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First published online December 14, 2006
Journal of Experimental Biology 210, 118-128 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02600
Electromyography of the buccal musculature of octopus (Octopus bimaculoides): a test of the function of the muscle articulation in support and movement
Department of Biology, CB# 3280 Coker Hall, University of North Carolina at Chapel Hill, NC 27599-3280, USA
* Author for correspondence (e-mail: uyeno{at}bio.unc.edu)
Accepted 17 October 2006
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Key words: biomechanics, Cephalopoda, electromyography, muscle articulation, Octopus bimaculoides
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), or in tension as in the forelimbs of a brachiating gibbon
(Bertram, 2004). Links also
provide skeletal support for the attached muscles and may amplify their force,
displacement or velocity.
Animal joints show great morphological diversity; however, all may be
divided into two categories, sliding and flexible, based on the nature of the
connection between the links (Wainwright
et al., 1982). Elephant knees and gibbon elbows are examples of
sliding joints, in which links are in contact and compressional forces are
transmitted directly through the joint. The morphology of the articulating
surfaces and joint capsule controls the range of motion and number of degrees
of freedom. The movement of links connected by a flexible joint relies on the
flexibility of the connecting material. But flexible material tends to buckle
when loaded in compression and thus a survey of flexible joints by Wainwright
et al. (Wainwright et al.,
1982) found only distal leg segments of smaller insects use this
mechanism.
The joint studied here, termed a `muscle articulation'
(Uyeno and Kier, 2005), is a
type of flexible joint: the muscle and connective tissues that connect the
links also hold them apart. In the cephalopod buccal mass the links are
represented by the two rigid beaks and the joint is composed of the connecting
musculature that allows the beaks to rotate and translate relative to one
another. We believe these beak motions are possible because the musculature
includes muscle groups with fibers oriented in a three-dimensional arrangement
known as a muscular hydrostat (Kier and
Smith, 1985). In such systems, one or more orientations may
function as an antagonist to the others. Uyeno and Kier suggested that, unlike
other flexible joints, the cephalopod beak joint relies on a muscular
hydrostatic mechanism to bear compression and create movement (see
Uyeno and Kier, 2005). Here,
we test the hypothesized functions of the buccal mass musculature and provide
the first experimental evidence of a mechanism that can open the beaks.
Cephalopod buccal mass morphology
We studied the buccal mass of the California two-spot octopus Octopus
bimaculoides (Pickford/McConnaughey 1949). This spherical structure is
located in a sinus formed by the base of the arms and includes an upper and a
lower beak made of chitin (Hunt and Nixon,
1981) that is embedded in the mandibular muscles
(Fig. 1). Each beak is a
roughly U-shaped link, with one end folded over itself to form the rostral tip
and the jaw angle, both of which are used in biting and shearing food, and the
hood that projects beyond the jaw angle
(Fig. 2). By convention, the
rostra are referred to as being anterior. The upper beak is inverted relative
to the lower beak. The rounded dorsal surface of the upper beak and the
analogous ventral surface of the lower beak are termed crests. The left and
right sides of the beaks are referred to as the lateral walls. The fold that
forms the rostrum and hood of the lower beak also has enlarged dorsal
extensions, termed the left and right wings. The upper beak fits within the
lower beak such that the lateral walls overlap, but they do not contact each
other within the joint. Only the biting surfaces (i.e. the rostra and jaw
angles) contact. A `pivot area' was described between the upper and lower
beak, in which the axis of rotation was typically located, suggesting the
position of the pivot is not fixed (Kear,
1994).
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Five mandibular muscles (the superior, left and right lateral, anterior and
posterior mandibular muscles) connect the beaks of O. bimaculoides to
each other and to the buccal mass sheath, a connective tissue sheet that
encapsulates the muscular part of the buccal mass
(Uyeno and Kier, 2005)
(Fig. 3). The superior
mandibular muscle (Fig. 3, SMM,
colored green) is a robust dorsal muscle with three divisions. This muscle
originates along the crest of the upper beak and includes a central division
and left and right divisions that extend anteroventrally to insert on the
enlarged wings of the lower beak. These robust left and right divisions
constitute the bulk of the superior muscle and include fibers oriented
parallel to the line from origin to insertion.
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The lateral mandibular muscles (Fig. 3, left and right LMMs, colored purple) are robust, cylindrical, and symmetrically paired muscles originating on a large area of the left and right lateral walls of the upper beak. The muscle extends laterally and has a somewhat smaller insertion on the buccal mass sheath. Three different orientations of muscle fibers are observed. The first group of fibers originates on the lateral walls of the upper beak and extends parallel to the long axis of the muscle to insert on the buccal mass sheath. The other two groups of muscle fibers are perpendicular to the orientation of the first as well as to each other, one group oriented dorsoventrally and the other anteroposteriorly.
The anterior mandibular muscle (Fig.
3, AMM, colored yellow) is relatively thin and originates on the
anterior portion of the lower beak crest and overlying buccal mass sheath and
follows the curve of the crest dorsally to insert on the lateral walls of the
upper beak just below the level of the upper beak crest. Its muscle fibers
follow a direct course from origin to insertion. The posterior mandibular
muscle (Fig. 3, PMM, colored
light blue) is the smallest and thinnest of the mandibular muscles. It is a
thin sheet of muscle that originates on the posterior region of the lower beak
crest and extends directly to an insertion on the lateral walls of the upper
beak below its crest. As the posterior edges of the trough-like beaks are
open, the posterior mandibular muscle, along with the overlying buccal mass
sheath, forms the posterior wall of the buccal cavity and serves to contain
and secure the buccal complex within the buccal cavity. This buccal complex
includes the radula, lateral buccal palps, salivary papilla, salivary glands
and radular support system (Nixon and
Young, 2003).
The sequence of activation of these muscles is controlled by the inferior
buccal ganglion (Fig. 4), which
receives input from the superior buccal lobe of the brain through the paired
interbuccal connectives (Young,
1965; Young,
1971). Boyle et al. (Boyle et
al., 1979b) noted that the inferior buccal ganglion functions as a
central pattern generator that is probably modulated by sensory feedback from
the musculature and the brain. After severing the interbuccal connectives and
excising the buccal mass, it performs biting movements that are similar to
in vivo beak movements with respect to the position of the upper beak
relative to the lower one throughout each bite cycle. Boyle at al.
(Boyle et al., 1979b) first
described this bite cycle, and Kear (Kear,
1994) later modified the description
(Fig. 5). Our observations
agree with those of Kear (Kear,
1994) and so we use her terminology here. There are five phases
during which the upper beak is: (A) closed in its resting position; (B)
opening; (C) fully opened; (D) closing; (E) closed with the upper beak rostrum
retracted behind the lower beak rostrum.
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The superior mandibular muscle
We hypothesize that the superior mandibular muscle
(Fig. 3, SMM, colored green) is
responsible for closing the beaks. Contraction of fibers in the left and right
divisions connecting the crest of the upper beak and the wings of the lower
beak is predicted to bring the beaks, and especially the rostra, closer
together in a closing motion (Fig.
6A). As these lateral divisions of the superior mandibular muscle
are robust muscles with a relatively large cross sectional area, we
hypothesize that they provide most of the closing force.
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Previous studies have provided some evidence for the role of the superior
mandibular muscle in closing. Boyle et al. clamped the lower beak of
Octopus vulgaris and attached a strain gauge to the upper beak with a
thread (Boyle et al., 1979a;
Boyle et al., 1979b). This
approach allowed beak movements to be monitored, although with some mechanical
loading from the apparatus. Fine wire electromyography was used to record
mandibular muscle electrical activity. Recordings were made during both
spontaneous bite cycles as well as evoked bites, in which the ligatured
interbuccal connectives were stimulated electrically. Boyle et al. concluded
that the superior mandibular muscle was active while the beaks were held
closed (Boyle et al., 1979a;
Boyle et al., 1979b). They also
suggested that the superior mandibular muscle was responsible for beak
retraction.
In a later study of the buccal masses of a variety of coleoid cephalopods,
Kear also clamped the lower beak and attached a strain gauge to the upper beak
(Kear, 1994). The superior
mandibular muscle was directly stimulated electrically at five locations along
the central division. Stimulation resulted in closing movements at every point
tested, but unlike the findings reported by Boyle et al., no retraction was
observed (Boyle et al., 1979b).
In this study, we observed the effect of superior mandibular muscle
contraction on the movement of the upper beak without mechanical loading.
The lateral mandibular muscles
We hypothesize that the paired lateral mandibular muscles
(Fig. 3, left and right LMMs
colored purple) generate force for opening movements and also help create a
dynamic pivot around which beak movements occur
(Uyeno and Kier, 2005). The
cylindrical lateral mandibular muscle (Fig.
6), consists of a densely packed three dimensional array of
muscle. Since it is essentially constant in volume, we hypothesize that
contraction of fibers that are parallel to the long axis
(Fig. 6, the red lateral fibers
of the central diagram) causes the muscle to become shorter and increase in
diameter and circumference. This action may push the upper beak away from the
lower one because the muscle originates on the lateral wall of the upper beak
and passes over the lateral wall edges of the lower beak. The lateral
mandibular muscles are the only sizeable muscle groups that include muscle
fiber orientations capable of generating the force required to open the beaks.
The definitive test of this hypothesis is whether the beaks can open in the
absence of lateral mandibular muscle activity.
The muscle fiber arrangement within the lateral mandibular muscles suggests that they may also serve as a dynamic pivot for the beaks. The fibers that are parallel to the long axis of the lateral mandibular muscles (Fig. 6, red lateral fibers of the central diagram) may elongate the other fiber orientations [the dorsoventral (Fig. 6, blue fibers in the central diagram) and anteroposterior muscle fibers (Fig. 6, green fibers in the central diagram)] that are arranged perpendicularly to the long axis. As the co-contraction of the perpendicular dorsal-ventral and anterior-posterior fiber orientations will elongate the parallel lateral fibers, the three muscle orientations may serve as antagonists of one another, controlling the shape and stiffness of the lateral mandibular muscle in the manner of many muscular hydrostats. Thus, it is important to note the potential dual function of the lateral mandibular muscles; they may generate force not only for beak opening, but may also be activated with other muscles to stabilize and control the hinge axis or pivot around which the two beaks rotate. This would allow, for instance, the superior mandibular muscle to contract and modulate the angle between the two rostra, instead of simply bringing the two beaks closer together. If the lateral mandibular muscles aid in forming a dynamic pivot for the beaks, they may show activity not only during opening movements but during other beak movements as well.
The hypothesized functions of the lateral mandibular muscle described above
differ from previous proposals, in part because they incorporate additional
morphological information (Uyeno and Kier,
2005). Boyle et al. observed electrical activity only during
closing movements and were unable to record from muscle locations that were
active during opening (Boyle et al.,
1979a). They therefore considered opening to be a passive movement
resulting from the flexion of the lateral walls of the upper beak
(Boyle et al., 1979b). Kear
simultaneously stimulated the buccal mass near the location of the left and
right lateral mandibular muscles and found that this opened the beaks
(Kear, 1994). Stimulation of
only one side resulted in lateral movement of the upper beak. Interpretation
of electrical stimulation experiments is difficult because it is unclear which
of the muscles in the lateral portion of the buccal mass were stimulated.
Indeed, the inferior mandibular ganglion itself may have been stimulated.
Kear described the lateral mandibular muscles as originating on the lateral
wall of the upper beak and extending both to the ventral side of superior
mandibular muscle and to the lateral walls of the lower beak
(Kear, 1994). She suggested
that contraction of these fibers pulled the posterior edges of the lateral
walls of the upper and lower beaks together. Although Kear did not identify
the pivot mechanism she identified the location of the axis of rotation as
being between the lateral mandibular muscles and beak rostra
(Kear, 1994). She concluded
that contractions drawing together the posterior portions of the beaks would
lever the rostra apart using the pivot area as a fulcrum. The fibers described
by Kear (Kear, 1994) as
connecting the upper and lower beak lateral walls were not observed in the
lateral mandibular muscles of Octopus bimaculoides, or the other
species investigated by Uyeno and Kier
(Uyeno and Kier, 2005), so
this mechanism cannot function in these species.
Kear (Kear, 1994) also noted
the outward flexion, described by Boyle et al.
(Boyle et al., 1979b), of the
upper beak lateral walls. Could this outward flexing cause a shape change in
the beaks that would result in opening of the rostra? Presumably this would
occur by the flexing of the crest in a way that levers the upper beak rostrum
dorsally. This mechanism predicts areas of flexibility of the upper beak
itself that can cause shape change. We tested for this possibility as
well.
The anterior and posterior mandibular muscles
Located anterior to both the lateral mandibular muscles
(Fig. 3, LMM, colored purple)
and the general pivot area around which the beaks rotate, the anterior
mandibular muscle (Fig. 3, AMM,
colored yellow) possesses fibers that connect the upper and lower beaks and is
thus hypothesized to function in their closing. The location of the posterior
mandibular muscle (Fig. 3, PMM,
colored light blue) is opposite to that of the anterior mandibular muscle: it
is located posterior to both the lateral mandibular muscles and the beak pivot
area. As the posterior mandibular muscle fibers directly connect the two
beaks, it is likely that their contraction brings the posterior edges of the
beaks together. Because it is positioned posterior to the pivot area, if the
pivot area is actively forming a fulcrum, the posterior mandibular muscles may
help in beak opening. However, if the pivot area is inactive, then the
contraction of the posterior mandibular muscle fibers may simply contribute to
the overall closing of the beaks. Given the relatively small cross-sectional
areas of these two muscles (Uyeno and
Kier, 2005), the forces generated by the anterior and posterior
mandibular muscles may be relatively lower than those generated by the
superior and lateral mandibular muscles.
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Materials and methods |
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). After the specimen was relaxed, the brain was
bisected, the interbuccal connectives were severed, and the buccal mass was
removed and placed in a glass test chamber containing artificial seawater
(NaCl, 470 mmol l-1; KCl, 10 mmol l-1;
CaCl2·6H2O, 60 mmol l-1;
MgCl2·6H2O, 50 mmol l-1; glucose, 20
mmol l-1; Hepes, 10 mmol l-1; adjusted to pH 7.8 with
2.0 mol l-1 NaOH) (Milligan et
al., 1997) chilled to 17°C. During the experiment, the buccal
mass was allowed to rest, unrestricted and ventral surface down, on the bottom
to minimize mechanical loading of the joint. Bipolar fine wire electrodes were
implanted in the muscles and a pair of silver/silver chloride electrodes was
glued to the upper and lower beak rostra and wired to a custom movement
monitor circuit (Fig. 4).
The electromyography electrodes were fabricated from Teflon-insulated, half
annealed, single stranded stainless steel wire with a bare diameter of 75
µm (A-M Systems, Inc., Carlsborg, WA, USA). Approximately 0.5 mm of
insulation was removed from the staggered electrode tips
(Basmajian and Stecko, 1962).
The inner sharp edge of a hypodermic needle was chamfered
(Loeb and Gans, 1986) to
prevent damaging the electrode wire. The electrode tips were inserted into the
end of the needle and the remaining electrode wire was then folded over the
chamfered edge of the needle tip. The needle was then used to insert the
electrodes in the muscle of interest and then withdrawn
(Parker, 1968), leaving the
hooked electrodes embedded in the tissue.
The electrodes were implanted into the left and right divisions of the
superior mandibular muscle and the left and right lateral mandibular muscles
(Fig. 4). We were unable to
reliably implant electrodes into the anterior or posterior mandibular muscles
because they were too thin. The signals from four sets of electrodes were fed
to an A-M Systems, Inc. Model 1700 four channel differential AC amplifier and
digitized at 5 kHz per channel using a Powerlab 4/20 (AD Instruments, Inc.,
Colorado Springs, CO, USA) analog to digital conversion unit. The electrodes
were dissected out at the end of each experiment to confirm placement. In two
of the preparations, the upper and lower beaks were dissected so as to
completely free them from their surrounding mandibular muscles. This was done
in order to assess the potential for beak openings based on flexure of the
lateral walls. The interbuccal connective and areas adjacent to the electrodes
were also electrically stimulated (2.5 V at 60 Hz for 2.5 s) in five of the
healthiest preparations (Boyle et al.,
1979a).
Beak movements were monitored by a custom movement monitoring circuit
(Uyeno and Hsiao, 2006)
designed to measure the resistance between two silver/silver chloride ball
electrodes affixed with cyanoacrylate glue to the rostra
(Fig. 4). The circuit converted
the resistance into an amplified voltage output signal that was fed to a
Powerlab 4/25 analog to digital conversion unit. The calibration of the
circuit allowed linear distance changes between the electrodes and hence the
beaks to be recorded. These data and the electromyographical data were
simultaneously recorded on a computer hard drive.
The electromyographical data were analyzed using a routine written for Matlab 7 (MathWorks, Natick, MA, USA). The data were DC adjusted to set the mean to zero, rectified (full wave) and then smoothed using a lowpass, second order Butterworth filter with a time constant of 79.5 ms. A Fast Fourier Transform (FFT) frequency domain plot was used to confirm that the cutoff frequency associated with 79.5 ms retained enough resolution to display all pertinent frequencies. Movements were correlated with the electromyographical activity. Onset of activity was calculated using a Matlab 7 routine that automatically determined the standard deviation of the rectified electromyogram signal during a 1 s steady state period prior to a muscle activation. Muscle activation onset time was defined as the time at which a threshold of 2.5 standard deviations was reached. These automatic onset events were visually confirmed and then correlated with movement monitor activity.
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Beak opening
The lateral mandibular muscles were active in 100% of all openings. The
lateral mandibular muscles were the only muscles active during 72.6% of beak
openings and were co-active with the superior mandibular muscle in 27.4% of
all openings. Fig. 9 shows an
example of three bursts of activity from the left lateral mandibular muscle
correlated with three brief beak openings from a half-opened gape. The
activity of the left superior mandibular muscle does not show any obvious
correlation with beak movements.
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Observations of beak activity during direct nerve and muscle stimulation
Electrical stimulation of the beak musculature and nerves was also
attempted in order to explore the functional role of the musculature in beak
movements. Stimulation of the left or right divisions of the superior
mandibular muscle results in asymmetrical beak closing. For example, if the
right division is stimulated, the upper beak rostrum closes to the right of
the lower beak rostrum. Likewise, stimulation of either the left or right
lateral mandibular muscle results in an asymmetrical opening movement. For
instance, stimulation of the left lateral mandibular muscle results in opening
between the left sides of the upper and lower beaks, but little change on the
right. This causes the upper beak to rotate around the anterior-posterior
axis, rolling the upper beak by as much as 30° relative to the lower beak.
Stimulation of the interbuccal connectives, the neural pathway that connects
the brain to the inferior buccal ganglion, elicits a nearly complete bite
cycle, in which only the retraction phase seemed to be diminished. The vigor
and completeness of the bite cycle decreased as the preparation aged.
Observations of beak movements
It is possible to observe beak movements in an isolated buccal mass of
O. bimaculoides because portions of both the lower and upper beak are
visible. The rostrum, angle and hood of the upper and lower beaks are exposed,
and the enlarged lateral wings of the lower beak are also visible (e.g.
Fig. 4). During biting
movements, the lower beak remains stationary relative to the buccal mass,
regardless of the direction of movement of the upper beak or whether the
buccal mass is resting on its side, dorsal surface or ventral surface. The
upper beak shows five degrees of freedom of movement relative to the lower
beak: (1) rotation about the dorsal-ventral axis or yaw; (2) rotation about
the anterior-posterior axis, or roll; (3) rotation about the left-right axis,
or pitch; (4) translations along the dorsal-ventral axis; and (5) translations
along the anterior-posterior axis. Side to side translations were not
observed, but were approximated by a combination of yaw and roll movements.
This diverse array of beak movements would be impossible with a simple hinge
joint between the two beaks. The musculature that serves as the joint thus
allows shearing between the beaks along multiple axes. In addition, it
provides for an axis of rotation that can be repositioned within the pivot
area, a zone that includes most of the lateral mandibular muscles and an area
dorsal and anterior to them.
Flexibility of the freshly dissected beak
The stiffest areas of O. bimaculoides beaks are a dark, opaque
brown/black color. Less stiff areas are a lighter shade of brown and the most
flexible and thinnest areas are tan colored or transparent. The only flexible
areas of the freshly dissected upper beak are the lateral walls, which are
capable of flexing outward. Maximal outward flexing results in a 30-40%
increase in distance between the lower edges of the upper beak lateral walls.
The flexible areas of the lower beaks include the tips of the lateral wings
and the posterior edges of the lateral wall. There is a sharp demarcation
approximately half way between the jaw angle and the tip of the lateral wing
where the wing becomes lighter in color, more flexible and thinner. A more
graded demarcation exists near the posterior tips of the lateral walls of the
lower beak. Neither the upper nor the lower beaks are capable of significant
longitudinal bending, perhaps due in part to their U-shaped cross-section and
consequent large second moment of area. Thus, the rostra and crests do not
move relative to each other.
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) noted that
the most conclusive evidence for the role of the various muscles in beak
movements requires in vivo intramuscular electromyography records
during feeding. Although in vivo experiments are indeed preferable,
they present substantial experimental difficulties because implanting
electrodes requires invasive surgery close to the brain, electrode placement
cannot be assured because the buccal mass is encapsulated within the base of
the arm musculature, and post-operative movements of the octopus often
dislodge embedded electrodes (Kear,
1994).
The excised buccal mass preparation represents a useful alternative
approach. Boyle et al. (Boyle et al.,
1979a) found the autonomous biting movements of the excised beak
to be similar to normal beak movements. They suggest that the bite cycle is
under the control of a central pattern generator in the inferior mandibular
ganglion, which is part of the excised preparation, and thus the similarity to
in vivo movements is less surprising
(Boyle et al., 1979a). The
biting cycles of the initial phase of the preparation are similar to those
observed in vivo, but they are difficult to analyze because of the
complexity of movement. Although this complexity is probably more
representative of the full range of muscle function in the intact animal,
analysis of the less complex, discrete movements found in the second phase is
more instructive because the opening, closing, and retracting movements are
similar to those of the normal bite cycle and isolated muscle activity can be
correlated with specific beak motions. We did not observe this second phase of
activity in buccal mass preparations of the other coleoids studied [the
Atlantic brief squid Lolliguncula brevis (Blainville 1823) or the
cuttlefish Sepia officinalis Linnaeus 1758] perhaps because these
movements are more apparent in species (such as Octopus bimaculoides)
in which excised buccal mass preparations have a longer life span.
Assessment of functional hypotheses for the mandibular muscles
The superior mandibular muscle
The superior mandibular muscle is active during the majority of the beak
closings and during all of the rapid closings in which the beaks quickly clamp
together. This, together with a previous analysis that showed that this muscle
contains the largest number of muscle fibers in an orientation that could
effect this motion (Uyeno and Kier,
2005), suggest that the superior mandibular muscle is the prime
force generator in beak closure. This muscle is also co-active with the
lateral mandibular muscle in 27% of openings, suggesting also that it may
either stabilize the beaks or modulate the movements produced by other beak
muscles.
The lateral mandibular muscles
No beak openings occurred in the absence of lateral mandibular muscle
activity. The lateral mandibular muscles were identified previously as the
only muscles that have a fiber arrangement that could produce opening force
and they are likely to be the major beak opening muscles
(Uyeno and Kier, 2005). The
competing hypothesis does not seem to be valid: contraction of the lateral
mandibular muscles probably does not elevate the upper beak by flexing the
lateral walls. No shape change that results in the movement of the upper beak
was observed in the freshly dissected beak. We did observe flexing of the
lateral walls in the buccal mass preparation, but we agree with Kear's
assessment that this flexion probably accommodates the movement of the palps
and radula/odontophore complex (Kear,
1994).
Mandibular muscles as a dynamic hinge
In addition to producing the force required to open the beaks, we
hypothesized previously that the lateral mandibular muscles may also form a
pivot for other beak motions. Our experimental results are consistent with
this hypothesis, but do not provide a definitive test. If the lateral
mandibular muscles are only involved in opening the beaks, activity would be
observed only during these motions. We also observed them to be active, often
in concert with the superior mandibular muscle, during closing and during
phases without motion. These data suggest that the lateral mandibular muscles
may modulate the effects of superior mandibular muscle contraction during the
production of complex beak movements, but we cannot determine from our data
whether they are simply stabilizing beak movements or if they are serving a
more dynamic role in altering the location of the pivot between the two beaks.
A definitive test of this hypothesis will require more precise
three-dimensional kinematics in conjunction with finer scale sampling of
electrical activity from the musculature.
The anterior and posterior mandibular muscles
We were unable to record from either the anterior or the posterior
mandibular muscles because the muscle layers were too thin for our electrodes
and the connective tissue sheath surrounding the buccal mass complicated
electrode placement. Although we were not able to test the functional
predictions for these muscles it is likely that these muscles produce less
force than the superior and lateral mandibular muscles because of their small
cross sectional areas (Uyeno and Kier,
2005). Based on the fiber arrangement, the anterior mandibular
muscle may retract the upper beak (Uyeno
and Kier, 2005). The posterior mandibular muscle may maintain
tonus of the posterior buccal wall and perhaps, in conjunction with the
lateral mandibular muscles, open the beak
(Kear, 1994). Tests of these
predictions will require a novel experimental approach.
Summary of the opening and closing movement
Closing
The superior mandibular muscles were active during the majority of beak
closures, especially the rapid ones of large amplitude. In approximately one
quarter of the cases, in which closing was slower and of smaller amplitude,
activity was observed only in the lateral mandibular muscle or no activity was
seen in either the lateral or superior mandibular muscles. This suggests three
possibilities: the anterior or posterior mandibular muscles may be able to
close the beak; elasticity of the buccal sheath may close the beaks; or
movement of structures within the buccal cavity, such as the bolsters or the
radula/odontophore complex may close the beak.
Our conclusions are in general agreement with the data provided by previous
studies. Boyle et al. (Boyle et al.,
1979a) correlated the activity of the superior mandibular muscle
with both closing and retraction movements. Kear
(Kear, 1994) observed closing
movements without retraction in response to stimulation of the superior
mandibular muscle. She attributed the retraction to either an artifact of the
experimental setup used by Boyle et al. or the activity of the inferior
mandibular muscle. Uyeno and Kier (Uyeno
and Kier, 2005) redescribed anterior portions of the inferior
mandibular muscle as the anterior mandibular muscle. The anterior mandibular
muscle may indeed be active in retraction, but as described above, we were
unable to implant electrodes in this muscle to explore its function.
Opening
We observed the lateral mandibular muscles to be active during every beak
opening and thus conclude that their activity is required for this movement.
In addition, during opening movements, we observed the axis of rotation of the
upper beak relative to the lower beak varied and could be located over a
rather large area that includes the lateral mandibular muscles
(Fig. 5). These results differ
in some respects from those of previous studies. Boyle et al.
(Boyle et al., 1979a) were
unable to correlate any muscular activity to beak opening movements and
proposed a passive mechanism. We are uncertain why Boyle et al.
(Boyle et al., 1979a) did not
observe muscle activity during opening, but Kear
(Kear, 1994) suggested that the
buccal mass sheath may have insulating properties that hampered recordings.
Kear (Kear, 1994) stimulated
the center of the lateral mandibular muscles and found this produced the
strongest opening movements. Her results are thus in general agreement with
our observations, although she suggested a different opening mechanism (see
above).
Conclusions and future directions
The cephalopod buccal mass is a flexible joint in which the lateral
mandibular muscle functions as a muscular hydrostat, providing force for
opening of the beaks. The superior mandibular muscle probably produces the
majority of the closing force. Co-contraction of the superior mandibular
muscle and lateral mandibular muscles may stabilize beak movements and might
also provide a means of actively controlling the position of the hinge between
the beaks. The upper and lower beaks are connected by the lateral mandibular
muscles so that they bear any reactive forces generated by the bite and thus
they replace the function of the contacting surfaces of articulating skeletal
elements. These three functions, a pivot, an antagonistic muscle, and the
element that bears compressive and shear forces, are all provided by soft
tissue and represent the key functional characteristic of the muscle
articulation. Such an arrangement may allow a larger range of motion and
greater number of degrees of freedom than a more conventional articulated
joint. In the case of the buccal mass, five degrees of freedom were identified
(anterior-posterior and dorsal-ventral translations as well as rotations in
all three orthogonal planes). A potential trade-off for the gain of this
flexibility may be the increased complexity of neuromuscular control that is
required to produce this diversity of movement.
Muscle articulation joints may be a more common biomechanical feature in invertebrates than previously recognized. The eversible jaws of marine polychaetes and the hooks of interstitial turbellarians are currently under investigation and appear to share many characteristics with the buccal mass of cephalopods. Perhaps the diversity and complexity of motion that are allowed by a muscle articulation provide important advantages in feeding and manipulation. These characteristics may also make them useful models for engineers designing biologically inspired artificial joint mechanisms.
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Acknowledgments |
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References |
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