Skip to main content
Log in

Some aspects of the synaptic circuitry underlying inhibition in the ventrobasal thalamus

  • Published:
Journal of Neurocytology

Summary

We describe here, and review, the ultrastructural features and synaptic relationships of flat-vesicle containing, presumptively inhibitory presynaptic elements in the glomerular and extraglomerular neuropils of the thalamic ventrobasal (VB) nucleus in monkey, cat and rat. This account is based on EM study of normal material, LM and EM immunocytochemistry for GABA, anterograde tracing with HRP and EM of physiologically characterized interneurons intracellularly injected with HRP. It emerges clearly from this study that attempts to categorize flat-vesicle containing terminals in thalamic tissue as either F-boutons (axon terminals with flattened synaptic vesicles and Gray type II synaptic specializations) or P-boutons (dendritic appendages of interneurons with flattened vesicles) by examining only single sections are likely to produce unreliable results. In many cases it is only by studying serial sections that such profiles can be unambiguously identified. Within glomeruli the P-boutons participate in triplet (triadic) synapses which are thought to mediate rapid feed forward inhibition of projection cells, and serial synaptic arrays involving other P-boutons. Since P-boutons from more than one interneuron are present in individual VB glomeruli, P-bouton to P-bouton synapses may mediate disinhibition of interneurons. We show that dendritic shafts of interneurons make and receive synaptic contacts and that in the monkey, at least, reciprocal synaptic contacts between shafts or between a shaft and a P-bouton are not uncommon. Finally, we confirm that in the rat VB there are insignificant numbers of P-boutons or cells with the morphological and transmitter characteristics of interneurons and we suggest that comparative electrophysiological studies of inhibitory events in rat VB versus those in cat or monkey VB during transmission of somatosensory information might help to clarify the roles of thalamic intrinsic neurons.

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

  • Famiglietti, E. V. &Peters, A. (1972) The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat.Journal of Comparative Neurology 144, 285–334.

    PubMed  Google Scholar 

  • Gabbott, P. L. A., Somogyi, J., Stewart, M. G. &Hamori, J. (1985) Neurons in the dorsal lateral geniculate nucleus of the rat: characterization using a combination of Golgi-impregnation and GABA-immunocytochemistry.Experimental Brain Research 61, 311–22.

    Google Scholar 

  • Gray, E. G. (1959) Axosomatic and axodendritic synapses of the cerebral cortex: an electron microscope study.Journal of Anatomy 93, 420–33.

    PubMed  Google Scholar 

  • Gray, E. G. (1969) Electron microscopy of excitatory and inhibitory synapses: a brief review.Progress in Brain Research 31, 141–55.

    PubMed  Google Scholar 

  • Gray, E. G. &Guillery, R. W. (1966) Synaptic morphology in the normal and degenerating nervous system.International Review of Cytology 19, 111–82.

    PubMed  Google Scholar 

  • Grossman, A., Lieberman, A. R. &Webster, K. E. (1973) A Golgi study of the rat dorsal lateral geniculate nucleus.Journal of Comparative Neurology 150, 441–65.

    PubMed  Google Scholar 

  • Guillery, R. W. (1969) The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat.Zeitschrift für Zellforschung 96, 1–38.

    Google Scholar 

  • Guillery, R. W. (1971) Patterns of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat and monkey: a brief review.Vision Research Supplement 3, 211–27.

    Google Scholar 

  • Hamori, J., Pasik, T., Pasik, P. &Szentagothai, J. (1974) Triadic synaptic arrangements and their possible significance in the lateral geniculate nucleus of the monkey.Brain Research 80, 379–93.

    PubMed  Google Scholar 

  • Hamori, J., Pasik, P. &Pasik, T. (1991) Different types of synaptic triads in the monkey dorsal lateral geniculate nucleus.Journal für Hirnforschung,32, 369–79.

    Google Scholar 

  • Hamos, J. F., Van Horn, S. C., Raczkowski, D., Uhlrich, D. J. &Sherman, S. M. (1985) Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat.Nature 317, 618–21.

    PubMed  Google Scholar 

  • Harris, R. M. &Hendrickson, A. E. (1987) Local circuit neurons in the rat ventrobasal thalamus-a GABA immunocytochemical study.Neuroscience 21, 229–36.

    PubMed  Google Scholar 

  • Hendrickson, A. E., Ogren, M. P., Vaughn, J. E., Barber, R. P. &Wu, J. -Y. (1983) Light and electron microscopic immunocytochemical localization of glutamic acid decarboxylase in monkey geniculate complex: evidence for GABAergic neurons and synapses.Journal of Neuroscience 3, 1245–62.

    PubMed  Google Scholar 

  • Houser, C. R., 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. (1985)The Thalamus. New York: Plenum Press.

    Google Scholar 

  • Korneliussen, H. (1972) Elongated profiles of synaptic vesicles in motor end plates. Morphological effects of fixative variations.Journal of Neurocytology 1, 279–96.

    PubMed  Google Scholar 

  • Lieberman, A. R. (1973) Neurons with presynaptic perikarya and presynaptic dendrites in the rat lateral geniculate nucleus.Brain Research 59, 35–59.

    PubMed  Google Scholar 

  • Lieberman, A. R. (1974) Comments on the fine structural organization of the dorsal lateral geniculate nucleus of the mouse.Zeitschrift für Anatomie und Entwicklungsgeschichte 145, 261–7.

    Google Scholar 

  • Lieberman, A. R. &Webster, K. E. (1972) Presynaptic dendrites and a distinctive class of synaptic vesicle in the rat dorsal lateral geniculate nucleus.Brain Research 42, 196–200.

    PubMed  Google Scholar 

  • Lieberman, A. R. &Webster, K. E. (1974) Aspects of the synaptic organization of intrinsic neurons in the dorsal lateral geniculate nucleus.Journal of Neurocytology 3, 677–710.

    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 

  • Montero, V. M. (1987) Ultrastructural identification of synaptic terminals from the axons of Type 3 interneurons in the cat lateral geniculate nucleus.Journal of Comparative Neurology 264, 268–83.

    PubMed  Google Scholar 

  • Montero, V. M. (1991) A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus.Experimental Brain Research 86, 257–70.

    Google Scholar 

  • Montero, V. M. &Scott, G. L. (1981) Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: a light and electron microscope autoradiographic study.Neuroscience 12, 2561–77.

    Google Scholar 

  • Ohara, P. T., Sefton, A. J. &Lieberman, A. R. (1980) Mode of termination of afferents from the thalamic reticular nucleus in the dorsal lateral geniculate nucleus of the rat.Brain Research 197, 503–6.

    PubMed  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 

  • Ohara, P. T., Ralston, H. J. III &Ralston, D. D. (1987) The morphology of neurons and synapses in the somatosensory thalamus of the cat and monkey. InThalamus and Pain (edited byBesson, J. -M., Guilbaud, G. &Peschanski, M.), pp. 171–84. New York, Elsevier.

    Google Scholar 

  • Ohara, P. T., Chazal, G. &Ralston, H. J. III (1989) Ultrastructural analysis of GABA-immunoreactive elements in the monkey thalamic ventrobasal complex.Journal of Comparative Neurology 283, 542–58.

    Google Scholar 

  • Paré, D., Dossi, R. C. &Steriade, M. (1991) Three types of inhibitory postsynaptic potentials generated by interneurons in the anterior thalamic complex of cat.Journal of Neurophysiology 66, 1190–204.

    PubMed  Google Scholar 

  • Pasik, P., Pasik, T. &Hamori, J. (1976) Synapses between interneurons in the lateral geniculate nucleus of monkeys.Experimental Brain Research 12, 1–13.

    Google Scholar 

  • Penny, G. R., Fitzpatrick, D., Schmechel, D. E. &Diamond, I. T. (1983) Glutamic acid decarboxylase-immunoreactive neurons and horseradish peroxidase-labelled projection neurons in the ventral posterior nucleus of the cat andGalago senegalensis.Journal of Neuroscience 3, 1868–87.

    PubMed  Google Scholar 

  • Peschanski, M., Ralston, H. J. III &Roudier, F. (1983) Reticularis thalami afferents to the VB complex of the rat thalamus. An EM study.Brain Research 270, 329–325.

    Google Scholar 

  • Peters, A., Palay, S. L. &Webster, H. Def. (1991)The Fine Structure of the Nervous System: Neurons and Supporting Cells. 3rd Edition. New York, Oxford: Oxford University Press.

    Google Scholar 

  • Ralston, H. J., III (1971) Evidence for presynaptic dendrites and a proposal for their mechanism of action.Nature 230, 585–7.

    PubMed  Google Scholar 

  • Ralston, H. J., III (1991) Local circuitry of the somatosensory thalamus in the processing of sensory information.Progress in Brain Research 87, 13–28.

    PubMed  Google Scholar 

  • Rapisardi, S. C. &Miles, T. P. (1984) Synaptology of the retinal afferent in the cat.Journal of Comparative Neurology 223, 515–34.

    PubMed  Google Scholar 

  • Sherman, S. M. &Koch, C. (1986) The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus.Experimental Brain Research 63, 1–20.

    Google Scholar 

  • Špaček, J. &Lieberman, A. R. (1974) Ultrastructure and three-dimensional organization of synaptic glomeruli in rat somatosensory thalamus.Journal of Anatomy 117, 487–516.

    PubMed  Google Scholar 

  • Spreafico, R., Schmechel, D. E., Ellis, L. C. &Rustioni, A. (1983) Cortical relay neurons and interneurons in the n. ventralis posterolateralis of cats: a horseradish peroxidase, electron-microscopic, Golgi and immunocytochemical study.Neuroscience 9, 491–509.

    PubMed  Google Scholar 

  • Steriade, M., Domich, L. &Oakson, G. (1986) Reticularis thalami neurons revisited: Activity changes during shifts in states of vigilance.Journal of Neuroscience 6, 68–81.

    PubMed  Google Scholar 

  • Steriade, M., Jones, E. G. &Llinas, R. R. (1990)Thalamic Oscillations and Signaling. New York: Wiley.

    Google Scholar 

  • Valdivia, O. (1971) Methods of fixation and the morphology of synaptic vesicles.Journal of Comparative Neurology 142, 257–74.

    PubMed  Google Scholar 

  • Weinberg, R. J. &Van Eyck, S. L. (1991) A tetramethyl-benzidine/tungstate reaction for horseradish peroxidase histochemistry.Journal of Histochemistry and Cytochemistry 39, 1143–8.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ohara, P.T., Lieberman, A.R. Some aspects of the synaptic circuitry underlying inhibition in the ventrobasal thalamus. J Neurocytol 22, 815–825 (1993). https://doi.org/10.1007/BF01181326

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01181326

Keywords

Navigation