In the decapod Crustacea, Palinurus vulgaris and Jasus lalandii, the reflex influences of one particular proprioceptor organ, the coxo-basal chordotonal organ (CB), on all the muscles operating the proximal and distal joints of the same leg, have been analysed. The distal end of CB was clamped in fine forceps mounted on a servo-controlled stretcher, and CB length changes of 2 mm were applied. Motor unit activity of the different muscles was recorded as electromyograms (EMGs).

  1. Two types of proprioceptive reflex evoked by CB length changes have been investigated: (a) resistance reflexes of the two levator and two depressor muscles of the same leg segment, the coxopodite, i.e. ‘intrasegmental reflexes’, (b) ‘intersegmental reflexes’ induced in the muscles operating the proximal (T-C) joint of the same leg, and in all eight muscles of the limb segments distal to CB.

  2. Both levator muscles respond reflexly to imposed CB stretch (which normally occurs with limb ‘depression’), while both depressors respond during CB shortening (or passive ‘elevation’ of the leg).

  3. Intersegmentally, CB stretch reflexly activates the M-C extensor muscle, and sometimes facilitates the T-C remotor and C-P bender muscles. Shortening of the single CB organ of a leg excites one or two tonic motor units of the T-C promotor and M-C flexor muscles, and also facilitates the remotor, I-M reductor, and the single stretcher-opener excitatory motoneurone.

  4. Some of these muscles, particularly the M-C flexor and extensor muscles, are also influenced intersegmentally by the resting length of CB, usually but not invariably in the same direction as for the corresponding dynamic reflexes.

The role of the CB chordotonal organ is discussed, with particular consideration of its intersegmental reflex influence on the posture of the entire leg, and on the more complex motor behaviour of locomotion, where it may be specially significant in coordination of the limb in lateral walking. A complex picture of both tonic and dynamic, intra- and intersegmental reflex regulation of the positions and movements of the limb segments, thus emerges.

In relatively complex behaviour involving jointed limbs, all the segments of a limb operate together. Accordingly, the neural activity patterns underlying such behaviour presumably comprise more or less synchronous motor commands to several muscles in different segments. For example, during lateral walking in decapod Crustacea like the rock lobster, levation of the leg at the coxo-basal (C-B) joint, flexion at the merocarpopodite (M-C) joint, and adduction (‘closing’) of the most distal (P-D) joint (see Fig. 1), commonly occur together in a trailing leg, and usually in conjunction with depression, flexion, and P-D abduction (‘opening’) in the contralateral, leading leg (Clarac & Ayers, 1977).

Fig. 1.

General disposition of the different segments (upper drawing: dorsal view) and joints (middle drawing: anterior lateral view) of a left third walking leg of the rock lobster, Palinurus vulgaris. The lower diagram is a schema of the muscles ; the joints are represented by rectangles and the fulcra as black dots. Abbreviations of muscles (in this and subsequent figures): rein. = (T-C) remotor, prom. = promotor; lev. = (C-B) levator, dep. = depressor; red. = (I-M) reductor; ext. = (M-C) extensor, flex. — flexor; ace. = accessory; stret. = stretcher (C-P retractor), bend. = bender (= C-P protractor); open. = opener (i.e. P-D extensor or abductor), clos. = closer (P-D flexor/adductor).

Fig. 1.

General disposition of the different segments (upper drawing: dorsal view) and joints (middle drawing: anterior lateral view) of a left third walking leg of the rock lobster, Palinurus vulgaris. The lower diagram is a schema of the muscles ; the joints are represented by rectangles and the fulcra as black dots. Abbreviations of muscles (in this and subsequent figures): rein. = (T-C) remotor, prom. = promotor; lev. = (C-B) levator, dep. = depressor; red. = (I-M) reductor; ext. = (M-C) extensor, flex. — flexor; ace. = accessory; stret. = stretcher (C-P retractor), bend. = bender (= C-P protractor); open. = opener (i.e. P-D extensor or abductor), clos. = closer (P-D flexor/adductor).

Intersegmental relationships are clearly important in such behaviour. Reflex interaction between different segments of a limb has been suggested by experiments involving joint immobilization during locomotion in crabs (Clarac & Coulmance, 1971). If, for instance, the M-C joint is fixed in an extreme position, the movements occurring at the C-B joint in the same leg during sideways walking are altered. Another, more specific, proximally directed, intersegmental reflex action has been briefly reported in crayfish walking legs (Moody, 1970). Bending or stretching the carpo-propodite (C-P) joint influences the tonic discharge frequency of a motoneurone innervating the thoracico-coxal muscle receptor, and of others supplying the coxal promotor muscle, of the same leg.

Recently Ayers & Davis (1977) have demonstrated in the lobster, Homarus americanas, that several leg muscles are excited phasically by passive movement of individual joints in the limb. These reflexes involve almost all walking leg joints, and they distinguish between ‘resistance’ and ‘distributed’ reflexes. Resistance reflexes have been extensively investigated in decapod crustacean limbs (e.g. Bush, 1962b; Barnes, Spirito & Evoy, 1972; Vedel, Angaut-Petit & Clarac, 1975). They are mediated by chordotonal organs at each joint and also the M-C myochordotonal organ (Bush, 1965; Evoy & Cohen, 1969; see also Mill, 1976), and by the single thoracico-coxal muscle receptor of the basal leg joint (Bush & Roberts, 1968; Bush, 1976, 1977). Like the analogous vertebrate stretch reflexes, these resistance reflexes tend to resist passively imposed joint movements, by reflex excitation of motoneurones innervating the stretched muscles.

The term ‘distributed reflex’ is used by Ayers & Davis to refer to reflex interaction between different segments of the same leg. For this type of reflex we prefer the term ‘intersegmental reflex’, in contrast to the resistance reflex which is an ‘intrasegmental reflex’. These two more general, complementary and essentially morphological, categories of proprioceptive reflex within individual limbs, can then be used to encompass other leg reflexes arising from different types of proprioceptor, including apodeme tension receptors (Macmillan & Dando, 1972) and cuticular stress detectors (Clarac, 1976). Thus each type of leg receptor mentioned above has now been implicated in intersegmental as well as intrasegmental reflexes (Clarac, 1977). Furthermore, as will be suggested below (see Discussion section 2b), certain intersegmental reflexes may be regarded as having a postural role comparable to the homeostatic action of the more extensively studied ‘resistance reflexes’. The latter term, therefore, though generally used hitherto to denote a particular kind of intrasegmental reflex, should in future preferably be thought of in a wider functional context.

The present paper, then, reports on an experimental study of both intrasegmental and intersegmental reflexes, proximally and distally directed, in walking legs of the intact rock lobster. The widespread reflex influences of one particular proprioceptor organ, the coxo-basal chordotonal organ (CB), on all the muscles operating the proximal and distal joints of the same leg, have been analysed. Preliminary accounts of these intersegmental reflexes have been presented previously (Bush & Clarac, 1975; Vedel, Clarac & Bush, 1975).

The rock lobsters Palinurus vulgaris and Jasus lalandii were used in this study. The animal was strapped with rubber bands dorsal side up in a Perspex dish. This was filled with cooled sea water, which was maintained throughout the experiment at about 10°C by means of a Peltier effect cooling element.

Experiments were usually performed on the fifth (posterior) or fourth pereiopod or sometimes on the third. The chosen leg was fixed horizontally so as to allow access to the coxo-basal chordotonal organ, CB, from the dorsal articular membrane of the coxo-basal (C-B) joint. This soft cuticle was dissected away to expose the receptor strand distally, where it inserts onto the proximal rim of the coxopodite, between the anterior and posterior levator muscle tendon insertions.

Before severing the distal attachment of the strand, it was clamped in the points of fine forceps mounted on a servo-controlled stretcher. This apparatus (Clarac & Vedel, 1971) allowed calibrated sinusoidal length changes to be applied to the CB strand. Usually CB length changes of 2 mm were applied, this being about 16−20% of the normal resting length of CB (about 10−12 mm), and well within the normal physiological limits (8·5−16·5 mm in a 700 g Palinurus; our specimens ranged from about 600 to 800 g). The monitored length changes are represented in the bottom trace of each record, increased C-B length (stretch) being indicated by upward deflexion.

For each reflex studied we repeated the following sequences of CB length changes (see figures): (i) a single stretch or a single release (sinusoidal function) to compare two steps of CB length; (ii) a single complete sinusoidal movement, starting with CB stretch or release, to further characterize the effects of direction of onset of the CB movement; (iii) four sinusoidal movements to observe the effect of a repeated stimulation.

Motor unit activity was recorded as electromyograms (EMGs) in the muscles, or in occasional fortuitous instances as impulses in the motor axon (e.g. the flexor response in Fig. 6). A bipolar needle electrode was inserted through a hole in the hard cuticle into the appropriate muscle, careful positioning being necessary to obtain good (differential) recordings. In most cases EMG recordings were made from two muscles simultaneously, in different combinations, though in some experiments three muscles were monitored simultaneously.

Each walking leg of the decapod Crustacea incorporates six joints (except in the Astacura which possess a seventh one between the basipodite and the ischiopodite). They move mainly in two perpendicular planes (Fig. 1): movement of the distal segment of the joint occurs primarily in an antero-posterior direction at the thoracico-coxal (T-C), ischio-meropodite (I-M) and carpo-propodite (C-P) joints, and in a dorso-ventral plane at the coxo-basal (C-B), mero-carpopodite (M-C) and propodactylopodite (P-D) joints. At the majority of joints the presence of two condyles limits the movement of the distal segment to one plane only. However, in the rock lobsters used in these experiments, the C-P joint is also able to rotate slightly (see Wales et al. 1970).

The different muscles of the leg were systematically investigated. We will first consider the muscles of the same joint as the CB chordotonal organ, next the proximal muscles controlling the thoracico-coxal joint, and then all the leg muscles distal to the CB joint.

(1) The coxo-basipodite (C-B) joint

This joint is controlled by the limb levator and depressor muscles, which lie predominantly within the coxa but whose proximal portions of the anterior levator and anterior depressor continue into the thorax (Fig. 1). The coxo-basal chordotonal organ, CB, runs from its distal insertion on the rim of the basipodite between the anterior and posterior levator insertions, to a special endophragmal peg inside the dorsal, proximal end of the coxa (Whitear, 1962). It is therefore stretched by limb depression (at the C-B joint), and shortens with levation.

All four coxal muscles in Palinurus respond to passive, imposed length changes of the CB receptor strand with classical ‘resistance reflexes’, similar to those previously described for the crabs, Carcinus (Bush, 1965) and Cardisoma guanhumi (Moffet, 1975). Thus both levator muscles respond reflexly to passive stretch of CB, while both depressors respond during CB release, i.e. shortening (Figs. 2, 3). That is, the functionally synergistic muscles are synchronously excited by CB strand stimulation, antagonistic muscles being modulated in opposition.

Fig. 2.

Electromyographic activity recorded in two different preparations of Palinuros, (A, B) from the two levators (posterior and anterior), and (C, D) from the two depressor muscles, during reflex activation by imposed length changes of the CB chordotonal organ strand. (A, C) Four sinusoidal CB length changes; (B, D) one CB stretch (B) and one release (D), CB length being maintained constant for the remainder of each record. In this and subsequent figures, stretching of CB is indicated by upward deflexion, releasing by downward deflexion of the lower traces.

Fig. 2.

Electromyographic activity recorded in two different preparations of Palinuros, (A, B) from the two levators (posterior and anterior), and (C, D) from the two depressor muscles, during reflex activation by imposed length changes of the CB chordotonal organ strand. (A, C) Four sinusoidal CB length changes; (B, D) one CB stretch (B) and one release (D), CB length being maintained constant for the remainder of each record. In this and subsequent figures, stretching of CB is indicated by upward deflexion, releasing by downward deflexion of the lower traces.

Fig. 3.

Electromyographic activity recorded from the anterior depressor, posterior levator, and promotor muscles during reflex activation by CB strand movement in Palinurus vulgaris. (A) Four sinusoidal CB strand movements ; (B) two single sinusoidal movements in opposite directions ; (C) one CB releasing followed by one stretching movement.

Fig. 3.

Electromyographic activity recorded from the anterior depressor, posterior levator, and promotor muscles during reflex activation by CB strand movement in Palinurus vulgaris. (A) Four sinusoidal CB strand movements ; (B) two single sinusoidal movements in opposite directions ; (C) one CB releasing followed by one stretching movement.

Levator muscles

The number of motoneurones supplying the two levators has been much discussed because of the role of these muscles in autotomy (Clarac, 1976). This number appears to vary with the species studied. Bush (1965) and McVean (1974) described three axons to the anterior levator of the shore crab. In a recent paper McVean & Findlay (1976) distinguish clearly in these crabs two parts in each levator muscle: ALM 1 and ALM 2 for the anterior levator, PPLM and RPLM for the posterior levator. They recorded at least two motoneurones in the rotator part (RPLM) and two in the PPLM, but one is common to both parts. In Cardisoma Moffett (1975) described nine units in the anterior levator and two in the posterior levator. In the rock lobster, the anatomical organization of the levator muscles does not seem as complex as in the brachyurans. By CB stimulation we have been able to distinguish only two excitatory units in each levator muscle.

An electrode in the posterior levator records a low-frequency tonic discharge, particularly with CB held stretched (Figs, 2, 3, 9). This resting motor discharge was strongly modulated by changes in CB length, being increased during stretching and decreased by release. The posterior levator EMG burst is sometimes at a higher frequency at the onset of the stretch movement (Figs. 2 A and B), while sometimes it reaches a maximum frequency in the middle of the stretch curve (Fig. 3). This leaves open the question of whether the reflex response frequency depends (primarily) upon the velocity of CB stretch (but cf. Bush, Vedel & Clarac, 1978). A fairly pronounced facilitation of the EMG response occurs, in close correspondence with the frequency of discharge (Figs. 2, 3). Most of the time only the tonic unit is recorded; however, if the animal displays a high level of activity, as indicated by a high discharge rate of the tonic unit, a second, phasic unit often also becomes active, and this too is modulated by mechanical stimulation of the CB strand.

The anterior levator shows a similar response, but usually at a lower and more variable frequency, sometimes with little or no resting discharge (cf. Figs. 2, 4). The anterior levator discharge is not always completely inhibited by releasing CB (Fig. 4), though it is always excited by CB stretch. Despite these small differences between the two levator muscles, it is evident that their reflex activation by CB is nearly identical.

Fig. 4.

Electromyographic activity of the remotor and anterior levator muscles during reflex activation by CB strand movement. (A) Four sinusoidal CB strand movements; (B) two opposite sinusoidal movements; (C) one CB stretch followed by a CB releasing when T-C is in a mid-position; (D) one CB stretch followed by a CB releasing with T-C completely promoted.

Fig. 4.

Electromyographic activity of the remotor and anterior levator muscles during reflex activation by CB strand movement. (A) Four sinusoidal CB strand movements; (B) two opposite sinusoidal movements; (C) one CB stretch followed by a CB releasing when T-C is in a mid-position; (D) one CB stretch followed by a CB releasing with T-C completely promoted.

Depressor muscles

Again both anterior and posterior depressor muscles respond qualitatively similarly to each other, but in opposite sense to the two levator muscles (Figs. 2C, D; 3 and 5). In contrast to the levators, both depressors showed two active units, that with the larger EMG spikes being more phasic. Occasional discharges in additional units were also sometimes seen. In each species studied (Jasus lalandii and Palinurus vulgaris) the depressor units recorded all responded strongly to CB shortening, and any tonic activity present was greater at the shorter lengths. The larger unit of both depressors commonly discharged at its highest frequency at the beginning of a release movement, though in Palinurus (Fig. 3) this was still at a much lower frequency than the smaller unit. Sometimes the response does not last the full duration of the movement, particularly after several repetitions (Fig. 3 A).

(2) The proximal, thoracico-coxal joint (T-C)

In Palinura (rock lobsters) the T-C joint is controlled by a single promotor muscle and two remotors, all situated within the thorax (Fig. 1). The exact number of moto-neurones innervating each of these muscles has not yet been clearly determined. There is also a single muscle receptor organ in this segment, the T-C MRO, lying in parallel with the promotor muscle (Alexandrowicz, 1967). Stretching this MRO in the shore crab, Carcinus, causes a reflex discharge in from 1 to 9 motor units of the promotor muscle (Bush & Roberts, 1968; Bush & Cannone, 1973; Bush, 1976, 1977). In the present work on rock lobsters, it has not been possible to identify as many motor units as this in the promotor muscle. Nevertheless several units in the promotor and remotor muscles are sensitive to CB stimulation.

Promotor muscle

Releasing CB evokes an increase in discharge frequency in at least one unit of the promotor muscle, while CB stretch completely or partially inhibits this discharge (Fig. 3). A clear modulation is evident when (four) successive sinusoidal CB length changes are applied (Fig. 3 A). The discharge frequency during releasing is somewhat variable, and depends markedly upon the direction of the first movement, i.e. whether this is a stretch or a release (Fig. 3 B). The tonic effect of CB length on this unit is also much less consistent than that on the motor units of the levator and depressor muscles. We have occasionally encountered other promotor units sensitive to CB movement (not illustrated), and in general their frequencies are also accelerated on releasing CB.

Remotor muscle

The number of motoneurones innervating this muscle is not well defined. Nevertheless one unit is clearly modulated by mechanical stimulation of the CB strand (Fig. 4), albeit much less prominently than that of the promotor muscle. Its discharge frequency is enhanced during both stretching and releasing CB. Sinusoidal movement evokes only a small modulation (Fig. 4A), and appears simply to cause a general activation of this unit. The influence of CB alone on this unit is in fact relatively slight, and seems also to depend strongly upon the position of the T-C joint. When the joint is completely promoted, for example, the remotor unit discharges at a high frequency, due to the T-C resistance reflex. CB then modulates the remotor activity more effectively, facilitating the unit when released and inhibiting it when stretched (Fig. 4D). Thus, as in the other segments of the limb, the intrasegmental resistance reflex and the intersegmental reflexes combine to provide a complex regulatory control mechanism.

(3) Joints distal to C-B

The ischio-meropodite joint (I-M)

Only a single muscle (with several muscular heads) controls this joint, the reductor muscle, which moves the meropodite posteriorly on the basi-ischium (Fig. 1). The effect of the CB receptor on this muscle is slight, and the resting length of CB does not appear to influence the reductor motor activity consistently. However, CB shortening usually causes some excitation of a small reductor motor unit, while any tonic discharge is transiently inhibited by stretching CB (Fig. 5). When, as often occurs in a lively preparation, the other legs move slowly and rhythmically from the thoracico-coxal joints in an antero-posterior direction, a large phasic reductor unit commonly discharges in the (stationary) leg under observation. The discharge of this unit, however, is not modified by CB movements.

Fig. 5.

Electromyograms from reductor and posterior depressor muscles during various CB strand movements (as indicated in lower traces).

Fig. 5.

Electromyograms from reductor and posterior depressor muscles during various CB strand movements (as indicated in lower traces).

The mero-carpopodite joint (M-C)

The meropodite is the longest segment in the leg, and contains the large main flexor and extensor muscles of the limb and in addition the small ‘accessory flexor muscle’ (Fig. 1). All three muscles show pronounced reflex responses to CB length changes, being much more clearly influenced by CB than any of the other limb muscles apart from the ‘intrasegmental’levators and depressors. CB stretch elicits phasic discharge in a single extensor unit (Fig. 6), while releasing CB excites both the flexor (Figs. 68) and the accessory flexor muscle. Stretching the receptor generally also inhibits the flexor units, while the extensor is inhibited by CB release. These reflexes are described in more detail in the following paper (Bush, Vedel & Clarac, 1978).

Fig. 6.

Simultaneous recordings of electromyograms from accessory flexor, extensor, and main flexor muscles, during one sinusoidal CB strand movement in opposite directions (A and B), and during a single CB stretch (C) and release (D). (Note that the single extensor unit was fortuitously recorded with the same electrode as the accessory flexor unit.)

Fig. 6.

Simultaneous recordings of electromyograms from accessory flexor, extensor, and main flexor muscles, during one sinusoidal CB strand movement in opposite directions (A and B), and during a single CB stretch (C) and release (D). (Note that the single extensor unit was fortuitously recorded with the same electrode as the accessory flexor unit.)

The carpo-propodite (C-P) and propo-dactylopodite (P-D) joints

The muscles of these two joints are much less strongly or consistently influenced by the CB chordotonal organ. Any reflex effects of CB on these muscles are dominated and often completely overridden by the much stronger reflexes from the chordotonal organs of their own joints, and to a lesser extent also by the M-C joint receptors. With these two distal joints well stabilized, however, the most commonly recorded reflex influences of CB upon their muscles are illustrated in Figs. 78.

Fig. 7.

Simultaneous electromyograms from flexor and bender muscles. (A) Four CB strand sinusoidal movements; (B) two single sinusoidal movements; (C) a single CB release.

Fig. 7.

Simultaneous electromyograms from flexor and bender muscles. (A) Four CB strand sinusoidal movements; (B) two single sinusoidal movements; (C) a single CB release.

The bender muscle (propodite productor) is innervated by two excitatory motoneurones, a ‘fast’ and a ‘slow’ unit (Wiersma & Ripley, 1952). The slow unit commonly discharges ionically. Other factors being constant, its tonic discharge frequency is somewhat greater when CB is stretched than when it is relatively relaxed (Fig. 7). Rapid CB length changes inhibit this bender unit, CB release being rather more effective in this than stretch. When the bender discharge is weak, it may sometimes be completely suppressed by a series of CB movements.

The shared stretcher-opener motoneurone is the only excitatory motor innervation of these two muscles (the propodite reductor and dactylopodite extensor, respectively), though each of them receives a separate peripheral inhibitory motoneurone (Wiersma & Ripley, 1952). Again the influence of CB on this excitor unit is small and variable. There is usually little effect on its tonic discharge frequency, though this may be slightly greater with CB stretched. Releasing CB, however, sometimes produces a small but definite excitation of the stretcher-opener unit, whereas stretching CB has an inhibitory influence (Fig. 8).

Fig. 8.

Electromyograms of opener (−stretcher) and M-C flexor during CB strand mechanical stimulation. (A) Four sinusoidal movements; (B) one sinusoidal movement; (C, D) a single releasing and a single stretch.

Fig. 8.

Electromyograms of opener (−stretcher) and M-C flexor during CB strand mechanical stimulation. (A) Four sinusoidal movements; (B) one sinusoidal movement; (C, D) a single releasing and a single stretch.

The closer muscle (dactylopodite flexor), like the bender, receives both a ‘fast’ and a ‘slow’ excitor. As with the bender, there is a tendency for any tonic discharge of the slow closer unit to be inhibited by CB length changes, in either direction, and also to be slightly greater when CB is held stretched than when it is relaxed (Fig. 9).

Fig. 9.

Simultaneous recording of electromyogram for posterior levator and closer muscles, during (A) one sinusoidal movement of CB ; and (B) a single CB release.

Fig. 9.

Simultaneous recording of electromyogram for posterior levator and closer muscles, during (A) one sinusoidal movement of CB ; and (B) a single CB release.

(4) Other legs

All the intersegmental reflexes described so far have been in muscles within the same leg as the CB organ stimulated. Several recordings from legs other than the stimulated one have not revealed any inter-leg reflex influences of CB. Thus, for example, CB movement in one leg does not appear to influence either the C-B levator and depressor muscles, or the M-C flexor and extensor muscles, of the contralateral leg, or of the next anterior or posterior legs. It may tentatively be concluded, therefore, that the reflex influences of the coxo-basal chordotonal organ are restricted to the muscles of its own leg.

The present study has shown that both the resting length (position) and change of length (movement) of the coxo-basal chordotonal organ can modulate the tonic motoneurone activity of all the muscles of the same limb. Fig. 10 and Table 1 summarize the reflex actions of CB established in this paper. This constitutes the first demonstration of multiple intersegmental reflexes mediated by an individual proprioceptor organ in Crustacean thoracic limbs.

Fig. 10.

Summary of typical electromyographic responses of all the muscles of a rock lobster walking leg during reflex activation by single sinusoidal movement of the CB strand (CB stretching indicated by upward, releasing by downward deflexion of monitor traces). Muscle and joint representation as in Fig. 1.

Fig. 10.

Summary of typical electromyographic responses of all the muscles of a rock lobster walking leg during reflex activation by single sinusoidal movement of the CB strand (CB stretching indicated by upward, releasing by downward deflexion of monitor traces). Muscle and joint representation as in Fig. 1.

(i) Technical constraints

The relatively simple experimental techniques employed in this investigation were adopted because they offered the possibility of simultaneously monitoring the activity of two or more muscles with minimal interference to the whole animal. More sophisticated procedures will be required to elucidate the underlying neural mechanisms, and to establish, for example, whether the CB organ makes direct, mono-or poly-synaptic connexions with the ‘intersegmental’ motoneurones, or only indirectly influences them via secondary reflex loops. Nevertheless, some attempt at interpreting the present results is warranted, provided certain technical limitations, noted below, are borne in mind.

(ii) ‘Silent’ motoneurones

Extracellular records of motoneurone activity obtained, as here, either indirectly from the muscles (EMGs) or directly from the motor nerve, clearly give no indication of any subthreshold influences upon non-discharging motoneurones. The absence of overt activity in a portion of the excitatory innervation of most of the limb muscles studied, therefore, cannot be taken to indicate a total lack of influence of the CB chordotonal organ upon these other, more phasic motoneurones. Some contribution of this sensory input to the excitability of these other motoneurones seems quite likely, at least in active, freely moving animals. However, intracellular recordings from the motoneurones within the ganglia will be necessary to establish this.

(b) Peripheral inhibition

The present experiments also provide no information about the activity of the peripheral inhibitory motoneurones known to innervate the distal limb muscles of decapod crustaceans (see Wiersma & Ripley, 1952). This is because it is very difficult to infer anything about their behaviour from extracellular EMG recordings (but cf. Bush, 1962 a). It is possible that some of the variation in excitatory junction potential (e.j.p.) amplitudes encountered in the present experiments was a consequence of partial suppression by peripheral inhibitor impulses (i.e. α-inhibition: Katz & Kuffler, 1946). However, in most of the present records, the e.j.p. amplitude variation is broadly explicable in terms of variation in degree of facilitation, due to the manifest fluctuation in discharge frequency. Nevertheless it remains quite possible, indeed probable, that peripheral inhibitor discharge frequencies are also modulated intersegmentally by CB movement (and by other chordotonal organs in the leg), as in the intrasegmental resistance reflexes (Bush, 1962b).

(c) CB movement compared with joint movement

The CB stimulation imposed by means of forceps is analogous to that elicited by C-B joint movement when the leg is levated or depressed. In our experiments the stimulation is limited to the CB organ; the other coxo-basal receptors, namely the levator and depressor receptors (Alexandrowicz, 1967), and the cuticular stress detectors, CSD 1 and CSD 2 (Clarac, Wales & Laverack, 1971), are not stimulated. This (and/or the species difference) could explain the difficulty in reconciling certain aspects of our results with those of Ayers & Davis (1977) in the astacuran lobster, Homarus americanus. They found, for example, a positive feedback influence of C-B joint movement on the levator and depressor muscles. In our experiments on the rock lobster, however, an inhibition of the motor output to the two depressor muscles occurs when CB is stretched, and conversely of the levator activity when CB is released. In some atypical records we observed that the tonic unit of the anterior levator is not inhibited during CB release, though on the other hand no facilitation of the discharge was evident either. In Ayers & Davis’ preparation, the combined effect of all the C-B receptors could evoke such a response. Accordingly, the functional summary presented here (Fig. 10) is not as complex as the relationships described by these other authors would indicate. This difference might, therefore, be explained by our much more specific proprioceptor stimulation.

(d) Secondary reflex effects

There exists the further possibility that additional reflex loops may be influencing the motor responses recorded here. In the experimental arrangement employed, the leg was clamped in a more or less natural position, with the meropodite roughly horizontal and the distal segments either fixed or, in some cases, free to move to some extent. Consequently the motor facilitation or inhibition elicited by CB might, for example, produce isometric tension changes in some muscles or, as was sometimes observed, overt movement of the unrestrained M-C (and occasionally more distal) joints. Such reflex movements could clearly cause secondary resistance reflexes in these muscles, though these would probably tend, if anything, to reduce the direct reflex effect of CB.

However, careful comparison of the various intersegmental reflex responses to CB length changes when the M-C joint moved with those when no overt movement occurred, shows no significant difference. Furthermore, in several control experiments, the tendon of the accessory flexor muscle was cut, thereby eliminating the possibility of any secondary reflex loop by this route. Again, the intersegmental reflexes resulting from CB movement were identical with those obtained when the accessory flexor was intact. It can therefore be concluded that, in the present experiments, secondary reflex effects via the accessory flexor and associated myochordotonal receptors did not influence the intersegmental reflexes evoked by CB length changes.

(e) Possible influence of other receptors

Whether the apodeme tension receptors (Macmillan & Dando, 1972) or the cuticular stress detectors (Clarac, 1976) could also have secondary reflex effects in these conditions is as yet unknown. Intersegmental reflex influences from chordotonal organs are certainly known to impinge upon the thoracico-coxal muscle receptor (Moody, 1970) and the myochordotonal organ (Bush & Clarac, 1975; Bush, Vedel & Clarac, 1978), so that these two proprioceptors might also contribute secondary reflex effects. Probably any such actions would be relatively slight, since the observed intersegmental modulations of motor discharge evoked by CB were on the whole relatively ‘weak’ (see below), compared to the intrasegmental reflexes. The possibility cannot, however, be excluded, and further experiments are needed to clarify this issue, including, if possible, denervation of the musculature with recording directly from the motoneurones, or even complete de-afferentation of the limb. Unfortunately such operations are not only technically very difficult, particularly the latter, but would probably also be so traumatic as to substantially reduce reflex responsiveness.

(f) EMG recordings and reflex strengths

Comparison of the relative strengths of reflexes cannot readily be made purely on the basis of electromyograms, since the forces involved depend upon the type of motor unit activated and the mechanical properties of the joints, as well as upon the discharge frequencies of the active units. Ideally the muscular forces exerted and their mechanical effects upon the joints should be measured, but such complex procedures would undoubtedly seriously impair reflex responsiveness and viability. Moreover, comparison of the absolute forces exerted by different muscles of radically different size, shape and power would be of limited value, as these forces could not alone define relative strengths of the reflex actions of one receptor organ on the different muscles and joints. A more meaningful comparison is between the reflex actions of different proprioceptors upon the same muscle - or between the intrasegmental resistance reflex and other, intersegmental reflex responses of the same muscle (or motoneurones). And since in any one muscle the same one, or two, tonic motor units were generally the only ones to respond in these reflexes, it seems reasonable to argue that their discharge frequencies do indeed reflect, at least qualitatively, the relative intensities, or ‘strengths’, of the different reflex influences impinging upon that muscle. This assumption is implicit in the ensuing discussion.

(2) CB receptor influences

(a) Proximo-distal CB control

A priori, it seems likely that CB should affect the muscles of its own joint more strongly and consistently than those of the other joints of the leg. The present results are not incompatible with this prediction, although, recognizing the reservations noted above, they cannot be taken as conclusive evidence for it. Further, CB influence appears in general to be greater on the next distal joint than on the proximal one: that is, T-C is evidently less ‘strongly’ affected than M-C. Moreover, joints moving in the same plane as C-B are on the whole more affected by CB stimulation than joints moving in a perpendicular plane: M-C and (to a lesser extent) P-D muscle activity is more modified by CB length and movement than T-C, I-M and C-P. Thus the predominant intersegmental influence of CB would appear to be upon the M-C muscles. Furthermore, CB evidently has an antagonistic action on flexor and extensor muscles, since quite often in these experiments a change in CB length elicited a clearly observable movement of the M-C joint. In contrast, the reflex effect of CB on the T-C or C-P joints is not altogether an antagonistic one: the remotor and promotor muscles are both facilitated on releasing CB. The bender and stretcher muscles seem to be affected rather more tonically, by CB length, than by its movement: their discharge is in both cases slightly greater when CB is stretched than when it is in the released condition.

(b) Postural action of CB

As a rule CB affects predominantly the tonic units of the various muscles. It has an influence on the phasic units, e.g. those of the coxal muscles, only when these are at the same time involved in a resistance reflex within their own segment. This would suggest that these intersegmental reflex influences of CB on the other joints of a leg may be of particular importance in postural control. It is therefore important to distinguish between the static and dynamic components of these presumed regulatory reflexes. In the static condition CB is evidently able to regulate the position of all the joints of a leg. This is not surprising if we consider the location of this chordotonal organ in the whole limb. It is clearly necessary to have a general adjustment of all the leg segments in relation to any given position of the C-B joint. A very small modification of the C-B angle evokes postural modification of all the more distal joints. A strong static reflex connexion between C-B and M-C would therefore seem eminently appropriate to help maintain a correct posture. The basipodite depressor and mero-podite flexor are both anti-gravity muscles, supporting the leg’s share of the weight of the animal. Accordingly they are both influenced in the same (i.e. synergistic) way by CB position: that is, both these muscles are more excited by CB release (which occurs with limb levation) and inhibited, centrally at the motoneurones, by CB stretch. These static, intersegmental reflexes can therefore be considered as an extension of the intrasegmental resistance reflexes, serving in part to maintain an efficient load distribution between segments, and hence a stable overall posture of the leg.

(c) CB activity and walking

The dynamic reflexes observed may be useful during locomotion. When the animal is walking sideways, the trailing leg alternately levates and flexes together, then depresses and extends (Clarac & Ayers, 1977). In this case, the intersegmental reflex seems efficient (in contrast to the intrasegmental one): CB shortening (which occurs during levation) reflexly increases the flexor muscle discharge, and CB stretching (which occurs during a depression movement) increases the extensor muscle discharge. Thus the centrally determined linkage of the motor commands during both the power stroke (depression-extension) and the return stroke (elevation-flexion) in the trailing leg is reinforced by the intersegmental reflexes originating in the coxo-basal chordotonal organ. For a leading leg, however, levation is synchronous with M-C extension, and depression with flexion. In this case, the inter-and intrasegmental reflexes elicited by CB act together, and may possibly strengthen the coupling between sequential bursts. For example, when the leg is completely elevated there is facilitation of both the depressor and the flexor muscles by CB, and this could help to initiate the onset of the powerstroke at the end of a return stroke.

(3) Proprioceptive reflexes and motor patterns

The role of proprioceptive reflexes in motor behaviour has been discussed several times (e.g. Barnes et al. 1972; Barnes, 1977; Vedel & Clarac, 1975; Clarac, 1977; Ayers & Davis, 1977). It appears that during a centrally driven movement, the whole reflex organization is arranged to facilitate it, the opposing neuronal activity being repressed. If we pursue this hypothesis, the CB reflex interactions in trailing legs during lateral walking appear more important than those elicited in the leading legs, except for its possible role in the latter at the end of the return stroke, suggested above. On the other hand, CB action during backward and forward walking appears less useful - or at any rate not so readily interpreted in functional terms.

A similar intersegmental reflex, initiated by the receptors of the M-C joint and controlling the C-B joint, has been described in crabs (Clarac & Coulmance, 1971). Imposed M-C extension increases the rhythmic variation in discharge of the levator muscle of a trailing leg, while at the same time extension inhibits the levator motor discharge of a leading leg. This reinforces the very close functional connexion of these two joints, C-B and M-C, seen in the present study, and also emphasizes the complexity of the regulatory influence of this class of proprioceptive feedback upon central motor patterning.

Finally, it must be emphasized that during walking, or any other motor behaviour involving limb movements or postural adjustments, proprioceptors of all the various types known in crustacean appendages are presumably activated together. These include not only the ‘pure’ chordotonal organs like CB, but also the myochordotonal organ and T-C muscle receptor, the apodeme tension receptors, and the cuticular stress detectors (see Barnes, 1975; Clarac, 1977). Further, each of these sense organs evokes its own characteristic type of reflex, whether from passive or active movements or force changes. Considering all the reflex interactions demonstrated here or inferred from previous work, therefore, a highly complex picture of both tonic and dynamic, intra- and intersegmental reflex regulation of positions and movements of the segments of a limb emerges. These reflex, regulatory controls can be modulated or, in appropriate circumstances dominated or totally overridden, by central ‘commands’ or extrinsic stimuli.

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