Tongues, tentacles and trunks: the biomechanics of movement in muscular-hydrostats

Abstract

Muscular-hydrostats, muscular organs which lack typical systems of skeletal support, include the tongues of mammals and lizards, the arms and tentacles of cephalopod molluscs and the trunks of elephants. In this paper the means by which such organs produce elongation, shortening, bending and torsion are discussed. The most important biomechanical feature of muscular-hydrostats is that their volume is constant, so that any decrease in one dimension will cause a compensatory increase in at least one other dimension. Elongation of a muscular-hydrostat is produced by contraction of transverse, circular or radial muscles which decrease the cross-section. Shortening is produced by rontraction of longitudinal muscles. The relation between length and width of a constant volume structure allows amplification of muscle force or displacement in muscular-hydrostats and other hydrostatic systems. Bending requires simultaneous contraction of longitudinal and antagonistic circular, transverse or radial muscles. In bending, one muscle mass acts as an effector of movement while the alternate muscle mass provides support for that movement. Torsion is produced by contraction of muscles which wrap the muscular-hydrostat in a helical fashion.

Three‐dimensional myoarchitecture of the bovine tongue demonstrated by diffusion spectrum magnetic resonance imaging with tractography

“…From a mechanical perspective, the tongue is believed to fall into a class of organs known as a muscular hydrostat, an organ whose musculature both creates motion and supplies the skeletal support for that motion (Kier and Smith, 1985;Smith and Kier, 1989;Napadow et al, 1999Napadow et al, , 2002. Such organs characteristically are isovolemic, i.e., maintain their volume while undergoing various changes of shape and form, and are composed of complex fiber arrays aligned at angles orthogonal to the direction of deformation.…”

Differential effects of targeted tongue exercise and treadmill running on aging tongue muscle structure and contractile properties

“…Thus, a promising translational pathway for tongue exercise may be through a route that upregulates breathing, such as treadmill running. Because the tongue is a muscular hydrostat with an interdigitated muscle fiber orientation, there may be a variety of muscle activation patterns to accomplish the same movement goal (8,31). This suggests that, for the tongue, exercise training may not need to be as specific.…”

Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation

“…The mammalian tongue is a muscular hydrostat, a constant-volume structure (Kier and Smith, 1985;Smith and Kier, 1989) with complex musculature-seven or eight muscles, each with extensive, overlapping terminations in the tongue body-often allowing for dramatic shape changes. Each side of the rat tongue body comprises over 3,000 motor units (Sokoloff, 2000(Sokoloff, , 2004, providing fine neuromotor control with subsequently great diversity of response.…”

“…The muscular hydrostat model (Kier and Smith, 1985), in linking positional and shape changes (e.g., protrusion accompanying reduced cross-sectional area), provides a more realistic conceptual approach. Activation of any lingual motor unit can alter shape, position, and stiffness.…”