Cruse H. Is the position of the femur tibia joint under feedback control in the walking stick insect?: I. Force measurements. The journal of experimental biology. 1981;92(1):87-95

Cruse, Holk

English

Publications at Bielefeld University

J. exp. Biol. (1981), 9». 87-95 8 7W'th 9 figuresrrinted in Great BritainIS THE POSITION OF THE FEMUR-TIBIA JOINT UNDERFEEDBACK CONTROL IN THE WALKING STICK INSECT?I. FORCE MEASUREMENTSBY H. CRUSEFB Biologie der Universitdt Kaiserslautern, FRG(Received 27 May 1980)SUMMARYIt is known that a feedback system is involved in the position control of thefemur-tibia joint of a fixed stick insect. Force measurements indicate thatthe control system also mediates negative feedback in the walking animal,the gain of the reflex loop and the half-time value of the reflex response beingdecreased. The biological significance of this effect is discussed. The resultsagree with similar experiments on man by other authors.INTRODUCTIONIn 1965 B&ssler described a negative feedback mechanism which controls theposition of the femur-tibia joint in the legs of the stick insect, Carausius morosus. Insubsequent papers the properties of this system were investigated in detail (Bassler,1967, 1972a, b, 1973, 1974, 1976; Godden, 1974; Bassler, Cruse & Pfliiger, 1974;Bassler & Storrer, 1980; Storrer & Cruse, 1977; Cruse & Storrer, 1977). When thefemur-tibia joint of the leg is flexed passively, the extensor muscle of this joint isexcited to oppose this movement. A similar response occurs in the flexor muscle whenthe joint is extended. In most experiments the femoral chordotonal organ was stimu-lated directly (rather than by bending the femur-tibia joint) as this is the feedbacktransducer of the system.In all of these previous experiments the animals were fixed and normally did notshow any active movements, other than those elicited by stimulation of the chordo-tonal organ. When such animals attempted to perform active movements as a resultof mechanical stimulation, for example by touching the abdomen, the system showsa different behaviour (Bassler, 1973, 1974, 1976). After such stimulation, relaxationof the chordotonal organ (corresponding to an extension of the femur-tibia joint)does not elicit a significant reaction of the flexor muscle. The negative feedback systemseems therefore to be absent in this situation. In contrast, extension of the chordotonalorgan (corresponding to a flexion of the femur-tibia joint) produces excitation of theflexor muscle. This could result from the system switching from negative to partialpositive feedback, a mechanism which seems to depend upon the internal state of theaiimal. How the system behaves during walking is unknown and is investigated inThis paper.88 H. CRUSEMETHODSIt is not possible to stimulate the chordotonal organ, by moving the receptorapodeme with fine forceps, in a free-walking stick insect. An alternative method wastherefore devised in which adult female stick insects (Carausius morosus) walked on ahorizontal path of 30 mm in width. A small piece of the margin of the path (5 mmwide, 8 mm long) was cut away and then fixed to a forcemeter (Hellige UL 50 p) soas to form a small platform (Cruse, 1976). The animal was then allowed to walk overthe path. When the animal then touched the platform, the force exerted during stancephase could be measured. In these experiments only the component of force parallelto the transverse axis of the body (lying in the horizontal plane and perpendicular tothe long axis of the body) was measured. Such a force directed toward the body ispositive (Cruse, 1976). In addition, the forcemeter together with the platform couldbe moved by hand, perpendicular to the long axis of the insect's body. During thestance phase of the leg - an additional flexion (F) or extension (E) of the femur-tibiajoint - could thus be superimposed on the walking movement of the leg (Fig. 1). Theduration of the platform movement ('stimulus ramp') was about 200 ms.Movement of the platform to or from the body changes the femur-tibia angle for,during stance phase, the middle leg is orientated more nearly perpendicular to thelongitudinal axis of the body than the front or hind legs. With the latter the thoracic-coxal angle would be altered and, therefore, only the middle legs were investigated.The platform was moved inward or outward by 5 mm. With the femur of the middleleg standing perpendicular to the long axis of the body this movement produced achange of 350 in the femur-tibia joint, 10° in the coxa-trochanterofemur joint and o°in the thoracic-coxal joint. The position of the platform was measured by an inductiveposition transducer (Hellige WL 150) and recorded together with the force values ona 2-channel pen recorder (Hellige He 18). In control experiments the receptor apo-deme of the femoral chordotonal organ was cut as described earlier (e.g. Bassler, 1965).Fig. 1. Schematic cross-section through an animal with a middle leg standing on the platformof the experimental device.Control of femur-tibia joint in stick insect. I 89RESULTSThe standing animalAs the experimental device differs from that used by previous authors, the experi-ments with standing animals had to be repeated. To do this, a free animal was placedon the walking path so that a middle leg stood on the platform. The platform wasthen moved stepwise outwards or inwards so as to extend or flex the femur-tibia joint.As expected from earlier observations, the response to extension of the femur-StandingRA intactV(B) StandingRA cutmN1 sFig. 2. Typical force response of a standing animal; (A) intact and (B) with the receptorapodeme cut. F, flexion; E, extension of the femur-tibia joint. Upper trace: position of theplatform of the force transducer. Lower trace: forces. Positive forces are directed towards thebody.A/(mN)Fig. 3. The change of the force value (A/) during an imposed flexion. Intact animal: blackcolumns (n = 84, 6 animals). Animals with cut receptor apodeme: white columns (n = 132,6 animals).H. CRUSE50oe 10-1 0ll111 n 11 111 i 1110 12 14i i16TTI18A/"(mN)Fig. 4. The change of the force value during an imposed extension. Intact animals: blackcolumns (n = 83, 6 animals). Animals with cut receptor apodeme: white columns (n = 130,6 animals).tibia joint has a higher amplitude than the response to flexion (Fig. 2 A). To obtain aquantitative estimate of the force reaction, the difference between the force value atthe beginning and end of the stimulus ramp was measured. The distribution of thesevalues is shown by the black columns in Fig. 3 (flexion) and Fig. 4 (extension). Thearithmetic mean values are — 30 mN (median — 2-5 mN) and 6-5 mN (median 6-o mN)respectively.These results cannot be compared quantitatively with earlier ones obtained withfixed animals for two reasons. First, the position of the leg is more variable than in theexperiments with fixed animals. Secondly, not only the torques developed by themuscles controlling the femur-tibia joint are measured but also those of the otherjoints (thoracic-coxal joint, coxa-trochanter joint). However, the contribution of thecontrol mechanism of the femur-tibia joint can be estimated if the experiments arerepeated with the receptor apodeme of the femoral chordotonal organ cut (Fig. 2B).The distribution of the values of these force changes is shown in Fig. 3 (flexion) andFig. 4 (extension). The arithmetic mean values are — 0-3 mN (median 0-5 mN) and0-3 mN (median 0-5 mN) respectively.These results show that in the free-standing animal the main part of the responseshown in Fig. 2 A results from stimulation of the femoral chordotonal organ. Thesecond part of the response might be due to stimulation of other reflex loops in thefemur-tibia joint, as well as in other joints of the leg, or to passive properties of themuscles.Considering the decay of the force after the ramp a semi-logarithmic plot shows thatthe time course closely approximates to two additive exponential functions withdifferent maximum amplitudes and time constants (see Fig. 5). The mean half-timevalue of the initial fast decay is o-6 (± 0-24) s (x + S.D., n = 66), after flexion and o-6(± 022) s (n = 59), after extension. To obtain the half times of the slow decay aseparate series of experiments was performed (with 30 min between two consecutiveramps). These values are 38 (+ 12) s (n = 13), after flexion, and 34 (± 14) s (n = 19),after extension. The ratio between the maximum amplitudes of the fast- and slow-falling exponential functions was I-I (+ 0-5) (n = 14), for the response to flexion, and<2*0 (± i-o) (n = 19), for extension. The half-time value of the whole function (nolControl of femur-tibia joint in stick insect. I• \10 20Fig. 5. The time course of an individual response to an imposed flexion. The two regressionlines shown are calculated for the values between o-i and 1 8 and between 2 and 25 s after theend of the ramp portion.measured here) would thus be ~ 1 s, after flexion, and somewhat shorter afterextension. During the 30 min of the constant input value the force does not completelyreach the final value. This difference amounts to 0-65 (+ 0-57) mN (/» = 25).The walking animalFor the middle leg of the intact walking animal the typical time course of the forcecomponent parallel to the transverse axis of the body shows a force at first directedtowards the body (' positive force value') and then away from the body. However, theindividual time course of the force varies considerably from step to step (Fig. 6).Because of the changing force during the stance phase the responses cannot beseen as clearly as in the standing animal. Nevertheless the following results areobvious. When a flexion is superimposed on the movement of the femur-tibia joint,then during the ramp part of the stimulus the force value decreases (see Fig. 7 A, B).When an extension movement is superimposed the force value is increased during theramp part of the stimulus (Fig. 7C, D). This is not dependent on whether the forcevalue before the stimulus is positive or negative (Fig. 7). To obtain quantitativeresults, the change of the force value during the ramp part of the stimulus wasmeasured. The results for flexions of the femur-tibia joint are shown in Fig. 8. TheFig. 6. Two examples showing the time course of the force of the middle leg of a walkinganimal during an undisturbed retraction (black bar). Positive forces (upward deflexion) aredirected towards the body.H. CRUSE1 mN1 sIVFig. 7. Four examples showing the time course of the force for a walking animal, when aflexion (A, B) or an extension (C, D) is superimposed on the movement of the femur-tibiajoint. The black bars show the duration of retraction.50 -LL10- 6 - 4 0A/(mN)Fig. 8. The change of the force value during an imposed flexion in the walking animal. Intactanimals: black columns (n = 128, 13 animals). Animals with cut receptor apodeme: whitecolumns (n = 131,4 animals).Control of femur-tibia joint in stick insect. I 9330oO>. 10zr 0£ 6^ -41 I T I i4 6Fig. 9. The change of the force value during an imposed extension in the walking animal.Intact animals: black columns (n = 130, 16 animals). Animals with cut receptor apodeme:white columns (n = 160, 5 animals).arithmetic mean value is — i-24mN (median — 1 mN). The corresponding resultsobtained from animals with cut receptor apodeme are shown by white columns. Thearithmetic mean value is 0-55 mN (median 0-5 mN). The distributions are signific-antly different (^-test, P 4, o-oi %). Fig. 9 shows results obtained during an ex-tension of the femur-tibia joint. The arithmetic mean value of intact animals (blackcolumns) is 073 mN (median 1 mN). The mean value of animals with cut receptorapodeme (white columns) is —0-39 mN (median —0-5 mN). Again the distributionsare significantly different (^-test, P <^  o-oi %). The distributions from the intactwalking animal also differ significantly from those obtained from the standing animalwith the receptor apodeme cut (^-test, P <^  o-oi %). Comparison of Figs. 8 and 9 withFigs. 3 and 4 shows that in the walking animals there is much less scatter in theamplitude of the reflex response.Because of the irregular time course of the forces, investigation of the responsefollowing the ramp is difficult. However, it appears that the reaction found in walkinganimals also differs in this respect from that of standing animals. After the ramp theforce value returns to that before commencement of the stimulus. This time intervalis much shorter in walking animals than in standing ones. The value of the half timecan be roughly estimated as 100 ms.DISCUSSIONWhile both standing and walking there are obvious differences between the intactanimals and those with the receptor apodeme cut. Thus during flexion of the femur-tibia joint the mean values of the force changes are — 2-7 mN in the standing and—1-8 mN in the walking animal. During an extension of the femur-tibia joint thedifferences are 6-2 mN in the standing and I-I mN in the walking animal. This showsthat in addition to the change of the half times the gain of the reaction of the walkinganimal is reduced to about 65% during flexion and to about 20% during extension ofthat in the standing animal (using the force as an output value). This corresponds toresults obtained by Wieneke & Denier van der Gon (1974) in man, where the gain ofthe reflex loop of the wrist joint was diminished to 25-50% during active movementscompared to the gain when the hand is held still (these authors used position notforce as output value). The reaction in man is also asymmetric. The reflex gain ispigher when the disturbance input acts in the opposite direction to the intendedEXB 9294 H. CRUSEmovement and is smaller when it acts in the same direction. In stick insects thjresponse to a flexion seems to be somewhat stronger than the response to an extension"of the femur-tibia joint. Wieneke & Denier van der Gon (1974) suggested that thereduced gain resulted from a decrease in the damping effect, caused by the feedbackmechanism, increasing the speed of limb movements. This effect might be emphasizedin the stick insect, for in addition to decrease in maximum amplitude (because of thesmaller half time) the duration of the reflex response is also shortened.The control experiments with the cut receptor apodeme indicate that the measuredreaction did not result from inertia properties of the leg or the force transducer.However, the force measurements alone do not conclusively show that the measuredreaction is a response of the femur-tibia control system. There are two other possibili-ties. If there are intra-leg reflexes between different joints, as found by Delcomyn(1971) in cockroaches, then stimulation of the femoral chordotonal organ, by bendingthe femur-tibia joint, would elicit a reaction in the coxa-trochanter joint. Secondly,cutting the receptor apodeme might decrease the tonus of the leg muscle. Thereforethe possibility cannot be excluded that in both standing and walking animals onlyreactions of the elastic properties of the muscle systems are measured, and that thesemight be changed in the absence of excitation from the femoral chordotonal organ.However, electrophysiological recordings have shown that the femur-tibia controlsystem is active in this experimental situation (Cruse & Pfliiger, 1981). On the otherhand, the electrophysiological experiments alone provide no quantitative measureof the gain or the half-time value of the whole system. Therefore, only with a combina-tion of both methods is a sufficient description of the system possible.In walking animals with severed receptor apodemes the reaction of the force differsslightly from zero and has a sign opposite to that of the reaction of the intact animal.This can, however, be explained by regarding the tibia as a passive strut. Afterextension the tibia is in an oblique position, pointing away from the body. Thus theforce which the tibia exerts on the ground has a horizontal component with negativesign (pointing away from the body). After a flexion the tibia is in an oblique position,pointing towards the body. Correspondingly a horizontal component with positivesign will occur. The forces developed by the femur-tibia control system are added tothese forces. These passive components are smaller in standing individuals. This isto be expected, for in an animal standing on six legs an individual one develops lessforce than in a walking insect, where less than six legs are in contact with the ground.This research was supported by DFG (Cr 58/2).REFERENCESBASSLER, U. (1965) Proprioreceptoren am Subcoxal- und Femur-Tibia-Gelenk der StabheuschreckeCarausius morosus und ihre Rolle bei der Wahrnehmung der Schwerkraftrichtung. Kybernetik 2,168-193.BASSLER, U. (1967). Zur Regelung der Stellung dea Femur-Tibia-Gelenkes bei der StabheuschreckeCarausius morosus in der Ruhe und im Lauf. Kybernetik 4, 18-26.BASSLER, U. (19720). Der ' Kniesehnenreflex' bei Carausius morosus: Obergangsfunktion und Fre-quenzgang. Kybernetik 11, 32-50.BASSLER, U. (19726). Der Regelkrei3 des Kniesehnenreflexes bei der Stabheuschrecke Carausiusmorosus: Reaktionen auf passive Bewegungen der Tibia. Kybernetik 13, 8-20.Control of femur-tibia joint in stick insect. I 95I|SLER, U. (1973). Zur Steuerung aktiver Bewegungen des Femur-Tibia-Gelenkes der Stabheu-chrecke Carausius morosui. Kybernetik 13, 38-53.BASSLEB, U. (1974). Vom femoralen Chordotonalorgan gesteuerte Reaktionen bei der StabheuschreckeCarausius morosus'. Messung der von der Tibia erzeugten Kraft 1m aktiven und inaktiven Tier.Kybernetik 16, 213-226.BASSLER, U. (1976). Reversal of a reflex to a single motoneuron in the stick insect Carausius morosus.Biol. Cybernetics 24, 47-49.BASSLER, U., CRUSE, H. & PFLOGER, H.-J. (1974). Der Regelkreis des Kniesehnenreflexes bei der Stab-heuschrecke Carausius morosus. Kybernetik 15, 117-125.BXSSLEB, U. & STORRER, J. (1980). The neural basis of the femur-tibia control system in the stickinsect Carausius morosus. I. Motoneurons of the extensor muscle. Biol. Cybernetics 38, 107-114.CRUSE, H. (1976). The function of the legs in the free walking stick insect, Carausius morosus. J. comp.Physiol. n a , 235-262.CRUSE, H. & PFLUCER, H.-J. (1981). Is the position of the femur-tibia joint under feedback control inthe walking stick insect? II. Electrophysiological recordings. .7. exp. Biol. 9a, 97-107.CRUSE, H. & STORRER, J. (1977). Open loop analysis of a feedback mechanism controlling the leg positionin the stick insect Carausius morosus: comparison between experiment and simulation. Biol. Cyber-netics 25, I43-I53-DELCOMYN, F. (1971). Computer aided analysis of a locomotor leg reflex in the cockroach Periplanetaamericana. Z. vergl. Physiol. 74, 427-445.GODDEN, D. H. (1974). The physiological mechanism of catalepsy in the stick insect Carausius morosus(Br.). J. comp. Physiol. 89, 251-274.STORRER, J. & CRUSE, H. (1977). Systemanalytische Untersuchung eines aufgeschnittenen Regelkreises,der die Beinstellung der Stabheuschrecke Carausius morosus kontrolliert: Kraftmessungen an denAntagonisten Flexor und Extensor tibiae. Biol. Cybernetics as, 131-142.WlENEKE, G. H. & DENIER VAN DER GON, J. J. (1974). Variations in the output impedance of the humanmotor system. Kybernetik 15, 159-178.

Der Regelkreis des Kniesehnenreflexes bei der Stabheuschrecke Carausius morosus.

Is the position of the femur-tibia joint under feedback control in the walking stick insect?

Open loop analysis of a feedback mechanism controlling the leg position in the stick insect Carausius morosus: comparison between experiment and simulation.

Proprioreceptoren am Subcoxal- und Femur-Tibia-Gelenk der Stabheuschrecke Carausius morosus und ihre Rolle bei der Wahrnehmung der Schwerkraftrichtung.

Reversal of a reflex to a single motoneuron in the stick insect Carausius morosus.

Systemanalytische Untersuchung eines aufgeschnittenen Regelkreises, der die Beinstellung der Stabheuschrecke Carausius morosus kontrolliert: Kraftmessungen an den Antagonisten Flexor und Extensor tibiae.

The function of the legs in the free walking stick insect, Carausius morosus.

The neural basis of the femur-tibia control system in the stick insect Carausius morosus. I. Motoneurons of the extensor muscle.

The physiological mechanism of catalepsy in the stick insect Carausius morosus (Br.).

Variations in the output impedance of the human motor system.

Vom femoralen Chordotonalorgan gesteuerte Reaktionen bei der Stabheuschrecke Carausius morosus'. Messung der von der Tibia erzeugten Kraft 1m aktiven und inaktiven Tier.

Zur Regelung der Stellung dea Femur-Tibia-Gelenkes bei der Stabheuschrecke Carausius morosus in der Ruhe und im Lauf.

Zur Steuerung aktiver Bewegungen des Femur-Tibia-Gelenkes der Stabheuchrecke Carausius morosui.

Is the position of the femur tibia joint under feedback control in the walking stick insect?: I. Force measurements

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Is the position of the femur tibia joint under feedback control in the walking stick insect?: I. Force measurements

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