Morphologically mixed chemical-electrical synapses formed by primary afferents in rodent vestibular nuclei as revealed by immunofluorescence detection of connexin36 and vesicular glutamate transporter-1

Neuroscience

Volumn 252, Issue , 2013, Pages 468-488

  Nagy, J I ^a   Bautista, W ^a   Blakley, B ^b   Rash, J E ^c  

^a UNIVERSITY OF MANITOBA   (Canada)

^b HEALTH SCIENCES CENTRE   (Canada)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Electrical synapses; Neuronal gap junctions; Vesicular glutamate transporter 1

Indexed keywords

CONNEXIN 36; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELL SIZE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CHEMICAL SYNAPSE; CONTROLLED STUDY; ELECTRICAL SYNAPSE; ELECTROPHYSIOLOGY; IMMUNOFLUORESCENCE; MOUSE; MUSCLE SPINDLE AFFERENT NERVE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; VESTIBULAR NUCLEUS;

CENTRAL NERVOUS SYSTEM; CNS; CONNEXIN36; CX36; DLVN; DORSOCAUDAL PORTION OF THE LVN; ELECTRICAL SYNAPSES; IGG; IMMUNOGLOBULIN G; KNOCKOUT; KO; LATERAL VESTIBULAR NUCLEUS; LVN; MEDIAL VESTIBULAR NUCLEUS; MEDIAL VESTIBULAR NUCLEUS MAGNOCELLULAR PART; MEDIAL VESTIBULAR NUCLEUS PARVICELLULAR PART; MVN; MVNMC; MVNPC; NEURONAL GAP JUNCTIONS; SEM; SPINAL VESTIBULAR NUCLEUS; SPVN; STANDARD ERROR OF MEAN; SUPERIOR VESTIBULAR NUCLEUS; SUVN; TBS CONTAINING 0.3% TRITON X-100; TBSTR; VESICULAR GLUTAMATE TRANSPORTER-1; VGLUT-1;

ANIMALS; CONNEXINS; FLUORESCENT ANTIBODY TECHNIQUE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NEUROGENESIS; NEURONS, AFFERENT; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESTIBULAR NUCLEI;

EID: 84885051177     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.07.056     Document Type: Article

References (81)

1. Arabshahi A., Giaume C., Peusner K.D. Lack of biocytin transfer at gap junctions in the chicken vestibular nuclei. Int J Dev Neurosci 1997, 15:343-352.
2. Babalian A.L., Shapovalov A.I. Mode of synaptic transmission between vestibular afferents and neurons of the vestibular nucleus in the frog. Brain Res 1984, 309:163-167.
3. Barmack N.H. Central vestibular system: vestibular nuclei and posterior cerebellum. Brain Res Bull 2003, 60:511-541.
4. Bautista W., Nagy J.I., Dai Y., McCrea D.A. Requirement of neuronal connexin36 in processes mediating presynaptic inhibition of low threshold afferents in functionally mature motor systems of mouse spinal cord. J Physiol 2012, 590:3821-3839.
5. Bautista W, McCrea DA, Nagy JI (2013) Connexin36 forms purely electrical synapses in sexually dimorphic lumbosacral motor nuclei in spinal cord of developing and adult rat and mouse. Submitted.
6. Bennett M.V.L., Pappas G., Gimenez M., Nakajima Y. Physiology and ultrastructure of electrotonic junctions - IV. Medullary electromotor nuclei in gymnotid fish. J Neurophysiol 1967, 30:236-300.
7. Bennett M.V.L. A comparison of electrically and chemically mediated transmission. Structure and function of synapses 1972, 221-256. Raven, NY. G.D. Pappas, D.P. Purpura (Eds.).
8. Bennett M.V.L. Flexibility and rigidity in electrotonically coupled systems. Synaptic transmission and neuronal interaction 1974, 153-178. Raven, NY. M.V.L. Bennett (Ed.).
9. Bennett MVL (1977) Electrical transmission: a functional analysis and comparison with chemical transmission. In Cellular Biology of Neurons, vol I, sec. I, The Handbook of Physiology - The Nervous System I (Kandel ER, ed), Williams and Wilkins, Baltimore, pp 357-416.
10. Bennett M.V.L., Goodenough D.A. Gap junctions, electrotonic coupling, and intercellular communication. Neurosci Res Prog Bull 1978, 16:373-485.
11. Bennett M.V.L. Gap junctions as electrical synapses. J Neurocytol 1997, 26:349-366.
12. Bennett M.V.L. Electrical synapses, a personal perspective (or history). Brain Res Rev 2000, 32:16-29.
13. Bennett M.V.L., Zukin S.R. Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 2004, 41:495-511.
14. Beraneck M., Uno A., Vassias I., Idoux E., De Waele C., Vidal P.-P., Vibert N. Evidence against a role of gap junctions in vestibular compensation. Neurosci Lett 2009, 450:97-101.
15. Brodal A. Neurological anatomy 1981, Oxford University Press, New York. 3rd ed.
16. Bruzzone R., Dermietzel R. Structure and function of gap junctions in the developing brain. Cell Tissue Res 2006, 326:239-248.
17. Clarac F., Vinay L., Cazalets J.-R., Fady J.-C., Jamon M. Role of gravity in the development of posture and locomotion in the neonatal rat. Brain Res Rev 1998, 28:35-43.
18. Condorelli D.F., Parenti R., Spinella F., Salinaro A.T., Belluardo N., Cardile V., Cicirata F. Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur J Neurosci 1998, 10:1202-1208.
19. Condorelli D.F., Belluardo N., Trovato-Salinaro A., Mudo G. Expression of Cx36 in mammalian neurons. Brain Res Rev 2000, 32:72-85.
20. Connors B.W., Long M.A. Electrical synapses in the mammalian brain. Annu Rev Neurosci 2004, 27:393-418.
21. Cowan W.M., Kandel E.R. A brief history of synapses and synaptic transmission. Synapses 2001, 1-88. Johns Hopkins University Press, Baltimore. W.M. Cowan, T.C. Sudhof, C.F. Stevens (Eds.).
22. Curti S., Hoge G., Nagy J.I., Pereda A.E. Synergy between electrical coupling and membrane properties promotes strong synchronization of neurons of the mesencephalic trigeminal nucleus. J Neurosci 2012, 32:4341-4359.
23. Furshpan E.J. Electrical transmission at an excitatory synapse in a vertebrate brain. Science 1964, 144:878-880.
24. Goldberg JM, Wilson VJ, Cullen KE, Angelaki DE, Broussard DM, Buttner-Ennever JA, Fukushima K, Minor LB (2012) In: The Vestibular System; A Sixth Sense. Oxford Univ Press, NY.
25. Hamzei-Sichani F., Davidson K.G.V., Yasumura T., Janssen W.G.M., Wearne S.L., Hof P.R., Traub R.D., Gutierrez R., Ottersen O.P., Rash J.E. Mixed electrical-chemical synapses in adult rat hippocampus are primarily glutamatergic and coupled by connexin-36. Front Neuroanat 2012, 6:1-26.
26. Highstein S.M., Holstein G.R. The anatomy of the vestibular nuclei. Prog Brain Res 2006, 151:157-203.
27. Hinojosa R., Robertson J.D. Ultrastructure of the spoon type synaptic endings in the nucleus vestibularis tangentialis of the chick. J Cell Biol 1967, 34:421-430.
28. Hinojosa R. Synaptic ultrastructure in the tangential nucleus of the goldfish (Carassius auratus). Am J Anat 1973, 137:159-186.
29. Hoge G.J., Davidson K.G.V., Yasumura T., Castillo P.E., Rash J.E., Pereda A. The extent and strength of electrical coupling between inferior olivary neurons is heterogeneous. J Neurophysiol 2010, 105:1089-1101.
30. Hormuzdi S.G., Filippov M.A., Mitropoulon G., Monyer H., Bruzzone R. Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks. Biochem Biophys Acta 2004, 1662:113-137.
31. Howland H.C., Masci J. The phylogenetic allometry of the semicurcular canals of small fishes. Z Morph Tiere 1973, 75:283-296.
32. Imagawa M., Isu N., Sasaki M., Endo K., Ikegami H., Uchino Y. Axonal projections of utricular afferents to the vestibular nuclei and the abducens nucleus in cats. Neurosci Lett 1995, 186:87-90.
33. Imagawa M., Graf W., Sato H., Suwa H., Isu N., Izumi R., Uchino Y. Morphology of single afferents of the saccular macula in cats. Neurosci Lett 1998, 240:127-130.
34. Ito M., Hongo T., Yoshida M., Okada Y., Obata K. Antidromic and transsynaptic activation of Deiters neurons induced from the spinal cord. Jap J Physiol 1964, 14:638-658.
35. Ito M., Hongo T., Okada Y. Vestibular-evoked postsynaptic potentials in Deiters' neurons. Exp Brain Res 1969, 7:214-230.
36. Jones G.M., Spells K.E. A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc R Soc Lond 1963, 157:403-419.
37. Kamasawa N., Furman C.S., Davidson K.G.V., Sampson J.A., Magnie A.R., Gebhardt B.R., Kamasawa M., Yasumura T., Zumbrunnen J.R., Pickard G.E., Nagy J.I., Rash J.E. Abundance and ultrastructural diversity of neuronal gap junctions in the OFF and ON sublaminae of the inner plexiform layer of rat and mouse retina. Neuroscience 2006, 142:1093-1117.
38. Karhunen E. Postnatal development of the lateral vestibular nucleus (Deiters' nucleus) of the rat. Acta OtoLaryngol Suppl 1973, 313:1-87.
39. Korn H., Sotelo C., Crepel F. Electrotonic coupling between neurons in the lateral vestibular nucleus. Exp Brain Res 1973, 16:255-275.
40. Korn H., Sotelo C., Bennett M.V.L. The lateral vestibular nucleus of the toadfish opsanus Tau: ultrastructural and electrophysiological observations with special reference to electrotonic transmission. Neuroscience 1977, 2:851-884.
41. Kriebel M.E., Bennett M.V.L., Waxman S.G., Pappas G.D. Oculomotor neurons in fish: electrotonic coupling and multiple sites of impulse initiation. Science 1969, 166:520-524.
42. Li X., Olson C., Lu S., Kamasawa N., Yasumura T., Rash J.E., Nagy J.I. Neuronal connexin36 association with zonula occludens-1 protein (ZO-1) in mouse brain and interaction with the first PDZ domain of ZO-1. Eur J Neurosci 2004, 19:2132-2146.
43. Li X., Kamasawa N., Ciolofan C., Olson C.O., Lu S., Davidson K.G.V., Yasumura T., Shigemoto R., Rash J.E., Nagy J.I. Connexin45-containing neuronal gap junctions in rodent retina also contain connexin36 in both apposing hemiplaques, forming bi-homotypic gap junctions, with scaffolding contributed by zonula occludens-1. J Neurosci 2008, 28:9769-9789.
44. Mehler W.R., Rubertone J.A. Anatomy of the vestibular nucleus complex. The rat nervous system, Vol 2, Hindbrain and spinal cord 1985, 185-219. Academic Press, San Diego. G. Paxinos (Ed.).
45. Meier C., Dermietzel R. Electrical synapses-gap junctions in the brain. Results Probl Cell Differ 2006, 43:99-128.
46. Mugnaini E., Walberg F., Brodal A. Mode of termination of primary vestibular fibres in the lateral vestibular nucleus. An experimental electron microscopical study in the cat. Exp Brain Res 1967, 4:187-211.
47. Mugnaini E., Walberg F., Hauglie-Hanssen E. Observations on the fine structure of the lateral vestibular nucleus (Deiters' nucleus) in the cat. Exp Brain Res 1967, 4:146-186.
48. Nagy J.I., Dermietzel R. Gap junctions and connexins in the mammalian central nervous system. Advances in molecular and cell biology 2000, vol. 30:323-396. JAI Press Inc, New York.
49. Nagy J.I., Dudek F.E., Rash J.E. Update on connexins and gap junctions in neurons and glia in the mammalian central nervous system. Brain Res Brain Res Rev 2004, 47:191-215.
50. Nagy J.I. Evidence for connexin36 localization at hippocampal mossy fiber terminals suggesting mixed chemical/electrical transmission by granule cells. Brain Res 2012, 1487:107-122.
51. Ostojic S., Brunel N., Hakim V. Synchronization properties of networks of electrically coupled neurons in the presence of noise and heterogeneities. J Comput Neurosci 2009, 26:369-392.
52. Pappas G.D., Bennett M.V.L. Specialized junctions involved in electrical transmission between neurons. Ann N Y Acad Sci 1966, 137:495-508.
53. Pereda A., O'Brian J.O., Nagy J.I., Bukauskas F., Davidson K.G.V., Yasumura T., Rash J.E. Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells. J Neurosci 2003, 23:7489-7503.
54. Pereda A., Rash J.E., Nagy J.I., Bennett M.V.L. Dynamics of electrical transmission at club endings on the Mauthner cells. Brain Res Rev 2004, 47:227-244.
55. Peusner K.D. An ultrastructural study of the development of synaptic endings in the nucleus vestibularis tangentialis of the chick embryo. Neuroscience 1981, 6:2335-2350.
56. Peusner K.D. The development of synapses and "spoon" synaptic terminal space in the tangential vestibular nucleus: a quantitative electron microscopic study. J Comp Neurol 1984, 230:372-385.
57. Peusner K.D. The first developing "mixed" synapses between vestibular sensory neurons mediate glutamate chemical transmission. Neuroscience 1994, 58:99-113.
58. Precht W., Richter A., Ozawa S., Shimazu S. Intracellular study of frog's vestibular neurons in relation to the labyrinth and spinal cord. Exp Brain Res 1974, 19:377-393.
59. Rash J.E., Dillman R.K., Bilhartz B.L., Duffy H.S., Whalen L.R., Yasumura T. Mixed synapses discovered and mapped throughout mammalian spinal cord. Proc Natl Acad Sci U S A 1996, 93:4235-4239.
60. Rash J.E., Staines W.A., Yasumura T., Pate D., Hudson C.S., Stelmack G.L., Nagy J. Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin36 (Cx36) but not Cx32 or Cx43. Proc Natl Acad Sci U S A 2000, 97:7573-7578.
61. Rash J.E., Yasumura T., Dudek F.E., Nagy J.I. Cell-specific expression of connexins, and evidence for restricted gap junctional coupling between glial cells and between neurons. J Neurosci 2001, 21:1983-2000.
62. Rash J.E., Olson C.O., Davidson K.G.V., Yasumura T., Kamasawa N., Nagy J.I. Identification of connexin36 in gap junctions between neurons in rodent locus coeruleus. Neuroscience 2007, 147:938-956.
63. Rash J.E., Olson C.O., Pouliot W.A., Davidson K.G.V., Yasumura T., Furman C.S., Royer S., Kamasawa N., Nagy J.I., Dudek F.E. Connexin36 vs connexin32, "miniature" neuronal gap junctions, and limited electrotonic coupling in rodent suprachiasmatic nucleus. Neuroscience 2007, 149:350-371.
64. Richter A., Precht W., Ozawa S. Responses of neurons of lizard's, lacerta viridis, vestibular nuclei to electrical stimulation of the ipsi and contralateral VIIIth nerves. Pflügers Arch 1975, 355:85-94.
65. Richter K., Langnaese K., Kreutz M.R., Olias G., Zhai R., Scheich H., Garner C.C., Gundelfinger E.D. Presynaptic cytomatrix protein bassoon is localized at both excitatory and inhibitory synapses of rat brain. J Comp Neurol 1999, 408:437-448.
66. Sato F., Sasaki H., Ishizuka N., Sasaki S.-I., Mannen H. Morphology of single primary vestibular afferents originating from the horizontal semicircular canal in the cat. J Comp Neurol 1989, 290:423-439.
67. Shamboul K.M. The lateral vestibular nucleus of the rat, with a note on its dorsal extension into the cerebellum. J Anat 1979, 129:107-116.
68. Shao M., Gottesman-Davis A., Popratiloff A., Peusner K.D. Dye coupling in developing vestibular nuclei. J Neurosci Res 2008, 86:832-844.
69. Söhl G., Degen J., Teubner B., Willecke K. The murine gap junction gene connexin36 is highly expressed in mouse retina and regulated during brain development. FEBS Lett 1998, 428:27-31.
70. Söhl G., Maxeiner S., Willecke K. Expression and functions of neuronal gap junctions. Nat Rev Neurosci 2005, 6:191-200.
71. Sotelo C. Morphological correlates of electrotonic coupling between neurons in mammalian nervous system. Golgi centennial symposium 1975, 355-365. Raven Press, New York. M. Santini (Ed.).
72. Sotelo C., Palay S.L. The fine structure of the lateral vestibular nucleus in the rat. II. Synaptic organization. Brain Res 1970, 18:93-115.
73. Sotelo C., Korn H. Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system. Int Rev Cytol 1978, 5:67-107.
74. Sotelo C. Morphological basis for electrical communication between neurons in the central nervous system of vertebrates. Neuron concept today 1977, 17-26. Akademiai Kiado, Budapest. J. Szentagothai, J. Hamori, E.S. Vizi (Eds.).
75. Sotelo C., Triller A. Morphological correlates of electrical, chemical and dual modes of transmission. Chemical neurotransmission, 75years 1981, 13-28. Academic Press, New York. L. Stjarne, L. Lagercrantz, H. Hedqvist, A. Wennmalm (Eds.).
76. Stefanelli A., Caravita S. Ultrastructural features of the synaptic complex of the vestibular nuclei of Lampetra planeri (Bloch). Z Zellforsch 1970, 108:282-296.
77. Vivar C., Traub R.D., Gutierrez R. Mixed electrical-chemical transmission between hippocampal mossy fibers and pyramidal cells. Eur J Neurosci 2012, 35:76-82.
78. Wilson V.J., Wylie R.M. A short latency labyrintine input to the vestibular nuclei in the pigeon. Science 1970, 168:124-127.
79. Wylie R.M. Evidence of electrotonic transmission in the vestibular nuclei of the rat. Brain Res 1973, 50:179-183.
80. Yang A., Hullar T.E. Relationship of semicircular canal size to vestibular-nerve afferent sensitivity in mammals. J Neurophysiol 2007, 98:3197-3205.
81. Zhang F.X., Pang Y.W., Zhang M.M., Zhang T., Dong Y.L., Lai C.H., Shum D.K.Y., Chan Y.S., Li J.L., Li Y.Q. Expression of vesicular glutamate transporters in peripheral vestibular structures and vestibular nuclear complex of rat. Neuroscience 2011, 173:179-189.