Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1973 Aug;70(8):2462–2466. doi: 10.1073/pnas.70.8.2462

Presynaptic Inhibition at Inhibitory Nerve Terminals. A New Synapse in the Crayfish Stretch Receptor

Yasuko Nakajima *, Ann D Tisdale *, Maryanna P Henkart †,‡
PMCID: PMC433757  PMID: 4365382

Abstract

Previous physiological evidence has shown that the receptor neuron of the slowly adapting stretch receptor organ of crayfish receives synapses from three inhibitory axons, while the receptor muscle is innervated by both excitatory and inhibitory axons. Fine structural studies have indicated that after certain preparative procedures synaptic vesicles in the inhibitory terminals on dendrites of the receptor neuron appear small and elongate, while those in the excitatory terminals on the receptor muscle are round and larger. This study describes a new synapse between two inhibitory nerve endings on the receptor neuron. One axon, containing small elongate vesicles, forms a presynaptic chemical contact with another morphologically similar axon that, itself, presumably releases inhibitory transmitter onto the receptor neuron. A second type of presynaptic axo-axonic synapse, analogous to one previously described in another crustacean muscle, was also found between presumed inhibitory and excitatory nerve terminals on the receptor muscle. Thus, the stretch receptor has a relatively complex organization with a morphological basis for two types of presynaptic inhibition: one on excitatory terminals and the other on inhibitory terminals.

Keywords: Procambarus, electron microscopy

Full text

PDF
2462

Images in this article

2464Image
on p.2464
2465Image
on p.2465

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Atwood H. L., Lang F., Morin W. A. Synaptic vesicles: selective depletion in crayfish excitatory and inhibitory axons. Science. 1972 Jun 23;176(4041):1353–1355. doi: 10.1126/science.176.4041.1353. [DOI] [PubMed] [Google Scholar]
  2. Atwood H. L., Morin W. A. Neuromuscular and axoaxonal synapses of the crayish opener muscle. J Ultrastruct Res. 1970 Aug;32(3):351–369. doi: 10.1016/s0022-5320(70)80015-6. [DOI] [PubMed] [Google Scholar]
  3. BURGEN A. D., KUFFLER S. W. Two inhibitory fibres forming synapses with a single nerve cell in the lobster. Nature. 1957 Dec 28;180(4600):1490–1491. doi: 10.1038/1801490a0. [DOI] [PubMed] [Google Scholar]
  4. Bodian D. An electron microscopic characterization of classes of synaptic vesicles by means of controlled aldehyde fixation. J Cell Biol. 1970 Jan;44(1):115–124. doi: 10.1083/jcb.44.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. DUDEL J., KUFFLER S. W. Presynaptic inhibition at the crayfish neuromuscular junction. J Physiol. 1961 Mar;155:543–562. doi: 10.1113/jphysiol.1961.sp006646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. FLOREY E., FLOREY E. Microanatomy of the abdominal stretch receptors of the crayfish (Astacus fluviatilis L.). J Gen Physiol. 1955 Sep 20;39(1):69–85. doi: 10.1085/jgp.39.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Jansen J. K., Ormstad K., Njå A., Walloe L. On the innervation of the slowly adapting stretch receptor of the crayfish abdomen. An electrophysiological approach. Acta Physiol Scand. 1971 Feb;81(2):273–285. doi: 10.1111/j.1748-1716.1971.tb04901.x. [DOI] [PubMed] [Google Scholar]
  8. KUFFLER S. W., EYZAGUIRRE C. Synaptic inhibition in an isolated nerve cell. J Gen Physiol. 1955 Sep 20;39(1):155–184. doi: 10.1085/jgp.39.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. KUFFLER S. W. Mechanisms of activation and motor control of stretch receptors in lobster and crayfish. J Neurophysiol. 1954 Nov;17(6):558–574. doi: 10.1152/jn.1954.17.6.558. [DOI] [PubMed] [Google Scholar]
  10. Kosaka K. Electrophysiological and electron microscopic studies on the neuromuscular junction of the crayfish stretch receptors. Jpn J Physiol. 1969 Apr 15;19(2):160–175. doi: 10.2170/jjphysiol.19.160. [DOI] [PubMed] [Google Scholar]
  11. Nadol J. B., Jr, De Lorenzo A. J. Observations on the abdominal stretch receptor and the fine structure of associated axo-dendritic synapses and neuromuscular junctions in homarus. J Comp Neurol. 1968 Mar;132(3):419–443. doi: 10.1002/cne.901320305. [DOI] [PubMed] [Google Scholar]
  12. Nakajima Y. Fine structure of the medial nucleus of the trapezoid body of the bat with special reference to two types of synaptic endings. J Cell Biol. 1971 Jul;50(1):121–134. doi: 10.1083/jcb.50.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Uchizono K. Inhibitory synapses on the stretch receptor neurone of the crayfish. Nature. 1967 May 20;214(5090):833–834. doi: 10.1038/214833a0. [DOI] [PubMed] [Google Scholar]
  14. Valdivia O. Methods of fixation and the morphology of synaptic vesicles. J Comp Neurol. 1971 Jul;142(3):257–273. doi: 10.1002/cne.901420302. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES