Skip to main content
Log in

Comparison of numbers of interneurons in three thalamic nuclei of normal and epileptic rats

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

The inhibitory sources in the thalamic nuclei are local interneurons and neurons of the thalamic reticular nucleus. Studies of models of absence epilepsy have shown that the seizures are associated with an excess of inhibitory neurotransmission in the thalamus. In the present study, we used light-microscopic gamma-aminobutyric acid (GABA) immunocytochemistry to quantify the interneurons in the lateral geniculate (LGN), ventral posteromedial (VPM), and ventral posterolateral (VPL) thalamic nuclei, and compared the values from normal Wistar rats and genetic absence epilepsy rats from Strasbourg (GAERS). We found that in both Wistar rats and GAERS, the proportion of interneurons was significantly higher in the LGN than in the VPM and VPL. In the LGN of Wistar rats, 16.4% of the neurons were interneurons and in the GAERS, the value was 15.1%. In the VPM, the proportion of interneurons was 4.2% in Wistar and 14.9% in GAERS; in the VPL the values were 3.7% for Wistar and 11.1% for the GAERS. There was no significant difference between Wistar rats and the GAERS regarding the counts of interneurons in the LGN, whereas the VPM and VPL showed significantly higher counts in GAERS. Comparison of the mean areas of both relay cells and interneuronal profiles showed no significant differences between Wistar rats and GAERS. These findings show that in the VPL and the VPM there are relatively more GABAergic interneurons in GAERS than in Wistar rats. This may represent a compensatory response of the thalamocortical circuitry to the absence seizures or may be related to the production of absence seizures.

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

  1. Montero VM. A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus. Exp Brain Res 1991, 86: 257–270.

    Article  CAS  PubMed  Google Scholar 

  2. Ohara PT, Lieberman AR, Hunt SP, Wu JY. Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat; immunohistochemical studies by light and electron microscopy. Neuroscience 1983, 8: 189–211.

    Article  CAS  PubMed  Google Scholar 

  3. Penny GR, Fitzpatrick D, Schmechel DE, Diamond IT. Glutamic acid decarboxylase-immunoreactive neurons and horseradish peroxidase-labeled projection neurons in the ventral posterior nucleus of the cat and Galago senegalensis. J Neurosci 1983, 3: 1868–1887.

    CAS  PubMed  Google Scholar 

  4. Ilinsky IA, Kultas-Ilinsky K. An autoradiographic study of topographical relationships between pallidal and cerebellar projections to the cat thalamus. Exp Brain Res 1984, 54: 95–106.

    Article  CAS  PubMed  Google Scholar 

  5. Jones EG. The Thalamus. New York: Plenum Press, 1985: 701–709.

    Book  Google Scholar 

  6. Balercia G, Kultas-Ilinsky K, Bentivoglio M, Ilinsky IA. Neuronal and synaptic organization of the centromedian nucleus of the monkey thalamus: a quantitative ultrastructural study, with tract tracing and immunohistochemical observations. J Neurocytol 1996, 25: 267–288.

    Article  CAS  PubMed  Google Scholar 

  7. Ilinsky IA, Yi H, Kultas-Ilinsky K. Mode of termination of pallidal afferents to the thalamus: a light and electron microscopic study with anterograde tracers and immunocytochemistry in Macaca mulatta. J Comp Neurol 1997, 386: 601–612.

    Article  CAS  PubMed  Google Scholar 

  8. Guillery RW, Feig SL, Lozsadi DA. Paying attention to the thalamic reticular nucleus. Trends Neurosci 1998, 21: 28–32.

    Article  CAS  PubMed  Google Scholar 

  9. Houser CR, Vaughn JE, Barber RP, Roberts E. GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 1980, 200: 341–354.

    Article  CAS  PubMed  Google Scholar 

  10. Spreafico R, Schmechel DE, Ellis LC Jr, Rustioni A. Cortical relay neurons and interneurons in the N. ventralis posterolateralis of cats: a horseradish peroxidase, electronmicroscopic, Golgi and immunocytochemical study. Neuroscience 1983, 9: 491–509.

    Article  CAS  PubMed  Google Scholar 

  11. Madarasz M, Somogyi G, Somogyi J, Hamori J. Numerical estimation of gamma-aminobutyric acid (GABA)-containing neurons in three thalamic nuclei of the cat: direct GABA immunocytochemistry. Neurosci Lett 1985, 61: 73–78.

    Article  CAS  PubMed  Google Scholar 

  12. Rinvik E, Ottersen OP, Storm-Mathisen J. Gammaaminobutyrate-like immunoreactivity in the thalamus of the cat. Neuroscience 1987, 21: 781–805.

    Article  CAS  PubMed  Google Scholar 

  13. Smith Y, Seguela P, Parent A. Distribution of GABAimmunoreactive neurons in the thalamus of the squirrel monkey (Saimiri sciureus). Neuroscience 1987, 22: 579–591.

    Article  CAS  PubMed  Google Scholar 

  14. Arcelli P, Frassoni C, Regondi MC, De Biasi S, Spreafico R. GABAergic neurons in mammalian thalamus: a marker of thalamic complexity? Brain Res Bull 1997, 42: 27–37.

    Article  CAS  PubMed  Google Scholar 

  15. Bentivoglio M, Spreafico R, Minciacchi D, Macchi G. GABAergic interneurons and neuropil of the intralaminar thalamus: an immunohistochemical study in the rat and the cat, with notes in the monkey. Exp Brain Res 1991, 87: 85–95.

    Article  CAS  PubMed  Google Scholar 

  16. Hunt CA, Pang DZ, Jones EG. Distribution and density of GABA cells in intralaminar and adjacent nuclei of monkey thalamus. Neuroscience 1991, 43: 185–196.

    Article  CAS  PubMed  Google Scholar 

  17. Bartho P, Freund TF, Acsady L. Selective GABAergic innervation of thalamic nuclei from zona incerta. Eur J Neurosci 2002, 16: 999–1014.

    Article  CAS  PubMed  Google Scholar 

  18. Bokor H, Frere SG, Eyre MD, Slezia A, Ulbert I, Luthi A, et al. Selective GABAergic control of higher-order thalamic relays. Neuron 2005, 45: 929–940.

    Article  CAS  PubMed  Google Scholar 

  19. Cavdar S, Onat F, Cakmak YO, Saka E, Yananli HR, Aker R. Connections of the zona incerta to the reticular nucleus of the thalamus in the rat. J Anat 2006, 209: 251–258.

    Article  PubMed Central  PubMed  Google Scholar 

  20. Bodor AL, Giber K, Rovo Z, Ulbert I, Acsady L. Structural correlates of efficient GABAergic transmission in the basal ganglia-thalamus pathway. J Neurosci 2008, 28: 3090–3102.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Gulcebi MI, Ketenci S, Linke R, Hacioglu H, Yanali H, Veliskova J, et al. Topographical connections of the substantia nigra pars reticulata to higher-order thalamic nuclei in the rat. Brain Res Bull 2012, 87: 312–318.

    Article  PubMed  Google Scholar 

  22. Paz JT, Chavez M, Saillet S, Deniau JM, Charpier S. Activity of ventral medial thalamic neurons during absence seizures and modulation of cortical paroxysms by the nigrothalamic pathway. J Neurosci 2007, 27: 929–941.

    Article  CAS  PubMed  Google Scholar 

  23. Winer JA, Larue DT, Huang CL. Two systems of giant axon terminals in the cat medial geniculate body: convergence of cortical and GABAergic inputs. J Comp Neurol 1999, 413: 181–197.

    Article  CAS  PubMed  Google Scholar 

  24. Urbain N, Deschenes M. Motor cortex gates vibrissal responses in a thalamocortical projection pathway. Neuron 2007, 56: 714–725.

    Article  CAS  PubMed  Google Scholar 

  25. Fitzpatrick D, Penny GR, Schmechel DE. Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. J Neurosci 1984, 4: 1809–1829.

    CAS  PubMed  Google Scholar 

  26. de Biasi S, Frassoni C, Spreafico R. GABA immunoreactivity in the thalamic reticular nucleus of the rat. A light and electron microscopical study. Brain Res 1986, 399: 143–147.

    Article  PubMed  Google Scholar 

  27. Wang S, Bickford ME, Van Horn SC, Erisir A, Godwin DW, Sherman SM. Synaptic targets of thalamic reticular nucleus terminals in the visual thalamus of the cat. J Comp Neurol 2001, 440: 321–341.

    Article  CAS  PubMed  Google Scholar 

  28. Steriade M, Deschenes M. The thalamus as a neuronal oscillator. Brain Res 1984, 320: 1–63.

    Article  CAS  PubMed  Google Scholar 

  29. Vergnes M, Marescaux C, Depaulis A, Micheletti G, Warter JM. Spontaneous spike and wave discharges in thalamus and cortex in a rat model of genetic petit mal-like seizures. Exp Neurol 1987, 96: 127–136.

    Article  CAS  PubMed  Google Scholar 

  30. Crunelli V, Leresche N. Childhood absence epilepsy: genes, channels, neurons and networks. Nat Rev Neurosci 2002, 3: 371–382.

    Article  CAS  PubMed  Google Scholar 

  31. Pinault D. Cellular interactions in the rat somatosensory thalamocortical system during normal and epileptic 5–9 Hz oscillations. J Physiol 2003, 552: 881–905.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Meeren H, van Luijtelaar G, Lopes da Silva F, Coenen A. Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory. Arch Neurol 2005, 62: 371–376.

    Article  PubMed  Google Scholar 

  33. Polack PO, Guillemain I, Hu E, Deransart C, Depaulis A, Charpier S. Deep layer somatosensory cortical neurons initiate spike-and-wave discharges in a genetic model of absence seizures. J Neurosci 2007, 27: 6590–6599.

    Article  CAS  PubMed  Google Scholar 

  34. Danober L, Deransart C, Depaulis A, Vergnes M, Marescaux C. Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog Neurobiol 1998, 55: 27–57.

    Article  CAS  PubMed  Google Scholar 

  35. Carcak N, Aker RG, Ozdemir O, Demiralp T, Onat FY. The relationship between age-related development of spike-andwave discharges and the resistance to amygdaloid kindling in rats with genetic absence epilepsy. Neurobiol Dis 2008, 32: 355–363.

    Article  CAS  PubMed  Google Scholar 

  36. Cavdar S, Hacioglu H, Dogukan SY, Onat F. Do the quantitative relationships of synaptic junctions and terminals in the thalamus of genetic absence epilepsy rats from Strasbourg (GAERS) differ from those in normal control Wistar rats. Neurol Sci 2012, 33: 251–259.

    Article  PubMed  Google Scholar 

  37. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 4th ed. San Diego, California: Academic Press, 1998: 8–74.

    Google Scholar 

  38. Spreafico R, Frassoni C, Arcelli P, De Biasi S. GABAergic interneurons in the somatosensory thalamus of the guinea-pig: a light and ultrastructural immunocytochemical investigation. Neuroscience 1994, 59: 961–973.

    Article  CAS  PubMed  Google Scholar 

  39. 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 1986, 382: 305–326.

    Article  CAS  PubMed  Google Scholar 

  40. LeVay S, Ferster D. Proportion of interneurons in the cat’s lateral geniculate nucleus. Brain Res 1979, 164: 304–308.

    Article  CAS  PubMed  Google Scholar 

  41. Cavdar S, Hacioglu H, Sirvanci S, Keskinoz E, Onat F. Synaptic organization of the rat thalamus: a quantitative study. Neurol Sci 2011, 32: 1047–1056.

    Article  PubMed  Google Scholar 

  42. Montero VM, Zempel J. The proportion and size of GABA-immunoreactive neurons in the magnocellular and parvocellular layers of the lateral geniculate nucleus of the rhesus monkey. Exp Brain Res 1986, 62: 215–223.

    Article  CAS  PubMed  Google Scholar 

  43. Montero VM. The GABA-immunoreactive neurons in the interlaminar regions of the cat lateral geniculate nucleus: light and electron microscopic observations. Exp Brain Res 1989, 75: 497–512.

    CAS  PubMed  Google Scholar 

  44. Sanchez-Vives MV, Bal T, Kim U, von Krosigk M, McCormick DA. Are the interlaminar zones of the ferret dorsal lateral geniculate nucleus actually part of the perigeniculate nucleus? J Neurosci 1996, 16: 5923–5941.

    CAS  PubMed  Google Scholar 

  45. Buzsaki G, Bickford RG, Ponomareff G, Thal LJ, Mandel R, Gage FH. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J Neurosci 1988, 8: 4007–4026.

    CAS  PubMed  Google Scholar 

  46. Vergnes M, Marescaux C. Cortical and thalamic lesions in rats with genetic absence epilepsy. J Neural Transm Suppl 1992, 35: 71–83.

    CAS  PubMed  Google Scholar 

  47. Snead OC, 3rd. Basic mechanisms of generalized absence seizures. Ann Neurol 1995, 37: 146–157.

    Article  PubMed  Google Scholar 

  48. Marescaux C, Vergnes M, Bernasconi R. GABAB receptor antagonists: potential new anti-absence drugs. J Neural Transm Suppl 1992, 35: 179–188.

    CAS  PubMed  Google Scholar 

  49. Liu Z, Vergnes M, Depaulis A, Marescaux C. Evidence for a critical role of GABAergic transmission within the thalamus in the genesis and control of absence seizures in the rat. Brain Res 1991, 545: 1–7.

    Article  CAS  PubMed  Google Scholar 

  50. Hosford DA, Clark S, Cao Z, Wilson WA Jr, Lin FH, Morrisett RA, et al. The role of GABAB receptor activation in absence seizures of lethargic (lh/lh) mice. Science 1992, 257: 398–401.

    Article  CAS  PubMed  Google Scholar 

  51. Charpier S, Leresche N, Deniau JM, Mahon S, Hughes SW, Crunelli V. On the putative contribution of GABA(B) receptors to the electrical events occurring during spontaneous spike and wave discharges. Neuropharmacology 1999, 38: 1699–1706.

    Article  CAS  PubMed  Google Scholar 

  52. Meeren HK, Pijn JP, Van Luijtelaar EL, Coenen AM, Lopes da Silva FH. Cortical focus drives widespread corticothalamic networks during spontaneous absence seizures in rats. J Neurosci 2002, 22: 1480–1495.

    CAS  PubMed  Google Scholar 

  53. Richards DA, Lemos T, Whitton PS, Bowery NG. Extracellular GABA in the ventrolateral thalamus of rats exhibiting spontaneous absence epilepsy: a microdialysis study. J Neurochem 1995, 65: 1674–1680.

    Article  CAS  PubMed  Google Scholar 

  54. Sitnikova E, van Luijtelaar G. Cortical control of generalized absence seizures: effect of lidocaine applied to the somatosensory cortex in WAG/Rij rats. Brain Res 2004, 1012: 127–137.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Safiye Çavdar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Çavdar, S., Bay, H.H., Yıldız, S.D. et al. Comparison of numbers of interneurons in three thalamic nuclei of normal and epileptic rats. Neurosci. Bull. 30, 451–460 (2014). https://doi.org/10.1007/s12264-013-1402-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-013-1402-3

Keywords

Navigation