Insights for Robotic Design From Studies of the Control of Abdominal Position in Crayfish

5 Pages·2001·2.4 MB·

by  David L Macmillan

Reference: Biol. Bull. 200: 201-205. (April 2001)
From
Insights for Robotic Design Studies of the
Control of Abdominal Position in Crayfish
DAVID MACMILLAN* AND BLAIR W. PATULLO
L.
Department ofZoology, University ofMelbourne, Park\'ille, Victoria 3052, Australia
Abstract. Studies of the control of position and move- biology with interesting implications for biologically in-
ment of the abdomen of crayfish illustrate a number of spired robots: that arthropods achieve complex behavioral
features of invertebrate sensory-motor systems that have outcomes with few neurons, that assumptions derived from
implications for their use to inform robotic design. We use reduced preparations orparts ofanimals need to be tested in
the abdominal slow extensormotorsystem toillustrate three biologically meaningful situations in intact animals, and
ofthem here: first, the way in which a behaviorally flexible that it is important to have an appreciation ofthe impact of
length-servo device can be achieved with very few ele- natural selection when examining biological solutions to
ments; second, the importance ofknowledge ofthe biolog- engineering design problems.
ical and behavioral context in which the elements operate; The abdomen, or tail, ofthe crayfish is composed offive
third, that design solutions resulting from natural selection similar, articulated tubes connected by simple lateral hinges
have been constrained by the previous evolutionary history that permit movement only in the pitch plane (Fig. 1A). The
of the animal, which can affect the outcomes in ways that connection between the thorax and the first abdominal seg-
may not be immediately apparent in a design context. ment is different. It is surrounded by strong, flexible mem-
branes enclosing stout muscles anchored deep within the
Introduction thorax. In addition to movement above and below the hor-
Crayfish, and other crustaceans with tubular bodies, have izontal line ofthe body, thejoint allows limited rotation in
proprioceptive structures called muscle receptor organs the roll and yaw planes so that it acts as a limited-range
(MROs) spanning the articulations between the segments universal joint. The functional outcome is flexibility of
(Alexandrowicz. 1951 ). Each MRO signals the relative po- position and movement at the otherend ofthe tail where the
sition and movement of the two segments to which it biramous appendages (uropods) ofthe sixth abdominal seg-
attaches. Since the discovery of MROs. many different ment, together with the telson. form a tailfan (Fig. 1A). The
aspects of their biology have attracted the interest of neu- tailfanelementselevate anddepress and also slideovereach
robiologists (Fields, 1976; Macmillan, 2001). In this paper other laterally so that the whole tailfan can vary in size and
we combine data from the literature with insights from our can change shape from paddle to scoop. This flexibility at
MRO
current work on crayfish to highlight three aspects of the end ofthe hinged leverthat is the tail permits the animal
to modify the direction and magnitude of the forces gener-
*Author to whom correspondence should be addressed. E-mail: ated when it flexes and extends its tail for swimming and
[email protected]. balancing. The arrangement presents an interesting case
This paper was originally presented at a workshop titled Invertebrate study for biological solutions to problems associated with
Season Information Processing: Implicationsfor Biologically Inspired the dynamics and control of multi-jointed levers.
ACeunttoenrofmoorutsheSyNsatteimosn.alThAecawdoerkmsyhoopf,Scwiheinccehs.waWsohoedlsdHatolteh.eJM.asEsraickhJuosneststosn, The muscles controlling the movement of the tail are
from 15-17April2000.wassponsoredbytheCenterforAdvancedStudies divided into four matching sets: the slow and fast flexors
intheSpaceLifeSciencesattheMarineBiologicalLaboratory,andfunded and extensors. The fast flexors ventrally and fast extensors
bAygArtbehbeermeNevanittaitoiNnoaCnlsC:Ae2Ar-oC8n9Ca6.u.tiacccseassnodrySpmaocteoArdmnienuirsotnr;atMiRonO.undmeurscCloeopreercaetpitvoer daorresraelslypooncsicbulpeyfmoorsetscoafptehetaialbdfloimpibneahlavciaovritayn(dFisgw.iImBm)inagn.d
organ; SEMN, slow extensor motor neuron; SR, stretch receptor. Although related developmentally to their segment of ori-
201
202 D. L. MACMILLAN AND B. W. PATULLO
SEGMENTAL
ARTICULATION
Figure 1. (A) Lateral view of the crayfish abdomen showing the changing position and shape of the
segments and tailt'an during a movement from a mid-flexed position to full extension. Thejoints between the
abdominal segments permit movement only in the pitch plane, whereas that between the thorax and first
abdominal segment permits movement in pitch, roll,andyaw planes. (B) Diagramofa sectionofthe abdomen
showingplacementofthemainmuscleblocksincross-sectionandtheventralnervecordanditsconnectionwith
the MRO in one segment. (C) Summary of the nerve-muscle connections operating when (i) the SEMN4
program is operating and the SR load-compensation loop can be recruited, and (iil the SEMN3 program is
operating and the SR load-compensation loop is not recruited. Triangles and circles represent excitatory and
inhibitory synapsesrespectively. (D)PatternofactivityoftheSEMNsandSRsrecordedfromthedorsalnerves
during a platform drop extension (i) in abdominal segment 4 when the movement is unhindered, and (ii) in
abdominal segment 2 when a rod and mechanical stopprevent straightening ofthejoint spanned by this MRO
throughout theextensiontaking placeatthe otherabdominaljoints. Note thatthese recordingsaredisplayedon
different time and amplitude scales.
gin, they are organized into the overlapping muscle spirals sequentially and, to a lesserextent, by heterogeneity oftheir
familiarto lovers oflobsteras agourmetdelicacy. Common nerve and muscle. The pools ofmotorneurons employed by
connective tissue strands that run the length of the tail vertebrates to achieve fine control of their muscles need
ensure that they act as a coordinated unit when delivering space that the small-bodied arthropods do not have. Arthro-
their power. The slow flexor and extensor muscles, which pods achieve comparable levels of control with far fewer
are responsible for slow movements and postural adjust- neurons (insects typically have only two or three motor
ments, lie ventrally and dorsally respectively, in thin sheets neurons per muscle and crustaceans have up to five or six).
external to the bulk of the fast muscles and immediately They achieved this reduction in part by employing nerve-
beneath the surface of the exoskeleton (Fig. IB). muscle combinations ranging in their contraction character-
istics fromslowandgradual tofastandtwitching, andpartly
The Remarkable Parsimony of Arthropod
by evolving motor neurons that inhibit muscle contraction
Neuromuscular Control
in parallel with the more familiar ones that cause contrac-
Vertebrates achieve fine control in muscles primarily by tion. These developments massively increase the possibili-
having large numbers of motor units that can be recruited ties for a continuously graded range of contraction outputs
CRAYFISH POSITIONAL CONTROL 20
and for the integration of excitatory and inhibitory inputs for twitch or brief, strong contractions; SEMN4 and
throughout the control mechanism without a concomitant SEMN3 for rapidly developing and decaying smooth con-
increase in the number of motor neurons. These ingenious tractions; and SEMN2 for slowly developing, sustained
and effective ways ofreducing the numberofneurons could smooth contractions. Activation of SEMN5 reduces the
well be ofinterest in robotic design. The fact that variations contractions evoked by any contemporaneous exciter activ-
of these arrangements are found throughout the arthropods ity and also returns the membrane potential ofslower fibers
suggests that they evolved early. Comparative studies show to their resting level more rapidly following slow exciter
that they have not necessarily been advantageous in all activity, thereby increasing the rate of muscle relaxation.
subsequent behavioral situations and provide interesting What do we know about how the potential flexibility of
insights into ways in which design flexibility is achieved this parsimonious arrangement is employedby the crayfish?
from abase model constrained by itsevolutionary history to To answer this question we have to make a brief side trip
very few motor neurons (Paul, 1991). into the sensory biology of the MROs.
Each of the segmental muscle groups in the crayfish is
innervated byjust six motor neurons per segment; these are
conventionally numbered from 6to 1 indescending orderof The Sensory Biology of the Muscle Receptor Organs
axonal diameter (Fields and Kennedy. 1965; Fields. 1966;
Drummond and Macmillan. 1998a,b). Each displays partic- A pair of MROs span the articulations between adjacent
ular functional characteristics exemplified by the slow ex- abdominal segments on each side of the body (Fig. IB).
tensor sensory-motor system about which most is known Each pair of MROs has two stretch receptor (SR) neurons,
andon whichwewillconcentrate here. Slowextensormotor a large, high-threshold phasic neuron and a smaller, low-
neuron 6 (SEMN6) is the largest motorneuron in the group. threshold, tonic one. These respond to changes in the ten-
It innervates predominantly the fastest fibers in the slow sion ofa small, innervated receptor muscle strand in which
extensor muscle. At low firing frequencies it produces large they are embedded. Because the muscle spans the articula-
membrane responses that facilitate rapidly and sum when tion, the SRs monitor the position of the abdominal seg-
the frequency of stimulation is high to produce strong, ments relative to one another, and because the strand is
twitch-type contractions. SEMN5 is slightly smaller in di- innervated, their level of activity, or set point, can be
ameter than SEMN6. Its effect on the muscle potential is adjusted from the central nervous system. SR activity levels
inhibitory that is. it produces ionic permeability changes can also be adjusted by the axons of inhibitory cells called
that hyperpolarize the muscle membrane and move its ex- accessory motor neurons (ACC) that synapse directly onto
citability away from the threshold for contraction, thereby the SR surface and inhibit or delay sensory spike activation
modifying the nature ofthe contraction produced by exciter (Fig. ICi). The receptormuscles lie in parallel with the slow
activity. SEMN4 and SEMN3 are almost indistinguishable extensor muscle but are not powerful enough to assist with
in size and innervate almost the same population of slow joint movement. These elements and theirarrangement sug-
extensor muscle fibers throughout all the slow extensor gest those an engineer might employ in designing a servo-
muscle bundles. They both evoke small to medium-sized controlled load-compensating device (Fig. ICi).
responses that show modest facilitation and sum readily to Analysis reveals that this sophisticated and economical
produce smooth contractions at higher frequencies. SEMN2 arrangement ofelements has the potential to deliver flexible
is a small neuron that innervates almost all the slow exten- abdominal control. Experiments on semi-intact and isolated
sor muscle fibers. Its activation produces small, non-facili- abdominal preparations (mainly in Procambarus clarkiiand
tating muscle responses that sum to produce strong, slow Cherax destructor) reveal a number of connections and
musclecontractions at high frequencies. SEMN1 is aneuron reflexes involving the tonic SRs and the motor neurons in
of about the same size, but its muscle potentials and con- the local and adjacent segments (Fields. 1976; Drummond
tractions are small, so its physiology is not well docu- and Macmillan, 1998a; summarized in Fig. 1C). Activation
mented. From a design perspective, these elements provide of the tonic SR excites ACC, which inhibits the sensory
for a full range of control options in the slow-fast and neuron itself (Eckert. 1961) a negative feedback loop that
fine-coarse spectra while preserving remarkable component radiates weakly to adjacent segments. Functionally, this
economy. loop provides a classic myotatic reflex: it damps small
This briefoutline ofthe innervation ofthis major muscle displacements ofthejoint by externally imposed force, and
series shows that although the slow extensors in each seg- it may also damp SR reflex loops. The tonic SR also excites
ment are controlled by bilateral pairs of only six motor the ipsilateral SEMN2 in its own segment, the motorneuron
neurons, the flexibility inherent in their properties and pat- that produces slow sustained contractions in most of the
terns of innervation together with the trick of peripheral slow extensor muscle fibers. This is the basis of a "resis-
inhibition provide the same sort of flexibility available to tance reflex." If the joint is flexed so that the tonic SR is
multi-neuronal vertebrate equivalents. SEMN6 can be used activated, it will excite SEMN2, which will fire and extend
204 D. L. MACMILLAN AND B. W. PATULLO
the joint until the receptor is unloaded and stops firing 1999a,b). When an immersedcrayfish loses contact with the
(Fields, 1966; Fields et at.. 1967). substrate, it extends its abdomen so that it falls in a bal-
Another important feature ofthe neuromuscular wiring is anced, feet-down attitude, ready to walk as soon as it lands.
that SEMN4 innervates both the slow extensor muscle and This type of extension movement can be evoked by drop-
the receptor muscle so that both could contract synchro- ping a hinged platform on which the animal is standing
nously when it is activated. This relationship spawned a (Larimer and Eggleston. 1971). The behavior was therefore
hypothesis about the way in which feedback could operate dubbed "a platform-drop extension." The outcome of our
on the tonic sensor to produce different behavioral outputs. platform-drop experiments provided a sharpreminderofthe
Ifcentral drive forextension included SEMN4, the tonic SR importance of evaluating hypotheses derived from reduc-
would not be activated during the extension because the tionist analysis by testing them in the real world of the
MRO
receptor muscle would contract with the main exten- animal. This caution is particularly germane ifthe interpre-
sormuscle. Ifthe movement met with resistance and therate tations are to inform or lead robotic design.
ofextension slowed, the receptor muscle would continue to In C. destructor, the tonic SR was invariably active when
contract at the rate determined by the central drive onto the animal was in the resting position with its abdomen
SEMN4. Rising tension in the receptor muscle would acti- curled beneath the body. The neuron fired very regularly,
vate the SRto recruit SEMN2 orincrease its firing rate until with a frequency around 16 Hz (Fig. ID), the actual rate
the receptor was again unloaded. The circuitry is also con- being slightly higher or lowerdepending on the whetherthe
figured to permit the same movement without activation of abdomen was more or less flexed. Activity was seen in the
SR-mediated load compensation (Fig. ICii). If the central SEMNs as soon as the platform was dropped to initiate the
drive for extension were directed through SEMN3 rather extension, but by the time extension movement was appar-
than SEMN4. the same muscle fibers wouldbe activatedbut ent to an observer, the SR had ceased firing (Fig. IDi). This
the receptor muscle would not contract during the move- result surprised us because previous results from other spe-
ment, and thus the length-servo loop would not be activated. cies suggested that the SR would fire throughout the exten-
This is how this sensory-motor clusterappears to operate in sion (Sokolove, 1973). It could, however, be explained in
isolated C. destructor preparations. The SEMN3 and system terms if the SR falls silent because the receptor
SEMN4 are not active together during spontaneous activity muscle and the working extensor muscle are contracting at
(Dnimmond and Macmillan, 1998a). and SEMN6 only fires about the same rate but with the straightening of the joint
at the peak of bursts of spontaneous activity in SEMN4 or just slightly leading the contraction of the receptor muscle.
SEMN3. SEMN2, on the other hand, can be recruited at any To test this possibility, we recorded from the SR in a
stage during ongoing activity in either unit. The pattern of segment that was prevented from straightening at all be-
firing in SEMN5, the inhibitor, suggests that it is used both cause of a small rod inserted between two acrylic plastic
to inhibit extensor contractions for example, by firing blocks glued either side of the joint. In this situation, the
during flexor muscle activity and also to move the con- expected load compensation occurred, as evidenced by the
tractions due to repetitive activation of the intermediate increase in output by the motorneuronscompared with their
fast-slow units SEMN3 and SEMN4 towards the more firing rates in the unblocked situation (Fig. IDii). It was not,
phasic end oftheir spectrum by suppressing their tendency however, due to recruitment ofthe local MRO. because the
to sum responses. In summary, there is ample potential for rate of firing in the SR remained constant throughout the
remarkable functional flexibility, notwithstanding the small extension movement (Fig. IDii). Some otherreceptors must
number of neurons involved. have been responsible. This outcome was also unexpected
because of earlier indications from other species that the
The Operation of the Receptors in Freely MROs might be involved in load compensation (Sokolove,
Behaving Animals 1973). We hypothesized, however, that the reason the SR
load-compensation pathway is not selected for platform-
The finding that circuitry is capable ofproducing outputs drop extensions is that, in this situation, the animal uses the
predicted by a hypothesis and that it does so in non-behav- SEMN3 mode ratherthan the SEMN4one. Extension in this
ioral, dissected preparations is a valuable step towards un- context is part ofa stability orbalancing behaviorthat gives
derstanding how it might function, but from a robotics the body a parachute-like profile. In the unlikely event that
viewpoint, observation of its function and role in the bio- the animal encounters resistance during its fall through the
logical and behavioral world ofthe animal is essential. We water, it can then change posture to prepare for defense or
therefore setouttoexamine how the MROs and SRsoperate other behaviors, some of which may involve the SR-
in intact, freely behaving animals. Using surface markings SEMN4 load-compensation loop. To test this hypothesis,
to locate the position of the MROs, we implanted fine wire we used ourability to record from freely moving animals to
electrodes to make long-term recordings from the SRs and study the activity ofthe SRs and SEMNs during a range of
the SEMNs in C. destructor (McCarthy and Macmillan, otherbehaviors, including some such as the extension that
CRAYFISH POSITIONAL CONTROL 20:.
accompanies the assumption of the defense posture in Australian Research Council to DLM and from NASA
which load compensation, possibly mediated by the SR under Cooperative Agreement NCC 2-896.
loop, could be expected to occur. As yet. we have found no
behavior in C. destructor in which the SR-SEMN4 loop is Literature Cited
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defence. J. Exp. Zoo/, (in press).
We gratefully acknowledge the support of NASA for Paul, D. H. 1991. Pedigrees of neurobehavioral circuits: tracing the
underwriting the stimulating cross-disciplinary ISIP-BIAS aevnodlunteiounroonfsnionvemlebmebhearvsiorosfbryelcatoemdpatraixna.g Bmroationr Bpaethtaevr.ns,Evmouls.cle3s8:,
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