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A new intrathalamic pathway linking modality-related nuclei in the dorsal thalamus

Abstract

Transmission of sensory information through the dorsal thalamus involves two types of modality-related nuclei, first order and higher order, between which there are thought to be no intrathalamic interactions. We now show that within the somatosensory thalamus, cells in one nucleus, the ventrobasal complex, can influence activity in another nucleus, the medial division of the posterior complex. Stimulation of ventrobasal complex cells evoked inhibitory postsynaptic currents in cells of the medial division of the posterior complex. These currents exhibited the reversal potential and pharmacology of a GABAA receptor-mediated chloride conductance, indicating that they result from the activation of a disynaptic pathway involving the GABAergic cells of the thalamic reticular nucleus. These findings provide the first direct evidence for intrathalamic interactions between dorsal thalamic nuclei.

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Figure 1: Horizontal sections showing the locations of labeled cells in TRN after an injection of WGA-HRP in VB or POm in the juvenile rat.
Figure 2: IPSCs were evoked in POm cells by glutamate stimulation in VB.
Figure 3: Current–voltage relationship of the IPSCs evoked in POm cells by glutamate stimulation in VB.
Figure 4: Bicuculline or picrotoxin blocks the IPSCs evoked in POm cells by glutamate stimulation in VB.
Figure 5: Horizontal section (schematic) through the thalamus showing an intrathalamic pathway linking VB with POm through TRN (R).

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References

  1. Rose, J. E. & Woolsey, C. N. Organization of the mammalian thalamus and its relationships to the cerebral cortex. Electroenceph. Clin. Neurophysiol. 1, 391–404 (1949).

    Article  CAS  Google Scholar 

  2. Altman, J. & Carpenter, M. B. Fiber projections of the superior colliculus in the cat. J. Comp. Neurol. 116, 157–177 (1961).

    Article  CAS  Google Scholar 

  3. Jones, E. G. & Powell, T. P. S. An analysis of the posterior group of thalamic nuclei on the basis of its afferent connections. J. Comp. Neurol. 143, 185–215 (1971).

    Article  CAS  Google Scholar 

  4. Schneider, G. E. Two visual systems. Brain mechanisms for localization and discrimination are dissociated by tectal and cortical lesions. Science, 163, 895–902, (1969).

    Article  CAS  Google Scholar 

  5. Guillery, R. W. Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J. Anat. 187, 583– 592 (1995).

    Google Scholar 

  6. Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367– 1395 (1996).

    Article  CAS  Google Scholar 

  7. Guillery, R. W., Feig, S. L. & Lozsádi, D. A. Paying attention to the thalamic reticular nucleus. Trends Neurosci., 21, 28– 32 (1998).

    Article  CAS  Google Scholar 

  8. Rose, J. E. The ontogenetic development of the rabbit's diencephalon. J. Comp. Neurol. 7, 61–129 (1942).

    Article  Google Scholar 

  9. Crabtree, J. W. Organization in the somatosensory sector of the cat's thalamic reticular nucleus. J. Comp. Neurol. 366, 207–222 (1996).

    Article  CAS  Google Scholar 

  10. Crabtree, J. W. Organization in the auditory sector of the cat's thalamic reticular nucleus. J. Comp. Neurol. 390, 167–182 (1998).

    Article  CAS  Google Scholar 

  11. Houser, C. R., Vaughn, J. E., Barber, R. P. & Roberts, E. GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res. 200, 341–354 ( 1980).

    Article  CAS  Google Scholar 

  12. Hendrickson, A. E., Ogren, M. P., Vaughn, J. E., Barber, R. P. & Wu, J.-Y. Light and electron microscopic immunocytochemical localization of glutamic acid decarboxylase in monkey geniculate complex: Evidence for GABAergic neurons and synapses. J. Neurosci. 3, 1245–1262 (1983).

    Article  CAS  Google Scholar 

  13. Oertel, W. H. et al. Coexistence of glutamic acid decarboxylase- and somatostatin-like immunoreactivity in neurons of the feline nucleus reticularis thalami. J. Neurosci. 3, 1322–1332 ( 1983).

    Article  CAS  Google Scholar 

  14. Montero, V. M. & Scott, G. L. Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: A light and electron microscope autoradiographic study. Neuroscience 6, 2561–2577 ( 1981).

    Article  CAS  Google Scholar 

  15. Montero, V. M. Ultrastructural identification of axon terminals from the thalamic reticular nucleus in the medial geniculate body in the rat: An EM autoradiographic study. Exp. Brain Res. 51, 338–342 (1983).

    Article  Google Scholar 

  16. Peschanski, M., Ralston, H. J. & Roudier, F. Reticularis thalami afferents to the ventrobasal complex of the rat thalamus: An electron microscope study. Brain Res. 270, 325–329 (1983).

    Article  CAS  Google Scholar 

  17. Jones, E. G. Some aspects of the organization of the thalamic reticular complex. J. Comp. Neurol. 162, 285–308 ( 1975).

    Article  CAS  Google Scholar 

  18. Sugitani, M. Electrophysiological and sensory properties of the thalamic reticular neurones related to somatic sensation in rats. J. Physiol. (Lond.) 290, 79–95 (1979).

    Article  CAS  Google Scholar 

  19. MacLeod, N. K., James, T. A., Kilpatrick, I. C. & Starr, M. S. Evidence for a GABAergic nigrothalamic pathway in the rat. II. Electrophysiological studies. Exp. Brain Res. 40, 55– 61 (1980).

    Article  CAS  Google Scholar 

  20. Barbaresi, P., Spreafico, R., Frassoni, C. & Rustioni, A. GABAergic neurons are present in the dorsal column nuclei but not in the ventroposterior complex of rats. Brain Res. 382, 305– 326 (1986).

    Article  CAS  Google Scholar 

  21. Ohara, P. T. & Lieberman, A. R. Some aspects of the synaptic circuitry underlying inhibition in the ventrobasal thalamus. J. Neurocytol. 22, 815–825 (1993).

    Article  CAS  Google Scholar 

  22. Steriade, M., Parent, A. & Hada, J. Thalamic projections of nucleus reticularis thalami of cat: A study using retrograde transport of horseradish peroxidase and fluorescent tracers. J. Comp. Neurol. 229, 531–547 (1984).

    Article  CAS  Google Scholar 

  23. Kolmac, C. I. & Mitrofanis, J. Organisation of the reticular thalamic projection to the intralaminar and midline nuclei in rats. J. Comp. Neurol. 377, 165–178 (1997).

    Article  CAS  Google Scholar 

  24. Conley, M., Kupersmith, A. C. & Diamond, I. T. The organization of projections from subdivisions of the auditory cortex and thalamus to the auditory sector of the thalamic reticular nucleus in Galago. Eur. J. Neurosci. 3, 1089–1103 (1991).

    Article  Google Scholar 

  25. Cornwall, J. & Phillipson, O. T. Afferent projections to the dorsal thalamus of the rat as shown by retrograde lectin transport. I. The mediodorsal nucleus. Neuroscience 24, 1035 –1049 (1988).

    Article  CAS  Google Scholar 

  26. Cicirata, F., Angaut, P., Serapide, M. F. & Panto, M. R. Functional organization of the direct and indirect projection via the reticularis thalami nuclear complex from the motor cortex to the thalamic nucleus ventralis lateralis. Exp. Brain Res. 79, 325– 337 (1990).

    Article  CAS  Google Scholar 

  27. Gonzalo-Ruiz, A. & Lieberman, A. R. Topographic organization of projections from the thalamic reticular nucleus to the anterior thalamic nuclei in the rat. Brain Res. Bull. 37, 17– 35 (1995).

    Article  CAS  Google Scholar 

  28. Lozsádi, D. A. Organization of connections between the thalamic reticular and the anterior thalamic nuclei in the rat. J. Comp. Neurol. 358, 233– 246 (1995).

    Article  Google Scholar 

  29. Lizier, C., Spreafico, R. & Battaglia, G. Calretinin in the thalamic reticular nucleus of the rat: Distribution and relationship with ipsilateral and contralateral efferents. J. Comp. Neurol. 377, 217–233 ( 1997).

    Article  CAS  Google Scholar 

  30. Pinault, D. & Deschênes, M. Projection and innervation patterns of individual thalamic reticular axons in the thalamus of the adult rat: A three-dimensional, graphic and morphometric analysis. J. Comp. Neurol. 391, 180–203 (1998).

    Article  CAS  Google Scholar 

  31. Conley, M. & Diamond, I. T. Organization of the visual sector of the thalamic reticular nucleus in Galago. Evidence that the dorsal lateral geniculate and pulvinar nuclei occupy separate parallel tiers. Eur. J. Neurosci. 2, 211–226 (1990).

    Article  Google Scholar 

  32. Harting, J. K., Van Lieshout, D. P. & Feig, S. Connectional studies of the primate lateral geniculate nucleus: Distribution of axons arising from the thalamic reticular nucleus of Galago crassicaudatus. J. Comp. Neurol. 310 , 411–427 (1991).

    Article  CAS  Google Scholar 

  33. Coleman, K. A. & Mitrofanis, J. Organization of the visual reticular thalamic nucleus of the rat. Eur. J. Neurosci. 8, 388–404 (1996).

    Article  CAS  Google Scholar 

  34. Emmers, R. Organization of the first and second somesthetic regions (SI and SII) in the rat thalamus. J. Comp. Neurol. 124, 215– 228 (1965).

    Article  CAS  Google Scholar 

  35. Waite, P. M. E. Somatotopic organization of vibrissal responses in the ventro-basal complex of the rat thalamus. J. Physiol. (Lond.) 228, 527– 540 (1973).

    Article  CAS  Google Scholar 

  36. Diamond, M. E., Armstrong-James, M. & Ebner, F. F. Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus. J. Comp. Neurol. 318, 462–476 (1992).

    Article  CAS  Google Scholar 

  37. Shosaku, A., Kayama, Y. & Sumitomo, I. Somatotopic organization in the rat thalamic reticular nucleus. Brain Res. 311, 57–63 ( 1984).

    Article  CAS  Google Scholar 

  38. Crabtree, J. W. The somatotopic organization within the rabbit's thalamic reticular nucleus. Eur. J. Neurosci. 4, 1343–1351 (1992).

    Article  Google Scholar 

  39. Crabtree, J. W. The somatotopic organization within the cat's thalamic reticular nucleus. Eur. J. Neurosci. 4, 1352–1361 (1992).

    Article  Google Scholar 

  40. Pinault, D., Bourassa, J. & Deschênes, M. The axonal arborization of single thalamic reticular neurons in the somatosensory thalamus of the rat. Eur. J. Neurosci. 7, 31–40 (1995 ).

    Article  CAS  Google Scholar 

  41. Cox, C. L., Huguenard, J. R. & Prince, D. A. Heterogeneous axonal arborizations of rat thalamic reticular neurons in the ventrobasal nucleus. J. Comp. Neurol. 366, 416–430 (1996).

    Article  CAS  Google Scholar 

  42. Jahnsen, H. & Llinás, R. Electrophysiological properties of guinea-pig thalamic neurones: An in vitro study. J. Physiol. (Lond.) 349, 205–226 ( 1984).

    Article  CAS  Google Scholar 

  43. Steriade, M. & Deschênes, M. The thalamus as a neuronal oscillator. Brain Res. Rev. 8, 1– 63 (1984).

    Article  Google Scholar 

  44. Lu, S.-M., Guido, W. & Sherman, S. M. The brainstem parabrachial region controls mode of response to visual stimulation of neurons in the cat's lateral geniculate nucleus. Visual Neurosci. 10, 631– 642 (1993).

    Article  CAS  Google Scholar 

  45. Godwin, D. W., Vaughan, J. W. & Sherman, S. M. Metabotropic glutamate receptors switch visual response mode of lateral geniculate nucleus cells from burst to tonic. J. Neurophysiol. 76, 1800–1816 (1996).

    Article  CAS  Google Scholar 

  46. Crick, F. Function of the thalamic reticular complex: The searchlight hypothesis. Proc. Natl Acad. Sci. USA 81, 4586–4590 (1984).

    Article  CAS  Google Scholar 

  47. Paxinos, G. & Watson, C. in The Rat Brain in Stereotaxic Coordinates (Academic Press, Sydney, 1986).

    Google Scholar 

  48. Mesulam, M. M. The blue reaction product in horseradish peroxidase neurohistochemistry: Incubation parameters and visibility. J. Histochem. Cytochem. 74, 1273–1280 (1976).

    Article  Google Scholar 

  49. Horikawa, K. & Armstrong, W. E. A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J. Neurosci. Methods 25, 1– 11 (1988).

    Article  CAS  Google Scholar 

  50. Benke, T. A., Lüthi, A., Isaac, J. T. R. & Collingridge, G. L. Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393, 793–797 ( 1998).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the U.K. Medical Research Council (G.L.C.) and The Wellcome Trust (J.T.R.I.) for their support.

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Correspondence to John W. Crabtree.

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Crabtree, J., Collingridge, G. & Isaac, J. A new intrathalamic pathway linking modality-related nuclei in the dorsal thalamus. Nat Neurosci 1, 389–394 (1998). https://doi.org/10.1038/1603

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