Insect Locomotion Proceedings of Symposium 4.5 from the XVII. International Congress of Entomology held at the University of Hamburg, August 1984 Organization: Deutsche Gesellschaft fiir allgemeine und angewandte Entomologie (German Society of General and Applied Entomology) Michael Gewecke and Gernot Wendler (eds.) With contributions from Moray Anderson, Ulrich Blssler, Christiane K. Bauer, Holk Cruse, Jeffrey Dean, Fred Delcomyn, John L. Eaton, Robert F. Franklin, Michael Gewecke, Karl Georg Gtitz, Graham J. Goldsworthy, Gerhard Heide, Lllrich Horsmann, Reinhold Hustert, Jiirg PeterJander, Klaus Kamper, Thomas Kriippel, Angela B. Lange, Thomas A. Miller, Bernhard Mtihl, Lutz Neumann, Ian Orchard, Reginald C. Rainey, Heinrich Reichert, Meldrum Robertson, Hugh Fraser Rowell, Georg Riippell, Hans Scharstein, Josef Schmitz,L.P. Schouest, Manfred Spiiler,Jasmine Stabel, HarryTeuber, Hermann Wagner, Gernot Wendler, Colin H. Wheeler 1985 ' With 170 figures and 5 tables Verlag Paul Parey Berlin and Hamburg
Transcript
Insect Locomotion
Proceedings of Symposium 4.5from the XVII. International Congress of Entomology
held at the University of Hamburg, August 1984
Organization:Deutsche Gesellschaft fiir allgemeine und angewandte Entomologie
(German Society of General and Applied Entomology)
Michael Gewecke and Gernot Wendler (eds.)
With contributions from Moray Anderson, Ulrich Blssler, Christiane K. Bauer, HolkCruse, Jeffrey Dean, Fred Delcomyn, John L. Eaton, Robert F. Franklin, MichaelGewecke, Karl Georg Gtitz, Graham J. Goldsworthy, Gerhard Heide, Lllrich Horsmann,Reinhold Hustert, Jiirg PeterJander, Klaus Kamper, Thomas Kriippel, Angela B. Lange,Thomas A. Miller, Bernhard Mtihl, Lutz Neumann, Ian Orchard, Reginald C. Rainey,Heinrich Reichert, Meldrum Robertson, Hugh Fraser Rowell, Georg Riippell, HansScharstein, Josef Schmitz,L.P. Schouest, Manfred Spiiler,Jasmine Stabel, HarryTeuber,Hermann Wagner, Gernot Wendler, Colin H. Wheeler
1985 ' With 170 figures and 5 tables
Verlag Paul Parey Berlin and Hamburg
heum, Universitit Hamburg,
Icyctel ll9, D-5000 Kiiln 41,
tLc *dc c 1rt of the materialr.c d iktilns, recitation,a,dnmgcin data banks.
-dcfudh.traplivate use,
GAyrilt lrrr. the "-ount of
5r,hy
PREFACE
January 1985
Locomotion permits local adaptation of an insect to its environment. By walking,jumping, swimming or flying, an insect reaehes an essential goal, e. g. food,a mate or wintering area, or it escapes from danger, e. g. drought or a predator.Insect locomotion is predominantly performed by leg or wing movements whichtransfer mechanical forces from the body to the opposing medium. To beeffective, these forces have to be adequate in magnitude, direction and timing.Nearly all organs of an insect contribute to locomotion either in gaining chemicalenergy from food or in its conversion into mechanical energy.
The co-ordinated movements of legs and wings as well as the movementsof the whole animal in space are dependent on metabolism, respiration, internaltransport, muscle contraction, neural, hormonal and sensory control, andmechanical, hydro- or aerodynamic mechanisms. Aspects of these topics formthe basis for the articles in this book. The analyses span from the cellular tothe system level, and from physiological principles to applied problems.
The book is based on lectures of the symposium rlnsect Locomotionr, andallied poster arid film sessions, held at the University of Hamburg during thelTth International Congress of Entomology in August 1984. This meeting offeredthe rare opportunity to present and compare the work of diverse groups ofphysiologists investigating the various forms of insect locomotion. The paperssummarized in the present proceedings give a topical synopsis of current problemsin the field of research, and of new perspectives for the future. Therefore, thisbook adresses both scientist and student.
We gratefully acknowledge the help of the organizing committee of thel Tth Internationat Congress of Entomology, especially Prof. Dr. BERNDTHEYDEMANN, Prof. Dr- HANS STRUMPEL and Dr. THOMAS TISCHLER, andof the president of the University Hamburg, Dr; Dr. PETER FISCHER-APPELT.We also like to thank those co-work€rs from the University of Hamburg whoprepared the manuscript of this book: HANNELORE SCHWARZ for conscientiouslytyping the papers and ULRICH BAHNSEN, EVELIN KRUSE and CHRISTIANWEYMAYR for skillfully producing a camera-ready layout. The publication ofthe book was enabled by the generosity of Dr. RUDOLF GEORGI; owner of VerlagPaul Parey. We are greatly indepted to him.
MTCHAEL GEWECKE, Hamburg
GERNOT WENDLER, K6IN
1.1 INSECT LOCOMOTION: PAST, PRESENT AND FUTIIRE
FRED DELCOMYN
ABSTRACT
In the decade or so since the last major conference on locomotion was held,research. in the field of insect locomotion has taken an entirely new direction.Ten years ago the major question being asked was, what is the nature of theneural mechanism that is responsible for the generation and coordination of therepetitive movements, associated with locomotion in animals? Now, however,there is an entirely different research emphasis, and the main question is, howdoes sensory feedback .from the moving body or its appendages interact. witha centrally generated program of motor control to produce the well coordinatedand well adapted behavior that can be observed in the intact animal? In thisarticle, the major themes of research being carried out a decade ago, the themesof current research, and the themes of research likely to be initiated in thenext few years, will be discussed.
INTRODUCTION
Symposia devoted to the topic of insect locomotion are relatively rare. In fact,except for a meeting in 1980 that was devoted only to .locomotor mechanicsand energetics (HERREID & ,FOURTNER, l98l), the meeting that was the occasionfor the papers that follow was the first at which the subject was consideredsince a conference held at Valley Forge, Pennsylvania, nearly a decade ago(HERMAN et al., 1976).
Since meetings at which insect locomotion is discussed are held soinfrequently, the occurrence of one is a good opportunity for researchers .totake stock of their field. Taking stock of a field is usually done by means ofa traditional review, in which the latest research results are served on a baseof the work that preceded them, occasionally garnished with the reviewerrs opinionas to their meaning. However, there are at least two reasons why this .articleshould not be a traditional review of this type. First, it would be redundant.Several'reviews of different aspects of. insect locomotion have recently appearedor will soon appear (walking: DELCOMYN, 1981, 1984, 1985a; GRAHAM, 1985;flying: ROBERTSON & PEARSON, 1984, 1985b). Therefore, there seems littlepoint to add yet another at this time. Secondly, a traditional review all toooften contains only a rehash of the same familiar data, with little discussionof trends in the field. Those interested in insect locomotion deserve better thanthis.
What I wish to do instead is to set out for readers what I .consider someof the recent trends in insect locomotion research. Naturally, specific examplesof the trends I discuss will be included, but my objective is to give readerssomething of the flavor of current research in locornotion, not just to summarizeall the recent results. By taking this approach, I hope to provide a context forthe research papers that follow, making it easier for readers to understand thepapers, and to app.reciate where in the field the papers fit. Since the ideas of
GcrreckeflAlendler (eds.), InieciLocomotionO 1985 Paul Parey
(
today arise from those of yesterday, I will discuss first the main ideas and the
thruit of research at the time of .the landmark Valley Forge meeting, and thenih. "on""pt.
that are receiving attention today. Finally, I will^ conclude withmy guess is to what might be expected from research in the near future.
THE PAST
The present is clearly shaped by the past. What main themes of research werepredorninant at the iir. of the Valley Forge -conference.of
a decade ago, and
irow did these lead to the main issues today? I suggest that at that time therewas just one major question with which researchers were primarily concerned'This question wai, what is the mechanism by which the central nervous systemgenerates patterned motor output?
The year 1975, when this conference was held, was one in which it was
becoming *idely .ecognized that in every animal, the repetitive movements and
muscle ictivities that" formed the basis of rhythmic behavior could in principle
be generated by the central nervous system in the com-plete absence of rhythmic;;d"ry- feeOUa6t from the moving paits of the body (DELCOMYN, 1980). Thus,
the emphasis of most of the papers during that conference, and most of theprivate discussion between reseaichers as well, was naturally on the mechanisms
ly which parterned output could be generated. It was clearly recognized thatr6nrory information played an important modulatory role in est-ablishing the precise
timing of muscle uition th.t wis observable in intact animals, but the emphasis
of m6st of the discussion was squarely on the issue of central mechanisms, not
on that of sensory effects.In order io give the reader the flavor of what was considered
state-of-the-art about a decade ago, I will discuss two examples of work thatwas belng pursued at that time. Both examples, one from research on flightand one irom walking, illustrate the main thrust of research at the time, which
was trying to underst;nd how rhythmic patterns are Senerated'
LOCUST FLIGHT. It had already been established by the landmark work of D'M'
wir_-soN (1961) rhar thl alternating elevation and depression of the wings of
;'fl;i;g lotust'could be produced in-the complete absence of any rhythmic sensory
input that could servl J, -,irning
cues. - lndeid, ir was WILSONIs pioneering work
that had served to stimutate riuch of the tremendous interest in the concept
of pattern Senerators that existed in the mid-1970rs'"' "-iiun-nbws (rgzsi, usirt-n"*ry devetoped intracellular rechniques to record
from flight *oto. n"Lronr "i.r tf," locust' central nervous system' investigated
ii," lGrri system. His objective .lvas to describe the cellular mechanisms that
allowed the generation- of in. flight pattern. One specific question that BURROWS
was interesteO in answlring was- whether motor neurons played an integral part
i, th" S"n.ration of the f'light patterR, or if motor neurons were only passive
followeri of a pattern generated by interneurons'His results, summ"arized in Fig. 1, strongly suggested that the motor neurons
couto nor by ihemselves generate an appropriately timed pattern of activity.
Instead, interneurons]- ."ptZt"n'"a '' tld iigute by unnumbered --"'l:]":, j:!
rectangles, *"ru n""urr"ry in orde-r-fo|-^t!r9 system to generate the proper tlmlng
of flighr. rrrtr,".*oi-"]'' nuniows (1973) and HOyLE & BURROWS (1973)
."gg"ri"o that the system .of jnterneurons could run without any feedback from
the motor neurons, since the latter never showed any flight output without the
presence of excitatolf'rynupii. potentials, and since properly timed epsprs could
be recorded just before the motor output in a preparation started, or just after
it stopped.
DELCOMYN
of walkingcocKROACH WALKING. InvestiSation of the physiological .basis of walkingr:-^ ^r ,,,^.t hoina ^q"ricd orrt in the mid-19701s.U"t"rio. \/as a second major linJ of wo-rk- being carried ou,' ,tl -t-h"Fil[i't"6*" e iLii" li6zoi,'"uti,i' "*ttucellular
ricording techniques' had alreadv
demonstrated that it was'possiSle to record patterned, alternating motor output
in extensor and flexor aotoa n"rr"s in a cockroach preparation that lacked all
DELCOMYN
rrls$ frrst the main ideas and thet \-a:ie;.' Forge meeting, and thenr1r. Fr:ail1', I will conclude withEarcj: ln the near future.
It xrarr rhemes of research werecmie::ice of a decade ago, andI s;4;ge-.r rhat at that time therercbe:,. -; ere primarily concerned.rhic:. t:e central nervous system
i he-:. * as one in which it wasaI, ::e .epetitive movements andtbm:c :e:ral'ior could in principler"lp .:::pleie absence of rhythmicr bocr DELCOMYN, 1980). Thus,hoa c::ierence, and most of thel"as :a:uiall)' on the mechanisms. It r-as clearly recognized thatry r:-: in establishing the preciseintecr arirnals, but the emphasisissue :f central mechanisms, not
lilor : f what was consideredEusi$ :a r eramples of work thatles, :--.e Iiom research on flightf cf :::earch at the time, whichlre gere:aced.
od by ::e landmark work of D.M.amc :::ression of the wings of
e ab-:.:e of any rhythmic sensoryit *:.: \\-lLSONrs pioneering workEtrel:.c,:irs interest in the conceptllilsima:e--::iar techniques to record[ra"] :e:',':us system, investigatedibe r:,e cellular mechanisms thate spe::f.e question that BURROWSr rrcL::ns played an integral partrro :: r-eurons were only passive
srgEestec that the motor neuronsimelr rimed pattern of activity.Ee li' unnumbered circles andEm r-a generate the proper timingd I101'LE & BURROWS (1973)ld ri:i n-ithout any feedback fromred::i'flight output rvithout thermce properly timed epsprs couldFe;.1:aiion started, or just after
o pai:ioiogical basls of walkingI car:red out in the mid-1970rs.rem::rng techniques, had alreadyDtter:,:c, alternating motor output\r<xrc: preparation that lacked all
lnsect locomotion
dep ress
ffivote
a lnhibitonyA Excitotor-y
Fig. l. A diagram of pathways suggested by BURROWS to be responsible forthe alternating activity of elevator and depressor wing muscles in a locust. Notethat only motor neurons (numbered circles) are individually identified. (FromBURROWS, 1973).
sensory connections in the thorax. It seemed likely, therefore, that walkingbehavior was also generated by one or more pattern generators.
This work was extended by the investigarions of pEARSoN & FOURTNER(1975). Using newly developed methods for recording intracellularly from neuriresin neuropile, they searched for neurons that were members of the neural networkthought to be responsible for controlling the alternating flexion and extensionmovements of individual legs during walking. Their efforts yielded a numberof small, identifiable, nonspiking interneurons (interneurons tlat generated noaction potentials) that seemed to have a strong influence over aciivity in legmotor neurons. Altogether they identified four different types of such nonspikin!interneurons. Each showed a dramatic, rhythmic fluctuation of membrane potentialsynchronized with the alternating extensor and flexor motor bursts recorded fromleg motor nerves. The interneurons differed in the phasing of their depolarizationsrelative to the activity of the extensor and flexor motoi neurons. That is, someof the interneurons were depolarized during extensor bursts, others weredepolarized during flexor bursts. Furthermore, exciting or inhibiting these cellsby passing depolarizing or hyperpolarizing current through them, resulted inexcitation or inhibition of extensor or flexor motor neurons; the details concerningwhich motor neurons were affected, and whether they were excited or inhibitedldiffered from one type of interneuron to another.
one line of evidence that these nonspiking interneurons were part of therhythm-generating network that controlled the activity of extensor and flexorleg muscles was especially strong. If a nonspiking interneuron that wasspontaneously exhibiting rhythmic oscillations in its membrane potential werestimulated (depolarized) with a brief pulse of currenr, the ongoing rhythm ofalternating activity in extensor and flexor motor neurons would be reiet (Fig.2). Neurons that were passive followers of signals that were patterned elsewherewould not be expected to reset the rhythm if they were stimulated, so PEARSoN& FOURTNER concluded that the nonspiking cells v/ere part of the rhyrhmgenerating network.
DELCOMYN
400 msFig. 2. Intracellular (bottom) and extracellular (top) records from a nonspiking
ini"rn"u.on and a leg motor nerve, respectively, showing the resetting effectof stimulating the inierneuron. The'recoid was taken from a cockroach' (From
PEARSON & FOURTNER, l97s).
Additional work by FOURTNER (1976) showed that other nonspiking cells
existed. These neurons appeared to control the activity of entire sets of the
cells FOURTNER and PbARSON had originally described, -for by stimulatinS
iA"p"f"riri"gt a single neuron, he could elicit alternating, rhythmic activity in
both e*tenior and Jtexor moto. nerves (Fig. 3)' None of the original neurons
could influence more than one set of motor neurons'
oTHER WORK. The selection for emphasis of just two examples of a single
line of work should not be interpreted to mean that other important work was
noi U"ing carried out at the time. This was certainly not the case. To take
i; ;; example, at about that time, GRAHAM (1922) was developing and
modeling important theoretical concepts about how the walking system might
Ue coniotted. ft. point is that the most important research, as perceived at
the time, was research that addressed the question of h9w _a .central pattern
i"r"r"tor' worked, in terms of the interactions of. individual neurons. The
i1nfortun". of sensory modulation of a centrally generated pattern for production
of'a behaviorally relevant motor pattern was acknowledged, but the emphasis
was firmly on the central part of the equation'
Fig. 3.nervesactivity1976).
Extracellular records from flexor (top)
from the leg of a cockroach, showing thewhen a single nonspiking interneuron is
ffiand extensor (bottom) motorgeneration of rhYthmic motor
stimulated. (From FOURTNER,
DELCOMYN
I O,'
the resetting effectfiom a cockroach. (From
rtat other nonspiking cellsof entire sets of the
for by stimulatingrhythmic activity in
of the original neurons
tro examples of a singleother important work was
not the case. To take(1972) was developing andthe walking system mightresearch, as perceived atof how a central pattern
of individual neurons. Thepattern for production
ledged, but the emphasis
'400ms '
ruords from a nonspiking
hd*.and extensor (bottom) motorgeneration of rhythmic motor
stimulated. (From FOURTNER,
Insect locomotion
THE PRESENT
Nearly a decade has passed since the Valley Forge meeting. what changes haveoccurred in the field of insect locomotion'during that timle, and what are themain themes of research in the field today? It seems to me that there are twomain issues or themes currently being pursued. The first, cellular analysis ofpattern Senerators, is a direct intellectual and technical descendent of the workconsidered so important a decade ago. Now, as then, it is being carried outmainly by a few exceptionally skillful investigators. The second major theme,what one might call behaviorally oriented studies, has also gained its importanceprimarily through the concerted efforts of a few individuals. These ind'ividuals,by emphasizing the careful analysis of an insectrs behavior in response tointerference with its locomotion, have forced other researchers to recognizethe important role of sensory feedback in coordinating the movements ofappendages. There is one especially interesting aspect of these two ratherdifferent lines of research. This is that in spite of the different nature of themain question being asked in each, researchers in both areas are recognizingthe critical importance of sensory feedback in locomotion.
Let us now consider a few selected examples of work in these areas.
CELLULAR ANALYSIS OF PATTERN GENERATORS. In the analysis of thecellular basis of pattern generation, the emphasis has shifted from ihe behaviorof walking to that of flight. Using the flight system, what advances have beenmade in our understanding of pattern generators? First, application of newlyrefined techniques for recording intracellularly from and staining even smallneurons has made it possible to identify a large number of interneurons thatappear to be involved in flight (ROBERTSON & PEARSON, lg83; Fig.4). Manyof these neurons, selected for study by meeting the criterion that they showa rhythmic oscillation of membrane potential that is synchronized with the flightrhythm recorded from the flight muscles, are identifiable. That is, they can
Fig. 4. Diagrams illustrating the morphology of sets of homologous interneuronsin the third thoracic ganglion (and the anatomically fused abdominal gangliaI - 3) of the locust. Each of these interneurons shows rhythmic activity -duringperiods of activity in flight muscles. (From ROBERTSON & PEARSON, l9g3).
DELCOMYN
be recognized individually by their unique location, structure, and physiologicalproperties. Others are not unique, but are members of small sets of cells thatare indistinguishable from one another, yet as a group can easily be distinguishedfrom other groups of cells by their physiological and morphological characteristics.Interneurons that showed rhythmic activity in time with the flight pattern havebeen found in the meso- and metathoracic ganglia, including that part of thelatter that derives embryologically from the first three abdominal ganglia. Findingneurons apparently involved in flight that are located in abdominal ganglia hasbeen taken to support the hypothesis that insect wings originated from pleuralappendages, not paranotal lobes (ROBERTSON et al., 1982).
Just because a neuron shows rhythmic fluctuations in membrane potentialin time with a particular piece of behavior does not mean that the neuron isresponsible for or aids in the generation of the rhythm itself. Many of theinterneurons found in the locust thoracic ganglia could be stimulated or inhibitedby the passage of current during the execution of the flight motor pattern withoutany noticeable effect on the pattern. Such neurons were assumed to be passivefollowers whose function did not include rhythm generation. However, a fewneurons were found to have the ability to reset the timing of the flight rhythmwhen they were stimulated out of synchrony with it (Fig. 5). Such neurons wereconsidered to be members of the network of neurons that was responsible forgenerating the rhythm of activity in the flight motor neurons (ROBERTSON &PEARSON, 1983, 1984, 1985a).
o.a
303!to: n = l6a
hth"SdmJtur Pfur
Fig. 5. A) A diagram illusrrating the morphology of one interneuron in the meso'and metathoracic ganglia of a locust. This interneuron has widespread synapticconnections to the neurons shown in Fig. 4. B) When this neuron is stimulated,ir has the ability to reset the rhythm of flight activity. (From ROBERTSON& PEARSON, 1985a).
The main question of interest still is, how does the system work? Thedefinitive answer cannot be given yet, but one unexpected new finding has been
reported: there are not separate and distinct pattern generators for each wing,noi even one for each pair of wings. Instead, there is just a single CPG thatcontrols the production of the properly timed motor output from all the wingmuscles at the same time (ROBERTSON & PEARSON, 1983, 1985b). It is clearthat this single, distributed network of neurons (Fig. 6) is much more complexthan had been thought previously, and that understanding its operation will notbe easy.
z6oat
Taca!
02
03
DELCOMYN
be recognized individually by their unique location, structure, and physiologicalproperties. Others are not unique, but are members of small sets of cells thatare indistinguishable from one another, yet as a group can easily be distinguishedfrom other groups of cells by their physiological and morphological characteristics.Interneurons that showed rhythmic activity in time with the flight pattern havebeen found in the meso- and metathoracic ganglia, including that part of thelatter rhat derives embryologically from the first three abdominal ganglia. Findingneurons apparently involved in fliSht that are located in abdominal ganglia hasbeen taken to support the hypothesis that insect wings originated from pleuralappendages, not paranotal lobes (ROBERTSON et al., 1982).
Just because a neuron shows rhythmic fluctuations in membrane potentialin time with a particular piece of behavior does not mean that the neuron isresponsible for or aids in the generation of the rhythm itself. Many of theinterneurons found in the locust thoracic ganglia could be stimulated or inhibitedby the passage of current during the execution of the flight motor pattern withoutany noticeable effect on the pattern. Such neurons were assumed to be passivefollowers whose function did not include rhythm generation. However, a fewneurons were found to have the ability to reset the timing of the flight rhythmwhen they were stimulated out of synchrony with it (Fig. 5). Such neurons wereconsidered to be members of the network of neurons that was responsible forgeneraring the rhythm of activity in the flight motor neurons (ROBERTSON &PEARSON, 1983, 1984, 1985a).
o = l6a
htJr"S-th.*.lPtux
Fig. 5. A) A diagram illustrating the morphology of one interneuron in the meso-
ani metathoracic ganglia of a locust. This interneuron has widespread synapticconnections to the neurons shown in Fig. 4. B) When this neuron is stimulated,it has rhe ability to reset the rhythm of flight activity. (From ROBERTSON
& PEARSON, 1985a).
The main question of interest still is, how does the system work? Thedefinitive answer cannot be given yet, but one unexpected new finding has been
reported: there are not separate and distinct pattern generators for each wing,noi even one for each pair of wings. Instead, there is just a single CPG thatcontrols the production of the properly timed motor output from all the wingmuscles at the same time (ROBERTSON & PEARSON, 1983, 1985b). It is clearthat this single, distributed network of neurons (Fig. 6) is much more complexthan had been thought previously, and that understanding its operation will notbe easy.
;":l
.']
02
o.3
+aE
7ooaf
?aca!
, DELCOMYN
adc:r. structure, and physiologicalmbers of small sets of cells thatr gr:rji can easily be distinguishedI ani norphological characteristics.rime a.ith the flight pattern havermgll=. rncluding that part of thetr i::- abdominal ganglia. Findingloca:ec in abdominal ganglia has
Ect E-:es originated from pleuralaL. : 332l.
ft,rcr:a:-:ns in membrane potentialbes -:: mean that the neuron isthe :.-,r'rnm itself. Many of the
n c:,u-: be stimulated or inhibitedof re :1rgnt motor pattern withoutErorns ;e!e assumed to be passivechm i::eration. However, a fe!i/tr r.e :rming of the flight rhythmrith r: Flg. 5). Such neurons were[F;:::s that was responsible for
!t :-::. reurons (ROBERTSON &
p' :: ::e interneuron in the meso-lt€r:€!::.: has widespread synapticB 'r\.i:: this neuron is stimulated,[igt: =.tif it]'. (From ROBERTSON
ho* :re: the system work? TheE u:er,:ecred new finding has beenpa::::: gelerators for each wing,
| ::-::: is just a single CPG thatI c:::: output from all the wingE{I{SO\. 1983, 1985b). It is clearus '--9. 6J is much more complexmde:::::::ing its operation will not
::g. 6. A diagram of part of thePE-{RSON to be responsible for the
n = '8. ; irg muscles in a locust. Note thatC ntrast this diagram with that inI 985b).
htlr"8tlnl6 Phae
neural circuit suggested by ROBERTSON &alternating activity of elevator and depressorall the numbered neurons are interneurons.Fig. l. (From ROBERTSON & PEARSON,
:.lsect locomotion
II,
The analysis of the pattern generator for flight outlined so far contains,-!rle that would have seemed out of place in discussions carried on a decade=go. However, there has been one significant change in the way investigatorsi:io are interested in cellular mechanisms think about the system. This change:as come in their view of the role played by sense organs that are phasically:ctive during repetitive behaviors. With regard to the flight system, WILSON5. GETTRUP (1963) had suggested that the only role of sense organs on or around:le wings was to provide a tonic influence over the frequency of wing beating.Tbat this was not entirely correct was suggested by WENDLER's (197 4lCemonstration that forced movement of a wing during flight could entrain the:tright rhythm. More recent work, on the wind-sensitive hairs on the head, hass_ho-1n that other phasic sensory input can also entrain the flight rhythmHORSMANN et al., lg83).
Investigations of this phenomenon at the level of individual, identifiable:ieurons (PEARSON et al., 1983) has made it clear thar wlLSoN & GETTRUpTs1963) original proposal was not correct. Instead, it has been shown that not
cnly can stretch receptors in the forewings entrain and reset the flight rhythm,as well as elevate the average wingbeat frequency, but that sensory feedbackrs essential to ensure proper timing between muscle bursts in the meso- and:rietathorax (HEDWIG & PEARS0N, 1984). Thus, the nerwork of neurons responsibletor producing the complete and proper flight behavior in the locust is not jusrihe cPG, the network of neurons that is primarily responsible for setting therasic rhythm of the motor output, but includes also the sensory signals that:relp to establish its final form and rhythm. This new view represents a radicaldeparture from the view held a decade ago, that sensory feedback acted primarilyro fine tune a centrally generated pattern that was already near normal. This.rewer view is supported by recent work of NEUMANN (19S5) and stronglydefended by WENDLER (1985) in his summary paper.
Interestingly enough, whereas a decade ago some of the most exciting and
ELFYATION- -------.SR
DELCOMYN
revealing work on pattern generators was being done on the walking system,work on this system has proved extremely difficult, and has therefore languished.In addition, some doubt has even been expressed that the results of PEARSON& FOURTNER (1975) were related to walking. Instead, it has been suggestedthat perhaps the rhythmic activity they observed represented grooming orsearching by the teg (ZILL, l98b). PEARSON (1985) himself has emphasized the
'unnaturilnesst of the deafferented preparation, and in view of the findings inthe locust, has suggested that one should no longer talk about pattern generationin walking systems lvithout considering sensory input.
BEHAVIORAL STUDIES. The second main line of work that has developed inthe field of insect locomotion over the last decade has been what I callbehaviorally oriented studies. There has been in locomotion research an oldtradition of investigating the mechanisms underlying the behavior by systematicallyinterfering with ai animalts ability to carry it out' then .carefully noting thebehavioral result. until recently, this approach has had few contemporaryadherents, as modern researcheri tended to work either on the behavior oflocomotion itself, or else directly on the physiological mechanisms thought tounderlie the behavior. However, suqh studies have become much more frequent
in recent years, and in my view represent a major line of research in the fieldtoday. The emphasis of these studies has been on how particular sense organs
cont;ibute to tLe coordination of appendages during locomotion. There have been
a few srudies of this type dealing with flight (such as those by WENDLER' 1974'
and HORSMANN et at., -1983,
cit-ed earlier), but for the most part' these studies
have been confined to investigations of the walking system.Two different approaches have been used to examine the role of sense
organs in walking behavior. These are, mechanical interference with walking,
ur"d int".f"."nce -*ith the operation of one or more sense organs in the legs'
in eactr case, one of the miin objects of the experiments is to learn something
about the way in which coordinated walking is regulated_ in the insect by
challenging the walking system, and observing how it responds. to- the challenge'
Several-oi the pup".r"in ihe present volumelake this approach (BASSLER' 1985;
rith the legs as the insectto adapt to the altered
has been to presentu rith a barrier or ditch.
&rn or a down and an up1976a; PEARSON &
obstacles of this kind? Thermder study. CRUSE (1976a)stepq barriers and ditches.to keep a fixed body height
rigid body, is less well ableit also is able to negotiate
ray in which it does thismove its two middle legs
rare in intact animals walking
Ee the obstruction that wasthis is made .impossible. For
the walking of a stick insectmoving as far forward as
yielded several observations,
and to a certain extent theio the cycle of stepping the
tered near the end of theprsh past the barrier for, a
rheel and moved backward in
Insect locomotion g
a- normal step, in good synchrony with the movements of the other legs. However,if the barrier was encountered halfway through the legrs forward swing, or .oon..,the leg made more vigorous and prolonged efforts ro get past the birrier, oftenpersisting in its attempts during several steps of the unobstructed legs. Movementsof the unobstructed legs were sometimes also measurably affected. Particularlynoticeable was a delay in the initiation of swing of the leg in front of theobstructed one.
_ Secondly, analysis of the walking gait suggested another feature of walkingunder these conditions: that the endpoint of the forward swing (protraction) o?rear or middle legs is guided by the leg just in fronr of each of them. Thatis, the position at which each middle or rear leg is placed down on the walkingsurface depends on the position of the anterior front or middle leg, respectively.The mode of control in which one leg follows the other is referred to asfollow-the-leader stepping, and was first described by CRUSE (lg7g). Althoughthis is a strategy that might be useful to an insect trying to negotiate roughrerrain, locusts seemed nor to use ir (PEARSON & FRANKLIN, 1gg4).
Another way of obstructing leg movements, in a sense, is to restrain themcompletely, by tying them up out of reach of the walking surface. Thisexperiment has been done with stick insecrs (GRAHAM, lg77) and withcockroaches (PEARSON & ILES, 1973). In both cases, an insecr in which thetwo middle legs have been restrained in this fashion has severe difficulty inwalking, and shows no or little coordination. The point to be emphasized hereis that the insects do not walk like those whose middle legs are missing entirely.
Another way of interfering with leg movements is less direct. This is bychanging the load on the legs. Changing load can be done by making the insectwalk up an incline or vertical wall, by making it drag a weight, or by havingit walk on a treadwheel and making it hard for the insect to turn the wheel.Two observations stand out. First, insects walking with an increased load, bywhatever means it is generated, tend to walk more slowly than do insects thatdo not have a load (GRAHAM & CRUSE, t96t; FOTH & GRAHAM, lg83a).Secondly, the legs tend to move farther forward during protraction before theyare placed back on the walking surface (BASSLER, l9z7; CRUSE, I976b).
In an elegant series of experiments, FOTH & GRAHAM (1983b) inducedstick insects to walk on a pair of treadwheels in which the load could be variedindependently in the two wheels. They found that as the load on the legs onone side of the body was increased, the legs on borh sides of the body slowedtheir stepping frequency, and remained synchronized. However, as the loaddifferential increased, the legs began to step at different frequencies, the lessheavily loaded legs stepping twice for every step of the others. In no case wasit observed that the legs of the loaded and unloaded sides stepped independently(out of synchrony) with one another.Interference with sense organ function. Mechanical interference with locomotionhas been carried out in order to observe the effect of a physical challengeto the walking control system. It is assumed implicitly by all of theinvestigators who have carried out this kind of experiment that the basis forthe animalrs adaptation to the experimental situation is detection of rheobstruction by one or more sense organs, generation of specific sensory signalsthat indicate the nature of the obstruction, and subsequent behavioral adjustmentof leg movements as a consequence of the presence of the specific sensorysignals. Experiments in which sense organs are interfered with directly are anattempt to test this assumption, as well as representing investigations of thespecific role that sense organs may play in coordinating leg movements.
Two somewhat different ways of interfering with normal sense organ functionhave been used. In one method, a sense organ is stimulated at a time duringwhich it is normally silent. Experiments of this type have been carried out onstick insects and locusts in which the femoral chordotonal organ of one leg hasbeen induced to give an incorrect signal (BASSLER, 1977, lgTg; GRAHAM &BASSLER, l98l). The chordotonal organ is normally anchored in the dorsal halfof the distal part of the femur. By cutting the receptor apodeme and reattachingit in the ventral half of the femur, to the tendon of the muscle that isresponsible for flexing the tibia, the organ will be stretched by tibial extensionrather than by tibial flexion, as is usually the case. Stretching this chordotonal
10 DELCOMYN
organ has a strong excitatory effect on muscles that extend the tibia.The results of this experiment have been similar in every case. When the
insect walks slowly, the tibia is not flexed or extended a great deal, and theleg with the crossed receptor is used entirely normally. However, if the animalstarts to move faster (an event that is accompanied by somewhat greater flexionand extension movements of its legs), the tibia of the operated leg is suddenlyextended, and held up and out from the body in what is known as the rsalutel
position (Fig. 7). This position may be maintained for many steps of the otherlegs, but if the insect slows down, the extended tibia may slowly relax and resumenormal stepping. As the tibia relaxes, it is often waved in proper synchronywirh the remaining legs (Fig. 7). While the operated leg is held in the saluteposition, the remaining legs adopt the gait typical of an animal with one leg(the operated one) missing (GRAHAM & BASSLER, 1981). If the tarsus of theleg being held in the salute position is gently touched, the leg is immediatelyflexed and placed on the walking surface. The leg takes one normal step, andis rhen lifted into a salute once again (GRAHAM & BASSLER, I98l).
R",R2
DEPRESSOR
lt.i'z
600
goo
ANGLE t20"
l-lls
Fig. 7. A drawing of the behavior during walking of the leg of a stick insectin which the receptor apodeme of the femoral chordotonal organ has been reversed(see text for more detail), as well as typical records of the movements of thatand other legs during walking. The trace labelled R2 DEPRESSOR is a schematicrepresentation of the electrical activity of the depressor muscle of the operatedleg during the wallc shown in the rop trace. (From BASSLER, 1983).
This behavior has been explained as follows. The output of the chordotonalorgan normally signals that the tibia of a leg has reached a particular stateof flexion, and that it should therefore extend. During slow walking, the organis in approximately the same state of tension in the operated leg as it is ina normal leg, and since the operated leg only flexes a little, it can still beused normally. However, as the leg is moved more vigorously, it is extendedfar enough that the repositioned chordotonal organ is strongly excited. The organin turn excites the tibial extensor muscles that normally would relieve the tensionon the organ. In this case, however, tibial extension only serves to excite itmore strongly yet, and the leg becomes locked into an extended position untilthe extensor muscle relaxes a bit.
MACMILLAN & KIEN (1983) have also succeeded in stimulating the femoralchordotonal organ of a locust at an inappropriate time. They implanted finewires into the femur over the organ, and stimulated it electrically at varioustimes during the stepping of the leg. When the stimulation rras applied late inthe step, the teg swung forward early. Stimulation at other times had no effect.
The second way in which sense organs have been interfered with has beento arrange for an organ to be stimulated continuously. It is not always possibleto stimulate a sense organ at some specific time, and applying continuous
-l Hz
R2
DELCOMYN
rh.ai: E\rend the tibia.r $.:ilai in every case. When ther ex:.i:ded a great deal, and thennr:,:.-y. However, if the animal
iarme: DI somewhat greater flexion& ,:: ::e operated leg is suddenlyItr x:r! is known as the rsalutel
um: ::r many steps of the othertib:= :ai slowly relax and resumeof:e: a aved in proper synchronyptr:::: :eg is held in the saluteyp,r,c'a, :: an animal with one leg[,ER. - 3811. If the tarsus of thep r:,.i::"1, the leg is immediatelYe.:5::ries one normal step, andlt & :issn-ER, 1981].
:.:ect locomotion 1t
::imulation is another way to assess the importance of the organ for normal:-,rrdination. Two different sense organs have been subjected to this procedure.: strck insects, hair plates and campaniform sensilla.
BASSLER (1977) has applied wax or orher similar substance to a hair plate-: the coxa of the leg of a stick insect. This procedure causes the haiis to-::d over permanently, as if the leg were at its normal extreme anterior position..:e procedure has no effect on a standing insect, and when the insect begins:. ri'alk, the treated leg retracts (that is, pushes the body forward) normally.::'.r'ever, while the leg is on the ground it moves back far beyond the position:::m which it would normally start its forward swing. If the insect walks rapidly,'-:.e leg may be picked up and swung forward from this extreme posterior position=. usual, but during slow walks, the affected leg will continue to grasp the,;=iking..surface at the end of its rearward movement, and not swing forward.
BASSLER (1977) has also arranged to srimulate campaniform sensilla:-:tinuously. The trochanter of many insects has a relatively dense population:: these cuticular stress receptors. If a small clamp is placed on the trochanter-: a stick insect (Fig. 8), the insect behaves similarly at some speeds of walking:-- animals with bent hair plates. That is, the leg pushes the body forward for,:e normal step, but then here too, instead of being protracted normally, keeps: -1\'ing to an extreme posterior position. One difference in this case is that.nas with a clamp on their campaniform sensilla do not step forward at all,='.en at high speeds of walking. It is clear that the clamp does not interfere:echanically with leg movements, because treated legs readily engage in searching::\'ements if they are deprived of tarsal contact when the animal is standing:'rll
: ig. 8. A drawing of the typical posture of: stick insect during walking, when a smallclamp has been attached to the trochanter:i a middle leg. The leg wirh the clampattached tends to maintain the positionshown throughout the entire sequence of'*alking. (From BASSLER, 1983).
IS THERE A CONSENSUS? I have discussed what I consider to be the two majorthemes of locomotion research over the last decade: research on the cellularmechanisms by which pattern generators operate, and behaviorally orientedresearch on the effects on walking of interfering with the animal in some way.It should be clear that in spite of the entirely different approaches and techniquesbeing used, and in spite of the different questions being asked in the two typesof work, they have converged to a single view of the control of insectlocomotion. In the case of both flying and walking, the view has evolved thatsensory input is essential to the proper performance of the behavior, Mostresearchers are convinced that central pattern generators exist, that is, thatthere are networks of neurons that are responsible for generating the basicrhythmicity of the locomotor pattern. But most workers are equally convinced,from both the single cell and the behavioral studies, that without phasic sensory
r"i.k;5 -- :ie leg of a stick insectEhc,ri-:::.:: organ has been reversedrec:::: :r the movements of that
ilec ?,1 DEPRESSOR is a schematic
' ie-::::;c: muscle of the operated
om f r-iSLER, 1983).
orys. l:: iutput of the chordotonal@ :.: reached a particular statenc. i-::r5 slow walking, the organ[I t:t i:e oPerated leg as it is inmrll :.r:,ies a little, it can still be
'1i ::: ::e r-igorously, it is extended
rga:: rs strongly excited. The organt :r:::::11.,' sould relieve the tensionerie: s r ::'r only serves to excite itrelc rr! r. an extended position until
secee::: in stimulating the femoralopri:i: irme. They implanted fineErmir-3::: it elecCrically at varioustlrc.:::.rlation was applied late intio"-: =: r:rer times had no effect.ha'ir ieen interfered with has beenEri:rL-Lsli. It 1s not always possibleitic:ine, and applying continuous
12 DELCOMYN
input it is impossible to get a motor pattern that is anything near the patternthat one can see in the intact animal. Thus, in our current view, iensoryinformation is not a mere supplement to a CPG-generated pattern, but is anessential component of the entire rhythm-generating system.
THE FUTURE
THE MAIN ISSUES. Prophecy is always a risky endeavor, and trying to predictwhere research will lead is no less risky than other kinds. One can extrapolateinto the future a few years from present lines of research, but going beyondthat is guesswork of the highest order. What I will try to do here, therefore,is not so much to say where research will go, as to point out what in my opinionare some of the areas in which research might be especially fruitful over thenext few years. Taking this approach, I would single out five areas of researchthat I think can make the most significant contributions to our understandingof insect locomotion in the near future.Cel7u7ar analysis of pattern generators. The first of these areas is a con-tinued analysis. of the cellular mechanisms that allow a rhythmic patternof motor output to be generated. The advances in our understanding of flying,for example, that have been brought about by the work of ROBERTSON andhis colleagues are enormous, and it seems only reasonable to think that furtherwork in this area will yield further advances.
What might be expected to come from continued analysis of the locustflight system? Mainly, a description of the interneurons that are necessary andsufficient for the production of the cen!ryrlly generated rhythm, and_how theyinteract to produce it. On this base can then be built a detailed picture of howthe sensory input from the wind-sensitive hairs on the head turn the systemon, and how the input from wing stretch receptors are able to modulate it.Similar advances in our understanding of walking could be expected if someonewere able to overcome the technical difficulties of doing intracellular work onan insect capable of moving its legs normally.RoTe of sense organs. The second area in which significant progress mightbe expected is a natural extension of the behaviorally oriented research thathas already been done. This is investigation of the precise role played by specificsense organs in the behavioral adaptations to'mechanical interference. The effectsof obstacles to walking or of changes in load are clearly due to signals generatedby one or more sense organs in the legs of the walking insect. However, noattempt has yet been made to discover which sense organ or organs areresponsible for providing the information that causes the animal to change itsbehavior.
From a technical standpoint, experiments of this kind ought to be relativelyeasy to carry out. Furthermore, availability of the information such experimentswould provide would mean that work designed to uncover the mechanism bywhich the sense organs exert their effects would be possible, and this in turnshould lead to a much better understanding of the role of sense organs in thecoordination of unimpeded walking.InterTinb coordination. The third area of potential progress is one that haslargely been neglected in insect locomotion research, at least from a physio-logical point of view. This is the issue of how appendages are coordinated.A preliminary resolution of this issue has already been provided for locust flightby ROBERTSON & PEARSON (1983, 1984, 1985a), who showed that there isonly a single pattern generator for flight, and that coordination between frontand rear wings is done by appropriate synaptic delays within the single generator.
The issue is nowhere as clear in walking systems. Although results fromsome of the experiments involving leg obstruction have been examined for interlegcoordination effects (e.9., FOTH & GRAHAM, 1983b; DEAN & WENDLER, 1983),rhis has not been done in all cases (BASSLER, 1977). Furthermore, in very fewcases has there been any explicit attempt to determine what coordinatingmechanisms might be at work to ensure properly coordinated leg movements.This is an area that therefore seems ripe for rapid progress.
DELCOMYN
fII1: .! .:,i:51n9 near the patternuc i: :u: current view, sensoryCFC-ie:re:ared pattern, but is anrirg :l, s!em.
_i* e.:.alor, and trying to predictot:e: !irnds. One can extrapolate
rcs r: :esearch, but going beyondJ *1.. :r] to do here, therefore,
as !: ::.:: out what in my opinionlr 5e:s-:ecially fruitful over thesfu:g,e -':r f ive areas of research
cDn:::::::L-lns to our understanding
f-\: :: :te.ie areas is a con-:I3: =:-:r a rhythmic patternes ;: : !.ir understanding of flying,,]" ::: r*, ;rk of ROBERTSON and; :e:-:-abie to think that further
c:.::.r-ec analysis of the locustulErr:E-:,1rS that are necessary and
Eer.:a:ec rhythm, and,-how theybe l;r-: a detailed picture of howrirs :: t:-e head turn the systemlqeFi::: are able to modulate it.rng ::.:-d be expected if someoneres :: rr:ng intracellular work on
ir:l::: s-gnificant progress mighteha'.::::iii' oriented research thatthe ::?:lse role played by specificrecr::::-l interference. The effectsLre :-:":.;' iue to signals Senerated
g1-6 ; :.sing insect. However, nort:c: :e::e organ or organs are
cz:tsa: ::e animal to change its
of ::-s r.lrd ought to be relativelyI ti,: r:::r:nation such experimentslC :: -:rcover the mechanism byu:lc :,e ocssible, and this in turnrf l:.e r -..e of sense organs in the
Er:e::.: - progress is one that hastrese.a:::1. at least from a physio-' hcr :ppendages are coordinated.@.' :,ee:r provided for locust flightl9d.5a . E'ro showed that there isd :::: coordination between front&lays ;i::in the single generator.Bg s-,-::€iTrs. Although results fromiotl ha',e been examined for interleg1353r; DL{N & WENDLER, 1983),t" 13;i,. Furthermore, in very few
rc :etermine what coordinatingrye: : coordinated leg movements.rrP{a ::: aress.
::sect locomotion 13
--:egration of sensory and centraT signals. The fourth area in which I think:..l'estigation may yield substantial new information in the near future is one:ia! to a certain extent overlaps some of the ones I have already discussed..his is the cellular analysis of the mechanisms by which sensory input shapes:i.e final motor output, but with explicit reference to the behavior of the insect.
In order to say that walking, flying or swimming are really understoodri lhe neurological level, it is necessary to explain the behavioral adaptations:escribed above, as well as the patterns of normal free locomotion, in terms,'f the actions of sets of individual neurons in an insectfs central nervous system.1,i1 too often in the past, however, work of this kind has been done with little:egard for any aspect of the animal except the central nervous system on which:\periments were being conducted. Fortunately, this old attitude is fading, being:eplaced with a healthy respect for the capacity of changed conditions to.:fluence strongly the physiological state of the animalrs nervous system.
This new approach, and the significant new perspective on a phenomenon::at it can give us, is exemplified in some of the recent work of SIEGLER (1981).,'i-orking with the locust, she has shown that the responsiveness of motor neuronsic excitation from other neurons is significantly affected by the behavioral history:: the leg innervated by the motor neuron under study. In her experiments, thise:fect seemed to be mediated by the action of nonspiking interneurons. As shown-i Fig. 9, moving one hind tibia from an extended to a half-flexed positionresulted in a striking reduction of the responsiveness of a motor neuron for that.eg to input from a nonspiking interneuron. Moving the tibia from a flexed tol:ie same half-flexed position sharply increased the motor neuronts responsiveness.i-iowever, although the final position was the same in the two cases, the motorreuron was considerably more responsive in the second instance than it was in:he first.
intracellular stimulationof a nonspiking interneuronlint) in a locust are shownin intracellular recordsfrom the neuron beingsrimulated and from amotor neuron (mn) whenthe nearest leg of theIocust is made to assumedifferent positions (mvmt).\ote that the effect isdifferent (compare Aand B) when the leg isbrought to a particularangle from differentdirections. (From SIEGLER,l 98 1).
q' !!i' a- aath\El
int 8mV.mn omvl
^ -l>Fig. 9. The effects of t
.{
In the present context, the importance of this work is twofold. First, itgives us an insight into the way in which some sensory signals may influencespecific motor output. Secondly, it serves as one of the few examples of thekind of analysis of physiological events in behaviorally relevant terms that willbe needed for other kinds of locomotion research in order for us to reach thegoal of explaining locomotor behavior in terms of the actions of individual,identifiable neurons.
t4 DELCOMYN
Higher order controT. The last area I wish to discuss may represent a majorarea of emphasis in the future. This is the study of higher order control oflocomotion, such as the control of starting, stopping, turning, etc. Until recently,such matters have been almost entirely ignored, on the practical grounds thatthere was not too much point in thinking about the physiology of these functionswhile the basic nature of locomotion itself was not understood. However, nowthat we have in many instances (especially for flight) a good outline of howa specific locomotor pattern is generated, the important question of how thesystem is controlled by the animal can usefully be investigated. The recent reportby KIEN (1983) that there are many different descending neurons in the neckconnectives of the locust that can influence walking points both to the complexityof the control system for this behavior and to the wealth of new informationto be obtained by its study.
Whereas work in this area can and has been done on the walking system(e.g., FRANKLIN et al., l98l), most recent research in the area has been carriedout on the flight system. The fact that 6 papers in this volume (GEWECKE,1985; HEIDE et al., 1985; M0HL, 1985; NEUMANN, l9E5; ROWELL & REICHERT,1985; WAGNER, 1985) represent work in this area suggests that it might developmore rapidly than any of the others I have mentioned.
OTHER RESEARCH. Readers who are familiar with the literature of insectlocomotion will recognize that I have ignored many other aspects of locomotionresearch in this overview, stressing as I have the particular areas that seemedto me to deserve special mention, However, there are clearly other avenuesof research that I have neglected, and that could possibly develop into areasof great theoretical or experimental significance over the next decade.Modeling and gait anaTysis. The most active area of locomotion researchthat I did not discuss is the area of modeling and analysis of insect walkinggaits. Models are formal expressions of hypotheses about how a system works.Models of insect walking by CRUSE (1980a, b) and GRAHAM (1978) haveincorporated much of our knowledge of how the walking system operates, andtherefore are useful summaries of this knowledge, and useful bases from whichto start thinking about the system. Recent reviews by DELCOMYN (t9El) andGRAHAM (1985) provide more detail.Mechanics of Toconotion. This is an area of research that has never at-tracted many adherents, yet which provides much information that is essentialin order for progress to be made in our understanding of the physiological basisof locomotion. HOYLE (1976) has discussed the mechanics of walking, but littlehas been done in the area since his paper appeared, although JANDER (1985)
has reported some recent results. Work is being carried out on the mechanicsof swimming by NACHTIGALL (19E0), and GEWECKE (1985). And insect flightstill receives some attention, as exemplified by the recent analysis of flightin blowflies by NACHTIGALL & ROTH (19E3), and in dragonflies by ALEXANDER( l e84).Swin ning. In this entire discussion of locomotion, I have entirely ignoredswimming, in spite of the fact that quite a number of insects have aquatic larvalor adult forms that are capable of swimming. To date, however, except foranalyses of the mechanics of swimming mentioned above, the subject has beenalmost entirely ignored, presumably because of the extra technical problemsof making physiological recordings from a submerged animal.M yctgenic flight. Finally, mechanisms by which the wingbeat of so-calledmyogenic fliers like flies is controlled, has also been largely neglected. In theseinsects the nervous system is required only to keep the flight muscles in an
active state so that the cycle of mechanical quick stretch and relaxation cantime their contractions. A precisely patterned neural output to these musclesis therefore not necessary, and few biologists have been interested in the problemsof control of wingbeat in these insects. One of the exceptions is HEIDE (1975),
who has studied the regulation of wingbeat when flies are making turningresponses induced by a moving optical stimulus. HEIDE et al. (1985) report onrecent work of this type.Other work. Every field can be defined in a number of different ways.The field of insect locomotion is often defined narrowly in terms only of the
dfrutlr -
DELCOMYN
i: - Ie Se flt a major' - ::.: order control of-- .-.. e!c. Until recently,
dtirr :-: :::clical grounds that
:::srood. However, nowhr : ..-: . good outline of howb -l:,:::.:: question of how the'he ,-,:=:rgared. The recent reportm i€.1:=rling neurons in the neckdhin; --,:-i:rs both to the complexityto ::ri ;:allh of new information
bee:. ::i:e on the walking systemrea::-::: !t-te area has been carriedFapei: r: this volume (GEWECKE,L\-\. 1:35; RO\YELL & REICHERT,u'ea s-aeesrs that it might developtElC,:1,=:.
ia: ;ii: rhe lilerature of insectma:ir -,r:er aspects of locomotion
) tie:3rricular areas that seemedtf€:a are clearly other avenues
cor-: :ossibly develop into areas! c;:- ::e next decade.E .iaf, of locomotion researchirg:':.: anall''sis of insect walkingEiles:. "bout how a system works.a!,r .:id GRAHAM (1978) haveth,e ';:iking system operates, and
E€Ee. ::rc useful bases from whichE1 ,.'i -. ' br DELCOMYN ( t 981) and
o: ::.earch that has never at-muc: -:iormation that is essentialrs::::-:g of the physiological basisle::=::ai:ics of walking, but littleappE::... although JANDER (1985)rrrg ::::iec out on the mechanics;Eltr ECIiE {1985). And insect flight
a:r ::. recent analysis of flight::,: -: .:3gonflies by ALEXANDER
cc::::.,:, I have entirely ignoredm!€: rl ,rsects have aquatic larvaln& l late, however, except for.ilone: :::r'e, the subject has been
:,::.-.. extra technical problemsera:: a:inal,*:.:.-, ::e u'ingbeat of so-calledrsc.:€:: largely neglected. In these:l r..::,:he ftight muscles in ano:"-:,. -iretch and relaxation canr::-:a: output to these musclestale :.ri: interested in the problemsai r..: erceptions is HEIDE (1975),E ;i ri:r f lies are making turningus- htr:DE et al. (1985) report on
i. l: " rumber of different ways.lec:=:::'r'h'in terms only of the
Insect locomotion
mechanisms by which locomotion is generated and controlled. But of courselocomotion interacts with organizational levels both above and below that ofindividual nerve cells in the nervous system. Thus, at a higher level, it is partol the entire behavioral repertoire of each insect, and should be viewed in thewider context of its behavioral relevance for the insect in order for the fullbiological significance of the behavior to be understood. And at a lower level,the metabolic and other subcellular demands of locomotion impinge on manyother bodily systems whose actions must be taken into account in order to fitlocomotion into the biology of the whole animal.
By defining our field narrowly, we sometimes loose sight of rhese wideraspects of our subject, to the detriment of our understanding of its biologicalimportance. This wider aspect of our subject is represented in the present workby several papers at different levels, both the biochemical (ORCHARD & LANGE,1985; WHEELER & GOLDSWORTHY, 1985) and the broadty behavioral (EATON,1985; RAINEY, 1985), as well as containing a glimpse inro some of the appliedwork that may be done using the locomotor system as a model (ANDERSONet a1., 1985).
SUMMARY
It has been my intent in this article to set out the development of recent ideasin the field of insect locomotion, showing how researchersr views of locomotionhave changed over just the last decade. The papers that follow represent manyof the different areas of research in the field of insect locomotion. By selectingsome of these areas for emphasis, my aim was to stimulate thought and discussionamong those in the field and those interested but not active in it. Any one ofthe areas I selected for emphasis, or any of the areas I neglected, might possiblyblossom and start providing new and exciting insights into the mechanisms by'*'hich locomotion works, or into the way locomotion is used in the life of theinsect. It is the merest speculation as to which of them, if any, might do so.\Yhat is predictable is that the future will continue to bring a rich harvest ofnew research results and ideas about how locomotion is regulated and the wayin which each animal uses it. I hope that reading the contributions of theparticipants of this symposium will stimulate your thoughts and whet your appetitefor the results and understanding that is yet to come, just as it did for theindividuals who were actually at the conference.
REFERENCES
ALEXANDER, D. E., 1984: Unusual phase relationships between the forewingsand hindwings in flying dragonflies. J. Exp. Biol., 109: 379-383.
ANDERSON, M., T. A. MILLER & L. P. SCHOUEST, lg85: The structure andphysiology of the tergotrochanteral depressor muscle in the housefly.In: M. GEWECKE & G. WENDLER (Eds.), Insect Locomotion. Paul Parey,Berlin, Hamburg: 97-102.
BASSLER, lJ., 1977: Sensory control of leg movement in the stick insect Carausiusilorosus. Biol. Cybern., 25: 61-72.
- -, 1979: Effects of crossing the receptor apodeme of the femoral chordotonalorgan on walking, jumping and singing in locusts and grasshoppers. J. Comp.Physiol., 134: 173-176.
- -, 1983: Neural basis of elementary behavior in stick insects. Springer, Berlin,Heidelberg, New York.1985: Proprioceptive control of stick insect walking. In: M. GEWECKE & G.WENDLER (Eds.), Insect Locomotion. Paul Parey, Berlin, Hamburg: 43-48.
BURROWS, M., 1973: The role of delayed excitation in the co-ordination of somemetathoracic flight motoneurons of a locust. J. Comp. Physiol.,83:135-164.
I.'
DELCOMYNl6
CRUSE, H., 1976a: The control of body position in the stick insect (Carau,g.trs
norosusl, when walking over uneven surfaces. Biol. Cybern., 24:. 25-33.- -, 1976b: The function of the legs in the free walking stick insect, Carausitts
morosus. J. Comp. Physiol., ll2: 235-262.- -, 1979: The control of the anterior extreme position of the hindleg of a walking
insect, Carar:.aus norosus. Physiol. Entomol. 4: l2l-124.- -, 1980a: A quantitative model of walking incorporating central and peripheral
influences. I. The control of the individual leg. Biol. Cybern., 37: 13l-136.- -, 1980b: A quantitative model of walking incorporating central and peripheral
influences. II. The connections between the different legs. Biol. Cybern.,37.. 137-144.
- -r 1985: The influence of load, position and velocity on the control of legmovement in a walking insect. In: M. GEWECKE & C. WENDLER (Eds.),
Insect Locomotion. Paul Parey, Berlin, Hamburg: 19-26.DEAN, J., lg85: A simulation of
'proprioceptive input from the_ coxal hair rows
of -the
stick insect: Possible effect of step velocity on the representationof joint angle. In: M. GEWECKE & G. WENDLER (Eds.), Insect Locomotion.Paul Parey, Berlin, Hamburg:49-57.& c. WENDLER, 1982: Stick insects walking on a wheel: pe,rtubations induced
by obstruction of leg protraction. J. Comp. Physiol', 148: 195-207'
& G. WENDLER, tdSS: Stick insect locomotion on a walking wheel: interlegcoordination of leg position. J- Exp. Biol', 103: 75-94'
DELCOMYN, F., lg80: Neural basis of rhythmic behavior in animals. Science,210: 492-498.
- -, l98l: Insect locomotion on land. In: C. F. HERREID & C. R. FOURTNER(Eds.), Locomotion and Energetics in Arthropods. Plenum, New York: 103-
125.- -, 1984: Walking and running In: G. A. KERKUT & L. I. GILBERT (Eds.), Com-
prehensive Insect Physiology, Biochemistry and Pharmacology. Pergamon,Oxford, 5: in press.
- -,1985b: Sense organs and the pattern of motor activity during walking inrhe American colkroach. In: M. GEWECKE & G. WENDLER (Eds.), InsectLocomotion. Paul Parey, Berlin, Hamburg: 87-96.
EATON, J. L., 1985: Actograph studies of light effects on Trichoplusia oi flightacrivity. Inr M. GEWECKE & G. WENDLER (Eds.), Insect Locomotion. PaulParey, Berlin, Hamburg: 233-239.
FOTH, E. & D. GRAHAM, 1983a: Influence of loading parallel to the body axison the walking coordination of an insect. I. Ipsilateral effects. Biol. Cybern.,47: 17-23.& D. GRAHAM, 1983b: Influence of loading parallel to the body axis on
the walking coordination of an insect. II. Contralateral changes. Biol. Cybern.48: 149-157.
FOURTNER, C. R., 1976: Central nervous control of cockroach walking. In: R.M. HERMAN, S. GRILLNER, P. S. G. STEIN & D. G. STUART (Eds.), NeuralControl of Locomotion. Plenum, New York: 401-418.
FRANKLIN, R. F., 1985: The locomotion of hexapods on rough ground. In:M. GEWECKE & G. WENDLER (Eds.), Insect Locomotion. Paul Parey, Berlin,Hamburg:69-78.
- -, W. J. BELL & R. JANDER, 1981: Rotational locomotion by the cockroachB1ate17a gernanica. J. Insect Physiol., 27: 249-255.
GEWECKE, M., 1985: Swimming behaviour of the water beetle Dltscus narginalisL. (ioleoptera, Dytiscidae). In: M. GEWECKE & G. WENDLER (Eds.), InsectLocomotion. Paul Parey, Berlin, Hamburg: lll-120.
GRAHAM, D., 1972: A behavioral analysis of the temporal organisation of walkingmovements in the first instar and adult stick insect (Carausus norosusl.
J. Comp. Physiol., 8l: 23-52.- -, 1977: The effect of amputation and leg restraint on the free walking coordi-
nation of the stick Inssst f,ar'6rr.qus norosus. J. Comp. Physiol., 116: 91-I 16.
p:E::-::. cf the hindleg of a walking:-L -i: - I 1- 124.:rc:::,:::ting central and peripheralI }e5. 3-':'-, Cybern., 37: l3l-136.::s:::,::3:ing central and peripherai::--e :: : ierent legs. Biol. Cybern.,
lmc i: :":1:i' on the control of legnECr,: & G. WENDLER (Eds.),rmrbr-:: - 3-26.rde ---:-: ::om the coxal hair rowss,'!e: .,: :.1j. on the representationfE).: -:L lEcs.), Insect Locomotion.
F" ;-=?REID & C. R. FOURTNERrt::::,:'::. Plenum, New York: 103-
LKL: & -. L GILBERT (Eds.), Com-ffa:] =:.: Prarmacology. Pergamon,
\m:--- F.e''. Entomol., 30: in press.f ::: -r activity during walking inIKE & G. \\'ENDLER (Eds.), Insect
lichopTusia ni flightInsect Locomotion. Paul
of -:::-:g parailel to the body axis, L l;.--::::al effects. Biol. Cybern.,
m::::a::--el to the body axis onC"::::..":-':al changes. Bioi. Cybern.
ofi::-- -: :lckroach walking. In: R.IEL\ & f. C. STUART (Eds.), Neuralk 4::-l-:.lae:,:: --, r:ugh ground. In:$ec: :,: -1:tation. Paul Parey, Berlin,
&"(r,:!::, - i.c,motion by the cockroach
ite a.::: beetle Dltrscus narginaTisacii= i G. \\'ENDLER (Eds.), Insect
tile :.:-'.-r,l13. organisation of walkingt:::. .-:::'- l'=rausius norosus).
res::=.-: :i the free walking coordi-!r*<. .. Comp. Physiol., I 16: 91-
Insect locomotion n- -,1978: Unusual step patterns in the free walking grasshopper Neoconocephalus
robustus. II. A critical test of the leg interactions underlying differentmodels of hexapod co-ordination. J, Exp. Biol, 73: 159-172.
- -,1985: Pattern and the control of walking in insects. Adv. Insect Physiol.,in press.& U. BASSLER, 1981: Effects of afference sign reversal on moror acrivityin walking stick insects {Carausius norosusl. J. Exp. Biol, 91: 179-193.& H. CRUSE, 1981: Coordinated walking of stick insects on a mercury sur-face. J. Exp. Biol, 92: 229-241.
HEDWIG, B. & K. G. PEARSON, 1984: Parrerns of synaptic input to identlfiedflight motoneurons in the locust. J. Comp. Physiol., 154: 745-760.
HEIDE, G., 1975: Properties of a motor output system involved in the optomotorresponse in flies. Biol. Cybern., 20:, 99-112.
- -, M. SPULER,K.G. GOTZ& K. KAMPER, 1985: Neural conrrol of asynchronousf light muscles in f lies during induced flight manoeuvres. in: M. GEWECKE& G. WENDLER (Eds.), Insect Locomotion. Paul Parey, Berlin, Hamburg:215-222.
HERMAN, R. M., S. GRILLNER, P. S. c. STEIN & D. G. STUART (Eds.), 1976:Neural Control of Locomotion. Plenum, New York,
HERREID, C. F. & C. R. FOURTNER (Eds.), 1981: Locomorion and Energericsin Arthropods. Plenum, New York.
HORSMANN, U., H.-G. HEINZEL & G. WENDLER, 1983: The phasic influenceof self-generated air current modulations on the locust flight motor. J.Comp. Physiol., 150: 427-438.
HOYLE, G., 1976: Arthropod walking. In: R.M. HERMAN, S. GRILLNER, P.S.G.STEIN & D.G. STUART (Eds.), Neural Control of Locomotion. Plenum, NewYork:137-179.& M, BURROWS, 1973: Neural mechanisms underlying behavior in rhe locustSchistocerca gregaria. II. Integrative activity in metathoracic neurons. J.Neurobiol., 4: 43-67.
HUSTERT, R., 1985: The contribution of proprioceptors to the control of motorpatterns of legs in orthopterous insects - the locust example.In: M. GEWECKE & G. WENDLER (Eds.), Insect Locomorion. Paul Parey,Berlin, Hamburg: 59-67.
JANDER, J. P., 1985: Mechanical stability in insects when walking straight andaround curves. In: M. GEWECKE & G. WENDLER (Eds.), Insect Locomorion.Paul Parey, Berlin, Hamburg: 33-42.
KIEN, J., 1983: The initiation and maintenance of walking in the locust: an alter-native to the command concept. Proc. R. Soc. Lond. B, 219: 137-174.
MACMILLAN, D. L. & J. KIEN, 1983: Intra- and intersegmental pathways activeduring walking in the locust. Proc. R. Soc. Lond.8,218:287-308.
MOHL, B., 1985: Sensory aspects of flight pattern generation in the locust. In:M. GEWECKE & G. WENDLER (Eds.), Insect Locomotion. Paul Parey, Berlin,Hamburg: 139-148.
NACHTIGALL, W., 1980: Mechanics of swimming in water-beetles. In: H.Y. ELDER& E.R. TRUEMAN (Eds.), Aspects of Animal Movement. Cambridge University,Cambridge: 107-124.& W. ROTH, 1983: Correlations between stationary measurable parametersof wing movement and aerodynamic force production in the blowfly(Calliphora viczna R.-D.). J. Comp. Physiol., 150: 251-260.
NEUMANN, L., 1985: Experiments on tegula function for flight coordinationin the locust. In: M. CEWECKE & G. WENDLER (Eds.), Insect Locomotion.Paul Parey, Berlin, Hamburg: 149-156.
ORCHARD, I. & A. B. LANGE, 1985: Dual role for octopamine in rhe conrrolof haemolymph lipid during flight in Locuste. In: M. GEWECKE & G.WENDLER (Eds.), Insect Locomotion. Paul Parey, Berlin, Hamburg:131-138.
PEARSON, K. G., 1985: Are there central pattern generators for walking andflight in insects? J. Exp. Biol., in press.& C. R. FOURTNER, 1975: Nonspiking interneurons in walking system ofthe cockroach. J. Neurophysiol., 38: 33-52.
18 DELCOMYN
& R. F. FRANKLIN, 1984: Characteristics of leg movements and patternsof coordination in locusts walking on rough terrain. Intl. J. Robotics Res.,3: 101-1 12.& J. F. ILES, 1970: Discharge patterns of coxal levator and depressor moto-neurones of the cockroach, PeripTaneta anericana. J. Exp. Biol.' 52: 139- 165.& J. F. ILES, lg73: Nervous mechanisms underlying intersegmental co-ordina-tion of leg movements during walking in the cockroach. J. Exp. Biol., 58:725-7 4.D. N. REYE & R. M. ROBERTSON, 1983: Phase-dependent influences ofwing stretch receptors on flight rhythm in the locust. J. Neurophysiol.,49: ll68-ll8l.
RAINEY, R. C., 1985: Insect flight: New facts - and old fantasies? In: M.GEWECKE & G. WENDLER (Eds.), Insect Locomotion. Paul Parey, Berlin,Hamburg: 241-244.
ROBERTSON, R. M. & K. G. PEARSON, 1983: Interneurons in the fliSht systemof the locust: distribution, connections, and resetting properties. J. Comp.Neurol., 215: 33-50.& K. G. PEARSON, 1984: Interneuronal organization in the flight systemof the locust. J. Insect Physiol., 30: 95-101.
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- -, K. G. PEARSON & H. REICHERT, 1982: Flight interneurons in the locustand the origin of insect wings. Science, 217: L77-179.
ROWELL, H. F. & H. REICHERT, 1985: Compensatory steering in locusts: Theintegration of non-phase locked input with a rythmic motor output. In:M. GEWECKE & G. WENDLER (Eds.), Insect Locomotion.Paul Parey, Berlin, Hamburg: 175-182.
SIEGLER, M. V. S., 19El: Postural changes alter synaptic interactions betweennonspiking interneurons and motor neurons of the locust. J. Neurophysiol.,46:3t0-3231
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WHEELER, C. H. & G. J. GOLDSWORTHY, 1985: Lipid transport to the fliShtmuscles in Locl:.sta. In: M. GEWECKE & G. WENDLER (Eds.), Insect Locomo-tion. Paul Parey, Berlin, Hamburg: l2l-129.
WILSON, D. M., 1961: The central nervous control of flight in a locust. J. Exp.Biol., 38: 471-490.& E. GETTRUP, 1963: A stretch reflex controlling wingbeat frequency ingrasshoppers. J. Exp. Biol, 40: 171-185.
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Address: Department of Entomology, 320 Morrill Hall, University of lllinois, 505S. Goodwin, Urbana, IL 61801, U.S.A.
2.I THE INFLUENCE OF LOAD, POSITION AND VELOCITY ON .ITIE CONTROLOF LEG MOVEMENT OT A WALKING INSECT
HOLK CRUSE
ABSTRACT
Experiments with walking insects suggest that the movement of an individual@ is controlled by a two-level system. One level determines whether or note ongoing phase (stance or swing) should be finished, depending upon the positionad load of the controlled leg and upon temporal coordinating . signals from thecher legs. The other level controls the way movement is performed during thertance or swing phase, using velocity as the controlled variable.
INTRODUCTION
There is general interest in the question of how behaviour is produced by theetrtral nervous . system. Given this problem, it makes sense for several reasonsb investigate walking behaviour. walking 'is easy to elicit and is repetitive, whichfmplifies the investigalion of this behaviour as compared to others which maypcur only rarely. Furthermore, ,walking seems to be a relatively simple behavioui,rhich sr.rggests that the underlying mechanism may. not be too. complicated. Onrhe other hand, it is still complicated enough to be interesting as sensoryfedback .pldys an important role in it. Finally, walking occurs not only in higheiErtebrates but also in arthropods, whose smaller nervous systems are probablynore easily understood than those of vertebrates. One of the anirirals studiedDost intensively in this. respect has been the stick insect; unless otherwiselentioned the results presented here will refer to this insect..
Walking behaviour presents two main problems. One is the question of howtte rhythmic movement of the different walking legs is coordinated to producea proper gait; the other is the question of how the movement of each individualleg is controlled. This arricle will deal mainly wirh the larrer question.
The rhythmic movement of a walking leg consists of two clearly separatedparts: the stance.. phase (often called the power stroke) when the leg touchesthe ground, and the swing phase (return stroke) when the leg is lifted off theground. (For forward walking, the corresponding expressioni rretractionr andlrotractiont are also used.)
FACTORS INVOLVED IN TERMINATING PHASES OF STEP
One important problem is how the nervous system controlling the movementof the leg decides whether an ongoing stance or swing phase should be continuedc brought to an end. For the middle and hind legs the end of the swing phaseis clearly determined by geometrical parameters (i.e. the position of the tarsus),since during the swing phase these legs use the position of the next anteriortarsus as a targer (CRUSE, 1979; DEAN & WENDLER, l98S; CRUSE et al., tg84).For the front legs, a similai mechanism exists that uses position informationprovided by the antennae (CRUSE. & KRIEGER, in prep.). However, in this caseas for the other legs, endogenous position values
- might. be used if no other
information is available (e.g. following amputation of an antenna or leg).
@rrecLeffendla (eds.), Insect LocomotionO 1985 Paul Piley
U
20
ICRUSE
Ending the stance phase poses more difficulties for the animal, as liftingthe leg at the wrong moment could lead to loss of postural stability. In addition,the end of the stance phase is generally considered to be the main point atwhieh the leg movement is coordinated with that of the other walking legs(BASSLER, 1977; GRAHAM & CRUSE, 1981; DEAN & WENDLER, 1982; CRUSE& EPSTEIN, 1982). Thus the decision to end the stance phase presumably dependsupon more than one parameter.
As long as a leg is under load or the corresponding sense organs (veryprobably the trochanteral campaniform sensillae) register excitation, the leg isnot lifred off the ground (BASSLER, 1977; for cockroach: PEARSON, 1972). Thusload is a parameter used for the decision whether or not to lift the tarsus offthe ground.
When a stick insect walks with the body supported over a treadwheel, oneleg can be placed on a small platform beside the wheel (WENDLER' 1964). Ifthe platform is positioned far enough anteriorly, this leg remains standing onthe platform while the other five legs continue to walk. This seems to indicatethat position is an important parameter; however, it may also be the case thata leg in an anterior position is under higher load and that load is the onlydecisive parameter. Nevertheless, position is an important parameter, as is shownby the following experiment. Some position-measuring sense organs (coxal hairplates and hair rows) are manipulated so that they register the leg as beingin an extreme anterior position regardless of the actual position of the leg. Inthis situation, the leg does not lift off the Sround even when it is in a posteriorposition (BASSLER, 1977). However, this experiment does not show whether anormal posterior leg position as such is sufficient to elicit the start of a swingphase. To decide whether the position of the leg is indeed a parameter whichalso can elicit swing phase, the following experiment was performed. Theplatform positioned beside the treadwheel was attached to a micromanipulatorwith a soft spring steel band which allowed the platform to move horizontallywhen loaded. The animal walked on the treadwheel with one leg on the platform.Using the micromanipulator, the standing leg of the walking animal could beplaced at any desired position relative to the body. At different positions, theplatform was suddenly unloaded horizontally backwards by means of a weightattached to the platform by a thread running over a pulley. It was noted whetherafter this unloading the leg started a swing movement or remained standingon the platform (CRUSE, 1985).
-liO -30 mm
o) PEP AEP b)PEP AEP
100
\o
Eso=
r0-10-50-50
Fig. l. Percentage of cases in which legs started swing phase after being un-
toiaeO.- a) hind l6gs, b) fronr legs wirh the middle leg on a fixed platform (o)
or with blocked swing phase (o). Abscissa: tarsus position, coordinate parallelto the longitudinal axis of the body. Origin is tip of the head. Positive values
are anterio=r. Below the ordinate the ranges of normal leg movement duringwalking are given by solid lines. The extension of the range of- the front legwhen blocking the swing phase of the middle leg is shown by the dashed line.AEP: anterior extreme position; PEP: posterior extreme position. The numbersnext each point show the sample size. Results from 4 animals.
CRUSE
ic--:l:. ic: the animal, as liftings :: :.-::ural stability. In addition,:s"f:::::o be the main point at
::.:: :: rhe other walking legs)tr--" 1
"i,E\DLER, i982; CRUSE
e ::: := frase presumably depends
:::::::-,rcing sense organs (veryE ::;.::.. excitation, the leg is::,:r ::::.-t: PEARSON, 1972). Thus
rr,-: - - :ri to lift the tarsus off
::--: -.:i :re: a treadwheel, OneI ::,. '"r :el 1\\'ENDLER, 1964). Ifr--, " : -, ! ieg remains standing onle :- ; =,,... This seems to indicatere.- .: :ai also be the case that'r:1:::::ila! IOad iS the On[y
:::,:::::: ,arameter, aS iS ShOWn!e3-s-:. - i :3.se organs (coxal hairli[:-:., ]-;rsler the leg as being::e :::-:- position of the leg. Inr.ri::,;: ;:el it is in a postefior!tri:::-::::s not show whether ate:::: =..:-t the start of a swing,ea , -::eed a parameter whiche$:e:-::a:[ \\'as performed. The
s r::::--r ro a micromanipulatorf:xe :.:::rm to move horizontallyhE€- r.:r lne leg on the platform.
:: ::: .; al<ing animal could be, :r:,:j..:.: cifferent positions, thebec:r-ir =::= D; means of a weightrue: = :-i,ei. It was noted whether; :: r ::.:.t or remained standing
PEP
3r:?: :i.rg phase after being un-@rc:-. ,:; on a fixed platform (o)
:: -,:::a. ieg movement duringcn :: ::: range of the front leg
r€!,: s.:,rii'n by the dashed line.cr:1-::::re position. The numbers'--- --,--t^
Control of leg movements of walking insects
Fig. 1a gives the results for the hind leg, showing the percentage of starts ofswing phase following unloading plorted against position. The data show thatlift-off occurs rarely when the leg is unloaded in the anterior part of its normalrange of movement. in contrast, the leg nearly always lif ts of f when it isunloaded in a position beyond the normal endpoint of the stance phase ('posteriorextreme positionr, PEP), Corresponding results were obtained for the middleand front legs. These results confirm that the lift-off is always prevented whenthe leg is under load - even when the leg is placed far beyond its normalposterior extreme position. However, when the load is small enough, lift-offoccurs only when the leg is placed near the normal lift-off position (PEP).
This critical position value can be influenced by signals from the nextDosterior leg. The unloading experiment with the front leg was performed intwo ways with each animal: a) with the middle leg standing on a separate fixedplatform, and b) with the swing phase of the middle leg blocked by a verticalstick (DEAN & WENDLER, 1982; CRUSE & EPSTEIN, 1982). In rhis way rheexperimental conditions held the middle leg in either prolonged stance phaseor prolonged swing phase. The results (Fig. lb) show that when the swing phaseof the middle leg is blocked, the position at which the swing phase of the frontleg is started shifts caudally.
In addition to position and load, coordinating signals from other legs mayalso influence the decision to finish the stance phase. Two types of such signalsrvhich influence the anterior and the posterior target positions were describedabove. Other types have been shown to run either caudally (BASSLER,1983;Fig. 4.21) or in both directions (CRUSE, 1984). In both cases the signals havean influence on the motoneuronal level: although the leg is in stance phase,:trong changes in excitation of the motoneurones and even excitation ofantagonistic muscles are found. Such changes in output force can affect theioad-sensitive organs; at least in this indirect way these coordinating signals:an influence the decision process. However, it is not clear whether they influencetae decision process directly as well.
Thus, the decision to continue or finish the stance phase is dependent upon:osition, load and (directly or indirectly) upon some coordinating signals. This:ecision has two effects: a) it decreases the excitation of those motoneuronesactive during stance phase, while it increases that of the motoneurones active:uring swing phase; and b) it changes the 'target' posirion from the posterior.o the anterior value. As a summary in Fig. 2 a schematic drawing of the circuit'decision systemr) is shown. The relay characteristic represents the change of
:re target position. The anterior target position (ranterior extreme positionr,AEP) can be influenced by signals describing the position of the anterior leg.The posterior target position (PEP) can be influenced by signals from the posterior-eg telling whether it is in stance or swing phase, The system produces swingphase when the output value is positive and stance phase when it is negative.Coordinating signals whose effects are not clear are ommited from the figure.
Fig. 2. A schematic drawing of the system'r'hich decides whether swing or srancephase should be finished. The relaycharacteristic produces the two alternativetarget positions AEP or PEP (anterior orposterior extreme position) when its input,,'alue is positive or negative, respectively.The AEP is determined by the acrualposition of the anterior leg. The PEPdepends on the state (stance - swing) ofthe posterior leg. The value of the targetposition is compared with the actual legposition. The result is affected by signalsfrom load-sensitive organs. The systemactivates rswing phase musclesr when theoutput value is positive and rstance phasemusclesr when the output value is negative.
positionont. leq
Iood
2t
AEP
coond.post. leg
position
.,i r lrr,r! l.i{!i[A[g*,r
22 CRUSE
FACTORS AFFECTING MOTOR OUTPUT
How might such a decision system affect the motor output? The absolute valueof the output of this system is high at the beginning of both the stance andswing phases, decreasing to zero towards their end as long as the load remainsconstant. This is because the output value depends on the difference betweentarget value and actual leg position. Therefore, the first prediction is that ifthis output value influenced the motoneurones directly, one would expect a legstanding on a platform in an anterior position to produce higher motor outputthan when the platform was in a more posterior position. Furthermore for eachleg position, the motor output should be higher when the next posterior leg isin swing phase than when it is in stance phase.
Fig. 3a shows the force developed by a front leg in backward directionas well as the position of the platform. The correlation between these two valuesis obvious; mean values are shown in Fig. 4 for all legs. Although at first sightthese data appear to support the assumption mentioned above that motor output(excitation of motoneurones) is correlated with the feedback signaling leg position,the following result is not compatible with it. The experiment with the frontleg is repeated so that practically only the femur-tibia ioint is moved. Whenthe receptor apodeme of the femoral chordotonal organ - the position receptorof this joint (for review see BASSLER, 1983) - is cut in order to prevent positioninformation from being sent to the central nervous system, the force responsesare about the same (Fig. 3b). This means that the changes of the force valuesdepend on leg position itself, rather than upon a system involving sensoryfeedback. Thus the forces measured most probably reflect the elastic propertiesof the muscles active at a constant level during the stance phase. This isconsistent with the experimental finding that excitation of the retractor anddepressor muscle of a middle leg standing on a platform remains constant whenthe platform is moved forwards and backwards (EPSTEIN & GRAHAM, in prep.).
mm
m.
"ot,t
tn ,[ ,t
o) t (s)
mN
b) t (s)
Fig. 3. D-c-force values depend upon leg position.- a) An example of an individu-al record of the force developed by a front leg standing on the platform whilethe other legs walk. Upper trace: relative position of platform - upward deflectionshows movement in anterior direction; lower traCe: force - positive forces actin posterior direction. b) as a) but with the receptor apodeme of the femoralchordotonal organ cut. Note that scale units are different.
The second prediction - that motor output should depend on whether thenext posterior leg is in stance or swing phase - also turnes out to be false.Fig. 5 shows the mean values for both situations; no significant differences(p ,, 10 o/o ) were found for any position measured. Thus, the decision system(Fig. 2) does not influence the motoneurones in a way proportional to thedifference between actual position and target position. Rather, only a yes-or-nodecision (swing - stance) is sent to the motoneuronal level. This could berepresented in the circuit shown in Fig. 2 by an additional relay characteristic.However, this has not been done in the figure because some questions remain.
CRUSE
motor output? The absolute valuebeginning of both the stance andend as long as the load remains
Epends on the difference betweenre, the first prediction is that ifdirectil', one would expect a leg
n to produce higher motor outputirr position. Furthermore for eacher s'hen the next posterior leg is
r froilt leg in backward directionrreiation between these two vaiuesor all legs. Although at first sightDentioned above that motor outPutthe ieedback signaling leg position,iL Tae experiment with the frontfernur-tibia joint is moved. When
oBal oigan - the position receptoris cut in order to prevent Position
Err-ol-:s system, the force responsest the changes of the force valuesupon a system involving sensoryBly; reflect the elastic propertiesduririg the stance phase. This isr e-acr!Btion of the retractor anda platform remains constant when
ESIE]N & GRAHAM, in prep.).
t (s)
tioo-- a) An example of an individu-teg st:nding on the platform whilerion of platform - upward deflectionfrace: force - positive forces actrece?ror apodeme of the femoral
e Cfferent.
qrrt srould depend on whether thetse - also turnes out to be false.[atio:r:; no significant differencespssured. Thus, the decision systemes ir a way proportional to the: posr:icn. Rather, only a Yes-or-noooro:euronal level. This could be
f a: 3cditional relay characteristic.lre lecsuse some questions remain.
Fig. 5. D-c-force values versusposition of front leg.- Mean valuesand standard deviations from a totalof 13124 measurements. l0 animalsq'ere tested with the ipsilateral middteleg either on a fixed platform (o)
ar with blocked swing phase (o).Coordinates as in Fig. 4. For lowerposition values not all 10 animalsremained on the force transducerin both experiments. Thus feweranimals were evaluated; the numbertested is shown in brackets. Belowrhe ordinate the range of normalleg movement is shown by the solidIine. The range is extended as shownby the dashed line when the swingphase of the ipsilateral middle legis blocked. AEP: anterior extremeposition; PEP: posterior extremeposition.
z.
e,Lo
Control of leg movements of walking insecrs 23
.ls was described above, some coordinating signals might act directly on thedecision sys[em only (i.e. might influence the system in front of the relaycharacteristic), on the motoneuronal level, or both. Stimulating load-sensitivecrgans clearly influences the decision process; however, it is not known whetherthis mechanism operates only in a yes-or-no manner via the relay characteristic:r whether it is also capable of exerting a proportional influence directly onto:he motoneurones.
HL ML
0 20mm+
F L onterior
nig. 4. Mean values and standard deviations of force versus position of the.;latform.- Abscissa: position coordinate parallel to the longitudinal axis of the:ody. Origin (= O) is tip of the head. Positive values are anterior. Below theoidinate the ranges of normal movement during walking are given for front legrFL, triangles), middle leg (ML, squares) and hind leg (HL, circles). Forces inFosterior direction are positive. FL: 153 measurement from 5 animals; ML: I l4rreasurements from 5 animals; HL:161 measurements from 6 animals. Eachreasurement produced a d-c-value from a walking period of at least 6 secondcuration during a continuous walk.
-20
I
10z.ed
o5
PEP AEP
24CRUSE
Affi;:,", "irr""i"i".?*.-.ry "rro
contribute ro these changes in force values.
Positionsignalsseemnottoinfluencethesemotoneurones'ashasbeenshown for the front urJ tfr" middle leg. However, geomet-rical parameters ,ofthe leg are monitored
--;.d used for difYferent pu.pos.s: Information about the
spatial position of the taisus is needed both for the targeting movement of the
;;;;-;"i;;i"; leg and for the decision whether or nor to finish the stance or
;;;g -;i.;r;- In
'addition-, the- muscles whrch control rhe distance between the
L.ar' ""a the walking' surface are influenced by geometric.al parameters
iilHNoiiir, "i6oa;" SLHialrZ, isos; CRUSE & BRAUN, in prep')' In order to
test whether the numerous sense organs monitoring geometrical parameters play
;; ;;i; i; controrring-i"g ;Lu"*Jnr during rhe stance . phase, the following
"ri,*i-"r, was perfori"J. "rl" animal walks wirh the body supported over the
treadwheel. tn ttre experii-"nt ,ting the fixed platform as described earlier (Figs'
3, 4 and 5) the leg investigated was stationary' To. investigate the leg in an
acrual srance pt,ur", rr,u'pi;;i:;;"*i;["tne-ioice i.ansducer is-now moved parallel
to and at about ,t" .uii" speed-as the.treadwheel. when by chance the leg
rouches the platform iJL"a '"i the wheel, then the force exerted by the leg
is measured. aue.agea"'ietuftt - fot the front leg are shown in Ii9: 6^1^ ?T,19
;;""r;;;; phase tie force increases ro a maximum and then decreases agatn'
often becoming slightly '"i"ii'" "t the end of the phase' As described above'
the muscles propelling'the body are assumed here to be excited at a more or
less constant rate during the entire stance phase' -Because of the low pass
properries of the musJi"r," ii ilr."r some rime for the force to reach its maximum
value. As the leg is - mtveO backward during the .stance '
phase the retracting
muscles are shortenea, "to -tf'"i the force pioduced bl :1t: I':::"^^1,""ttf^1t*'
,o rr]1
0
=Ed -lLoe-3
-4
-5
6
5
l+z,E;3Loa
L
1
0
b. n=32
3taaaa
taao!
a
!,,1,,',,. .,,,.,.,,,t?
.qriiiiiiiiiiiiiiiiiiiiiiiiiiit{il,0 1 '2
ii
i$iaa!\o!
o
n=63
b)
0123time Isl
o)
Fig. 6. Forces measured during a step of.the front leg with the force transducer
beins moved parallel ,"it"'i.&J*t"L'f.- ut The.platforh with the leg was.moved
;:li;;#r"p""i. ii.ai."t"t-absolute force. b)'The leg movement was changed
by shortly decreasing 1ii" -tpL"J oi -the
platform' thu upPel trace shows
schematically tne movemenl oi ttre platform. ordinate: changes of force relative
to force value when ,t" 'rii*rr"r
bLgan. Averaged .results, from 5 animals. The
magnitude of rhe ,runJu.a a"riations- is represe-nted by the dotted area above
,f,"'uUt"itt". Forces in posterior direction are positive'
To investigate whether an unexpected.disturbance in the movement produces
any specific reactions,'if" tlrp"ii*"'i *ut then modified' This time the movement
of the platform *", -no'
continuous but was stopped for a short time' The
averaged results in nig.'"du .r,.*'-atr-", the foice values increase for about 0'3 s
CRUSE
lrese :otoneurones, as has beennerEr. geometrical parameters of
purp,lses: Information about ther ti:e targeting movement of the' o. rot to finish the stance orpntr:- the distance between theced l!' geometrical parametersBR{U\, in prep.). In order to
rrn5 geometrical parameters PlaYthe -.rance phase, the followingrith i:e body supported over the,iat i::: as described earlier (Figs.
-r.:: investigate the leg in anI trar:sc:.lcer is now moved parallelfrtre€i. \\'hen by chance the iegEo !::e force exerted bY the leg
Bg a:: shown in Fig. 6a. Duringrrmr-: and then decreases again,I the :nase. As described above,Dene i: be excited at a more orpbas€. Because of the low Passr Lte ::rce to reach its maximumthe s:ance phase the retracting
6rce- by' this muscle decreases.o t:re= changes in force values.
n=63
time Is I
fronr .e; r'ith the force transducerp[a:ii::r *'ith the leg was moved
d The .eg movement was changed6cfo:i:. The upper trace shows),rdilate: changes of force relativeagec :esults from 5 animals. The$enie: 31- the dotted area aboveBtir-E.
mrbe-1:e in the movement Producesmocr:r:i. This time the movementr s:::ped for a short time. Thece 1:.ues tncrease for about 0.3 s
^a..at..jt tLoa!\r!
)
Control of leg movements of walking insects Zs
after the platform has stopped, but then start to decrease before the platformbegins to move again. This effect is unlikely to be produced by stimulation of.oad-sensitive organs because the load increase produced by the decelerationof the leg is less than 0.01 mN. The decrease of the force during the movemenr:f the platform corresponds to that found in the undisturbed stance phase and;s assumed to reflect the elastic properties of the muscles. During the stop ofrhe platform this mechanism alone would lead to a constant force value. Thelncrease found during the stop shows that at least the first order derivative:f position, the velocity, plays a role in controlling the motor output. This leads!o the conclusion that during the stance phase, Ieg movement is velocity:ontrolled. If the velocity of the leg deviates from the desired value then the:iegative feedback mechanism changes the motor output correspondingly. The:act that the response is not of pure tonic nature but has a phasic component:'.rrther indicates that the second order derivative (i,e. acceleration), also contribu-ies to the effect. Both results are consistent with earlier findings. It was foundirat the ref lex of the femur-tibia joint which is slowly phasic in the standinganimal decreases its time constant when walking; therefore, in this situationi. appears to function as a velocity rransducer (CRUSE, l98l; CRUSE &PFLUGER, 1981; CRUSE & SCHMITZ, I983; SCHMITZ, 1985). HOFMANN & KOCH1984) recently have shown the existence of acceleration sensitve units in the
lemoral chordotonal organ.Feedback control is also active in the fast protraction movement of the
sn'ing phase. As in the stance phase, the parameter position appears to contribute:c the decision as to when the swing is terminated, but velocity appears to be:he parameter which is controlled during the movement (DEAN, lg84).
These results imply the following. The system controlling the movementrf a leg can be separated theoretically into two subsystems. One monitors the?osition and load of the leg in order to decide whether or not to complete thestance phase. This tdecision systemr is also influenced by two types ofcoordinating signals which change the anterior and posterior target value butmay also be influenced by other types. The end of the swing phase is determinedby geometrical parameters.
The second subsystem controls the way movement is performed during thestance or swing phase. The motoneurones controlling the force which propelsthe body during stance phase depend upon the output of the decision system,upon coordinating influences and upon velocity; probably acceleration and possiblyload are involved as well. The output of the decision system can formally beconsidered as the reference input of the feedback loop. It is possible that allthese influences summate at the motoneuronal level. The muscles controllingthe distance between body and walking surface seem to be controlled by positionsignals as well. The feedback system is active until the decision system finishesthe actual stance or swing phase.
Finally, it should be mentioned that this theoretical separation into twofunctional subsystems does not necessarily imply that the subsystems arecompletely separate on the anatomical level. Load influences or some coordinatingsignals may produce effects on both levels. Thus, it seems likely that there issome overlap between them.
AcknowTedgenent. I want to express my thanks to Dr. D. F0RSYTHE for proofreading the English manuscript.
26
REFERENCES
CRUSE
BASSLER, U., 1977: Sensory control of leg movement in the stick insectCarausius norosus. Biol. Cybern.,25: 6l-72.
- -, 1983: Neural basis of elementary behaviour in stick insects. Springer, Berlin,Heidelberg, New York.
CRUSE, H., 1979: The control of the anterior extreme position of the hindlegof a walking insect, Carar.qus norostrs. Physiol. Entomol., 4: 121-124.
- -, l98l: Is the position of the femur-tibia joint under feedback control inthe walking stick insect? I. Force measurements. J. exp. Biol., 92: 87-95.
- -, 1984: Coactivating influences between neighbouring legs in walking insects.J. exp. Biol., in press.
- -, 1985: Which parameters control the legVelocity control during the stance phase.
J. exp. Biol., in press.- -, J. DEAN & M. SUILMANN, 1984: The contributions of diverse sense organs
to the control of leg movement by a walking insect. J. comp. Physiol.A, 154: 695-705.& S. EPSTEIN, 1982: Peripheral influences on the movement of the legsin a walking Inssst f,6r-6r,.qus norosus. J. exp. Biol., l0l: 16l-170.& H.-J. PFLUGER, 1981: Is the position of the femur-tibia joint underfeedback control in the walking stick insect? II. Electrophysiologicalrecordings. J. exp. Biol., 92: 97-107.& J. SCHMITZ, lg83: The control system of the femur-tibia joint in thestanding leg of a walking stick insect Carausius morosus. J. exp. Biol.,102:175-185.
DEAN, J., 1984: Control of leg movement in the stick insect: a targetedmovement showing compensation for externally applied forces. J. comp.Physiol., in press.& G. WENDLER, 1982: Stick insects walking on a wheel: Perturbationsinduced by obstruction of leg protraction. J. comp. Physiol., 148: 195-207.& G. WENDLER, 1983: Stick insect locomotion on a walking wheel: Interlegcoordination of leg position. J. exp. Biol., 103: 75-94.
EPSTEIN, S. & D. GRAHAM, 1985: Behaviour and motor output of stick insectwalking on a slippery surface. III. Temporary blocking of intended movementsin forward and backward walking. J. exp. Biol., submitted.
GRAHAM, D. & H. CRUSE, 1981: Coordinated walking of stick insects on a
mercury surface. J. exp. Biol., 92: 229-241.HOFMANN, T. & U. KOCH, 1984: Acceleration receptors in the femoral
chordotonal organ of the stick insect Cuniculua inpigra. J. exp. Biol.,in press.
PEARSON, K. G., 1972: Central programming and reflex control of walking inthe cockroach. J. exp. Biol., 56: 173-193.
SCHMITZ, J., 1985: Control of the leg joints in stick insects: Differences inthe reflex properties between the standing and the walking states. In: M.GEWECKE & G. WENDLER (Eds.), Insect Locomotion. Paul Parey, Berlin,Hamburg:
WENDLER, C., 1964: Laufen und Stehen der Stabheuschrecke: Sinnesborsten inden Beingelenken als Glieder von Regelkreisen. Z. vergl. Physiol., 48: 198-250.
