Statocysts in Crabs: Short-Term Control of Locomotion and Long-Term Monitoring of Hydrostatic Pressure

5 Pages·2001·2 MB·English

by  Peter J Fraser

Reference: Biol. Bull. 200: 155-159. (April 2001)
Statocysts in Crabs: Short-Term C< ol of
Locomotion and
Long-Term
Monitoring
of Hydrostatic Pressure
PETER ERASER
J.
Zoology Department, Aberdeen University, Tilly-drone Avenue. Aberdeen AB24 2TZ Scotland
Abstract. Crabs show well-coordinated locomotion. They of bouts of activity, with peaks that correspond to times of
have proprioceptors similar to those of lobsters, but they high tide.
differ in terms of their balancing systems and their con-
densed nervous system, which allows rapid interganglionic Introduction
conduction. Typically they exhibit dynamically stable loco-
motion with a highly developed semicircular canal system Brachyuran crabs are conspicuous animals that occupy a
that codes angular acceleration in each of three orthogonal variety of habitats and show well-coordinated locomotor
planes (horizontal and vertical at 45 and 135 to the pitch- ability while walking, crawling, climbing, swimming, or
ing plane). Left and right interneurons each code one direc- burrowing under a variety of hydrostatic pressure condi-
tion of angular acceleration, carrying information between tions. Compared with the ladder-like nerve cord of macru-
the brain and the thoracic ganglia. Cell A codes head-up rans (crayfish and lobsters), their nervous system shows
vertical plane angular accelerations. Cell B codes rotations condensation and fusion ofthoracic ganglia, allowing rapid
in the horizontal plane. Interneurons C and D code head- interganglionic conduction of impulses. The abdomen has
down vertical plane information, carrying it ipsilaterally and been much reduced and, in contrast to that ofmacrurans, is
contralaterally respectively. These interneurons have a cen- little used in normal or escape swimming. These crabs can
tral role in locomotion. They are activated and have their survive leg autotomy: 13%-43% of individual Carcimis
responsiveness to angular acceleration enhanced before and sampled from the wild have missing legs (McVean, 1982).
during locomotion. Such simple activation pathways point Typically they exhibit dynamically stable locomotion, with
tohow an angular-acceleration-controlled robot (CRABOT) statocyst (or balancing organ) interneurons having a central
could be constructed. Hydrostatic pressure information car- role (Fig. 1; Eraser, 1982; Eraser et al., 1987). Thread hair
ried by the thread hairs, which also sense angular acceler- receptors, which respond to fluid displacements in the sta-
ation, is filtered out from direct pathways onto the interneu- tocyst, have been shown to have their spontaneous activity
rons, but spectral analysis shows that it still has an influence and sensitivity to angular acceleration modulated by small
via central pathways. Long-term recordings from equilib- changes in hydrostatic pressure (Eraser and Macdonald.
rium interneurons in free-walking crabs taken from the wild 1994; MacdonaldandEraser, 1999). Clearly, elucidating the
into constant conditions show tidally changing frequencies simplifying principles underlying such versatility anddiver-
sification of function is an important aim. One approach to
dissecting such complexityis toconcentrateon afundamen-
E-mail: [email protected] tal difference between crabs and lobsters that is, the elab-
This paper was originally presented at a workshop titled Invertebrate oration in crabs of the statocyst and its central pathways.
Sensor,- Information Processing: Implications for Biologically Inspired
AutonomousSystems.Theworkshop,whichwasheldattheJ.ErikJonsson
CenterfortheNationalAcademyofSciences,WoodsHole.Massachusetts, Statocysts and Leg Proprioceptors Involved
from 15-17April2000.wassponsoredbytheCenterforAdvancedStudies in Locomotion
intheSpaceLifeSciencesattheMarineBiologicalLaboratory,andfunded
by the National Aeronautics and Space Administration underCooperative The statocyst contains a statolith and angularacceleration
Agreement NCC 2-896. receptors. In the crab, the crescent of statolith hairs (Sand-
155
156 P. J. ERASER
the trailing legs push to move the body (Clarac and Coul-
mance, 1971; Evoy and Ayers. 1982). Crabs do not exhibit
regulargait patterns, buthave agreat variety ofgaits and leg
activation sequences. Hence Evoy and Ayers (1982) state
that "changes in gait occur andconditions strictly satisfying
the alternating tetrapod gait are rarely seen." During high-
speed running, ghost crabs may even become bipedal, with
only two legs alternating on the trailing side (Burrows and
Thread Hairs
A Hoyle, 1973). Statocyst ablation affects sideways walking
and the rearing reflex (Cohen and Dijkgraaf, 1961; Fraser,
Connective
*Esophageal 1974). Swimming activity is more stereotyped and again
highly dependent on statocyst input (Fraser el al., 1987).
During swimming, all muscles in the fifth legs are active in
a sequence that causes cyclical sculling. Only muscles that
operate joints controlling dorsolateral movements are in-
volved in sideways walking, and they are used in a different
temporal pattern than in swimming (Fraser et al., 1987).
Leg proprioceptors are used in the fine motor control to
produce coordinated behavior, but during rhythmic behav-
ior, sensory information does not vary much on each cycle
unless a leg hits an obstacle. A variety ofreceptors include
muscle receptor organs, which measure muscle stretch
(Bush, 1977); chordotonal organs, which are articular (joint
Fused Thoracic Ganglia rotation) receptors measuring stretch around joints; and
apodeme receptors and cuticular stress receptors, which
Figure 1. Equilibriumcell Ainbrain (A) and thoracic ganglia (B) of record musculartension via tendons andcuticle respectively
the crab Carcinusmaenas. The large axon runs in the esophageal connec- (Wales et al., 1971). The funnel canal organs at the ends of
tive.Threadhairafferents(C), whichareactivatedbyangularacceleration the dactylopodites must be silent for the animal to swim,
iinnttehrenepulraonnesodfirtehcetlyv.er(tiRceadlrcaawnnalforfomthFerassteart,ocy1s9t8,9)c.ontact the equilibrium whereas their rhythmic firing in walking is used for step
regulation (Libersat etal., 1987). Although it is not possible
here to dojustice to the complexity of information relayed
eman and Okajima. 1972) is much smaller than the macru- by these proprioceptors, in general their role in locomotion
ran crescent (see Lemmnitz and Wolff, 1990). The fluid- in crabs is broadly similar to that in lobsters and crayfish.
filled sac has been shaped from a simple cavity in the
macruran statocyst into two orthogonal semicircular canals. Equilibrium Interneurons Involved in Locomotion
Angular accelerations in the planes of the horizontal or
vertical canals are monitored by a row of long, slender The angularacceleration sensors, the thread hairs, project
thread hairs (Fig. 1C; Sandeman and Okajima. 1972; Fraser onto a small set of eight large interneurons that link the
and Takahata, 2001). Typically the response ofthread hairs brain to the fused thoracic and abdominal ganglia (Fig. 1;
to an angular acceleration is unidirectional, with two oppo- Fraser, 1974, 1990). These fire in the short term during
sitely responding directional classes. Analogous to those of angular accelerations caused by locomotion (Fig. 2A, B;
vertebrates, the receptors integrate angular acceleration and Fraser. 1982). but are also activated centrally before and
code angular velocity in the horizontal plane or in vertical duringbouts ofwalkingorswimming (Fig. 2B; Fraseretal.,
planes either at 45 or at 135 to the median line. Thread 1987; Fraser, 1975. 1989). Their activity long term consists
hairs are the main sensory component involved in a variety ofquiescent periods with short bouts ofextremely elevated
of statocyst-driven behaviors ranging from walking to eye- activity. Cells are not coupled and are more likely to act in
stalk movement, with free hook hairs and statolith hairs anti-phase during short-term oscillations that form part of
playing a lesser role (Cohen and Dijkgraaf. 1961; Fraser, the locomotion. Over a longer time scale, on the order of
1989; Fraser and Takahata, 2001). An inertial angular ac- minutes, their overall activity is well synchronized. Vector
celeration detector based on an orthogonal semicircular information is hence preserved (Fraser et al., 1997. 2001).
canal system could be easily added to a robot by using During these bouts of firing, the gain in the statocyst path-
connectivity and coding principles derived from crab equi- ways alters greatly so that perturbations ofangular acceler-
librium interneurons, which are described below. ation have a large effect (Fig. 3).
Crabs normally walk sideways. The leading legs pull and In the context ofdiscussing the role ofthe interneurons in
STATOCYSTS AND CRAB LOCOMOTION 157
Left Walking
2 3
1
Time in Seconds
A
Cell A, Left Connective
Figure 2. (A) Extension phases ofleft and right 2nd to5thlegs during a short sequence ofwalking tothe
left by a crab. The extracellularrecording shows cell A inthe leftesophageal connective. The series ofbursts
ofactivityaremorerelatedtoslightangularexcursionsofthebody(<j>)thantothegaitpattern.<f>istheclockwise
angulardisplacementofthe body ofthe crab around the horizontal longitudinal axis. (B)The effect ofcutting
the right esophageal connective on locomotion in the crab Carcinus maenas. Gait alters and the crab prefers
walkingleft. Regardlessofthedirectionofwalking,thecrabalwaysturnscounterclockwise(Bethe, 1897).This
isthedirectionthatoptimally excitesCell B in therightconnective. Electrical stimulation ofthecutendofthe
connective will straighten orreverse the counterclockwise movement.
locomotion. Fraser (1982) points out that "where a behavior sors, and phase- and amplitude-modulating sensory feed-
involves vectorial output in more than one dimension, or back(Ayersetal., 1998). Stepping rates forsuchmodelsare
where feedback loops are involved, then the output mea- low. Itmaybe thatthe crabhas more similarities tothe stick
sured by displacement ofappendages or by muscle activity insect model than to the lobster model in terms of its
is no longer an adequate measure of the behavior ... in reliance on sensory control, and an orthogonal command set
terms ofunderstanding the underlying neural activity, loco- based on the equilibrium interneurons may be sufficient to
motion in crabs may be better described in terms of com- control a large part of its locomotion.
ponents of force and torque in the planes used by the The finding that the statocyst thread hair receptors alter
equilibrium cells rather than in terms of the gaits em- their activity under the influence of hydrostatic pressure
ployed." The angular displacements of crabs have been makes understanding oftheirrole more complicated (Fraser
monitored in orthogonal planes with a miniature triaxial and Macdonald, 1994; Fraser et al., 1996; Macdonald and
accelerometer. Fraser, 1999). Positive-going and negative-going modula-
Although proprioceptor input affects the activity of the tion ofthread hair spike frequency is thought to arise from
interneurons, their outputs in free-walking animals are not activation of the two directional classes of mechanorecep-
particularly complicated (Fraser, unpubl. data; Fraser. tors via the linking chorda because of the slight volume
1995). Interestingly, Cruse etal. (1998) and Schmitz (2001) changes associated with differential compressibility of the
state that in the stick insect there is little evidence for a cuticle and other tissue components. Although thread hairs
central pattern generator. Instead sensory information de- respond directly to alterations in hydrostatic pressure,
rived from leg position and ground contact, together with thread hair interneurons do not seem to do so. Tidal period
six different coupling mechanisms, allows selection be- rhythms of firing pattern in equilibrium interneurons occur
tween swing networks and stance networks. Lobster walk- and match those found for general locomotor activity (Nay-
ing has been successfully modeled with five main classes of lor and Atkinson, 1972; Fraser and Takahata. 2001). These
components: central pattern generators, command systems, are affected by hydrostatic pressure pulses or cycles, and
coordinating systems, proprioceptive andexteroceptive sen- spectral analyses of long sequences show that some of the
158 P. J. ERASER
10 15 20 25
Time
(hours)
Figure3. Long-termrecording fromequilibrium interneurons (spike frequency measuredevery 100s) in a
free-walkingcrab. Caninnsmaenas, takenintoconstantconditionsinanaquariumaftercaptureatlow tide.The
recording starts6h aftercapture. Arrows mark the occurrenceofhigh tides. High bouts ofactivity in thecells
correspond to loccmotor behavior in the crab, and there is clear tidal rhythmicity. (Redrawn from Eraser and
Takahata, 2001).
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