Skip to main content
Log in

Synaptic connections of the common inhibitory motoneurone within the fifth thoracic ganglion of crayfish

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

The common inhibitor (CI) has been studied morphologically and electrophysiologically in the fifth thoracic ganglion of crayfish (Procambarus clarkii). It has a large soma and possesses two separate dendritic fields arising from distinct integrative segments.

In vitro preparations display motor outputs ranging from tonic activity to fictive locomotion. The CI's tonic firing frequency increases as more excitors are recruited, and displays two peaks of frequency during fictive locomotion, one during stance, the other during swing.

Paired intracellular recordings have been used to demonstrate the different central synaptic connections received or made by the CI. At least 27% of the proximal excitors receive monosynaptic connections from the CI corresponding to post-synaptic depolarizations of small amplitude mediated by GABA. However as they do not change the overall activities of the excitors which receive them, they may be used for local inhibition within the dendrites. Besides, electrical synapses between several proximal excitors and the CI may synchronize their activity.

The CI receives synaptic connections arising from interneurones. Some are direct either by inhibitory monosynaptic connections or by electrical couplings whereas others arise through polysynaptic pathways. All these connections are functionally significant in the control of the CI firing activity and in its motor coordinations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atwood HL (1976) Organization and synaptic physiology of crustacean neuromuscular systems. Prog Neurobiol 7: 291–391

    Google Scholar 

  • Atwood HL, Bittner GD (1971) Matching of excitatory and inhibitory inputs to crustacean muscle fibers. J Neurophysiol 34: 157–170

    Google Scholar 

  • Ballantyne D, Rathmayer W (1981) On the function of the common inhibitory neurone in the walking legs of the crab, Eriphia spinifrons. J Comp Physiol A 143: 111–122

    Google Scholar 

  • Baxter DA, Bittner GD (1991) Synaptic plasticity at crayfish neuromuscular junctions: presynaptic inhibition. Synapse 7: 244–251

    Google Scholar 

  • Bévengut M, Clarac F (1990) Motoneuronal commands during swimming behaviour in the shore crab. Brain Res 520: 330–333

    Google Scholar 

  • Bévengut M, Cournil I (1990) GABA-inhibitory motor command of the leg muscle of the shore crab. Eur J Neurosci 2: 132–139

    Google Scholar 

  • Bévengut M, Simmers AJ, Clarac F (1983) Central and neuronal projections and basal limb neuromusculature in the shore crab, Carcinus maenas. J Comp Neurol 221: 5–198

    Google Scholar 

  • Cattaert D, Bévengut M, Clarac F (1993) Synaptic connections between sensory afferents and the common inhibitory motoneuron in the crayfish. J Comp Physiol A 172: 71–79

    Google Scholar 

  • Chrachri A, Clarac F (1989) Synaptic connections between motor neurons and interneurones in the fourth thoracic ganglion of the crayfish Procambarus clarkii. J Neurophysiol 62: 1237–1250

    Google Scholar 

  • Chrachri A, Clarac F (1990) Fictive locomotion in the fourth thoracic ganglion of the crayfish, Procambarus clarkii. J Neurosci 10: 707–719

    Google Scholar 

  • Clarac F, El Manira A, Cattaert D (1992) Presynaptic control as a mechanism of sensory-motor integration. Curr Opin Neurobiol 2: 764–769

    Google Scholar 

  • Dudel J, Kuffler SW (1961) Presynaptic inhibition at the crayfish neuromuscular junction. J Physiol (Lond) 155: 543–562

    Google Scholar 

  • El Manira A, Cattaert D, Clarac F (1991) Monosynaptic connections mediate resistance reflex in crayfish (Procambarus clarkii) walking legs. J Comp Physiol A 168: 337–349

    Google Scholar 

  • Ellaway PH (1978) Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroenceph Clin Neurophysiol 45: 302–304

    Google Scholar 

  • Garnett R, Stephens JA (1980) The reflex responses of single motor units in human first dorsal interosseous muscle following cutaneous afferent stimulation. J Physiol (Lond) 303: 351–364

    Google Scholar 

  • Godden DH, Graham D (1984) A preparation of the stick insect Carausius morosus for recording intracellularly from identified neurones during walking. Physiol Entomol 9: 275–286

    Google Scholar 

  • Govind CK, Atwood HL (1982) Organization of neuromuscular systems. In: Atwood HL, Sandeman DC (eds) The biology of Crustacea, neurobiology: structure and function. Academic Press, New York, pp. 63–103

    Google Scholar 

  • Homberg U, Bleick A, Rathmayer W (1993) Immunocytochemistry of GABA and glutamic acid decarboxylase in the thoracic ganglion of the crab Eriphia spinifrons. Cell Tissue Res 271: 279–288

    Google Scholar 

  • Maïer L, Rathmayer W, Pette D (1984) pH lability of myosin ATP-ase permits discrimination of different muscle fiber types in crustaceans. Histochemistry 81: 75–77

    Google Scholar 

  • Moffet S, Yox DP (1986) The common inhibitor innervates muscles proximal to the autotomy fracture plane in Carcinus maenas. Brain Res 366: 388–391

    Google Scholar 

  • Ogonowski MM, Lang F (1979) Histochemical evidence for enzyme differences in crustacean fast and slow muscle. J Exp Zool 207: 143–151

    Google Scholar 

  • Otsuka M, Iversen LL, Hall ZW, Kravitz EA (1966) Release of gamma-aminobutyric acid from inhibitory nerves of lobster. Proc Natl Acad Sci USA 56: 1110–1115

    Google Scholar 

  • Rathmayer W (1990) Inhibition through neurons of the common inhibitory type (Cl-neurons) in crab muscles. In: Wiese K, Krentz WD, Tautz J, Reichert H, Mulloney B (eds) Frontiers in crustacean neurobiology. Birkhäuser, Basel, pp 271–278

    Google Scholar 

  • Rathmayer W, Bévengut M (1986) The common inhibitory neuron innervates every leg muscle in crabs. J Comp Physiol A 158: 665–668

    Google Scholar 

  • Rathmayer W, Erxleben C (1983) Identified muscle fibers in a crab. I. Characteristics of excitatory and inhibitory neuromuscular transmission. J Comp Physiol 152: 411–420

    Google Scholar 

  • Sandeman DC (1969a) The site of synaptic activity and impulse initiation in an identified motoneurone in the crab brain. J Exp Biol 50: 771–784

    Google Scholar 

  • Sandeman DC (1969b) Integrative properties of a reflex motoneuron in the brain of the crab Carcinus maenas. Z Vergl Physiol 64: 450–464

    Google Scholar 

  • Sillar KT, Skorupski P (1986) Phase-dependent reversal of reflexes mediated by the thoracocoxal muscle receptor organ in the crayfish, Pacifastacus leniusculus. J Neurophysiol 55: 689–695

    Google Scholar 

  • Skorupski P, Sillar KT (1988) Central synaptic coupling of walking leg motoneurons in the crayfish: implication for sensorimotor integration. J Exp Biol 140: 355–380

    Google Scholar 

  • Skorupski P, Rawat BM, Bush BMH (1992) Heterogeneity and central modulation of feedback reflexes in crayfish motor pool. J Neurophysiol 67: 648–663

    Google Scholar 

  • Takeuchi A, Takeuchi N (1966a) A study of the inhibitory action of γ-aminobutyric acid on neuromuscular transmission in the crayfish. J Physiol (Lond) 183: 418–432

    Google Scholar 

  • Takeuchi A, Takeuchi N (1966b) On the permeability of the presynaptic terminal of the crayfish neuromuscular junction during synaptic inhibition and the action of γ-aminobutyric acid. J Physiol (Lond) 183: 433–449

    Google Scholar 

  • Takeuchi A, Takeuchi N (1969) A study of the action of picrotoxin on the inhibitory neuromuscular junction of the crayfish. J Physiol (Lond) 205: 377–393

    Google Scholar 

  • Usherwood PNR, Runion HI (1970) Analysis of the mechanical responses of metathoracic extensor tibia muscles of free-walking locusts. J Exp Biol 52: 39–58

    Google Scholar 

  • Wiens TJ (1988) Common and specific inhibition in leg muscles of decapods: sharpened distinctions. J Neurobiol 20: 458–469

    Google Scholar 

  • Wiens TJ, Atwood HL (1975) Dual inhibitory control in crab leg muscles. J Comp Physiol 99: 211–230

    Google Scholar 

  • Wiens TJ, Rathmayer W (1985) The distribution of the common inhibitory neuron in brachyuran limb musculature. I. Target muscles. J Comp Physiol A 156: 305–313

    Google Scholar 

  • Wiens TJ, Wolf H (1993) The inhibitory motoneuron of crayfish thoracic limbs: identification, structures, and homology with insect common inhibitors. J Comp Neurol 33: 261–278

    Google Scholar 

  • Wiens TJ, Maïer L, Rathmayer W (1988) The distribution of the common inhibitory neuron in brachyuran limb musculature. II. Target fibers. J Comp Physiol A 163: 651–664

    Google Scholar 

  • Wiersma CAG, Ripley SH (1952) Innervation patterns of crustacean limbs. Physiol Comp Oecol 2: 391–405

    Google Scholar 

  • Wolf H (1990) Activity patterns of inhibitory motoneurones and their impact on leg movement in tethered walking locusts. J Exp Biol 152: 281–304

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bévengut, M., Cattaert, D. & Clarac, F. Synaptic connections of the common inhibitory motoneurone within the fifth thoracic ganglion of crayfish. J Comp Physiol A 178, 337–350 (1996). https://doi.org/10.1007/BF00193972

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00193972

Key words

Navigation