Muscle receptor organs of the crayfish,Cherax destructor: Organisation of central projections of stretch receptor neurons

THE JOURNAL OF EXPERIMENTAL ZOOLOGY 279:243–253 (1997)

© 1997 WILEY-LISS, INC.

JEZ 842

Muscle Receptor Organs of the Crayfish, Cheraxdestructor: Organisation of Central Projections ofStretch Receptor Neurons

DAVID L. MACMILLAN* AND PAUL J. VESCOVIDepartment of Zoology, University of Melbourne, Parkville Vic. 3052,Australia

ABSTRACT The stretch receptor neurons of the abdominal muscle receptor organs of crayfishenter the ventral nerve cord and branch to send axons to the brain and to the last abdominalganglion. They mediate local reflexes in the ganglion of entry and adjacent ganglia but evidencefrom previous cobalt filling and histology suggested that local branching is limited and variableand does not accord closely with physiological evidence. We examined the fine structure of thebranching in a large number of preparations from large animals of the crayfish Cherax destructor,which is also a large species, to determine whether the increased resolution afford by size wouldpermit us to detect previously undetected patterns. We found some predictable features in thepattern of fine branching in the ganglion of entry and adjacent ganglia that could explain some ofthe apparent anomalies. We also examined the relative positions of the hook-shaped projectionsfrom different segments where they terminate in the last abdominal ganglion by differentiallystaining the stretch receptors with Co++ and Ni++. We found evidence for somatotopic organisationin the longitudinal position of the endings. J. Exp. Zool. 279:243–253, 1997. © 1997 Wiley-Liss, Inc.

*Correspondence to: Dr. D.L. Macmillan, Department of Zoology,University of Melbourne, Parkville, Vic. 3052, Australia. E-mail:[email protected]

Received 15 November 1996; revision accepted 10 June 1997.

Allen (1864) first described some simple sensorycells which were later named muscle receptor or-gans (MROs) by Alexandrowicz (’51) in his studieson the abdomen of the lobsters Homarus vulgarisand Palinurus vulgaris. Since Alexandrowicz’s de-scription there have been numerous studies car-ried out on the microanatomy, neurophysiology,and neuropharmacology of the MRO. MROs havesince been identified in more than ten species ofdecapod crustacean (Pilgrim, ’60; Fields, ’76). EachMRO consists of a stretch receptor neuron (SR)with its dendrites embedded in a thin musclebundle in parallel with the dorsal extensor mus-culature. They are found in pairs on either sideof the midline in each abdominal segment. TheMROs that make up a pair have distinct anatomi-cal and physiological characteristics and respondto different features of abdominal movement. Themedial organ has a SR with a broad dendritic areaand responds tonically to maintained stretch(MRO1 and SR1). The lateral receptor organ hasa shorter, thinner muscle and its conically-shapedSR responds phasically to maintained stretch(MRO2 and SR2).

There is a considerable amount of evidence fromextracellular studies that the SRs are involvedin a number of local reflexes (Eckert, ’61; Fieldsand Kennedy, ’65; Fields, ’66; Fields et al., ’67;

Sokolove, ’73; Nja and Walloe, ’75) involving theganglion of entry and adjacent ganglia. These ap-pear to be present in the range of crayfish speciesstudied (for review see Fields, ’76) and some ofthem have been confirmed and further investi-gated with intracellular techniques (Hausknecht,’96, and in preparation). One might have pre-dicted, therefore, that there would be clear andconsistent patterns in the branching and projec-tions of the SRs in these ganglia. Histological stud-ies of the abdominal ganglia of Procambarusclarkii failed to find substantial branches (Lieseet al., ’87; Skinner, ’85a,b) or stereotyped projec-tion patterns. Bastiani and Mulloney (’88a) alsoexamined this aspect of the SRs in their study ofthe morphology of the projections anteriorly andposteriorly in the cord. They stained the SRs bycobalt infusion into the cut peripheral ends of theaxons and noted a number of small branches inthe ganglion of entry and in other ganglia throughwhich the axons passed but could find no consis-tency in the position or shape of those branches.While this result was suggestive, it was not con-

244 D.L. MACMILLAN AND P.J. VESCOVI

clusive because this aspect of the work was sub-ordinate to the main aim of the project which wasto visualise the terminations. To achieve this theyused small animals (2–3 cm) which meant thatdetails of the fine branching in the ganglia in be-tween were difficult to determine and may not rep-resent the mature condition. One of the objectivesof the experiments described here was to use largeanimals and target the local ganglia specificallyso that all details of even the finest brancheswould be apparent following intensification of thecobalt filled preparations. The SRs from eachMRO pair enter the ventral nerve cord in the sec-ond root of the next anterior segmental ganglion.Bastiani and Mulloney (’88a) demonstrated thatAlexandrowicz’s (’51) conjecture about the possiblefate of the SR axons was correct. Upon enteringthe ganglion, the sensory axons bifurcate and runin opposite directions. They demonstrated furtherthat one branch travels all the way to the brainand the other to the last abdominal ganglion, A6.A6 is the major integrating centre for the motorsystem controlling the various appendages thatcomprise the tailfan (Dumont and Wine, ’87a,b).The sensory axons of the SRs travel the entirelength of the body, passing through every ganglionand running together in a single bundle in thedorsal medial tract (DMT) (Wiersma and Hughes,’61). The sensory axons from all the abdominalmuscle receptors terminate in the same dorsalarea of A6 with a characteristic, hooked structurethat is symmetrically disposed across the midline.The hook is formed near the posterior end of theinterconnective fissure where the axons turn me-dially across the midline in commissures A6 DCIIor A7 DCII (terminology from Kondoh and Hisada,’86) and, after crossing the midline, run anteriorlyto the end of the core of A6.

This labelled-line input and extensive branch-ing in A6 suggests that MRO input plays someimportant role in the tailfan control. The tailfanis a highly specialised terminal structure in thecrayfish, formed by a fusion of the telson and thepaired appendages of the sixth abdominal seg-ment, the uropods. Many of the neurons in theterminal ganglion and muscles of the tailfan havebeen characterised morphologically and physiologi-cally and some of their functional relationships havebeen determined (Larimer and Kennedy, ’69; Wineand Krasne, ’82; Hisada et al., ’84a,b; Wine, ’84;Dumont and Wine, ’87a,b; Kondoh and Hisada,’87; Takahata and Hisada, ’85; Vescovi et al., ’97).

Bastiani and Mulloney (’88a) recorded intracel-lularly from a number of neurons of different

classes in A6 that were postsynaptic to SR axonsin P. clarkii. They found local interneurons, plu-risegmental interneurons and motor neurons thatresponded to SR activation. Vescovi et al. (’97)identified some of those neurons in Cherax de-structor. Bastiani and Mulloney (’88b) also foundthat SR input from posterior abdominal segmentswas more likely to cause larger EPSPs in uniden-tified terminal ganglion neurons than input fromanterior segments of P. clarkii and demonstratedevidence of an anterior-posterior gradient in thestrength of the response. Vescovi et al. (’97) foundthat similar gradients occur in C. destructor, butnot in any of the neurons they identified. Studiesin insects have demonstrated some highly orderedprojections from mechanosensory afferents, withsomatotopic relationships between the location ofthe sensory structure and the projection in thecentral nervous system (Teugels and Ghysen, ’83;Johnson and Murphey, ’85; Kent and Levine, ’88;Murphey et al., ’89). We hypothesized that thephysiological gradients in some postsynaptic cellsin both P. clarkii and C. destructor could be re-lated to some kind of somatotopic order of the SRendings in A6, perhaps echoing the topologicalorganisation of hair projections from different tail-fan nerves into the last abdominal ganglion de-scribed by Kondoh and Hisada (’87). The searchfor evidence for such organisation was a secondobjective of this study.

MATERIALS AND METHODSAustralian freshwater crayfish, Cherax destruc-

tor, from the Murray River system were obtainedfrom a commercial supplier and kept indoors at22°C in polystyrene aquaria. They remained ac-tive and in good condition for long periods whenprovided with shelters, normal light-dark cyclesand a change of water following a weekly feedingwith dry-pellet cat food. Seventy five inter-moultspecimens of both sexes were used in the experi-ments. Specimens with a carapace length of 6–10cm were used. Animals were anaesthetised by im-mersion in ice for ten minutes and the brain de-stroyed. Specimens were immobilised and dissectedto expose the nerves to be stained.

Details of SR morphology were visualised by in-fusing CoCl2 intracellularly through the cut endsof the appropriate axons for periods of up to 24hours. Some of the infusions were done in wholepreparations, others were done in vivo by dissect-ing nerves and ganglia free and pinning the prepa-rations in a Sylgard-lined (Dow-Corning, Midland,MI) dish flooded with physiological saline (modi-

CRAYFISH ABDOMINAL STRETCH RECEPTOR PROJECTIONS 245

fied van Harreveld’s (’36) solution: 11.68 g/l NaCl;0.40 g/l KCl; 0.55 g/l MgCl2.6H2O; 1.51 g/l Trisma;made up in distilled H2O, pH = 7.4; developed byPasztor and Macmillan, ’90). In most cases, 1.5%CoCl2 was used but a range of concentrations upto 5% CoCl2 solution was used to reduce the prob-ability of missing details of fine axonal and den-dritic branches because of factors associated withionic concentration and penetration. The time andtemperature were varied to achieve a balance thatbest suited the part of the neuronal morphologyunder examination. Once determined, a particu-lar regime was used over and over to examine anyarea in detail because typically a regime designedfor one purpose was unsuitable for others e.g., aregime to show the detail of the endings in A6produces an overstained preparation in the gan-glion of entry. A typical filling regime would be10–12 hours at 4°C. The cobalt ions were precipi-tated with 0.1% ammonium sulphide (four dropsper 10 ml) and left for 10 minutes. The tissue wasthen washed in several changes of saline over aperiod of 30 minutes and fixed in Bouins for 2hours. The preparation was dehydrated andcleared and mounted in methyl salicylate. Somepreparations were also silver intensified using theTimm’s method (Bacon and Altman, ’77; Altmanand Tyrer, ’80; Altman, ’81) before being clearedand mounted. The mounted preparations weredrawn using a drawing tube attached to a Zeisscompound microscope (Thornwood, NY). To im-prove our ability to differentiate between SRs fromdifferent segments, in some experiments we usedNiCl2 to fill the SR from one segment and CoCl2to fill from the other. The infused ions were thenprecipitated with Rubeanic Acid to obtain fills withcolour differentiation (Altman, ’81; Jones andPage, ’83). These preparations were always drawnbefore and after intensification because the colourdifference disappears following the silver intensi-fication process.

RESULTSThe general morphology of the abdominal MROs

in C. destructor is essentially the same as thatdescribed in other species (Alexandrowicz, ’51;Macmillan and Field, ’94; Pilgrim, ’60, ’64). Uponentering the abdominal ganglion the SRs bifur-cate and send a branch to the head and a branchto A6 as in P. clarkii (Bastiani and Mulloney, ’88a).In all cases (n = 72), the tonic and phasic SR filledsimultaneously and there were no obvious differ-ences in the point of bifurcation, although the pha-sic SR usually has a slightly larger diameter than

the tonic SR. To determine whether there was anas yet undisclosed pattern to the fine branchingin the ganglion of entry we conducted a numberof fills (n = 24) of the second nerve of the third ab-dominal ganglion (A3) in large animals. As in P.clarkii (Bastiani and Mulloney, ’88a), no branchesare found in consistent positions in C. destructorand all branches are short and fine. Because ofthe larger size of our preparations, we are able toprovide further details of the branching. In C. de-structor, the point of bifurcation of the two axonsis invariably very close and there are numerousfine branches from both axons (Fig. 1). Thebranches are all short and run perpendicular tothe main axon with very little branching and arefound along the axons throughout the whole cen-tral region of the ganglion from the point of entryof the first nerve to slightly posterior to the entryof the second nerve.

We also used large animals (n = 24) to examinethe branching patterns of the SRs in the adjacentanterior (A2) and posterior (A4) ganglia. There arealways some branches in both the anterior andposterior ganglion but they occur over a shorterlength of the axons in the central region of theganglia. It should be noted in respect of this lastobservation, however, that in C. destructor the dis-tance between exit points of the first and secondnerves is commonly greater in A3 than in A2 orA4. In the anterior ganglion the branches aresimilar to those in the ganglion of entry butthere are far fewer of them. In the posteriorganglion there are also fewer branches but theycommonly give rise to long transverse second-ary branches running parallel and in close lat-eral proximity to the main axon (Fig. 2B). Inmany of the experiments designed to reveal SRbranching in the posterior ganglion we alsofilled an accessory neuron (Fig. 2B) (Alexand-rowicz, ’51, ’67; Wine and Hagiwara, ’77).

The projections of the SRs into the last ab-dominal segment (A6) in C. destructor (Mac-millan and Field, ’94) are closely similar inposition and form to those described in P. clarkii(Bastiani and Mulloney, ’88a). The hook-shapedendings of the phasic and tonic units from thesame segment are almost identical and in somepreparations are intertwined (Fig. 3A). We filledpairs of SRs entering in different nerves of seg-ments A3, A4, and A5 simultaneously to studythe spatial relationship between them in A6 (n= 48). Simultaneous SR fills from both sides ofsegments A3, A4, and A5 showed that the lon-gitudinal position of the hooked part of the pro-


jection in A6 is always the same so that the pairsfrom the same segments are bilaterally symmetri-cal in this regard (Fig. 3B). Most of the second-ary branching also matches closely although thefinest branches show differences. In some prepa-rations in which we filled the second nerves ofA5, we stained a neuron with a contralateral cellbody in A6 (Fig. 3C).

To investigate the relationship between the A6projections of the SRs from different segments wefilled SRs from different segments simultaneouslywith Co++ and Ni++. Although we were technicallyable to fill more than two segments simulta-neously, we found that we could not interpret thebranching patterns in A6 unambiguously becauseof the tangle of projections. We also concentrated

Fig. 1. Two examples of branching pattern of the SR ax-ons in the ganglion of entry. Cobalt backfill of SRs into ab-dominal ganglion A3. The axons pass medially into theganglion and then bifurcate to send a branch anteriorly tothe brain and also posteriorly to the last abdominal ganglion,

A6. The phasic and tonic axons branch at the same point.Both axons give rise to many short fine branches in the re-gion between the first and second nerves but no single branchis consistent in position or shape.


on contralateral pairs because we found the prepa-rations were easier to interpret than ipsilateralones and on segments A3, A4, and A5 because tofill from A1 or A2 it was necessary to use suchsmall animals that the relationship in A6 couldnot be determined with any reliability. The resultsreported here are based on 23 successful fills ofcombinations of SRs from segments 3 and 4, 4

and 5, and 3 and 5. In all cases examined thelongitudinal position of the transverse part of theSR hook in A6 reflected the antero-posterior or-der of the segments of SR origin. The transversebranches from adjacent segments are 5–10 µ apartlongitudinally (Figs. 4, 5A) and simultaneous fillsof A3 and A5 express a multiple of this spatialorder (Fig. 5B).

Fig. 2. Examples of branching patterns of the SR axonsin the adjacent ganglia. A: Branching pattern in A4 of cobaltfilled SRs entering second nerve of A3. There are typicallyfewer branches but some of these give rise to long transverse

secondary branches that lie parallel and close to the mainaxons. B: In some preparations we filled accessory neuronsas well as SRs. Branching pattern and accessory neuron inA4 stained in a fill of the ipsilateral second nerve of A3.


Fig. 3. Projections of filled SR axons in the last abdomi-nal ganglion (A6). A: Example of the hook-shaped endings ofthe phasic and tonic units that enter the ipsilateral secondnerve of A5. Note the closely similar branching pattern inthe phasic and tonic SRs. B: Example of a simultaneous fill

of both pairs of SRs from A5. The transverse branch thatforms the hook is always at the same longitudinal position incontralateral pairs. In some preparations we stained a neu-ron with a cell body in A6 when we filled the second nervesof A5.


DISCUSSIONEarly extracellular recordings from abdominal

extensor motor neurons indicated, and later in-tracellular studies confirmed, that the SRs excite

the motor neurons in the ganglion of entry morestrongly than they excite those in other ganglia(Eckert, ’61; Wine. ’77; Wine and Hagiwara, ’77;Hausknecht, ’96 and in preparation). The detailed

Fig. 4. Two examples of pairs of filled SR axons from contralateral sides of the adjacentsegments A4 and A5.


Fig. 5. Examples of pairs of filled SR axons from contralateral sides of the (A) the adja-cent A3 and A4 segments and (B) the A3 and A5 segments which are two segments apart.


information provided to us by Hausknecht (’96)from her thesis about the morphology of the ex-tensor motor neurons in C. destructor, shows thatmost of them, including number 2 (for numberingdetails see Kennedy and Takeda, ’65; Fields, ’66;Sokolove and Tatton, ’75), which responds reflexly,have long side branches running parallel to theSR axon through the ganglionic regions close tothe SR axons where the SR short branches lie(Liese et al., ’87). These branches are thus essen-tially perpendicular to the short SR branches andthere is a considerable longitudinal overlap whereconnections between them or their associated neu-rons could occur. It may be this aspect of the re-lationship that explains why neurons that havebeen shown to have a close functional relation-ship (some are probably monosynaptic) do nothave a stereotyped morphological one. It is pos-sible that the precise contact points of the SRs ortheir associated neurons on the dendritic tree ofthe motor neurons are not important so long asthere are sufficient at the right distance from theintegrating sites. The difference in the number offine branches found in this study of C. destructorin comparison with the study on P. clarkii (Bas-tiani and Mulloney, ’88a) could reflect species dif-ference or perhaps a difference in the maturity ofthe animals used.

Given the physiological background to the SRmotor neuron relationship, our finding that thereare always more fine SR branches in the ganglionof entry would not be surprising except that a de-tailed histological study by Liese et al. (’87) foundthat the total length of axonal branches from SRaxons was always greatest in the adjacent poste-rior ganglion. While this could be a species differ-ence between Pacifastacus leniusculus, which theyused, and C. destructor, which we used, some ofthe other possible explanations could prove moreinteresting. There are typically long secondaryparallel branches in the posterior ganglion of C.destructor and in any measurement of the totallength of SR branches these might well compen-sate for any effect that a greater number of shortbranches in the ganglion of entry might have.

From morphological analyses in other species(Liese et al., ’87) and intracellular dye fills ofsingle neurons in C. destructor (Hausknecht, ’96and in preparation) we conclude that the acces-sory neuron that we filled was Accessory 1 (Acc-1). We found, like Liese et al. (’87) in their studyof the Acc-1 projections, that the dendritic tree inthe ganglion with the soma is not extensive. InC. destructor, however, as in the case of the ex-

tensor motor neurons, there are again long sec-ondary branches from the main neurite that runparallel to the long axis of the cord in regionswhere the short and long parallel SR branches arefound. In C. destructor the dendritic tree is moreextensive in the ganglion of entry and there areeven more parallel branches (Hausknecht, ’96 andin preparation) which might be expected given thestrong intra and interganglionic reflex connectionsbetween the SRs and the accessory neurons.

In a number of preparations in which we filledthe second nerve of A5 we stained a neuron witha soma in A6 (n = 16). The morphology of the neu-ron is consistent with its being an accessory and,based on Hausknecht’s (’96 and in preparation)individual staining of all four accessory neuronsin more anterior ganglia of C. destructor, it re-sembles Acc-2 most closely. The result was com-pletely unexpected because no accessory neuronshave been found associated with the A5 nerves inother species in spite of specific searching. Larimerand Kennedy (’69b) could not detect physiologicalevidence for their presence when they looked foran MRO-accessory reflex associated with the SRentering A5 in P. clarkii. Wine and Hagiwara (’77)confirmed that conclusion when they filled the sec-ond nerve of A5 stating that “Larimer and Kennedyconcluded that the accessory efferent neuron ismissing in the terminal segment; our anatomicalevidence is consistent with that conclusion.” It ispossible that we have described a species differ-ence, it is also possible that it is a very difficultneuron to fill from A5 in P. clarkii. It did not fillin some C. destructor preparations, even ones inwhich the SRs projections filled well in the sametime over the same distance. The assumption isthat if this is indeed an accessory neuron, it is anaccessory from the ganglion posterior to A5. Butbecause A6 is a fused ganglion (Dumont and Wine,’87a), the simplest supposition would be that itwas originally associated with the anterior pri-mordial ganglion. If this is so, it is surprising thatthe soma of the neuron lies so posteriorly in A6,almost certainly in the domain of the second pri-mordial ganglion. Dumont and Wine (’87a,b; P.clarkii) and Vescovi and Macmillan (this volume;C. destructor) both found that the relative posi-tion of the motor neurons associated with the twoprimordial ganglia are generally maintained. Thisanomaly warrants further investigation for whatit may reveal about the evolution of both A6 andthe MRO-accessory complex.

Somatotopic organisation of mechanosensoryprojections has been described in a number of situ-


ations in insects (e.g., Murphey et al., ’80, ’89;Johnson and Murphey, ’85). Kondoh and Hisada(’87) also showed that the projections of the dif-ferent nerves associated with the last abdominalganglion in P. clarkii are topologically organisedbut such organisation remains to be documentedat the single cell level in crustaceans. Liese et al.(’87) looked for evidence for its presence in theirdetailed study of sensory projections in crayfishabdominal ganglia but found none. Our data sug-gest that the segment of origin of each SR maydetermine where its terminal ending is positionedin A6. The strength of that case is dependent ona number of considerations. First, we were lim-ited by technical considerations to pairs of neu-rons, so the argument is based on the finding thatin no case was the projection of an SR from themore anterior segment ever found posterior to itsfilled pair. Second, our assumption of longitudi-nal position is based on the position of the trans-verse part of the hook and there is no a priorireason for arguing that this is representative ofthe functional position of the neuron. We analy-sed other structural features such as prominentbranches, the length between branches, and thenumber of secondary branches to see if we coulddetect any other markers for longitudinal positionbut the variation in the level of secondary branch-ing (also remarked by Bastiani and Mulloney, ’88a)obscured any order that might be present. Third,we found analysing bilateral pairs improved ourability to compare the neurons but this means thatany interpretation of the relative longitudinal po-sition of two filled neurons from different seg-ments will depend to an extent on the relationshipbetween bilateral homologues as well. We are rea-sonably confident that this issue does not put theconclusion about the order at risk because all bi-lateral homologues that we filled crossed the mid-line at the same point and where we did fillipsilateral pairs of cells from different segments,the outcome was the same as that predicted bythe rest of our results. Fourth, to see the rela-tionship of the neurons in A6 clearly we were lim-ited to large animals and because of this were onlyable to fill reliably from A3 back so we cannot besure that the apparent order we found applies tothe rest of the abdominal segments. Even withthese caveats, the evidence appears to point tosomatotopic organisation, but even if only threeof the ganglia are involved, the result remains in-teresting, particularly in light of the physiologi-cal evidence of gradients in the strength of SR

synapses in A6 (Bastiani and Mulloney, ’88b; Ves-covi et al., ’97).

ACKNOWLEDGMENTSSupported by a grant from the Australian Re-

search Council to D.L.M. P.J.V. was the holder ofan Australian Post-Graduate Research Award.

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Documents

Muscle receptor organs of the crayfish,Cherax destructor: Organisation of central projections of stretch receptor neurons