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. 1985 Nov;82(22):7772–7776. doi: 10.1073/pnas.82.22.7772

Dendritic sprouting and compensatory synaptogenesis in an identified interneuron follow auditory deprivation in a cricket.

R R Hoy, T G Nolen, G C Casaday
PMCID: PMC391416  PMID: 3865195

Abstract

We examined the effect of chronic afferent deprivation on an identified interneuron (Int-1) in the auditory system of the Australian field cricket Teleogryllus oceanicus. In normal intact crickets, the auditory afferents from each ear terminate ipsilaterally onto a single Int-1. Each bilaterally paired Int-1 is excited by ultrasound stimulation of its ipsilateral ear but not by the contralateral ear. Unilateral removal of an ear early in postembryonic development deprives the developing Int-1 of ipsilateral auditory innervation. Consequently, the ipsilateral dendrites of the deprived interneuron sprout, grow aberrantly across the ganglionic midline, and terminate specifically in the intact auditory neuropile of the contralateral (unlesioned) side, where they form functional synapses with the contralateral afferents. This unusual compensatory dendritic sprouting restores auditory function to the neuron. Thus, it is demonstrated that the dendritic shape of an identified Int, as well as its synaptic connectivity, is altered as a consequence of chronic sensory deprivation.

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Selected References

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

  1. Ball E., Young D. Structure and development of the auditory system in the prothoracic leg of the cricket Teleogryllus commodus (Walker) II. Postembryonic development. Z Zellforsch Mikrosk Anat. 1974 Mar 11;147(3):313–324. doi: 10.1007/BF00307467. [DOI] [PubMed] [Google Scholar]
  2. Goodman C. S., Spitzer N. C. Embryonic development of identified neurones: differentiation from neuroblast to neurone. Nature. 1979 Jul 19;280(5719):208–214. doi: 10.1038/280208a0. [DOI] [PubMed] [Google Scholar]
  3. Kimmel C. B., Schabtach E., Kimmel R. J. Developmental interactions in the growth and branching of the lateral dendrite of Mauthner's cell (Ambystoma mexicanum). Dev Biol. 1977 Feb;55(2):244–259. doi: 10.1016/0012-1606(77)90170-1. [DOI] [PubMed] [Google Scholar]
  4. LEVI-MONTALCINI R. The development to the acoustico-vestibular centers in the chick embryo in the absence of the afferent root fibers and of descending fiber tracts. J Comp Neurol. 1949 Oct;91(2):209-41, illust, incl 3 pl. doi: 10.1002/cne.900910204. [DOI] [PubMed] [Google Scholar]
  5. Murphey R. K., Levine R. B. Mechanisms responsible for changes observed in response properties of partially deafferented insect interneurons. J Neurophysiol. 1980 Feb;43(2):367–382. doi: 10.1152/jn.1980.43.2.367. [DOI] [PubMed] [Google Scholar]
  6. Murphey R. K., Mendenhall B., Palka J., Edwards J. S. Deafferentation slows the growth of specific dendrites of identified giant interneurons. J Comp Neurol. 1975 Feb 1;159(3):407–418. doi: 10.1002/cne.901590307. [DOI] [PubMed] [Google Scholar]
  7. Nolen T. G., Hoy R. R. Initiation of behavior by single neurons: the role of behavioral context. Science. 1984 Nov 23;226(4677):992–994. doi: 10.1126/science.6505681. [DOI] [PubMed] [Google Scholar]
  8. Perry V. H., Linden R. Evidence for dendritic competition in the developing retina. Nature. 1982 Jun 24;297(5868):683–685. doi: 10.1038/297683a0. [DOI] [PubMed] [Google Scholar]
  9. Peusner K. D., Morest D. K. Neurogenesis in the nucleus vestibularis tangentialis of the chick embryo in the absence of the primary afferent fibers. Neuroscience. 1977;2(2):253–270. doi: 10.1016/0306-4522(77)90092-6. [DOI] [PubMed] [Google Scholar]
  10. Pitman R. M., Tweedle C. D., Cohen M. J. Branching of central neurons: intracellular cobalt injection for light and electron microscopy. Science. 1972 Apr 28;176(4033):412–414. doi: 10.1126/science.176.4033.412. [DOI] [PubMed] [Google Scholar]
  11. Raper J. A., Bastiani M. J., Goodman C. S. Guidance of neuronal growth cones: selective fasciculation in the grasshopper embryo. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 2):587–598. doi: 10.1101/sqb.1983.048.01.063. [DOI] [PubMed] [Google Scholar]
  12. Shankland M., Bentley D., Goodman C. S. Afferent innervation shapes the dendritic branching pattern of the medial giant interneuron in grasshopper embryos raised in culture. Dev Biol. 1982 Aug;92(2):507–520. doi: 10.1016/0012-1606(82)90195-6. [DOI] [PubMed] [Google Scholar]
  13. Steward O., Rubel E. W. Afferent influences on brain stem auditory nuclei of the chicken: cessation of amino acid incorporation as an antecedent to age-dependent transneuronal degeneration. J Comp Neurol. 1985 Jan 15;231(3):385–395. doi: 10.1002/cne.902310308. [DOI] [PubMed] [Google Scholar]
  14. Tweedle C. D., Pitman R. M., Cohen M. J. Dendritic stability of insect central neurons subjected to axotomy and de-afferentation. Brain Res. 1973 Oct 12;60(2):471–476. doi: 10.1016/0006-8993(73)90805-6. [DOI] [PubMed] [Google Scholar]
  15. Tyrer N. M., Bell E. M. The intensification of cobalt-filled neurone profiles using a modification of Timm's sulphide-silver method. Brain Res. 1974 Jun 14;73(1):151–155. doi: 10.1016/0006-8993(74)91014-2. [DOI] [PubMed] [Google Scholar]

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