Skip to main content
Log in

Axonal regeneration from GABAergic neurons in the adult rat thalamus

  • Published:
Journal of Neurocytology

Summary

Peripheral nerve grafts were inserted into the thalamus in 27 Sprague-Dawley rats. From 6 weeks to 15 months later, horseradish peroxidase (HRP) was applied to the extracranial end of each graft and sections of the brains reacted for peroxidase histochemistry. Of the thalamic neurons that were retrogradely labelled with HRP, more than 80% were located in the reticular nucleus of the thalamus (RNT), a distinct group of nerve cells that contain glutamic acid decarboxylase (GAD)-like immunoreactivity and are presumably GABAergic. By combining immunocytochemistry with HRP histochemistry, it was possible to confirm that the RNT neurons that had grown axons into the peripheral nerves grafts retained their GAD-like immunoreactivity. The apparent selectivity in their regenerative responses of RNT neurons to peripheral nerve grafts may relate to special properties of the neurons that did and did not grow into the grafts.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Aguayo, A. J. (1985) Axonal regeneration from injured neurons in the adult mammalian central nervous system. InSynaptic Plasticity (edited byCotman, C. W.). Guilford Press (in press).

  • Aguayo, A. J., Benfey, M. &David, S. (1983) A potential for axonal regeneration in neurons of the adult mammalian nervous system.Birth Defects:Original Article Series, Vol. 19,Nervous System Regeneration (edited byHaber, B., Perez-Polo, J. R., Hashim, G. A. andGiuffrida-Stella, A. M.), pp. 327–40. New York: Alan R. Liss.

    Google Scholar 

  • Aguayo, A. J., Björklund, A., Stenevi, U. &Carlstedt, T. (1984) Fetal mesencephalic neurons survive and extend long axons across peripheral nervous system grafts inserted into the adult rat striatum.Neuroscience Letters 45, 53–8.

    PubMed  Google Scholar 

  • Barron, K. D., Means, E. D. &Larsen, E. (1973) Ultrastructure of retrograde degeneration in thalamus of rat. I. Neuronal somata and dendrites.Journal of Neuropathology and Experimental Neurology 32, 218–44.

    PubMed  Google Scholar 

  • Benfey, M. &Aguayo, A. J. (1982) Extensive elongation of axons from rat brain into peripheral nerve grafts.Nature 296, 150–2.

    PubMed  Google Scholar 

  • Björklund, A., Dunnett, S. B., Stenevi, U., Lewis, M. E. &Iversen, S. D. (1980) Reinnervation of the denervated striatum by substantia nigra transplants: functional consequences as revealed by pharmacological and sensorimotor testing.Brain Research 199, 307–33.

    PubMed  Google Scholar 

  • Björklund, A., Segal, N. &Stenevi, U. (1979) Functional reinnervation of rat hippocampus by locus coeruleus implants.Brain Research 170, 409–26.

    PubMed  Google Scholar 

  • Cragg, B. C. (1970) What is the signal for chromatolysis?Brain Research 23, 1–21.

    PubMed  Google Scholar 

  • David, S. &Aguayo, A. J. (1981) Axonal elongation into PNS ‘bridges’ after CNS injury in adult rats.Science 214, 931–3.

    PubMed  Google Scholar 

  • Dooley, J. T. &Aguayo, A. J. (1982) Axonal elongation from cerebellum into PNS grafts in the adult rat.Annals of Neurology 12, 221 (abstract).

    Google Scholar 

  • Emson, P. C., Björkland, A. &Steveni, U. (1977) Evaluation of the regenerative capacity of central dopaminergic, noradrenergic and cholinergic neurons using iris implants as targets.Brain Research 135, 87–105.

    PubMed  Google Scholar 

  • Friedman, B. &Aguayo, A. J. (1985) Injured neurons in the olfactory bulb of the adult rat grow axons along grafts of peripheral nerve.Journal of Neuroscience (in press).

  • Gage, F. H., Dunnett, S. B., Stenevi, U. &Björklund, A. (1983) Aged rats: recovery of motor impairments by intrastriatal nigral grafts.Science 221, 966–9.

    PubMed  Google Scholar 

  • Grafstein, B. &Ingoglia, N. A. (1982) Intracranial transection of the optic nerve in adult mice: preliminary observations.Experimental Neurology 76, 318–30.

    PubMed  Google Scholar 

  • Hale, P. T., Sefton, A. J., Baur, L. A. &Cottee, L. J. (1982) Interrelations of the rat's thalamic reticular and dorsal lateral geniculate nuclei.Experimental Brain Research 45, 217–29.

    Google Scholar 

  • Houser, C., Vaughn, J. E., Barber, R. P. &Roberts, E. (1980) GABA neurons are the major cell type of the nucleus reticularis thalami.Brain Research 200, 341–54.

    PubMed  Google Scholar 

  • Jones, E. G. (1975) Some aspects of the organization of the thalamic reticular complex.Journal of Comparative Neurology 162, 285–308.

    PubMed  Google Scholar 

  • Jones, E. G. (1981) Functional subdivision and synaptic organization of the mammalian thalamus. InInternational Review of Physiology, Vol. 25,Neurophysiology IV (edited byPorter, R.), pp. 173–245. Baltimore: University Park Press.

    Google Scholar 

  • Kawamura, Y. &Dyck, P. J. (1981) Permanent axotomy by amputation results in loss of motor neurons in man.Journal of Neuropathology and Experimental Neurology 40, 658–66.

    PubMed  Google Scholar 

  • König, J. F. R. &Klippel, R. A. (1963)The Rat Brain. A Stereotaxic Atlas of the Forebrain and Lower Parts of the Brain Stem. New York: R.E. Krieger Publishing Co. Inc.

    Google Scholar 

  • Lieberman, A. R. (1974) Some factors affecting retrograde neuronal responses to axonal lesions. InEssays on the Nervous System (edited byBellairs, R. andGray, E. G.), pp. 71–105. Oxford: Clarendon Press.

    Google Scholar 

  • McQuarrie, I. G. &Grafstein, B. (1973) Axon outgrowth enhanced by a previous nerve injury.Archives of Neurology 29, 53–5.

    PubMed  Google Scholar 

  • Mendell, L. M. (1984) Modifiability of spinal synapses.Physiological Reviews 64, 260–324.

    PubMed  Google Scholar 

  • Mesulam, M.-M. (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents.Journal of Histochemistry and Cytochemistry 26, 106–17.

    PubMed  Google Scholar 

  • Montero, V. M. (1983) Ultrastructural identification of axon terminals from the thalamic reticular nucleus in the medial geniculate body in the rat: an EM autoradiographic study.Experimental Brain Research 51, 338–42.

    Google Scholar 

  • Munz, M., Rasminsky, M., Aguayo, A. J., Vidal-Sanz, M. &Devor, M. (1985) Functional activity of rat brain stem neurons regenerating axons along peripheral nerve grafts.Brain Research (in press).

  • Nadler, J. V., Cotman, C. W. &Lynch, G. S. (1974) Biochemical plasticity of short-axon interneurons: increased glutamate decarboxylase activity in the denervated area of rat dentate gyrus following entorhinal lesions.Experimental Neurology 45, 403–13.

    PubMed  Google Scholar 

  • Nornes, H., Björklund, A. &Stenevi, U. (1983) Reinnervation of the denervated adult spinal cord of rats by intraspinal transplants of embryonic brainstem neurons.Cell and Tissue Research 230, 15–36.

    PubMed  Google Scholar 

  • Oertel, W. H., Graybiel, A. M., Mugnaini, E., Elde, R. P., Schmechel, D. E. &Kopin, I. J. (1983) Co-existence of glutamic acid decarboxylase and somatostatin-like immunoreactivity in neurons of the feline nucleus reticularis thalami.Neuroscience 3, 1322–32.

    PubMed  Google Scholar 

  • Oertel, W. H., Schmechel, D. E., Tappaz, M. L. &Kopin, I. J. (1981a) Production of an antiserum to glutamate decarboxylase by injection of an antigen-antibody complex.Neuroscience 6, 2700–14.

    Google Scholar 

  • Oertel, W. H., Schmechel, D. E., Mugnaini, E., Tappaz, M. L. &Kopin, I. J. (1981b) Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum.Neuroscience 6, 2715–35.

    Google Scholar 

  • Ohara, P. T., Lieberman, A. R., Hunt, S. P. &Wu, J.-Y. (1983) Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat: immunohistochemical studies by light and electron microscopy.Neuroscience 8, 189–211.

    PubMed  Google Scholar 

  • Olson, L., Seiger, A. &Stromberg, I. (1983) Intraocular transplantation in rodents. A detailed account of the procedure and examples of its use in neurobiology with special reference to brain tissue grafting. InAdvances in Cellular Neurobiology (edited byFedoroff, S.) Vol. 4, pp. 407–42. New York: Academic Press.

    Google Scholar 

  • Paxinos, G. &Watson, C. (1982)The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.

    Google Scholar 

  • Richardson, P. M. &Issa, V. M. K. (1984) Peripheral injury enhances regeneration of spinal axons.Nature 309, 791–3.

    PubMed  Google Scholar 

  • Richardson, P. M., Issa, V. M. K. &Aguayo, A. J. (1984) Regeneration of long spinal axons in the rat.Journal of Neurocytology 13, 165–82.

    PubMed  Google Scholar 

  • Richardson, P. M., McGuinness, U. M. &Aguayo, A. J. (1982) Peripheral nerve autografts to the rat spinal cord: studies with axonal tracing methods.Brain Research 237, 147–62.

    PubMed  Google Scholar 

  • Rye, D. B., Saper, C. B. &Wainer, B. H. (1984) Stabilization of the tetramethylbenzidine (TMB) reaction product: application for retrograde and anterograde tracing, and combination with immunohistochemistry.Journal of Histochemistry and Cytochemistry 32, 1145–53.

    PubMed  Google Scholar 

  • Scheibel, M. E. &Scheibel, A. B. (1966) The organization of the nucleus reticularis thalami: a Golgi study.Brain Research 1, 43–62.

    PubMed  Google Scholar 

  • Schneider, G. E. (1973) Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections.Brain, Behavior and Evolution 8, 73–109.

    Google Scholar 

  • Singer, P. A., Mehler, S. &Fernandez, H. L. (1982) Blockade of retrograde axonal transport delays the onset of metabolic and morphologic changes induced by axotomy.Journal of Neuroscience 2, 1299–306.

    PubMed  Google Scholar 

  • So, K.-F. &Aguayo, A. J. (1985) Lengthy regrowth of cut ganglion cell axons after transplantation of peripheral nerve into the retina of adult rats.Brain Research 328, 349–54.

    PubMed  Google Scholar 

  • Sugitani, M. (1979) Electrophysiological and sensory properties of the thalamic reticular neurones related to somatic sensation in rats.Journal of Physiology 290, 79–95.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benfey, M., Bünger, U.R., Vidal-Sanz, M. et al. Axonal regeneration from GABAergic neurons in the adult rat thalamus. J Neurocytol 14, 279–296 (1985). https://doi.org/10.1007/BF01258453

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01258453

Keywords

Navigation