Skip to main content
SpringerLink
Log in

Neuronal and synaptic organization of the centromedian nucleus of the monkey thalamus: a quantitative ultrastructural study, with tract tracing and immunohistochemical observations

  • Published:
Journal of Neurocytology

Summary

The ultrastructure of the centromedian nucleus of the monkey thalamus was analysed qualitatively and quantitatively and projection neurons, local circuit neurons, and synaptic bouton populations identified. Projection neurons were mostly medium-sized, with oval-fusiform or polygonal perikarya, few primary dendrites, and frequent somatic spines; local circuit neurons were smaller. Four basic types of synaptic boutons were distinguished: (1) Small- to medium-sized boutons containing round vesicles (SR) and forming asymmetric contacts, identified as corticothalamic terminals. (2) Heterogeneous medium-sized boutons with asymmetric contacts and round vesicles, similar to the so-called large round (LR) boutons, which were in part of cortical origin. (3) Heterogeneous GAD-positive small- to medium-sized boutons, containing pleomorphic vesicles and forming symmetric contacts (F1 type), which included pallidothalamic terminals. (4) Presynaptic profiles represented by GAD-positive vesicle-containing dendrites of local circuit neurons. Complex synaptic arrangements, serial synapses and triads with LR and SR boutons engaging all parts of projection neuron dendrites and somata, were seen consistently, whereas classical glomeruli were infrequent. LR and SR boutons also established synapses on dendrites of local circuit neurons. F1 boutons established synapses on projection neuron somata, dendrites and initial axon segments. Compared to other previously studied motor-related thalamic nuclei, differences in synaptic coverage between proximal and distal projection neuron dendrites were less pronounced, and the density of synapses formed by local circuit dendrites on projection neuron dendrites was lower. Thus, compared to other thalamic nuclei, the overlap of different inputs was higher on monkey centromedian cells, and centromedian inhibitory circuits displayed a different organization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

  • Bentivoglio, M., Spreafico, R., Minciacchi, D. &Macchi, G. (1991) GABAergic interneurons and neuropil of the intralaminar thalamus: an immunohistochemical study in the rat and the cat, with notes in the monkey.Experimental Brain Research 87, 85–95.

    Google Scholar 

  • Carpenter, M. B., Nakano, K. &Kim, R. (1976) Nigrothalamic projections in the monkey demonstrated by autoradiographic technics.Journal of Comparative Neurology 165, 401–16.

    Google Scholar 

  • Cucchiaro, J. B., Uhlrich, D. J. &Sherman, S. M. (1991) Electron-microscopic analysis of synaptic input from the perigeniculate nucleus of the A-laminae of the lateral geniculate nucleus in cats.Journal of Comparative Neurology 310, 316–36.

    Google Scholar 

  • Famiglietti, E. V. Jr &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.

    Google Scholar 

  • Grofova, I. &Rinvik, E. (1974) Cortical and pallidal projections to the nucleus ventralis lateralis thalami: electron microscopical studies in the cat.Anatomy and Embryology 146, 113–32.

    Google Scholar 

  • Guillery, R. W. &Colonnier, M. (1970) Synaptic patterns in the dorsal lateral geniculate nucleus of the monkey.Zeitschrift für Zellforschung und Mikroskopische Anatomie 103, 90–108.

    Google Scholar 

  • Hallanger, A. E. &Wainer, B. H. (1988) Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat.Journal of Comparative Neurology 274, 483–515.

    Google Scholar 

  • Hallanger, A. E., Levey, A. I., Lee, H. J., Rye, D. B. &Wainer, B. H. (1987) The origins of cholinergic and other subcortical afferents to the thalamus in the rat.Journal of Comparative Neurology 262, 105–24.

    Google Scholar 

  • Hallanger, A. E., Price, S. D., Lee, H. J., Steininger, T. L. &Wainer, B. H. (1990) Ultrastructure of cholinergic synaptic terminals in the thalamic anteroventral, ventroposterior, and dorsal lateral geniculate nuclei of the rat.Journal of Comparative Neurology 299, 482–92.

    Google Scholar 

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

    Google Scholar 

  • Harding, B. N. (1973a) An ultrastructural study of the centre median and ventrolateral thalamic nuclei of the monkey.Brain Research 54, 335–40.

    Google Scholar 

  • Harding, B. N. (1973b) An ultrastructural study of the termination of afferent fibres within the ventrolateral and centre median nuclei of the monkey thalamus.Brain Research 54, 341–6.

    Google Scholar 

  • Harding, B. N. &Powell, T. P. S. (1977) An electron microscopic study of the centre-median ventrolateral nuclei of the thalamus in the monkey.Philosophical Transactions of the Royal Society of London B. 279, 357–412.

    Google Scholar 

  • Hazlett, J. C., Dutta, C. R. &Fox, C. A. (1976) The neurons in the centromedian-parafascicular complex of the monkey (Macaca mulatta): a Golgi study.Journal of Comparative Neurology 168, 41–73.

    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.

    Google Scholar 

  • Hunt, C. A., Pang, D. Z. &Jones, E. G. (1991) Distribution and density of GABA cells in intralaminar and adjacent nuclei of monkey thalamus.Neuroscience 43, 185–96.

    Google Scholar 

  • Ilinsky, I. A. &Kultas-Ilinsky, K. (1982) Stereotactic surgery in the rheusus monkey (Macaca mulatta) utilizing intracerebral landmarks.Applied Neurophysiology 45, 563–72.

    Google Scholar 

  • Ilinsky, I. A. &Kultas-Ilinsky, K. (1987) Sagittal cytoarchitecture maps of theMacaca mulatta thalamus with a revised nomenclature of the motor-related nuclei validated by observations on their connectivity.Journal of Comparative Neurology 262, 331–64.

    Google Scholar 

  • Ilinsky, I. A. &Kultas-Ilinsky, K. (1990) Fine structure of the magnocellular subdivision of the ventral anterior thalamic nucleus (VAmc) ofMacaca mulatta: I. Cell types and synaptology.Journal of Comparative Neurology 294, 455–78.

    Google Scholar 

  • Ilinsky, I. A., Kultas-Ilinsky, K. &Smith, K. R. (1982) Organization of basal ganglia inputs to the thalamus. A light and electron microscopic study in the cat.Applied Neurophysiology 45, 230–7.

    Google Scholar 

  • Jones, E. G. (1985)The Thalamus. New York: Plenum Press.

    Google Scholar 

  • Jones, E. G. &Powell, T. P. S. (1969) An electron microscopic study of the mode of termination of corticothalamic fibres within the sensory relay nuclei of the thalamus.Proceedings of the Royal Society of London 172, 173–85.

    Google Scholar 

  • Kemp, J. M. &Powell, T. P. S. (1971) The connexions of the striatum and globus pallidus: synthesis and speculation.Philosophical Transactions of the Royal Society of London B 262, 441–57.

    Google Scholar 

  • Kultas-Ilinsky, K. &Ilinsky, I. A. (1986) Synaptic organization of the motor thalamus. InCurrent Topics on Research on Synapses, Vol. 3 (edited byJones, D. G.) pp. 77–145. New York: Alan Liss.

    Google Scholar 

  • Kultas-Ilinsky, K. &Ilinsky, I. A. (1988) GABAergic systems in the feline motor thalamus. Neurons, synapses and receptors. InCellular Thalamic Mechanisms (edited byBentivoglio, M. &Spreafico, R.) pp. 349–63. Amsterdam: Elsevier.

    Google Scholar 

  • Kultas-Ilinsky, K. &Ilinsky, I. A. (1991) Fine structure of the ventral lateral nucleus (VL) of theMacaca mulatta thalamus: cell types and synaptology.Journal of Comparative Neurology 314, 319–49.

    Google Scholar 

  • Kultas-Ilinsky, K., Ilinsky, I. A., Young, P. A. &Smith, K. R. (1980a) Ultrastructure of degenerating cerebellothalamic terminals in the ventral medial nucleus of the cat.Experimental Brain Research 38, 125–35.

    Google Scholar 

  • Kultas-Ilinsky, K., Warton, S., Tolbert, D. L. &Ilinsky, I. A. (1980b) Quantitative and qualitative characteristics of dentate and fastigial afferents identified by electron microscopic autoradiography in the cat thalamus.Brain Research 201, 220–6.

    Google Scholar 

  • Kultas-Ilinsky, K., Ribak, C. E., Peterson, G. M. &Oertel, W. H. (1985) A description of the GABAergic neurons and axon terminals in the motor nuclei of the cat thalamus.Journal of Neuroscience 5, 1346–69.

    Google Scholar 

  • Kultas-Ilinsky, K. I., Yi, H. &Ilinsky, I. A. (1995) Nucleus reticularis thalami input to the anterior thalamic nuclei in the monkey: a light and electron microscopy study.Neuroscience Letters 186, 25–8.

    Google Scholar 

  • Leontovich, T. A. &Zhukova, G. P. (1963) The specificity of the neuronal structure and topography of the reticular formation in the brain and spinal cord of carnivora.Journal of Comparative Neurology 121, 347–80.

    Google Scholar 

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

    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.

    Google Scholar 

  • Macchi, G. &Bentivoglio, M. (1986) The intralaminar nuclei and the cerebral cortex. InCerebral Cortex, Vol. 5 (edited byJones, E. G. &Peters, A.) pp. 355–401. New York: Plenum Press.

    Google Scholar 

  • Mehler, W. R. (1981) The basal ganglia-circa 1982. A review and commentary.Applied Neurophysiology 44, 261–90.

    Google Scholar 

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

    Google Scholar 

  • Montero, V. M. &Singer, W. (1985) Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat.Experimental Brain Research 59, 151–65.

    Google Scholar 

  • Oertel, W. H., Tappaz, M. L., Kopin, I. J., Ransom, D. H. &Schmechel, D. E. (1980) Production of an antiserum to rat brain glutamate (GAD)/Cysteine sulfinate (SCD) decarboxylase.Brain Research Bulletin 5, 713–19.

    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, 541–58.

    Google Scholar 

  • Olucha, F., Martinez-Garcia, F. &Lopez-Garcia, C. (1985) A new stabilizing agent for tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP).Journal of Neuroscience Methods 13, 131–8.

    Google Scholar 

  • Paré, D., Smith, Y., Parent, A. &Steriade, M. (1988) Projections of brainstem core cholinergic and noncholinergic neurons of cat to intralaminar and reticular thalamic nuclei.Neuroscience 25, 69–86.

    Google Scholar 

  • Parent, A. &De Bellefeuille, L. (1982) Organization of efferent projections from the internal segment of globus pallidus in primate as revealed by fluorescent retrograde labeling method.Brain Research 245, 201–13.

    Google Scholar 

  • Parent, A., Paré, D., Smith, Y. &Steriade, M. (1988) Basal forebrain cholinergic and noncholinergic projections to the thalamus and brainstem in cats and monkeys.Journal of Comparative Neurology 277, 281–301.

    Google Scholar 

  • Pasik, P., Pasik, T. &Hamori, J. (1976) Synapses between interneurons in the lateral geniculate nucleus of monkeys.Experimental Brain Research 25, 1–13.

    Google Scholar 

  • Pearson, J. C., Norris, J. R. &Phelps, C. H. (1984) The cytoarchitecture and some efferent projections of the centromedian-parafascicular complex in the lesser bushbaby (Galago senegalensis).Journal of Comparative Neurology 225, 554–69.

    Google Scholar 

  • Pierce, J. P. &Levin, G. R. (1994) An ultrastructural size principle.Neuroscience 58, 441–6.

    Google Scholar 

  • Raczkowski, D. &Fitzpatrick, D. (1989) Organization of cholinergic synapses in the cat's dorsal lateral geniculate and perigeniculate nuclei.Journal of Comparative Neurology 288, 676–90.

    Google Scholar 

  • Ralston, H. J., III (1969) The synaptic organization of lemniscal projections to the ventrobasal thalamus of the cat.Brain Research 14, 99–116.

    Google Scholar 

  • Ralston, H. J., III &Daly Ralston, D. (1993) Local circuit processing in the primate thalamus: neurotransmitter mechanisms. InThalamic Networks for Relay and Modulation (edited byMinciacchi, D., Molinari, M., Macchi, G. &Jones, E. G.) pp. 109–22, Oxford: Pergamon Press.

    Google Scholar 

  • Ralston, H. J., III &Herman, M. M. (1969) The fine structure of neurons and synapses in the ventrobasal thalamus of the cat.Brain Research 14, 77–97.

    Google Scholar 

  • Ralston, H. J., III, Ohara, P. T., Ralston, D. D. &Chazal, G. (1988) The neuronal and synaptic organization of the cat and primate somatosensory thalamus. InCellular Thalamic Mechanisms (edited byBentivoglio, M. &Spraafico, R.) pp. 127–41. Amsterdam: Elsevier.

    Google Scholar 

  • Rinvik, E. &Grofova, I. (1974a) Light and electron microscopical studies of the normal nuclei ventralis lateralis and ventralis anterior thalami in the cat.Anatomy and Embryology 146, 57–93.

    Google Scholar 

  • Rinvik, E. &Grofova, I. (1974b) Cerebellar projections to the nuclei ventralis lateralis and ventralis anterior thalami.Anatomy and Embryology 146, 95–111.

    Google Scholar 

  • Royce, G. J., Bromley, S. &Gracco, C. (1991) Subcortical projections to the centromedian and parafascicular thalamic nuclei in the cat.Journal of Comparative Neurology 306, 129–55.

    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 immunocytochemistry.Journal of Histochemistry and Cytochemistry 32, 1145–53.

    Google Scholar 

  • Sadikot, A. F., Parent, A. &François, C. (1992a) Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a PHA-L study of subcortical projections.Journal of Comparative Neurology 315, 137–59.

    Google Scholar 

  • Sadikot, A. F., Parent, A., Smith, Y. &Bolam, J. P. (1992b) Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity.Journal of Comparative Neurology 320, 228–42.

    Google Scholar 

  • Scheibel, M. E. &Scheibel, A. B. (1966) Patterns of organization in specific and nonspecific thalamic fields. InThe Thalamus (edited byPurpura, D. P. &Yahr, M. D.) pp. 13–46. New York: Columbia University Press.

    Google Scholar 

  • Schwartz, M. L., &Mrzljak, L. (1993) Cholinergic innervation of the mediodorsal thalamic nucleus in the monkey: ultrastructural evidence supportive of functional diversity.Journal of Comparative Neurology 327, 48–62.

    Google Scholar 

  • Schwartz, M. L., Dekker, J. J. &Goldman-Rakic, P. S. (1991) Dual mode of corticothalamic synaptic termination of the mediodorsal nucleus of the rheusus monkey.Journal of Comparative Neurology 309, 289–304.

    Google Scholar 

  • Sherman, S. M. &Koch, C. (1990) Thalamus. InSynaptic Organization of the Brain (edited byShepherd, G. M.) pp. 246–78. New York: Oxford University Press.

    Google Scholar 

  • Tai, Y., Yi, H., Ilinsky, I. A. &Kultas-Ilinsky, K. (1995) Nucleus reticularis thalami connections with the mediodorsal nucleus: a light and electron microscopic study in the monkey.Brain Research Bulletin 38, 475–88.

    Google Scholar 

  • Tömböl, T., Bentivoglio, M. &Macchi, G. (1990) Neuronal cell types in the thalamic intralaminar central lateral nucleus of the cat.Experimental Brain Research 81, 491–99.

    Google Scholar 

  • Tseng, G.-F. &Royce, G. J. (1986) A Golgi and ultrastructural analysis of the centromedian nucleus of the cat.Journal of Comparative Neurology 245, 359–78.

    Google Scholar 

  • Van Buren, J. M. &Borke, R. C. (1972)Variations and Connections of the Human Thalamus. I. The Nuclei and Cerebral Connections of the Human Thalamus. Berlin: Springer-Verlag.

    Google Scholar 

  • Yamamoto, T., Noda, T., Samejima, A. &Oka, H. (1988) Electrophysiological and morphological features of thalamic neurons with special reference to the cerebellar and pallidal inputs. InCellular Thalamic Mechanisms (edited byBentivoglio, M. &Spreafico, R.) pp. 239–60. Amsterdam: Excerpta Medica.

    Google Scholar 

  • Yen, C. T., Conley, M. &Jones, E. G. (1985) Morphological and functional types of neurons in cat ventral posterior thalamic nucleus.Journal of Neuroscience 5, 1316–33.

    Google Scholar 

  • Yi, H., Rachman, Y., Kultas-Ilinsky, K. &Ilinsky, I. A. (1992) Pallidal territory of the monkey thalamus: cell types and GABAergic structures.Society for Neuroscience Abstracts 18, 309.

    Google Scholar 

  • Yi, H., Ilinsky, I. A. &Kultas-Ilinsky, K. (1993) Reticular thalamic nucleus input to the nuclei of the monkey thalamus: light and electron microscopic study.Society for Neuroscience Abstracts 19, 1436.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Anatomy and Histology, University of Verona, Italy

    G. Balercia & M. Bentivoglio

  2. Department of Anatomy, University of Iowa, IA, USA

    K. Kultas-Ilinsky & I. A. Ilinsky

Authors
  1. G. Balercia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Kultas-Ilinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Bentivoglio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. A. Ilinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Balercia, G., Kultas-Ilinsky, K., Bentivoglio, M. et al. Neuronal and synaptic organization of the centromedian nucleus of the monkey thalamus: a quantitative ultrastructural study, with tract tracing and immunohistochemical observations. J Neurocytol 25, 267–288 (1996). https://doi.org/10.1007/BF02284802

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02284802

Keywords

Search

Navigation