The femoral chordotonal organs of Decticus albifrons (Orthoptera: Tettigoniidae)—II. Function

Camp. Biochem. Physiol. Vol. 84A, No. 3, pp. 531-543, 1986 Printed in Great Britain

THE FEMORAL ALBIFRONS

0300-9629/86 $3.00 + 0.00 Pergamon Journals Ltd

CHORDOTONAL ORGANS OF DECTICUS (ORTHOPTERA: TETTIGONIIDAE)-II. FUNCTION G. THEOPHILIDIS

Aristotelian

University

of Thessaloniki, School of Science, Laboratory Thessaloniki, 54006, Greece

of Animal

Physiology,

(Received 11 November 1985) Abstract-l. The electrophysiological properties of the pro-meso and metathoracic chordotonal organs of Decticw albifron were studied. 2. All three show minimum tonic response at a femur-tibiae angle of 90”, maximum response during tibia1 fiexion (FTA of 0”) and they show a relatively small increase in their firing frequency during extension (FTA of 180”). 3. The tonic activity of the COs adapts faster in the metathoracic than in the pro and mesothoracic. 4. There are indications that some tonic sensory units are bidirectionally sensitive. 5. The sensory neurons which respond only to tibia1 movement (phasic response) are much larger than those which are active when the tibia is stationary. 6. The responses of the femoral motoneurons to the tibia1 movement represent resistance reflexes.

INTRODUCTION

In Orthoptera the proprioceptor most like to be involved in regulating the activities of the femoral muscles in each leg, is the femoral chordotonal organ (CO). Therefore the COs of the locust’s meso and metathoracic legs were thoroughly investigated (Usherwood et al., 1968; Bums, 1974); both respond to extension and flexion of the tibia; the metathoracic shows the maximum response when its was fully extended (minimum at femur-tibia angle of 60”) and the mesothoracic when it was fully flexed (minimum response at 90“). Also the COs evoked strong reflexes in the extensor and the flexor (see also Theophilidis, 1979) and their removal affects the activity of the femoral muscles. The possible role of the locust’s COs in the neuronal control of the tibia was further investigated. (Hoyle and Burrows, 1973; Burrows and Horridge, 1974; Heitler and Burrows, 1976a,b; Field and Burrows, 1982; Biissler, 1979,1983). However, the physiological studies of the Orthopteran femoral COs have been restricted to the locust, as happened with the structural studies, and there is little information about the function of this proprioceptor in the rest of the species in this order (it has approximately 17,000 identified species). In an attempt to fill this gap, the structure of the COs has been investigated in Decticus albifrons, from the family of Tettigoniidae (Theophilidis, 1985), since strong differences in the structure and the innervation of the extensor tibia muscle (Theophilidis, 1983) have already been reported in this particular species. These studies have shown that there are also some very distinct structural differences between the femoral COs of Decticus and the locust (Theophilidis, 1986). For example, the metathoracic CO of De&us: (a) it is located at the very proximal region of the femur, while in locust it is located at the very distal region; (b) it consists of two closely connected sensory units---there is only one in the locust. The mesothoracic CO consists also of two 537

sensory units almost fused into one, while in the locust the units are completely separate. Also, in all three COs (pro, meso and metathoracic) of Decticus there are no ligaments connecting their sensory regions to the femoral muscle, as is found in locust, while their strands have strong structural differences from the homologous region of locusts’ COs. All these structural differences inevitably lead to the question: are there any significant differences between the physiological properties of the COs of Decticus and those of the locust? The purpose of this work is to study the electrophysiological properties of the pro, meso and metathoracic femoral chordotonal organs of Decticus, to compare the differences between them and to see how these compare with the well studied homologous organs of the locust. MATERIALS AND METHODS To record chordotonal responses to mechanical stimuli (tibila movement) the insect (Decticus albfions, Tettigoniidae) was mounted, ventral side up, on a block of special curved plasticine. All the joints of the legs were restrained except the femoretibial and tibio-tarsal joints of the leg under investigation. A small window was cut in the cuticle of the thorax to expose the ganglia and most of n5 (numbering from Campbell, 1961) with its branches. To record neuronal activity only from the metathoracic Chordotonal Organ (mtC0) a fine hook-in-oil electrode (modified from Wilkens and Wolf, 1974) was attached to nerve SB. Nerves 5B,, 5B,.. SB,.. 5B,.. and the sensorv nerves running distall; fron?;he rhtC0 were all cut off (fo; the exact location of the nerves see Theophilidis, 1986), limiting the afference elicited by tibia1 movement to that from the mtC0. The approximate position of the recording electrode is indicated by the arrows in the insert on Fig. 2. Things were more simple when recordings were required from the mesothoracic or prothoracic chordotonal organs (msC0 or prC0). In this case the sensory nerve (nSB,) separates very early from n5B, almost inside the thorax, so the recording electrode can be placed almost directly on the

G. THEOPHILIDIS

538

nerve. (See the upper arrow, in the insert on Fig. 2). Nerve 5B,, was cut off distal to the msC0 or prC0 to eliminate any other source of sensory activity in n5B,. In all cases the part of n5 between the ganglion and the recording electrode was squeezed using a pair of forceps to eliminate any motor activity reaching the recording chordotonal

electrode. In the experimental set-up described above, care was taken to leave most of the trachial system intact and to disturb the blood circulation as little as possible. Also, the use of tbe saline (Usherwood et al., 1968, pH 7.2 plus 90 mM n-glucose) was minimized in a few drops during the

dissection of the thorax. These precautions were taken to eliminate various factors which may affect and alter the responsiveness of the COs. It has been previously reported that the immersion of the locust metathoracic CO (Usherwood et al., 1968) and the tibia-femoral joint receptors (Coillot and Boistel, 1969) in insect saline, altered the responses of the sense organs. Also, Burns (1974), in order to maintain the responsiveness of the mesothoracic CO of the locust over long periods in saline, found it necessary to aerate the saline and to arrange that it flowed continuously through the channel with the CO. To stimulate the COs mechanically, the tibia of an immobilized femur was extended from w-135” and 180 (full extension) or flexed from 9P-45” and 0” (full flexion) with a constant velocity movement. This movement was imposed on the tibia by a lever which had one end attached to a pen-motor and the other end to the tibia. The axis of rotation of the lever was through the pivot of the femoro-tibial joint, and the rotation of the lever was monitored with a low friction potentiometer. Linear ramp functions were obtained by integrating a square wave by means of an integrated circuit operational amplifier, which in turn drove the pen-motor. The femur-tibia angle (FTA) was visually measured on a miniature protractor scale. When the tibia was at rest, chordotonal activity was analyzed by selecting spikes of certain amplitude and measuring their frequency over a fixed period of time with a counter-timer and print-out. The height of the nerve impulses (they were amplified x 5000) was analyzed using a multichannel analyzer (pulse height analysis). When the dynamic responses were being investigated, the analysis of the activity was accomplished with a spike amplitude selector driving an instantaneous frequency display unit. The changes in frequency were displayed on a pen recorder. To study the reflex effects of the femoral chordotonal organs upon the extensor tibiae motor neurons, in an immobilized insect (as described previously), the femur was dissected to expose the extensor tibiae muscle. Care was taken to leave the CO intact while most of the rest of the sensory inputs to the ganglion were cut off. The recording electrode was placed in the extensor motor nerve while the CO was mechanically stimulated by imposing sinusoidal movement on the tibia. RESULTS The physiological properties of all three COs (pro, meso and metathoracic) of Decticus albifrons were examined separately and in most cases the results were arranged in such a way as to allow their comparison. The tonic response Using the experimental set up described in the Materials and Methods section, neural activity from all three COs was recorded from an almost intact insect. Fig. 1 shows the records from the mtC0 when the tibia was set to different femur-tibia angles (FTA)

and left there for 60 set before the records were made.

Fig. 1. Extracellular records from the sensory nerve of the metathoracic chordotonal organ. Bach trace was photographed after the tibia was placed to the femur-tibia angle, indicated by the number at the left of the record. The arrow, in the middle trace, shows the typical threshold used with the electronic window discriminator. Scale bar: 2Omsec.

The records show that the neural activity was much higher when the tibia was fully flexed than when it was fully extended. The lowest activity occurred in the intermediate angles. Only 12-14 of the tonically active axons can be identified by the height and the shape of their action potentials, during visual inspection, although the mtC0 contains more than 60 axons (Theophilidis, 1986). There are four tonic axons with spike amplitude between 0.08-O.lOmV, four between O.lO-Q.30mV and four between 0.31 to 0.90mV. Similar records, as those shown in Fig. 1, were obtained from the prC0 and msC0, but their overall firing frequency was too high, especially during extreme flexion, to distinguish individual spikes. To study more accurately the response of the COs to different femur-tibia angles, the firing frequency of all the spikes in the chordotonal nerve, that were larger than the noise level, was plotted against FTA in an almost intact insect, as Fig. 2 (top curves) shows. There are some strong similarities, but also some distinct differences in the responses of Decticus COs. All three show a minimum response at a FTA of 90”, and a maximum response and sensitivity (Hz/“, Table 1) during flexion. They also show a relatively small increase in their firing frequency during extension. The differences mainly concern the mtC0, which has a much lower overall frequency, but higher sensitivity (only during flexion, Table 1) than the other two COs. Fig. 2 (lower curves) and Table 1 also show the response and the sensitivity of the COs of the locust. Higher responses and sensitivity of Deticus COS during flexion should be expected; they are arranged in such a way inside the femur that they are stretched only by the tibia1 flexion, showing the maximum

Decticur chordotonal

organs-II

539

‘*

&Jo

l&P

l&y-

FTA

0

is.

6iP

l&P

liOO

FTA

Fig. 2. The responses of the femoral chordotonal organs of Deck-us albifrons (upper curves) and locust (low curves, after Usherwood et al., 1968; Burns, 1974) to different fixed femur tibia angles. The arrows in the insert diagram indicate the region of the sensory nerves where the electrodes were placed to record from the mesothoracic CO (upper arrow) and metathoracic CO (low arrow). For upper curves the activity was counted during the second minute after the positioning of the tibia. These curves represent measurements from five animals (three repetitions for each animal). The vertical bars show + SD of mean. Bars were not placed on the curves of the pro and mesothoracic COs for reasons of convenience. In these cases the + SD is between 15 to 30 imp/set. Solid triangle: proC0, solid circles: msC0, solid squares: mtC0. Open circles: msC0 of locust, Open squares: mtC0 of locust, F’TA: Femur-tibia angle.

displacement of their apodeme during flexion from 90”45” and 4S-O” (Fig. 3). Thus one would expect the minimum response at the point of minimum apodeme displacement (full extension, Fig. 3). The displacement of the apodemes of the msC0 and prC0 is approximately linear from O”-180” and only in the latter, the apodeme is pulled between 140” and 180”. However, the tonic activity was minimized at a FTA of 90”, where all three COs were still stretched, and it was increased again when the displacement of the apodeme (and of course the stretch of the sensory region) was minimized. When at the point of mini-

Fig. 3. Relationship between the movement of the apodeme of the femoral COs and the angle of the femoretibial joint. The movement of the apodeme was determined by measuring the positions (along the longitudinal axis of the femur) of the distal attachment in relation to a fixed point of the femur. This was achieved by an occular micrometer, under a dissecting microscope, whilst setting the femoretibial joint at different angles. The curves represent measurement from four animals. The squares represent the curve of the metathoracic apodeme. The circles represent the curves from the pro and mesothoracic COs which are very similar and are shown in one curve. Their only difference is that, during extreme extension, the prothoracic is relaxed (dotted line) while the mesothoracic is not. FTA: femur-tibia angle. Vertical bars: f SD of mean.

mum displacement the apodemes of the COs were cut off, eliminating any tension developed on their sensory region, the overall firing frequency of all three COs was increased. The increase was between 10 and 20% of the initial frequency at a FTA of 180”, for seven of the ten mtCOs. For the msC0, in five of the six cases, and for the prC0, in seven of the nine cases, the increase was between 40 and 55%. To study the dynamic responses of the msC0 and the mtC0 in relation to tibia1 positioning, their firing frequency was measured when the tibia was placed at various FTAs (Fig. S), using an instantaneous frequency display unit. Typical records of these experiments are shown in Fig. 5a. At FTA of 90” there is a steady tonic activity. When the tibia was flexed to 45” and after a few seconds to O”, the frequency of both COs shows for each step a sudden peak which lasts for 2-3 set, the phasic response, and then adapts reaching a lower steady level. The adaptation curves of the overall activity of the three COs at a FTA of 0” are shown in more detail in Fig. 4. Finally, tibia1

Table I. The sensitivity (impulses/degree) of the femoral chordotonal organ of Decricus albifrom and locust (after Usherwood ef al., 1968 and Bums. 1974). The values were obtained from the curves in Fig. 2 Decticus albfrom Prothoracic CO Mesothoracic CO Metathoracic CO Locust Mesothoracic CO Metathoracic CO *Flexion from 60” to 45”. tExtension from 135” to 160”.

45”+0 2.80 4.42 4.15 5.5 I .28

45”+90”

I .70 I .72

90”+135”

135”+180

1.50

0.35 0.65 0.49

0.35 0.26 0.32

1.31 0.45t

0.85 1.46

1.48. I .90

G. THEOPHILIDIS

540

2’0

’

8'0

'

106

Sec.

Fig. 4. Time course of adaptation of the tonic units in the pro, meso and metathoracic chordotonal organ for the femur-tibia angle of 0” (full flexion). The chordotonal discharges were counted starting at 30 set after the tibia was set. The f SD of mean is approximately l&15% (n5). The bars are not shown for convenience.

extension from 90”-135” has almost the same effect, on the firing frequency of the COs, as the tibia1 flexion from 90”45”. However, extension of the tibia (full extension for example) does not cause any significant changes in the response of either COs. With the recording techniques used in the above experiments it was not possible to study the activity of individual tonic units. From records like those shown in Fig. 1, it is very difficult to justify, by visual inspection or even by using a single channel analyzer, whether certain sensory axons of the mtC0 are excited only by tibia1 flexion or extension. This might happen for some axons, since certain large action potentials occur only during tibia1 extension but not during flexion and vice versa (see the spikes marked with an asterisk in Fig. 1). In an attempt to investigate the response of individual axons, neural activity of the mtC0 was analyzed using a multi-

mV Fig. 6. Pulse height analysis of the action potentials recorded from the metathoracic chordotonal organ when the tibia was placed at various femur-tibia angles for 50 sec. Dotted line: full flexion (integral = 6435 events), Solid line: full extension (integral =4143), dashed line: 90 (integral = 823).

channel analyzer (pulse height analysis, Fig. 6). As Fig. 6 shows, it was not possible to separate many peaks corresponding to the height of the various spikes, due to the small differences in their amplitude. However, two distinct peaks, one at 0.881 mV and the other at 0.962mV, occurred when the tibia was either fully flexed or fully extended. At a FTA of 90”, the two peaks occurred at different points (0.816 mV and 1.050 mV, see Fig. 6). This is an indication that the same tonic axons (or axons with a very similar diameter) are activated by the two extreme positions of the tibia. Units which are bi-directionally sensitive have been found also in the tibio-tarsal chordotonal

b

Fig. 5. Instantaneous frequency display of the metathoracic and mesothoracic chordotonal organs (mtC0, msC0) when the tibia was flexed to 45” and 0” and extended to 135” and 180”. a: The threshold of the window discriminator was set at a very low level to monitor all the spikes in the chordotonal nerve. b: The threshold was exactly above the spikes recorded at a femur tibia angle of 90” (see arrow in Fig. 1). Vertical bar: 250imp/sec. Horizontal bar: IOsec.

Decticus

chordotonal organs-II

organ of the cockroach (Young, 1970) and in the femoral CO of the stick insect. (Hofmann et al., 1985). Phasic response of the COs

To study the way the phasic sensory cells respond, the activity of the meso and metathoracic COs was analyzed using a window discriminator. Although at the beginning of these experiments, various bands of spike amplitude were selected, finally two bands were chosen. To separate the first band (called band A), the window selector was set up to a level to detect only the spikes of the tonically active sensory cells at a FTA of 90” (the spikes below the level indicated by the horizontal arrow in Fig. 1). In the second band (band B) were classified all the action potentials having higher spike amplitudes than those of band A (see Fig. 1). The tibia1 position responses that resulted from this sort of selection are shown in Fig. 5b. Tibia1 flexion causes a fast rising peak of activity for the axons in band B for each step (see steps at 45” and 0” in Fig. 5b), which lasts 1 to 2 set (phasic response), and rapidly declines (not so rapidly for the msC0) to a very low level (tonic response). The most dramatic phasic response occurs when the tibia is fully flexed, while when the tibia is extended, there is a small response by the axons in band B (see steps of 135” and 180” in Fig. 5b). When the window discriminator was set to monitor only the spikes of band A and the tibia was moved to various femur-tibia angles, the records obtained were very similar to those shown in Fig. 5a. In this figure, the comparison of the records a and b shows that the large spikes of band B contribute very little to the overall frequency of the COs (the sensitivity of the pen recorder for the records in 5b was increased). Reflexes in the extensor tibiae motoneurons

Records were made from the motor nerve to the extensor tibiae muscle of an intact, immobilized insect, while stimulating the mtC0 by imposing a sinusoidal movement on the tibia. Figure 7 shows that tibia1 flexion activates the “slow” excitatory motor neurone (SETi). It was found that the resulting frequency of firing and duration of activity increased with the rate of movement of the tibia. If the flexion was faster and larger, in some cases it was also

Fig. 7. Activity recorded from the motor nerve of the metathoracic extensor tibiae muscle, in response to excitation of the chordotonal organ caused by tibia1 movement. The second trace represents the movement imposed on the tibia and it was between a femur tibia angle of 60” (trace up) and 90” (trace down). The spikes are from the &hibito& (I) and “slow” excitatory (SETi) in order of increasing amplitude. Horizontal bar: 50msec. E: Extension. F: Flexion.

541

possible to record activity from the “fast” excitatory motoneuron (FETi). The inhibitor was activated only during tibia1 extension (Fig. 7). Thus, the responses of the three motoneurons represent resistance reflexes. Similar responses have been reported for the femoral chordotonal organ of the locust (Usherwood et al., 1968; Burns, 1974) and the stick insect (Blssler, 1979). DISCUSSION

The tibiae of Decticus albifrons and the locust are very similar in shape and size. However, the proprioceptors which monitor their position and the angular velocity of their movement have some significant structural and anatomical differences (Theophilidis, 1986). The results obtained here show that they also have some significant functional differences. The physiological properties of the COs of Decticus will be discussed and will be compared with the properties of the well studied COs of the locust. Tonic activity

The tonic responses of Decticus COs seem to have interesting similarities. All three: pro, meso and metathoracic, show a maximum tonic response during tibia1 flexion, and a minimum response at a femur-tibia angle of 90”, while during tibia1 extension there is a relatively small increase of their activity. This would be expected since all three COs have a lot of common anatomical and structural features; they consist of two scolopidia, almost fused into one, lying at the very proximal region of the femur and having approximately the same number of sensory axons (Theophilidis, 1986). On the contrary such physiological similarities do not appear in the locust’s COs. The metathoracic shows maximum tonic response when the tibia is fully extended (minimum at femur-tibia angle of 60”) while the mesothoracic responds maximally when the tibia is fully flexed (minimum at FTA of 90”). To explain these differences, someone has to account for the structural differences between these COs. The metathoracic consists of one sensory unit located at the very distal region of the femur, while the mesothoracic has two completely separate scolopidia anchored at the very proximal region of the femur. At this point the question arises as to why the anatomical and physiological properties of the femoral COs are so similar in Decticus and so different in the locust. Decticus has been adapted to lead a very active life on the ground (Theophilidis, 1982) where it can achieve high running speed using its metathoracic legs. Preliminary studies have shown that during fast walking the accurate activation of the fast extensor tibiae (FETi) motor neuron creates quick short jumps which allow fast and precise movement of the insect, a vital factor for its survival on the ground. The extensive use of the metathoracic legs in walking indicated that the CNS should receive approximately the same data on the position of the metathoracic tibiae as it does for the position of the pro and mesothoracic legs, which, in most Orthoptera, are used mainly in posture and walking (Bums, 1973). Possibly, the fact that all three pairs of legs are used for the same purpose (walking) is the reason for

542

G. THEOPHILIDIS

the strong similarities found in the structure and function of their COs. In the locust, which is an excellent flyer, the metathoracic tibiae is mainly used for the defensive kick and the jump which is important for the initiation of flight (Heitler, 1974, 1977; Heitler and Burrows 1976a,b). In this case, the massive activation of the extensor tibiae muscle is caused by the FETi which seems to be inactive in most of the other activities of the insect, in walking for example it is usually silent (Burns, 1973). In the locust, the fact that the metathoracic legs are used for a completely different purpose from the two front legs could be the reason for the strong differences in the construction and physiology of their femoral COs. One of the basic structural differences is that the metathoracic has fewer cells than the mesothoracic and appears to contain no homologue of the proximal scolopidium. This part of the CO may have been lost in the evolution of the jumping mechanism, which means that the CNS must receive considerably less detailed data on the position of the metathoracic tibiae than on the position of the others. Apart from the similarities in the tonic responses of Decticus COs, discussed above, there are some distinct differences. For example, the overall firing frequency of the metathoracic, at various femur-tibia angles, is lower than the responses of the other two (pro > meso > meta), although their chordotonal nerves contain approximately the same number of sensory axons. (Theophilidis, 1986). One possible explanation is that the sensory cells of the two front COs have lower thresholds since they are smaller. Differences in axon diameter, especially between the meta and mesothoracic chordotonal nerves, have been reported elsewhere (Theophilidis, 1986). The other possibility is that the tension developed on the sensory region of the COs is higher in the pro and mesothoracic than the metathoracic, due to the difference in the construction of their strand (see Theophilidis, 1986). The comparison of Decticus and locusts COs shows that the tonic activity, for the same femur-tibia angle, is much higher in the former than in the latter. However, despite this difference, the sensitivity of all COs remains within the same range for each FTA. The advantage of this high firing rate could be that the high level of activation of the sensory neurons permits more gradation of information transmission than if the neurons were less active, and the only effect of an input was to start them firing. Another interesting difference between the COs of Decticus is that although their sensitivity iswithin the same range for each femur-tibia angle, during tibia1 flexion, from 45”-0”, the sensitivity of the metathoracic is much higher than that of the other two. To explain this difference, one inevitably has to account for the unusually large displacement of the apodeme of the metathoracic CO which occurs only during tibia1 flexion from 90-O”. During extension, the displacement of the apodemes of all three COs is very similar. Phasic response

The COs are very sensitive to tibia1 movement and the sensory neurons which respond only to tibia1

movement are much larger than those which are active when the tibia is stationary. This can be concluded from the fact that the phasic responses gave a recorded spike amplitude up to five times that of the largest tonic spike, implying that the axon diameters may be up to two and a half times greater (Pearson et al., 1970). Such differences in axon diameter can also be easily seen in the cross sections of the chordotonal nerves (Theophilidis, 1986). The large axons conduct action potentials much faster than the small ones (for the relationship of axon diameter and conduction velocity see Aidley, 1971; Rushton, 1951), and this ensures that the information about changes in the angular velocity of the tibia, which in a free walking insect is a very quick event, will arrive at the CNS as soon as possible. Adaptation

In the COs the large axons (band B) generally adapt very quickly, showing a phasic-tonic response, while the smaller axons adapt much more slowly. The interesting point in Decticus is that the small axons (band A) of the metathoracic CO adapt faster than the axons of the mesothoracic which finally adapt faster than the axons of the prothoracic. This may be caused by the difference in the construction of the strand, the only elastic movable part of the COs, which consists in the metathoracic of connective tissue and the cuticular tube, and in the mesothoracic, of the strand cells packed with microtubules while in the prothoracic it is a combination of the previous two (Theophilidis, 1986). Possibly the unusually large number of the microtubules, which generally are supporting elements of the cells, may change the rigidity of the strand. This may effect the longitudinal tension finally applied to the sensory neurons of the scolopidia, changing their adaptation rate and possibly their tonic response. It has been already suggested by Lewis (1970) that the visco-elastic components of cuticular mechanoreceptors may play an important role in receptor adaptation. Similar function may have the cuticular tube inside the strand of the metathoracic CO, since specialized mechanical components have been shown to be important in the adaptation behaviour of a number of mechanoreceptors (Loewenstein and Mendelson, 1965; Boyd, 1976). At least two causes of receptor adaptation have been distinguished in mechanoreceptors (Mellon, 1968). On the one hand, the visco-elastic properties of the tissue linking the receptor neuron to the stimulus source, may bring about a decline in the generator potential, even though the applied stimulus remains constant. On the other hand, the properties of the spike generating membrane may bring about a decline in spike frequency even though the generator potential remains constant. Further investigations are required to find out which of the two applies to the COs of Decticus. From the physiology of the COs, generally, it is obvious that the adequate stimulus in the scolopidia, is an increase in their longitudinal tension (see also Young, 1970). Although this principle is generally accepted, it is worth noting that in both Decticus and the locust COs, the minimum firing frequency occurs at a FTA of 90” (60” for the metathoracic of the

Decticus

chordotonal organs-11

locust), when the scolopidia are still stretched. When the tension of the strand is minimized (full tibia1 extension), the firing frequency increases. Also in Decticw, when the apodemes of the COs were cut off, eliminating any mechanical tension developed on the scolopidia, their firing frequency was increased although one would expect a dramatic reduction, since the longitudinal tension was eliminated. These contradictory results may give some clues concerning the mechanotransducing mechanism of the COs. Possibly in each scolopidium, the tissue (connective or layers of chitin) surrounding the sensory cells creates a rigid wall, like an elastic capsule, where the sensory endings are embedded. If it is assumed that this capsule shows the minimum distortion of its spherical shape when the scolopidia are stretched to a certain length (for example, in the resting position of the tibia, a PTA of go”), further stretch or relaxation of the scolopidia will change the shape of the capsule, creating forces which excite the sensory ending. However, further combined EM and electrophysiological studies are required to explain this phenomenon.

543

metathoracic du criquet Schistocerca gregaria. J. Insect Physiol. 15, 14491470. Field L. H. and Burrows M. (1982) Reflex effects of the femoral chordotonal organ upon leg motor neurones of the locust. J. exp. Biol. 101, 265-285. Heitler W. J. (1974) The locust jump: Specializations of the metathoracic femor-tibia1 joint. J. camp. Physiol. 89, 93-104.

Heitler W. S. (1977) The locust jump. III. Structural specialization of the metathoracic tibiae. J. exp. Biol. 67, 29-36. Heitler W. J. and Burrows M. (1976a) The locust iumn. I. The motor programme. J. exp. BioL 66, 203-2l!2. _ Heitler W. J. and Burrows M. (1976b) The locust iumn. II. Neural circuits of the motor programme. J. exp.-Bioi. 66, 221-241. Hofman T., Koch U. T. and Biissler U. (1985) Physiology of the femoral chordotonal organ in’ the. stick insect Cuniculina imuigra. J. exv. Biol. 114. 207-223.

Hoyle G. and-Burrows M. (1973) Neural mechanisms underlying behaviour in the locust, Schistocerca gregaria. I. Physiology of identified motoneurons in the metathora& ganglion. J. Neurobiol. 4, 341. Lewis C. T. (1970) Structure and function in some external receptors. .Symi. R. Entomol. Sot. (London) 5, 59-76. Loewenstein W. R. and Mendelson M. (1965) Components of receptor adaptation in Pacinian corpuscle. J. Physiol., (Land.) 177, 377-397.

REFERENCES Aidley D. J. (1911) The Physiology of the Excitable Cells. Cambridge University Press. Biissler U. (1979) Effects of crossing the receptor apodeme of the femoral chordotonal organ on walking, jumping and singing in locust and grasshoppers. J. Comp. Physiol. 134A, 173-176. BBssler U. (1983) Influence of femoral chordotonal organ afferences on ecdysis and on the development of motor programmes in locust larvae. Physiol. Entomol. 8, 353-357.

Boyd I. A. (1976) The mechanical properties of dynamic nuclear bag fibres, static nuclear bag fibres and nuclear chain fibres in isolated cat muscle spindles. Prog. Brain Res. 44, 3349.

Burns M. D. (1973) The control of walking in Orthoptera. I. Leg movement in normal walking. J. exp. Biol. 58, 45-58.

Bums M. D. (1974) Structure and physiology of the locust femoral chordotonal organ. J. Insect Physiol. 20, 13191339.

Burrows M. and Horridge G. A. (1974) The organization of inputs to motoneurons of the locust metathoracic leg. Phil. Trans. R. Sot. Lond. B 269, 49-94. Campbell J. I. (1961) The anatomy of the nervous system of the mesothorax of Iocusta migratoria migratoroides. Proc. Zoo/. Sot. Land. 137, 403432. Coillot J. P. and Boistel J. (1969) Etude de l’activite Clectrique propagee de recepteurs a l’ttirement de la patte

Mellon de F. (1968) The Physiology of Sense Organs. Edinburgh and London: Oliver & Boyd. Pearson K. G., Stein R. B. and Mulhotra S. K. (1970) Properties of action potentials from insect motor nerve fibres. J. exp. Biol. 53, 290-316. Rushton W. A. H. (1951) A theory of the effects of fibre size in medullated nerve. J. Physiol., Lond. 115, 101-122. Theophilidis G. (1979) The neuronal control of the mesothoracic flexor tibiae muscle of the locust. Ph.D. Thesis, Glasgow University. Theophilidis G. (1982) Comparative studies of Orthoptera species adapted to living on the ground and of some strong fliers from the same order. In Adaptations to Terrestrial Environment (Edited by Mergaris, Arianoutsou-Faraggitaki and Reiter). Theophilidis G. (1983) A comparative study of the anatomy and innervation of the metathoracic extensor tibiae muscle in three orthopteran species. Comp. Biochem. Physiol. 75A, 285-292.

Theophilidis G. (1986) The femoral chordotonal organs of Decficus albtjions (Orthoptera: TettigoniidaetI. Structure. Comp. Biochem. Physiol. 84, 527-534. Usherwood P. N. R., Runion H. I. and Campbell J. I. (1968) Structure and physiology of a chordotonal organ in the locust leg. J. exp. Biol. 48, 305-323. Wilkens L. A. and Wolfe G. E. (1974) A new electrode design for en passant recording, stimulation and intracellular dye infusion. Comp. Biochem. Physiol. 48A, 2 17-220. Young D. (1970) The structure and function of a connective chordotonal organ in the cockroach leg. Phil. Trans. R. Sot. B 256, 401428.