Electromyography of the buccal musculature of octopus (<i>Octopus bimaculoides</i>): a test of the function of the muscle articulation in support and movement

Uyeno, Theodore A.; Kier, William M.

doi:10.1242/jeb.02600

Cited by 31 publications

(34 citation statements)

References 14 publications

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“…This study, in combination with previous research, suggests that muscle articulations are an important joint mechanism; they are used as joints in four invertebrate phyla [inarticulate brachiopods (Trueman and Wong, ) cephalopods (Uyeno and Kier, ), kalyptorhynch turbellarian flatworms (Uyeno and Kier, ) and jawed polychaetes] and serve critical functions typically related to feeding and defense. The mouthparts of onychophorans (Manton and Harding, ) and some wood‐boring beetle larvae (Nieves‐Aldrey et al, ) show characteristics that suggest that they may also function as muscle articulations.…”

Section: Discussionsupporting

confidence: 54%

“…The pharyngeal bulb of A. virens resembles the octopus beak joint (Uyeno and Kier, ) in a number of aspects, suggesting that the bulb is also a muscle articulation. The muscle and fibrous ECM are arranged as a muscular hydrostat that serves common and multiple roles: the soft tissues separate and connect the jaws; they bear compressional forces transferred across the joint; and they generate the force that moves the jaws.…”

Section: Discussionmentioning

confidence: 93%

“…Complex deformations and movements can be created and the stiffness of the entire structure is under active control (Kier and Smith, ; Smith and Kier, ). Although the structure and function of this joint type has been investigated the beaks of octopus (Uyeno and Kier, ) and in extensible hook bearing proboscides of interstitial flatworms (Uyeno and Kier, ), the taxonomic distribution and general principles of form and function have yet to be thoroughly explored. Here, we present an analysis of the movement, morphology, and biomechanics of the Nereididae jaw joint to elucidate the general principles of support and movement in this dynamic joint type.…”

Section: Introductionmentioning

confidence: 99%

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The structure and function of a muscle articulation‐type jaw joint of a polychaete worm

Uyeno

Kier

2014

Journal of Morphology

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The arrangement of the musculature and the fibers of the extracellular matrix (ECM) in the flexible jaw joint of the sandworm Alitta virens (Annelida, Polychaeta) was studied using dissection and histology. The jaws are capable of a wide range of motions principally related to defense and feeding. The left and right jaws are embedded in and moved by a compact pharyngeal bulb of muscle and ECM that also forms the mouth and esophagus. Eight pharyngeal bulbs were removed and dissected to document gross anatomical features or preserved and embedded in plastic for sectioning in multiple planes. The sections were stained with toluidine blue and basic fuchsin to differentiate muscle and ECM. The sections were then digitized and used to develop a three-dimensional computer illustration. We hypothesize that the muscle and fibers in the ECM are arranged as a muscular hydrostat to support the movement of the jaws. Four specimens were recorded using a digital video camera and a tank with an angled mirror to record lateral and ventral views of jaw movements during locomotion and biting associated with burrow guarding and feeding. Frame by frame kinematic analysis of this video showed that the jaws move symmetrically in a roughly horizontal plane. Although the angle between the jaws increases and then decreases after maximum gape has been reached, the jaws also translate relative to each other such that the axis of rotation is not fixed. Together, these functional morphological and behavioral data identify the jaw mechanism as a flexible joint known as a muscle articulation. As muscle articulations have been previously described only in the beaks of cephalopods and flatworms, this study implies that this type of joint is more common and important than previously recognized.

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Section: Discussionsupporting

confidence: 54%

Section: Discussionmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

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The structure and function of a muscle articulation‐type jaw joint of a polychaete worm

Uyeno

Kier

2014

Journal of Morphology

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“…The elongate arms and tentacles of squid (Kier, 1982;Van Leeuwen and Kier, 1997), the arms of octopuses (Kier and Stella, 2007), and the tentacles or cirri of the chambered nautilus (Kier, 1987) all depend on muscular hydrostatic support, with transverse (octopus arms, squid arms and squid tentacles), circular (squid tentacles), radial (chambered nautilus cirri), longitudinal (all), and helical or oblique muscle fibers (all) represented. In addition to these more or less cylindrical structures, muscular-hydrostatic support is also used to support and create substantial subambient pressures in the suckers (Kier and Smith, 1990;Kier and Smith, 2002), to support and actively bend the fins of squid and cuttlefish (Kier, 1989;Kier et al, 1989;Johnsen and Kier, 1993), to support and create the movement of the beaks (Uyeno and Kier, 2005;Uyeno and Kier, 2007), to provide muscular antagonism for the mantle during respiration and jet locomotion, with contributions from elastic energy storage in the connective tissues (Curtin et al, 2000;Gosline and Shadwick, 1983;MacGillivary et al, 1999), and to provide support and antagonism for a variety of other structures and organs (Kier, 1988;Kier and Thompson, 2003).…”

Section: W M Kiermentioning

confidence: 99%

The diversity of hydrostatic skeletons

Kier

2012

Journal of Experimental Biology

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209

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Summary A remarkably diverse group of organisms rely on a hydrostatic skeleton for support, movement, muscular antagonism and the amplification of the force and displacement of muscle contraction. In hydrostatic skeletons, force is transmitted not through rigid skeletal elements but instead by internal pressure. Functioning of these systems depends on the fact that they are essentially constant in volume as they consist of relatively incompressible fluids and tissue. Contraction of muscle and the resulting decrease in one of the dimensions thus results in an increase in another dimension. By actively (with muscle) or passively (with connective tissue) controlling the various dimensions, a wide array of deformations, movements and changes in stiffness can be created. An amazing range of animals and animal structures rely on this form of skeletal support, including anemones and other polyps, the extremely diverse wormlike invertebrates, the tube feet of echinoderms, mammalian and turtle penises, the feet of burrowing bivalves and snails, and the legs of spiders. In addition, there are structures such as the arms and tentacles of cephalopods, the tongue of mammals and the trunk of the elephant that also rely on hydrostatic skeletal support but lack the fluid-filled cavities that characterize this skeletal type. Although we normally consider arthropods to rely on a rigid exoskeleton, a hydrostatic skeleton provides skeletal support immediately following molting and also during the larval stage for many insects. Thus, the majority of animals on earth rely on hydrostatic skeletons.

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“…It has been used in a subsequent study using electromyography to correlate muscle activation patterns with the movement of beaks in the octopus buccal mass (Uyeno & Kier 2007). Our calibrations showed a change of B8 mV mm À1 within our 1 cm working range.…”

Section: Discussionmentioning

confidence: 90%

A novel device to monitor small changes in underwater distances

Uyeno

Hsiao

2007

Invertebrate Biology

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Abstract. This study describes a technique to record small (1 cm) distance changes or movements occurring in seawater using a simple electronic circuit and miniature ball electrodes. This low-cost technique was designed to directly measure such changes in a broad range of experiments involving small marine invertebrates while minimizing the mechanical loading of the structures of interest. The circuit detects and amplifies small changes in the resistance of seawater between two electrodes as the distance between them varies; these are then converted to voltage changes. After calibrating the output of the device with known distance measurements, it was evaluated using a test organism by monitoring and recording the body flushing behavior of the sea squirt, Styela plicata. Electrodes were sewn to the tunic at the base of the atrial siphon and changes in its diameter were recorded424-h periods. UsingB3-cm-tall sea squirts, the distance between the electrodes expanded and contracted with a range of 5.5 mm during rhythmic flushings. Flushes occurred on average every 4.1 min and showed a rapid initial contraction, followed by a slower expansion while refilling. Attaching electrodes to the tunic had little mechanical or behavioral effect; the untouched control specimen had similar flushing rates. The movement monitor circuit is stable, sensitive, and performed well in fullstrength seawater experiments where good spatial and high temporal resolution, low inertial loading, and low noise were required. The technique, as shown here, can be used to record a wide range of animal movements and further suggested modifications of the circuit may suit a broad range of other experimental situations.Additional key words: measurement, movement, behavior, electronic distance A frequent difficulty in testing biomechanical functions in marine invertebrates is the accurate and precise measurement of small linear distances over time. Here, we present an electronic circuit design for recording such data with low construction costs and good spatial and temporal resolution. We tested this technique by monitoring the flushing behavior of the leathery (or pleated, or rough) sea squirt, Styela plicata LESUEUR 1823, as quantified by measured changes through time in the base diameter of the atrial siphon (Fig. 1).Directly monitoring changes in distance in seawater can be technically challenging. The chosen technique must be compatible with the high conductivity of seawater. It must minimize the mechanical loading of structures of often small or soft-bodied invertebrates. In addition, it should not interfere with other techniques such as electromyography or pressure measurements. Previously used techniques include a number of methods: sonomicrometric, magnetic, optic, mechanical, and electric. As reviewed below, each has limitations.Ultrasonomicrometry is a common technique that uses piezoelectric crystal transducers. Distance is measured by recording the time taken by ultrasonic waves to travel between crystals. This technique offers high tempo...

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Electromyography of the buccal musculature of octopus (Octopus bimaculoides): a test of the function of the muscle articulation in support and movement

Cited by 31 publications

References 14 publications

The structure and function of a muscle articulation‐type jaw joint of a polychaete worm

The structure and function of a muscle articulation‐type jaw joint of a polychaete worm

The diversity of hydrostatic skeletons

A novel device to monitor small changes in underwater distances

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