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The activity of abdominal stretch receptors during non-giant swimming in the crayfish Cherax destructor and their role in hydrodynamic efficiency

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Abstract

Recordings were made from the nerve innervating the stretch receptors of the abdominal muscle receptor organs and slow extensor muscles of tethered crayfish, Cherax destructor, during so-called “non-giant swimming”. The stretch receptors were active during the flexor phase of swimming but the duration and pattern of activity varied from cycle to cycle. Their pattern of firing was modified by the activity of the large accessory neurons which make direct inhibitory synapses upon them. Neither the stretch receptors nor the accessory neurons were active during the extensor phase of the cycle. The timing and extent of tailfan movements during the period of stretch receptor activity were measured from video records before and after the stretch receptor nerves were cut in the second to fifth segments. The promotion of the tailfan during flexion was significantly delayed and the minimum angle to which the uropods were remoted at the end of flexion significantly larger in denervated animals. We propose that afferent information from the stretch receptors coordinates the timing and extent of tailfan movements according to variations in the positioning and movement of the abdominal segments such that the hydrodynamic efficiency of the tailfan is enhanced on a cycle by cycle basis during non-giant swimming.

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Abbreviations

A#:

abdominal segment number

Acc:

accessory neuron

LUU:

large unidentified unit

MRO:

muscle receptor organ

NGS:

non-giant swimming

SEMN:

slow extensor motor neuron

SR:

stretch receptor neuron

References

  • Alexandrowicz JS (1951) Muscle receptor organs in the abdomen of Homarus vulgaris and Palinurus vulgaris. Q J Microsc Sci 92:163–200

    Google Scholar 

  • Bastiani MJ, Mulloney B (1988a) The central projections of the stretch receptor neurons of the crayfish: structure, variation, and postembryonic growth. J Neurosci 8:1254–1263

    PubMed  Google Scholar 

  • Bastiani MJ, Mulloney B (1988b) The central projections of the stretch receptor neurons of crayfish: segmental gradients of synaptic probability and strength. J Neurosci 8:1264–1272

    PubMed  Google Scholar 

  • Cooke IRC, Macmillan DL (1985) Further studies of crayfish escape behaviour. I. The role of the appendages and the stereotyped nature of non-giant escape swimming. J Exp Biol 118:351–365

    Google Scholar 

  • Drummond JM, Macmillan DL (1998a) The abdominal motor system of the crayfish, Cherax destructor. I. Morphology and physiology of the superficial extensor motor neurons. J Comp Physiol A 183:583–601

    Article  Google Scholar 

  • Drummond JM, Macmillan DL (1998b) The abdominal motor system of the crayfish, Cherax destructor. II. Morphology and physiology of the deep extensor motor neurons. J Comp Physiol A 183:603–619

    Article  Google Scholar 

  • Drummond JM, Macmillan DL (2002) The cord stretch receptors in the abdominal nerve cord of the crayfish Cherax destructor: physiology and relationships. J Comp Physiol A 188:349–357

    Article  Google Scholar 

  • Faulkes Z, Macmillan DL (2002) Effects of removal of muscle receptor organ input on the temporal structure of non-giant swimming cycles in the crayfish, Cherax destructor. Mar Fresh Behav Physiol 35:149–155

    Google Scholar 

  • Fields HL (1976) Crustacean abdominal and thoracic muscle receptor organs. In: Mll PJ (ed) Structure and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 65–114

  • Fields HL, Kennedy D (1965) Functional role of muscle receptor organs in crayfish. Nature 206:1235–1237

    CAS  PubMed  Google Scholar 

  • Fields HL, Evoy WH, Kennedy D (1967) Reflex role played by efferent control of an invertebrate stretch receptor. J Neurophysiol 30:859–874

    CAS  PubMed  Google Scholar 

  • Jones KA, Page CH (1986) Postural interneurons in the abdominal nervous system of lobster. I. Organization, morphologies and motor programs for flexion, extension and inhibition. J Comp Physiol A 158:259–271

    CAS  PubMed  Google Scholar 

  • Larimer JL, Eggleston AC (1971) Motor programs for abdominal positioning in crayfish. Z Vergl Physiol 74:338–402

    Google Scholar 

  • Macmillan DL (2002) The abdominal muscle receptor organ of crayfish and lobsters: current issues. In: Wiese K (ed) Crustacean experimental systems in neurobiology. Springer, Berlin Heidelberg New York, pp 109–117

  • Macmillan DL, Patullo BW (2001) Insights for robotic design from studies of the control of abdominal position in crayfish. Biol Bull 200:201–205

    PubMed  Google Scholar 

  • Macmillan DL, Vescovi PJ (1997) The muscle receptor organs of the crayfish Cherax destructor : organisation of central projections of stretch receptor neurons. J Exp Zool 279:243–253

    Article  Google Scholar 

  • McCarthy BJ, Macmillan DL (1995) The role of the muscle receptor organ in the control of abdominal extension in the crayfish Cherax destructor. J Exp Biol 198:2253–2259

    PubMed  Google Scholar 

  • McCarthy BJ, Macmillan DL (1999a) Control of abdominal extension in the freely moving intact crayfish Cherax destructor. I. Activity of the tonic stretch receptor. J Exp Biol 202:171–181

    PubMed  Google Scholar 

  • McCarthy BJ, Macmillan DL (1999b) Control of abdominal extension in the freely moving intact crayfish Cherax destructor. II. Activity of the superficial extensor motor neurones. J Exp Biol 202:183–191

    PubMed  Google Scholar 

  • Miall RC, Larimer JL (1982) Central organization of crustacean abdominal posture motoneurons of the crayfish abdomen. J Exp Zool 224:45–56

    PubMed  Google Scholar 

  • Nakagawa H, Mulloney B (2001) Local specification of relative strengths of synapses between different abdominal stretch-receptor axons and their common target neurons. J Neurosci 21:1645–1655

    PubMed  Google Scholar 

  • Page CH (1975) Command fibre control of crayfish abdominal movement. I. MRO and extensor motor neuron activity in Orconectes and Procambarus. J Comp Physiol 102:65–76

    Google Scholar 

  • Page CH (1978) Load compensation in the crayfish abdomen. J Comp Physiol 123:349–356

    Google Scholar 

  • Page CH (1982) Control of posture. In: Bliss DE, Atwood H, Sandeman DC (eds) The biology of Crustacea, vol 4. Academic Press, New York, pp 33–59

  • Patullo BW, Faulkes Z, Macmillan DL (2001) Muscle receptor organs do not mediate load compensation during body role and defence response in crayfish. J Exp Zool 290:783–790

    Article  PubMed  Google Scholar 

  • Sokolove PG (1973) Crayfish stretch receptor and motor unit behaviour during abdominal extensions. J Comp Physiol 84:251–266

    Google Scholar 

  • Sukhdeo SC, Page CH (1992) Abdominal postural motor responses initiated by the muscle receptor organ in lobster depend on centrally generated motor activity. J Exp Biol 162:167–183

    PubMed  Google Scholar 

  • Vescovi PJ, Macmillan DL, Simmers AJ (1997) The muscle receptor organs of the crayfish Cherax destructor: input to telson motor neurons. J Exp Zool 279:228–242

    Article  Google Scholar 

  • Wiersma CAG, Hughes GM (1961) On the functional anatomy of neuronal units in the abdominal cord of the crayfish, Procambarus clarkii (Girard). J Comp Neurol 116:209–228

    CAS  Google Scholar 

  • Wiersma CAG, Furshpan E, Florey E (1953) Physiological and pharmacological observations on muscle receptor organs of the crayfish, Cambarus clarkii (Girard). J Exp Biol 30:136–150

    CAS  Google Scholar 

  • Williams BJ, Larimer JL (1981) Neural pathways of reflex-evoked behaviours and command systems in the abdomen of the crayfish. J Comp Physiol 143:27–42

    Google Scholar 

  • Wine JJ, Krasne FB (1972) The organisation of escape behaviour in the crayfish. J Exp Biol 56:1–18

    Google Scholar 

  • Wine JJ, Krasne FB (1982) The cellular organization of crayfish escape behavior. In: Bliss DE (ed) The biology of Crustacea, vol 4. Academic Press, New York, pp 241–292

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Acknowledgements

Animal handling and experimentation procedures were in accordance with the Australian National Health and Medical Research Council Code of Practice. Research was supported by an Australian Research Council grant to D.L.M. We wish to thank Jo Drummond, Garry Jolley-Rogers, and Blair Patullo for stimulating discussions and assistance with preparation of the manuscript. D.L.M. wishes to acknowledge the generous hospitality of Dr. François Clarac and colleagues who provided facilities at the Laboratoire de Neurobiologie et Mouvements, CNRS, Marseille.

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Correspondence to D. L. Macmillan.

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McCarthy, B., Daws, A. & Macmillan, D.L. The activity of abdominal stretch receptors during non-giant swimming in the crayfish Cherax destructor and their role in hydrodynamic efficiency. J Comp Physiol A 190, 291–299 (2004). https://doi.org/10.1007/s00359-003-0491-2

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