Skip to main content
Log in

Mechanosensory integration in the crayfish abdominal nervous system: Structural and physiological differences between interneurons with single and multiple spike initiating sites

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

Cobalt backfills were used to demonstrate a population of approximately 50 paired interneurons in the 6th abdominal ganglion of the crayfish,Procambarus clarkii. Intracellular recordings from somata were used to study the response properties of individual interneurons, which were subsequently injected with Lucifer yellow. This report deals with 22 identified mechanosensory interneurons, which were each studied 2 to 20 times. (The total number of cells studied was 177). All but two of the interneurons could be assigned to one of two homogeneous classes, based on their receptive field sizes and four other consistent features: amplitude of soma spikes, duration of afterdischarge, presence of postsynaptic inhibition, and structure of the neuropilar processes.

Unisegmental interneurons (Type I) (n=9) had excitatory receptive fields restricted to one segment, small soma spikes, little afterdischarge, and received extensive postsynaptic inhibition from contralateral and occasionally anterior sensory fields. All of these interneurons had a large diameter neuropilar segment (integrating segment) that was separated from the main axon by a constricted region.

Multisegmental interneurons (Type II) (n=11) had excitatory receptive fields of at least six hemisegments (one half of the abdomen), large (sometimes overshooting) soma spikes, prolonged afterdischarge, and little evidence of postsynaptic inhibition. These interneurons lacked any expanded region of the dendritic tree that could be called an integrating segment.

Anomalous interneurons (n=2) had multisegmental receptive fields, but in all other respects they resembled unisegmental interneurons, although their soma spikes were somewhat larger in amplitude.

We hypothesize that the fundamental difference between the two main kinds of interneurons is that Type II interneurons have multiple spike initiating sites distributed throughout their dendritic trees, with any site being capable of initiating a spike that propagates to the main axon, while Type I interneurons have a single spike initiating site. The properties of anomalous interneurons are consistent with them having a single spike initiating site in each of several ganglia.

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

  • Calabrese RL (1976a) Crayfish mechanoreceptive interneurons: I. The nature of ipsilateral excitatory inputs. J Comp Physiol 105:83–102

    Google Scholar 

  • Calabrese RL (1976b) Crayfish mechanoreceptive interneurons: II. Bilateral interactions and inhibition. J Comp Physiol 105:103–114

    Google Scholar 

  • Calabrese RL, Kennedy D (1974) Multiple sites of spike initiation in a single dendritic system. Brain Res 82:316–321

    Google Scholar 

  • Goodman CS, Heitler WJ (1979) Electrical properties of insect neurones with spiking and non-spiking somata: normal, axotomized, and colchicine-treated neurones. J Exp Biol 83:95–121

    Google Scholar 

  • Harreveld A Van (1936) A physiological solution for fresh water crustaceans. Proc Soc Exp Biol Med 34:428–432

    Google Scholar 

  • Hughes GM, Wiersma CAG (1960) Neuronal pathways and synaptic connexions in the abdominal cord of the crayfish. J Exp Biol 37:291–307

    Google Scholar 

  • Jack JJB, Noble D, Tsien RW (1975) Electric current flow in excitable cells. Oxford University Press, London

    Google Scholar 

  • Johnson GE (1924) Giant nerve fibers in crustaceans with special reference toCambarus andPalaemonetes. J Comp Neurol 36:323–373

    Google Scholar 

  • Kennedy D (1971) Crayfish interneurons. Physiologist 14:5–30

    Google Scholar 

  • Kennedy D, Mellon D (1964a) Synaptic activation and receptive fields in crayfish interneurons. Comp Biochem Physiol 13:275–300

    Google Scholar 

  • Kennedy D, Mellon D (1964b) Receptive-field organization and response patterns in neurons with spatially distributed input. In: Reiss RF (ed) Neural theory and modeling. Stanford University Press, Stanford, pp 400–413

    Google Scholar 

  • Kennedy D, Preston JB (1963) Post-activation changes in excitability and spontaneous firing of crustacean interneurons. Comp Biochem Physiol 8:173–179

    Google Scholar 

  • Krasne FB, Bryan JS (1973) Habituation: regulation through presynaptic inhibition. Science 182:590–592

    Google Scholar 

  • Kusano K, Grundfest H (1965) Circus reexcitation as a cause of repetitive activity in crayfish lateral giant axons. J Cell Comp Physiol 65:325–336

    Google Scholar 

  • Kuwada JY, Wine JJ (1981) Transient, axotomy-induced changes in the membrane properties of crayfish central neurones. J Physiol (Lond) 317:435–461

    Google Scholar 

  • Llinás R, Nicholson C (1971) Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J Neurophysiol 34:532–551

    Google Scholar 

  • Payton BW, Bennett MVL, Pappas GD (1969) Permeability and structure of junctional membranes at an electrotonic synapse. Science 166:1641–1643

    Google Scholar 

  • Pitman RM, Tweedle CD, Cohen MJ (1972a) Branching of central neurons: intracellular cobalt injection for light and electron microscopy. Science 176:412–414

    Google Scholar 

  • Pitman RM, Tweedle CD, Cohen MJ (1972b) Electrical responses of insect central neurons: augmentation by nerve section or colchicine. Science 178:507–509

    Google Scholar 

  • Preston JB, Kennedy D (1960) Integrative synaptic mechanisms in the caudal ganglion of the crayfish. J Gen Physiol 43:671–681

    Google Scholar 

  • Prosser CL (1935) Action potentials in the nervous system of the crayfish. III. Central responses to proprioceptive and tactile stimulation. J Comp Neurol 62:495–505

    Google Scholar 

  • Rall W (1964) Theoretical significance of dendritic trees for neuronal input-output relations. In: Reiss RF (ed) Neural theory and modeling. Stanford University Press, Stanford, California, pp 73–97

    Google Scholar 

  • Reichert H, Plummer MR, Hagiwara G, Roth RL, Wine JJ (1981) Sensory characteristics of local neurons in the last abdominal ganglion of the crayfish. Neurosci Abstr 7:252

    Google Scholar 

  • Ringham GL (1971) Origin of nerve impulse in slowly adapting stretch receptors of crayfish. J Neurophysiol 34:773–784

    Google Scholar 

  • Roberts A, Bush BMH (1981) Neurones without impulses. Cambridge University Press, Cambridge (England)

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Siegel S (1956) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York

    Google Scholar 

  • Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759

    Google Scholar 

  • Takeda K, Kennedy D (1965) The mechanism of discharge pattern formation in crustacean interneurons. J Gen Physiol 48:435–453

    Google Scholar 

  • Traub RD, Llinás R (1977) The spatial distribution of ionic conductances in normal and axotomized motoneurons. Neurosci 2:829–850

    Google Scholar 

  • Traub RD, Llinás R (1979) Hippocampal pyramidal cells: significance of dendritic ionic conductances for neuronal function and epileptogenesis. J Neurophysiol 42:476–496

    Google Scholar 

  • Vedel JP, Moulins M (1977) Functional properties of interganglionic motor neurons in the stomatogastric nervous system of the rock lobster. J Comp Physiol 118:207–325

    Google Scholar 

  • Wiersma CAG (1947) Giant nerve fiber system of the crayfish. A contribution to comparative physiology of synapse. J Neurophysiol 10:23–38

    Google Scholar 

  • Wiersma CAG (1958) On the functional connections of single units in the central nervous system of the crayfishProcambarus clarkii (Girard). J Comp Neurol 110:421–471

    Google Scholar 

  • Wiersma CAG, Bush BMH (1963) Functional neuronal connections between the thoracic and abdominal cords of the crayfish,Procambarus clarkii (Girard). J Comp Neurol 121:207–235

    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

    Google Scholar 

  • Wiese K (1976) Mechanoreceptors for near-field water displacements in crayfish. J Neurophysiol 39:816–833

    Google Scholar 

  • Wiese K, Calabrese RL, Kennedy D (1976) Integration of directional mechanosensory input by crayfish interneurons. J Neurophysiol 39:834–843

    Google Scholar 

  • Wilkens LA, Larimer JL (1972) The CNS photoreceptor of crayfish: morphology and synaptic activity. J Comp Physiol 80:389–407

    Google Scholar 

  • Wine JJ (1975) Crayfish neurons with electrogenic cell bodies: correlations with function and dendritic properties. Brain Res 85:92–98

    Google Scholar 

  • Wine JJ, Krasne FB (1982) The cellular organization of crayfish escape behavior. In: Atwood H, Sandeman DC (eds) Biology of the Crustacea, vol 4. Academic Press, New York

    Google Scholar 

  • Wine JJ, Mittenthal JE, Kennedy D (1974) The structure of tonic flexor motoneurons in crayfish abdominal ganglia. J Comp Physiol 93:315–335

    Google Scholar 

  • Zucker RS (1972) Crayfish escape behavior and central synapses. I. Neural circuit exciting lateral giant fiber. J Neurophysiol 35:599–620

    Google Scholar 

  • Zucker RS, Kennedy D, Selverston AI (1971) Neuronal circuit mediating escape responses in crayfish. Science 173:645–650

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sigvardt, K.A., Hagiwara, G. & Wine, J.J. Mechanosensory integration in the crayfish abdominal nervous system: Structural and physiological differences between interneurons with single and multiple spike initiating sites. J. Comp. Physiol. 148, 143–157 (1982). https://doi.org/10.1007/BF00619122

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00619122

Keywords

Navigation