Serotonin modulates muscle function in the medicinal leechHirudo verbana

Abstract

The body wall muscles of sanguivorous leeches power mechanically diverse behaviours: suction feeding, crawling and swimming. These require longitudinal muscle to exert force over an extremely large length range, from 145 to 46 per cent of the mean segmental swimming length. Previous data, however, suggest that leech body wall muscle has limited capacity for force production when elongated. Serotonin (5-HT) alters the passive properties of the body wall and stimulates feeding. We hypothesized that 5-HT may also have a role in allowing force production in elongated muscle by changing the shape of the length -tension relationship (LTR). LTRs were measured from longitudinal muscle strips in vitro in physiological saline with and without the presence of 10 mM 5-HT. The LTR was much broader than previously measured for leech muscle. Rather than shifting the LTR, 5-HT reduced passive muscle tonus and increased active stress at all lengths. In addition to modulating leech behaviour and passive mechanical properties, 5-HT probably enhances muscle force and work production during locomotion and feeding.

Serotonin as an integrator of leech behavior and muscle mechanical performance

“…It can exert force across a much wider range of lengths than vertebrate, cross-striated muscle (Miller, 1975;Milligan et al, 1997;Gerry and Ellerby, 2011), likely through the shearing of adjacent myosin filaments (Rosenbluth, 1967;Lanzavecchia et al, 1985;D'Haese and Ditgens, 1987). Therefore, this muscle type can drive movements that require extremely high muscle strains.…”

“…Body wall muscle strips maintain substantial passive tension (Tian et al, 2007;Gerry and Ellerby, 2011), and when stimulated a persistent tonus can elevate stress levels for over 30 s post-stimulation (Miller and Aidley, 1973;Gerry and Ellerby, 2011). Persistent residual forces mean that substantial work would have to be done by antagonistic muscle layers or muscle in adjacent body segments to elongate muscle fibers that drive cyclical movements.…”

“…Therefore, this muscle type can drive movements that require extremely high muscle strains. For example, the obliquely striated body wall musculature of sanguivorous leeches powers both suction feeding, during which leeches may undergo a tenfold increase in volume (Lent et al, 1988;Claflin et al, 2009), and locomotion which can involve threefold changes in body length (Stern-Tomlinson et al, 1986;Gerry and Ellerby, 2011).…”

The length-force behavior and operating length range of squid muscle varies as a function of position in the mantle wall

“…Using leeches as a model, they provided morphological evidence that overlap between the thick and thin filaments of the longitudinal body wall muscles is maintained over a fivefold increase in body length. Gerry and Ellerby (Gerry and Ellerby, 2011) showed recently that the longitudinal fibers of the body wall of the medicinal leech (Hirudo verbena) operated solely on the descending limb of the length-tension curve at very long muscle lengths during swimming and feeding. In the presence of serotonin, the longitudinal fibers produced relatively high forces (≥0.5P 0 ) at muscle lengths of nearly 2.5L 0 .…”

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

“…However, at least some of the increase seen in the stimulated heart with SGRN is likely a direct effect of the neuropeptide on the muscle because there is some increase in pre-stretch transverse passive force even in the absence of the CG. To our knowledge, this is the first report of a significant effect of neuroactive compounds on passive muscle properties in crustaceans; however, serotonin has been shown to decrease passive muscle tension in leeches (Gerry and Ellerby, 2011;Gerry et al, 2012). Because passive forces at low extensions are dominated by titin, perhaps neuropeptides affect titin function in lobster cardiomyocytes.…”