Selective GABAergic innervation of thalamic nuclei from zona incerta

European Journal of Neuroscience

Volumn 16, Issue 6, 2002, Pages 999-1014

  Bartho P ^a   Freund, T F ^a   Acsády, László ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

GABA; Higher order nuclei; Rat; Reticular nucleus; Thalamocortical; Zona incerta

Indexed keywords

MUSCARINIC RECEPTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; FEEDBACK SYSTEM; GABAERGIC SYSTEM; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INNERVATION; MALE; NEOCORTEX; NERVE ENDING; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; THALAMUS NUCLEUS; ULTRASTRUCTURE; ZONA INCERTA;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; DENDRITES; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON; NEURAL PATHWAYS; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTOR, MUSCARINIC M2; RECEPTORS, MUSCARINIC; SUBTHALAMUS; THALAMUS;

EID: 0036457181     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02157.x     Document Type: Article

References (70)

1. Acsády, L., Barthó, P. & Freund, T.F. (2000) Subcellular localization of M2 muscarinic receptors in dorsal thalamic nuclei - Spatial relationship to cholinergic terminals. Soc. Neurosci. Abstr., 26, 1710.
2. Ahissar, E., Sosnik, R. & Haidarliu, S. (2000) Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature, 406, 302-306.
3. Arai, R., Jacobowitz, D.M. & Deura, S. (1994) Distribution of calretinin, calbindin-D28k, and parvalbumin in the rat thalamus. Brain Res. Bull., 33, 595-614.
4. Baimbridge, K.G. & Miller, J.J. (1982) Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res., 245, 223-229.
5. Bartlett, E.L., Stark, J.M., Guillery, R.W. & Smith, P.H. (2000) Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neuroscience, 100, 811-828.
6. Bender, D.B. (1983) Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Res., 279, 258-261.
7. 2+/calmodulin protein kinase gene expression in the rat central nervous system. Neuroscience, 46, 825-849.
8. Bourassa, J., Pinault, D. & Deschenes, M. (1995) Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: A single-fibre study using biocytin as an anterograde tracer. Eur. J. Neurosci., 7, 19-30.
9. Buzsaki, G. & Chrobak, J.J. (1995) Temporal structure in spatially organized neuronal ensembles: A role for interneuronal networks. Curr. Opin. Neurobiol., 5, 504-510.
10. Churchill, L., Zahm, D.S. & Kalivas, P.W. (1996) The mediodorsal nucleus of the thalamus in rats - I. forebrain gabaergic innervation. Neuroscience, 70, 93-102.
11. Cobb, S.R., Buhl, E.H., Halasy, K., Paulsen, O. & Somogyi, P. (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature, 378, 75-78.
12. Crespo, C., Blasco-Ibanez, J.M., Brinon, J.G., Alonso, J.R., Dominguez, M.I. & Martinez-Guijarro, F.J. (2000) Subcellular localization of m2 muscarinic receptors in GABAergic interneurons of the olfactory bulb. Eur. J. Neurosci., 12, 3963-3974.
13. Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1991) Electron-microscopic analysis of synaptic input from the perigeniculate nucleus to the A-laminae of the lateral geniculate nucleus in cats. J. Comp. Neurol., 310, 316-336.
14. Deschenes, M., Bourassa, J. & Pinault, D. (1994) Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res., 664, 215-219.
15. Diamond, M.E., Armstrong-James, M., Budway, M.J. & Ebner, F.F. (1992b) Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: Dependence on the barrel field cortex. J. Comp. Neurol., 319, 66-84.
16. Diamond, M.E., Armstrong-James, M. & Ebner, F.F. (1992a) 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.
17. Forsythe, I.D. & Barnes-Davies, M. (1993) The binaural auditory pathway: Excitatory amino acid receptors mediate dual timecourse excitatory postsynaptic currents in the rat medial nucleus of the trapezoid body. Proc. R. Soc. Lond. B Biol. Sci., 251, 151-157.
18. Gerfen, C.R. & Sawchenko, P.E. (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: Immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res., 290, 219-238.
19. Hajos, N., Papp, E.C., Acsady, L., Levey, A.I. & Freund, T.F. (1998) Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience, 82, 355-376.
20. Henze, D.A., Urban, N.N. & Barrionuevo, G. (2000) The multifarious hippocampal mossy fiber pathway: A review. Neuroscience, 98, 407-427.
21. Hohmann, C.F., Potter, E.D. & Levey, A.I. (1995) Development of muscarinic receptor subtypes in the forebrain of the mouse. J. Comp. Neurol., 358, 88-101.
22. Hoogland, P.V., Wouterlood, F.G., Welker, E. & Van der Loos, H. (1991) Ultrastructure of giant and small thalamic terminals of cortical origin: A study of the projections from the barrel cortex in mice using Phaseolus vulgaris leuco-agglutinin (PHA-L). Exp. Brain Res., 87, 159-172.
23. Jones, E.G. (1975) Some aspects of the organization of the thalamic reticular complex. J. Comp. Neurol., 162, 285-308.
24. Jones, E. (1985). The Thalamus. Plenum Press, New York.
25. Jones, E.G. (1998) Viewpoint: The core and matrix of thalamic organization. Neuroscience, 85, 331-345.
26. Jones, E.G. (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci., 24, 595-601.
27. Kim, U., Gregory, E. & Hall, W.C. (1992) Pathway from the zona incerta to the superior colliculus in the rat. J. Comp. Neurol., 321, 555-575.
28. Kim, U., Sanchez-Vives, M.V. & McCormick, D.A. (1997) Functional dynamics of GABAergic inhibition in the thalamus. Science, 278, 130-134.
29. Kinomura, S., Larsson, J., Gulyas, B. & Roland, P.E. (1996) Activation by attention of the human reticular formation and thalamic intralaminar nuclei. Science, 271, 512-515.
30. Kolmac, C. & Mitrofanis, J. (1998) Distribution of various neurochemicals within the zona incerta: An immunocytochemical and histochemical study. Anat Embryol (Berl.), 199, 265-280.
31. Kolmac, C.I., Power, B.D. & Mitrofanis, J. (1998) Patterns of connections between zona incerta and brainstem in rats. J. Comp. Neurol., 396, 544-555.
32. Komura, Y., Tamura, R., Uwano, T., Nishijo, H., Kaga, K. & Ono, T. (2001) Retrospective and prospective coding for predicted reward in the sensory thalamus. Nature, 412, 546-549.
33. Landisman, C.E., Long, M.A., Beierlein, M., Deans, M.R., Paul, D.L. & Connors, B.W. (2002) Electrical synapses in the thalamic reticular nucleus. J. Neurosci., 22, 1002-1009.
34. Lieberman, A.R. & Spacek, J. (1997) Filamentous contacts: The ultrastructure and three-dimensional organization of specialized non-synaptic interneuronal appositions in thalamic relay nuclei. Cell Tissue Res., 288, 43-57.
35. Lin, C.S., Nicolelis, M.A., Schneider, J.S. & Chapin, J.K. (1990) A major direct GABAergic pathway from zona incerta to neocortex. Science, 248, 1553-1556.
36. Liu, X.B. & Jones, E.G. (1999) Predominance of corticothalamic synaptic inputs to thalamic reticular nucleus neurons in the rat. J. Comp. Neurol., 414, 67-79.
37. Liu, X.B., Warren, R.A. & Jones, E.G. (1995) Synaptic distribution of afferents from reticular nucleus in ventroposterior nucleus of cat thalamus. J. Comp. Neurol., 352, 187-202.
38. Mitrofanis, J. & Mikuletic, L. (1999) Organisation of the cortical projection to the zona incerta of the thalamus. J. Comp. Neurol., 412, 173-185.
39. 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, 6, 2561-2577.
40. Nicolelis, M.A., Chapin, J.K. & Lin, R.C. (1992) Somatotopic maps within the zona incerta relay parallel GABAergic somatosensory pathways to the neocortex, superior colliculus, and brainstem. Brain Res., 577, 134-141.
41. Ojima, H. (1994) Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. Cereb. Cortex, 4, 646-663.
42. Pare, D. & Smith, Y. (1996) Thalamic collaterals of corticostriatal axons: Their termination field and synaptic targets in cats. J. Comp. Neurol., 372, 551-567.
43. Paxinos, G., Kus, L., Ashwell, K.W.S. & Watson, C. (1999) Chemoarchitectonic Atlas of the Rat Forebrain. Academic Press, London.
44. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th Edn. Academic Press, London.
45. Peruzzi, D., Bartlett, E., Smith, P.H. & Oliver, D.L. (1997) A monosynaptic GABAergic input from the inferior colliculus to the medial geniculate body in rat. J. Neurosci., 17, 3766-3777.
46. Pierret, T., Lavallee, P. & Deschenes, M. (2000) Parallel streams for the relay of vibrissal information through thalamic barreloids. J. Neurosci., 20, 7455-7462.
47. Pinault, D. & Deschenes, M. (1998) 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.
48. Pinault, D., Smith, Y. & Deschenes, M. (1997) Dendrodendritic and axoaxonic synapses in the thalamic reticular nucleus of the adult rat. J. Neurosci., 17, 3215-3233.
49. Plummer, K.L., Manning, K.A., Levey, A.I., Rees, H.D. & Uhlrich, D.J. (1999) Muscarinic receptor subtypes in the lateral geniculate nucleus: A light and electron microscopic analysis. J. Comp. Neurol., 404, 408-425.
50. Power, B.D., Kolmac, C.I. & Mitrofanis, J. (1999) Evidence for a large projection from the zona incerta to the dorsal thalamus. J. Comp. Neurol., 404, 554-565.
51. Power, B.D. & Mitrofanis, J. (2001) Zona incerta: Substrate for contralateral interconnectivity in the thalamus of rats. J. Comp. Neurol., 436, 52-63.
52. Power, B.D. & Mitrofanis, J. (1999) Evidence for extensive inter-connections within the zona incerta in rats. Neurosci. Lett., 267, 9-12.
53. Ricardo, J.A. (1981) Efferent connections of the subthalamic region in the rat. II. The zona incerta. Brain Res., 214, 43-60.
54. Rockland, K.S. (1994) Further evidence for two types of corticopulvinar neurons. Neuroreport, 5, 1865-1868.
55. Rogers, J.H. (1989) Two calcium-binding proteins mark many chick sensory neurons. Neuroscience, 31, 697-709.
56. Rouiller, E.M. & Welker, E. (2000) A comparative analysis of the morphology of corticothalamic projections in mammals. Brain Res. Bull., 53, 727-741.
57. Sherman, S.M. & Guillery, R.W. (1996) Functional organization of thalamocortical relays. J. Neurophysiol., 76, 1367-1395.
58. Sherman, S.M. & Guillery, R.W. (1998) On the actions that one nerve cell can have on another: Distinguishing 'drivers' from 'modulators'. Proc. Natl. Acad. Sci. USA, 95, 7121-7126.
59. Somogyi, P., Hodgson, A.J., Chubb, I.W., Penke, B. & Erdei, A. (1985) Antisera to gamma-aminobutyric acid. II. Immunocytochemical application to the central nervous system. J. Histochem. Cytochem., 33, 240-248.
60. Steriade, M. (2001) Impact of network activities on neuronal properties in corticothalamic systems. J. Neurophysiol., 86, 1-39.
61. Steriade, M., Jones, E. & McCormick, D. (1997) Thalamus, Vol. 1. Elsevier Science Ltd, Oxford. pp. 533-687.
62. Steriade, M., Parent, A., Ropert, N. & Kitsikis, A. (1982) Zona incerta and lateral hypothalamic afferents to the midbrain reticular core of cat - HRP and electrophysiological study. Brain Res., 238, 13-28.
63. Veinante, P. & Deschenes, M. (1999) Single- and multi-whisker channels in the ascending projections from the principal trigeminal nucleus in the rat. J. Neurosci., 19, 5085-5095.
64. Veinante, P., Jacquin, M.F. & Deschenes, M. (2000a) Thalamic projections from the whisker-sensitive regions of the spinal trigeminal complex in the rat. J. Comp. Neurol., 420, 233-243.
65. Veinante, P., Lavallee, P. & Deschenes, M. (2000b) Corticothalamic projections from layer 5 of the vibrissal barrel cortex in the rat. J. Comp. Neurol., 424, 197-204.
66. Vidnyanszky, Z., Borostyankoi, Z., Gorcs, T.J. & Hamori, J. (1996) Light and electron microscopic analysis of synaptic input from cortical area 17 to the lateral posterior nucleus in cats. Exp. Brain Res., 109, 63-70.
67. Wang, X.-J. & Rinzel, J. (1993) Spindle rhytmicity in the reticularis thalami nucleus: Synchronization among mutually inhibitory neurons. Neuroscience, 53, 899-904.
68. Watanabe, K. & Kawana, E. (1982) The cells of origin of the incertofugal projections to the tectum, thalamus, tegmentum and spinal cord in the rat: A study using the autoradiographic and horseradish peroxidase methods. Neuroscience, 7, 2389-2406.
69. Williams, M.N., Zahm, D.S. & Jacquin, M.F. (1994) Differential foci and synaptic organization of the principal and spinal trigeminal projections to the thalamus in the rat. Eur. J. Neurosci., 6, 429-453.
70. Winer, J.A., Larue, D.T. & Huang, C.L. (1999) Two systems of giant axon terminals in the cat medial geniculate body: Convergence of cortical and GABAergic inputs. J. Comp. Neurol., 413, 181-197.