtons for consistency with other studies that have studied single locations on the length-tension curve (Fort et al, 2004(Fort et al, , 2007aStevens et al, 2009;Christie et al, 2010b;Dickinson et al, 2015).…”

“…The concentrations of SGRN (10 −9 mol l −1 ) and GYS (5×10 −10 mol l −1 ) were selected as the lowest concentrations that consistently produced a significant increase in contraction amplitude and frequency (Dickinson et al, 2015).…”

“…Immediately after the final stretch pyramid, the peptide was washed from the heart for 1 h with physiological saline; previous work has shown that the effects of GYS and SGRN generally wash out after approximately 20 min (see fig. 1A in Dickinson et al, 2015). Baseline passive force was readjusted if necessary.…”

“…Neuropeptides, including SGRN and GYS, can exert modulatory effects at several locations within the cardiac neuromuscular system, including the CG and the cardiac muscle or neuromuscular junction (Dickinson et al, 2015). To eliminate effects of the peptides on ganglionic output and record the responses of the periphery (muscle/ neuromuscular junction) to peptides, the CG was removed from the whole heart, while the motor nerves remained intact.…”

“…Although the effects of neuromodulators on crustacean CPGeffector systems are well documented, these studies have only examined the physiological effects at single locations on the lengthtension curve (Mercier and Russenes, 1992;Fort et al, 2004;Wilkens et al, 2005;Fort et al, 2007a,b;Stevens et al, 2009;Christie et al, 2010b;Dickinson et al, 2015). However, it is important to consider the functional space in which the neurotransmitters are working.…”