Triadic synaptic interactions of large corticothalamic terminals in non-lemniscal thalamic nuclei of the cat auditory system

Hearing Research

Volumn 274, Issue 1-2, 2011, Pages 40-47

  Ojima, Hisayuki ^a,b   Murakami, Kunio ^b  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b TOHO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; CAT; CONTROLLED STUDY; INTERNEURON; LARGE CORTICOTHALAMIC TERMINAL; MALE; MEDIAL GENICULATE COMPLEX DORSAL NUCLEUS; NERVE PROJECTION; NONHUMAN; PRESYNAPTIC NERVE; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; SYNAPSE; THALAMUS NUCLEUS; TRIADIC SYNAPTIC INTERACTION;

ANIMALS; AUDITORY CORTEX; AUDITORY PATHWAYS; BRAIN MAPPING; CATS; ELECTROPHYSIOLOGY; GENICULATE BODIES; HEARING; MALE; MICROSCOPY, ELECTRON; MODELS, ANATOMIC; MODELS, BIOLOGICAL; NEURONS; THALAMIC NUCLEI; THALAMUS;

EID: 79953320428     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heares.2010.05.009     Document Type: Article

References (68)

1. Andersen R.A., Snyder R.L., Merzenich M.M. The topographic organization of corticocollicular projections from physiologically identified loci in the AI, AII, and anterior auditory cortical fields of the cat. J. Comp. Neurol. 1980, 191:479-494.
2. Arcelli P., Frassoni C., Regondi M.C., De Biasi S., Spreafico R. GABAergic neurons in mammalian thalamus: a marker of thalamic complexity?. Brain Res. Bull. 1997, 42:27-37.
3. Bajo V.M., Nodal F.R., Bizley J.K., Moore D.R., King A.J. The ferret auditory cortex: descending projections to the inferior colliculus. Cereb. Cortex 2007, 17:475-491.
4. Bajo V.M., Rouiller E.M., Welker E., Clarke S., Villa A.E., de Ribaupierre Y., de Ribaupierre F. Morphology and spatial distribution of corticothalamic terminals originating from the cat auditory cortex. Hear. Res. 1995, 83:161-174.
5. Bartlett E.L., Stark J.M., Guillery R.W., Smith P.H. Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neuroscience 2000, 100:811-828.
6. Bartlett E.L., Smith P.H. Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. J. Neurophysiol. 1999, 81:1999-2016.
7. Bourassa J., Deschênes M. Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. Neuroscience 1995, 66:253-263.
8. Bourassa J., Pinault D., Deschênes M. 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. 1995, 7:19-30.
9. Chomiak T., Peters S., Hu B. Functional architecture and spike timing properties of corticofugal projections from rat ventral temporal cortex. J. Neurophysiol. 2008, 100:327-335.
10. Cucchiaro J.B., Uhlrich D.J., Sherman S.M. Electron-microscopic analysis of synaptic input from the perigeniculate nucleus to the A-laminae of the lateral geniculate nucleus in cats. J. Comp. Neurol. 1991, 310:316-336.
11. Deschênes M., Bourassa J., Pinault D. Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res. 1994, 664:215-219.
12. Feig S., Harting J.K. Corticocortical communication via the thalamus: ultrastructural studies of corticothalamic projections from area 17 to the lateral posterior nucleus of the cat and inferior pulvinar nucleus of the owl monkey. J. Comp. Neurol. 1998, 395:281-295.
13. Guillery R.W. The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Z. Zellforsch Mikrosk Anat. 1969, 96:1-38.
14. Guillery R.W. Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J. Anat. 1995, 187:583-592.
15. Guillery R.W., Feig S.L., Van Lieshout D.P. Connections of higher order visual relays in the thalamus: a study of corticothalamic pathways in cats. J. Comp. Neurol. 2001, 438:66-85.
16. Hazama M., Kimura A., Donishi T., Sakoda T., Tamai Y. Topography of corticothalamic projections from the auditory cortex of the rat. Neuroscience 2004, 12:655-667.
17. Hoogland P.V., Welker E., Van der Loos H. Organization of the projections from barrel cortex to thalamus in mice studied with Phaseolus vulgaris-leucoagglutinin and HRP. Exp. Brain Res. 1987, 68:73-87.
18. Hoogland P.V., Wouterlood F.G., Welker E., Van der Loos H. 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. 1991, 87:159-172.
19. Hu B., Senatorov V., Mooney D. Lemniscal and non-lemniscal synaptic transmission in rat auditory thalamus. J. Physiol. 1994, 479:217-231.
20. Huppé-Gourgues F., Bickford M.E., Boire D., Ptito M., Casanova C. Distribution, morphology, and synaptic targets of corticothalamic terminals in the cat lateral posterior-pulvinar complex that originate from the posteromedial lateral suprasylvian cortex. J. Comp. Neurol. 2006, 497:847-863.
21. Jones E.G. The Thalamus 2007, Cambridge University Press, Cambridge. second ed.
22. Jones E.G., Powell T.P. Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat. Proc. R. Soc. Lond. B Biol. Sci. 1969, 172:153-171.
23. Jones E.G., Powell T.P. An electron microscopic study of the mode of termination of cortico-thalamic fibres within the sensory relay nuclei of the thalamus. Proc. R. Soc. Lond. B Biol. Sci. 1969, 172:173-185.
24. Kakei S., Na J., Shinoda Y. Thalamic terminal morphology and distribution of single corticothalamic axons originating from layers 5 and 6 of the cat motor cortex. J. Comp. Neurol. 2001, 437:170-185.
25. Kelly J.P., Wong D. Laminar connections of the cat's auditory cortex. Brain Res. 1981, 212:1-15.
26. Kimura A., Donishi T., Okamoto K., Tamai Y. Topography of projections from the primary and non-primary auditory cortical areas to the medial geniculate body and thalamic reticular nucleus in the rat. Neuroscience 2005, 135:1325-1342.
27. Kudo M., Niimi K. Ascending projections of the inferior colliculus in the cat: an autoradiographic study. J. Comp. Neurol. 1980, 191:545-556.
28. Kuroda M., Sugiura T., Shinkai M., Murakami K., Oda S., Kishi K. Synaptic organization and prefrontal corticothalamic termination in the mediodorsal thalamic nucleus of the cat. J. Hirnforsch. 1993, 34:417-430.
29. Li J., Guido W., Bickford M.E. Two distinct types of corticothalamic EPSPs and their contribution to short-term synaptic plasticity. J. Neurophysiol. 2003, 290:3429-3440.
30. Li J., Wang S., Bickford M.E. Comparison of the ultrastructure of cortical and retinal terminals in the rat dorsal lateral geniculate and lateral posterior nuclei. J. Comp. Neurol. 2003, 460:394-409.
31. Liu X.B., Warren R.A., Jones E.G. Synaptic distribution of afferents from reticular nucleus in ventroposterior nucleus of cat thalamus. J. Comp. Neurol. 1995, 352:187-202.
32. Llano D.A., Sherman S.M. Evidence for nonreciprocal organization of the mouse auditory thalamocortical-corticothalamic projection systems. J. Comp. Neurol. 2008, 507:1209-1227.
33. 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 1981, 6:2561-2577.
34. Montero V.M. Ultrastructural identification of axon terminals from the thalamic reticular nucleus in the medial geniculate nucleus in the rat: an EM autoradiographic study. Exp. Brain Res. 1983, 51:338-342.
35. Ogren M.P., Hendrickson A.E. The morphology and distribution of striate cortex terminals in the inferior and lateral subdivisions of the Macaca monkey pulvinar. J. Comp. Neurol. 1979, 188:179-199.
36. Ohyama J., Ojima H. Labeling of pyramidal and nonpyramidal neurons with lectin Vicia villosa during postnatal development of the guinea pig. J. Comp. Neurol. 1997, 389:453-468.
37. Ojima H. Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. Cereb. Cortex 1994, 4:646-663.
38. Ojima H., Honda C.N., Jones E.G. Characteristics of intracellularly injected infragranular pyramidal neurons in cat primary auditory cortex. Cereb. Cortex 1992, 2:197-216.
39. Ojima H., Murakami K. Intracellular characterization of suppressive responses in supragranular pyramidal neurons of cat primary auditory cortex in vivo. Cereb. Cortex 2002, 12:1079-1091.
40. Ojima H., Murakami K., Kishi K. Dual termination modes of corticothalamic fibers originating from pyramids of layers 5 and 6 in cat visual cortical area 17. Neurosci. Lett. 1996, 208:57-60.
41. Ojima H., Taoka M., Iriki A. Adaptive changes in firing of primary auditory cortical neurons following illumination shift from light to dark in freely moving guinea pigs. Cereb. Cortex 2010, 20:339-351.
42. Peruzzi D., Bartlett E., Smith P.H., Oliver D.L. A monosynaptic GABAergic input from the inferior colliculus to the medial geniculate body in rat. J. Neurosci. 1997, 17:3766-3777.
43. Robson J.A., Hall W.C. The organization of the pulvinar in the grey squirrel (Sciurus carolinensis). II. Synaptic organization and comparisons with the dorsal lateral geniculate nucleus. J. Comp. Neurol. 1977, 173:389-416.
44. Rockland K.S. Further evidence for two types of corticopulvinar neurons. Neuroreport 1994, 5:1865-1868.
45. Rouiller E.M., Durif C. The dual pattern of corticothalamic projection of the primary auditory cortex in macaque monkey. Neurosci. Lett. 2004, 358:49-52.
46. Rouiller E.M., Liang F.Y., Moret V., Wiesendanger M. Patterns of corticothalamic terminations following injection of Phaseolus vulgaris leucoagglutinin (PHA-L) in the sensorimotor cortex of the rat. Neurosci. Lett. 1991, 125:93-97.
47. Rouiller E.M., de Ribaupierre F. Arborization of corticothalamic axons in the auditory thalamus of the cat: a PHA-L tracing study. Neurosci. Lett. 1990, 108:29-35.
48. Rouiller E.M., Tanné J., Moret V., Kermadi I., Boussaoud D., Welker E. Dual morphology and topography of the corticothalamic terminals originating from the primary, supplementary motor, and dorsal premotor cortical areas in macaque monkeys. J. Comp. Neurol. 1998, 396:169-185.
49. Rouiller E.M., Welker E. Morphology of corticothalamic terminals arising from the auditory cortex of the rat: a Phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study. Hear. Res. 1991, 56:179-190.
50. Rouiller E.M., Welker E. A comparative analysis of the morphology of corticothalamic projections in mammals. Brain Res. Bull. 2000, 53:727-741.
51. Saint Marie R.L., Stanforth D.A., Jubelier E.M. Substrate for rapid feedforward inhibition of the auditory forebrain. Brain Res. 1997, 765:173-176.
52. Schwartz M.L., Dekker J.J., Goldman-Rakic P.S. Dual mode of corticothalamic synaptic termination in the mediodorsal nucleus of the rhesus monkey. J. Comp. Neurol. 1991, 309:289-304.
53. Sherman S.M., Guillery R.W. Exploring the Thalamus 2006, Academic Press, New York.
54. Smith P.H., Bartlett E.L., Kowalkowski A. Cortical and collicular inputs to cells in the rat paralaminar thalamic nuclei adjacent to the medial geniculate body. J. Neurophysiol. 2007, 98:681-695.
55. Szentágothai J. The structure of the synapse in the lateral geniculate body. Acta Anat. (Basel) 1963, 55:166-185.
56. Takayanagi M., Ojima H. Microtopography of the dual corticothalamic projections originating from domains along the frequency axis of the cat primary auditory cortex. Neuroscience 2006, 142:769-780.
57. Thompson G.C., Cortez A.M., Lam D.M. Localization of GABA immunoreactivity in the auditory brainstem of guinea pigs. Brain Res. 1985, 339:119-122.
58. Van Horn S.C., Sherman S.M. Differences in projection patterns between large and small corticothalamic terminals. J. Comp. Neurol. 2004, 475:406-415.
59. Vidnyánszky Z., Borostyánkõi Z., Görcs T.J., Hámori J. Light and electron microscopic analysis of synaptic input from cortical area 17 to the lateral posterior nucleus in cats. Exp. Brain Res. 1996, 109:63-70.
60. Veinante P., Lavallée P., Deschênes M. Corticothalamic projections from layer 5 of the vibrissal barrel cortex in the rat. J. Comp. Neurol. 2000, 424:197-204.
61. Wanaverbecq N., Bodor A.L., Bokor H., Slézia A., Lüthi A., Acsády L. Contrasting the functional properties of GABAergic axon terminals with single and multiple synapses in the thalamus. J. Neurosci. 2008, 28:11848-11861.
62. Winer J.A., Diehl J.J., Larue D.T. Projections of auditory cortex to the medial geniculate body of the cat. J. Comp. Neurol. 2001, 430:27-55.
63. Winer J.A., Larue D.T. Anatomy of glutamic acid decarboxylase immunoreactive neurons and axons in the rat medial geniculate body. J. Comp. Neurol. 1988, 278:47-68.
64. Winer J.A., Larue D.T. Evolution of GABAergic circuitry in the mammalian medial geniculate body. Proc. Natl. Acad. Sci. U S A 1996, 93:3083-3087.
65. Winer J.A., Larue D.T., Diehl J.J., Hefti B.J. Auditory cortical projections to the cat inferior colliculus. J. Comp. Neurol. 1998, 400:147-174.
66. Winer J.A., Larue D.T., Huang C. 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.
67. Winer J.A., Saint Marie R.L., Larue D.T., Oliver D.L. GABAergic feedforward projections from the inferior colliculus to the medial geniculate body. Proc. Natl. Acad. Sci. U S A 1996, 93:8005-8010.
68. Zikopoulos B., Barbas H. Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. J. Neurosci. 2006, 26:7348-7361.