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

Abstract

Mechanical and neurophysiological anisotropies mediate threedimensional responses of the heart of Homarus americanus. Although hearts in vivo are loaded multi-axially by pressure, studies of invertebrate cardiac function typically use uniaxial tests. To generate whole-heart length-tension curves, stretch pyramids at constant lengthening and shortening rates were imposed uniaxially and biaxially along longitudinal and transverse axes of the beating whole heart. To determine whether neuropeptides that are known to modulate cardiac activity in H. americanus affect the active or passive components of these length-tension curves, we also performed these tests in the presence of SGRNFLRFamide (SGRN) and GYSNRNYLRFamide (GYS). In uniaxial and biaxial tests, both passive and active forces increased with stretch along both measurement axes. The increase in passive forces was anisotropic, with greater increases along the longitudinal axis. Passive forces showed hysteresis and active forces were higher during lengthening than shortening phases of the stretch pyramid. Active forces at a given length were increased by both neuropeptides. To exert these effects, neuropeptides might have acted indirectly on the muscle via their effects on the cardiac ganglion, directly on the neuromuscular junction, or directly on the muscles. Because increases in response to stretch were also seen in stimulated motor nerve-muscle preparations, at least some of the effects of the peptides are likely peripheral. Taken together, these findings suggest that flexibility in rhythmic cardiac contractions results from the amplified effects of neuropeptides interacting with the length-tension characteristics of the heart.

The neural control of heartbeat in invertebrates

“…The neuropeptide work [2–4], in the American Lobster, illustrates the complex nature of neuromodulation when operating on multiple components of the multilayered neuromuscular system: interneurons (SCs) and motor neurons (LCs), the neuromuscular junctions (NMJs) and muscles, and importantly feedback systems. Both SCs and LCs have stretch sensitive dendrites on the heart, which feedback positively to decrease cycle period [5], and both SCs and LCs are modulated by NO released by heart muscle during contraction, which slows their burst period [6].…”

Cloning of the first cDNA encoding a putative CCRFamide precursor: identification of the brain, eyestalk ganglia, and cardiac ganglion as sites of CCRFamide expression in the American lobster, Homarus americanus

“…If so, the peptide could be delivered via the circulatory system to a diverse array of potential targets. The presence of CCRFamide in the CG suggests a potential role in modulating cardiac output, a role played by a number of -RFamide-containing peptides in H. americanus (Dickinson et al, 2015(Dickinson et al, , 2016Stevens et al, 2009).…”

“…Drosophila melanogaster) typically employed for functional studies (Veenstra, 2019). However, given that the neural circuit contained within the CG, the neuromuscular junction between the ganglion and cardiac muscle, and the muscle itself are all potential targets for CCRFamide modulation (e.g., Dickinson et al, 2015Dickinson et al, , 2016Fort et al, 2007aFort et al, , 2007bStevens et al, 2009), additional transcriptomic studies may provide insights into CCRFamide function and receptor elucidation. nervous system-specific transcriptomic data.…”

Neuropeptide modulation of pattern-generating systems in crustaceans: comparative studies and approaches

“…When the whole heart is stretched in either the longitudinal or transverse direction, contraction amplitude increases; the extent of this increase is enhanced by the FLPs [50]. Interestingly, this effect is anisotropic; that is, GYSNRNYLRFamide enhanced amplitude only to transverse stretch, while SGRNFLRFamide increased the effects of longitudinal stretch.…”