Heterotypic gap junctions at glutamatergic mixed synapses are abundant in goldfish brain

Neuroscience

Volumn 285, Issue , 2015, Pages 166-193

  Rash, J E ^a   Kamasawa, N ^b   Vanderpool, K G ^a   Yasumura, T ^a   O'Brien, J ^c   Nannapaneni, S ^d   Pereda, A E ^d   Nagy, J I ^e  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b MAX PLANCK FLORIDA INSTITUTE FOR NEUROSCIENCE   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Connexin34.7; Connexin35; Freeze fracture replica immunogold labeling (FRIL); Gap junctions; Immunofluorescence microscopy

Indexed keywords

GLUTAMIC ACID; FISH PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN; DEPOLARIZATION; ELECTRICAL SYNAPSE; EVOKED RESPONSE; GAP JUNCTION; GOLDFISH; LARGE MYELINATED CLUB ENDING SYNAPSE; LATENT PERIOD; MAUTHNER CELL; NERVE ENDING; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC POTENTIAL; ANIMAL; AXON; CONFOCAL MICROSCOPY; DENDRITE; ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; METABOLISM; SYNAPSE;

ANIMALS; AXONS; BRAIN; DENDRITES; FISH PROTEINS; GAP JUNCTIONS; GLUTAMIC ACID; GOLDFISH; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; SYNAPSES;

EID: 84919480681     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.10.057     Document Type: Article

References (113)

1. Amores A., Force A., Yan Y.L., Joly L., Amemiya C., Fritz A., Ho R.K., Langeland J., Prince V., Wang Y.L., Westerfield M., Postlethwait J.H. Zebrafish hox clusters and vertebrate genome evolution. Science 1998, 282:1711-1714.
2. Apostolides P.F., Trussell L.O. Regulation of interneuron excitability by gap junction coupling with principal cells. Nat Neurosci 2013, 16:1764-1772.
3. Arai I., Tanaka M., Tachibana M. Active roles of electrically coupled bipolar cell network in the adult retina. J Neurosci 2010, 30:9260-9270.
4. Auerbach A.A., Bennett M.V.L. A rectifying electrotonic synapse in the central nervous system of a vertebrate. J Gen Phys 1969, 53:211-237.
5. Baker R., Llinás R. Electrotonic coupling between neurones in the rat mesencephalic nucleus. J Physiol 1971, 212:45-63.
6. Bartelmez G.W. Mauthner's cell and the nucleus motorius tegmenti. J Comp Neurol 1915, 25:87-128.
7. Bautista W., McCrea D.A., Nagy J.I. Connexin36 identified at morphologically mixed chemical/electrical synapses on trigeminal motoneurons and at primary afferent terminals on spinal cord neurons in adult mouse and rat. Neuroscience 2014, 263:159-180.
8. Bennett M.V., Pappas G.D., Gimenez M., Nakajima Y. Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish. J Neurophysiol 1967, 30:236-300.
9. Bennett M.V.L., Aljure E., Nakajima Y., Pappas G.D. Electrotonic junctions between teleost spinal neurons: electrophysiology and ultrastructure. Science 1963, 141:262-264.
10. Bennett M.V.L., Goodenough D.A. Gap junctions, electrotonic coupling and intercellular communication. Neurosci Res Prog Bull 1978, 16:373-486.
11. Bennett M.V.L., Pappas G.D., Aljure E., Nakajima Y. Physiology and ultrastructure of electrotonic junctions. II. Spinal and medullary electromotor nuclei in mormyrid fish. J Neurophysiol 1967, 30:180-208.
12. Bennett M.V.L., Sandri C., Akert K. Neuronal gap junctions and morphologically mixed synapses in the spinal cord of a teleost, Sternarchus albifrons (gymnotoidei). Brain Res 1978, 143:43-60.
13. Bennett M.V.L., Zukin R.S. Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 2004, 41:495-511.
14. Bennett M.V., Nakajima Y., Pappas G.D. Physiology and ultrastructure of electrotonic junctions. I. Supramedullary neurons. J Neurophysiol 1967, 30:1-179.
15. Bodian D. The structure of the vertebrate synapse. A study of the axon endings on Mauthner's cell and neighboring centers in the goldfish. J Comp Neurol 1937, 68:117-160.
16. Branton D., Bullivant S., Gilula N.B., Karnovsky M.J., Moor H., Northcote D.H., Packer L., Satir B., Satir P., Speth V., Staehelin L.A., Steere R.L., Weinstein R.S. Freeze-etching nomenclature. Science 1975, 190:54-56.
17. Carr C.E., Maler L., Taylor B. A time-comparison circuit in the electric fish midbrain. II. Functional morphology. J Neurosci 1986, 6:1372-1383.
18. Castello M.E., Caputi A., Trujillo Cenóz O. Structural and functional aspects of the fast electrosensory pathway in the electrosensory lateral line lobe of the pulse fish Gymnotus carapo. J Comp Neurol 1998, 401:549-563.
19. Castelló M.E., Caputi A., Trujillo-Cenóz O. Structural and functional aspects of the fast electrosensory pathway in the electrosensory lateral line lobe of the pulse fish Gymnotus carapo. J Comp Neurol 1998, 401:549-563.
20. Chandler D.E., Heuser J. Membrane fusion during secretion: cortical granule exocytosis in sea urchin eggs as studied by quick-freezing and freeze-fracture. J Cell Biol 1979, 83:91-108.
21. Christie J.M., Jelinek H.F. Dye-coupling among neurons of the rat locus coeruleus during postnatal development. Neuroscience 1993, 56:129-137.
22. Ciolofan C., Li X., Olson C., Kamasawa N., Yasumura T., Morita M., Rash J.E., Nagy J.I. Association of connexin36 and ZO-1 with ZO-2 and the MsY3 transcription factor ZO-1 associated nucleic acid-binding protein (ZONAB) in mouse retina. Neuroscience 2006, 140:433-451.
23. Cohen S.A., Pumplin D.W. Clusters of intramembrane particles associated with binding sites for alpha-bungarotoxin in cultured chick myotubes. J Cell Biol 1979, 82:494-516.
24. 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.
25. Connors B.W., Long M.A. Electrical synapses in the mammalian brain. Ann Rev Neurosci 2004, 27:393-418.
26. Diamond J., Huxley A.F. The activation and distribution of GABA and l-glutamate receptors on goldfish Mauthner neurones: an analysis of dendritic remote inhibition. J Physiol 1968, 194:669-723.
27. Dinchuk J.E., Johnson T.J.A., Rash J.E. Postreplication labeling of E-leaflet molecules: membrane immunoglobulins localized in sectioned labeled replicas examined by TEM and HVEM. J Electron Microsc Tech 1987, 7:1-16.
28. Eastman S.D., Chen T.H.P., Falk M.M., Mendelson T.C., Iovine M. Phylogenetic analysis of three complete gap junction gene families reveals lineage-specific duplications and highly supported gene classes. Genomics 2006, 87:265-274.
29. Eaton R.C., Farley R.D., Kimmel C.B., Schabtach E. Functional development in the Mauthner cell system of embryos and larvae of the zebra fish. J Neurobiol 1977, 8:151-172.
30. Flores C.E., Nannapaneni S., Davidson K.G.V., Yasumura T., Bennett M.V.L., Rash J.E., Pereda A.E. Trafficking of gap junction channels at a vertebrate electrical synapse in vivo. Proc Natl Acad Sci U S A 2012, 109:E573-E582.
31. Fujimoto K. Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J Cell Sci 1995, 108:3443-3449.
32. Fujimoto K. SDS-digested freeze-fracture replica labeling electron microscopy to study the two-dimensional distribution of integral membrane proteins and phospholipids in biomembranes: practical procedure, interpretation and application. Histochem Cell Biol 1997, 107:87-96.
33. Fukuda T., Kosaka T. Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J Neurosci 2000, 20:1519-1528.
34. Fukuda T., Kosaka T., Singer W., Galuske R.A.W. Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network. J Neurosci 2006, 26:3434-3443.
35. Fukuda T., Kosaka T. The dual network of GABAergic interneurons linked by both chemical and electrical synapses: a possible infrastructure of the cerebral cortex. Neurosci Res 2000, 38:123-130.
36. Furshpan E.J. "Electrical transmission" at an excitatory synapse in a vertebrate brain. Science 1964, 144:878-880.
37. Hackett J.T., Buchheim A. Ultrastructural correlates of electrical chemical synaptic transmission in goldfish cranial motor nuclei. J Comp Neurol 1984, 224:425-436.
38. Haggis G.H. Electron microscope replicas from the surface of a fracture through frozen cells. J Biophys Biochem Cytol 1961, 9:841-852.
39. 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.
40. Hanneman E., Trevarrow B., Metcalfe W.K., Kimmel C.B., Westerfield M. Segmental pattern of development of the hindbrain and spinal cord of the zebrafish embryo. Development 1988, 103:49-58.
41. Harris K.M., Landis D.M.D. Membrane structure at synaptic junctions in area CA1 of the rat hippocampus. Neuroscience 1986, 19:857-872.
42. Hoge G., Davidson K.G., Yasumura T., Castillo P.E., Rash J.E., Pereda A.E. The extent and strength of electrical coupling between inferior olivary neurons is heterogeneous. J Neurophysiol 2011, 105:1089-1101.
43. Ito H. Fine structure of the torus semicircularis of some teleosts. J Morph 1974, 142:137-152.
44. Kamasawa N., Furman C.S., Davidson K.G.V., Sampson J.A., Magnie A.R., Gebhardt B., Kamasawa M., Morita M., Yasumura T., Pieper M., 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.
45. A receptor subunits on hippocampal pyramidal cells by freeze-fracture replica immunolabelling. Eur J Neurosci 2010, 32:1868-1888.
46. Katsumaru H., Kosaka T., Heizmann C.W., Hama K. Gap junctions on GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region). Exp Brain Res 1988, 72:363-370.
47. 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.
48. Korn H., Sotelo C., Crepel F. Electrotonic coupling between neurons in rat lateral vestibular nucleus. Exp Brain Res 1973, 16:255-275.
49. Kosaka T. Gap junctions between non-pyramidal cell dendrites in the rat hippocampus (CA1 and CA3 regions). Brain Res 1983, 271:157-161.
50. Kosaka T., Hama K. Gap junctions between non-pyramidal cell dendrites in the rat hippocampus (CA1 and CA3 regions): a combined golgi-electron microscopy study. J Comp Neurol 1985, 231:150-161.
51. Kosaka T., Hama K. Structure of the mitral cell in the olfactory bulb of the goldfish (Carassius auratus). J Comp Neurol 1982, 212:365-384.
52. Kosaka T., Kosaka K. Neuronal gap junctions between intraglomerular mitral/tufted cell dendrites in the mouse main olfactory bulb. Neurosci Res 2004, 49:373-378.
53. Kosaka T., Kosaka K. Intraglomerular dendritic link connected by gap junctions and chemical synapses in the mouse main olfactory bulb: electron microscopic serial section analyses. Neuroscience 2005, 131:611-625.
54. Kothmann W.W., Li X., Burr G.S., O'Brien J. Connexin 35/36 is phosphorylated at regulatory sites in the retina. J Neurosci 2007, 24:363-375.
55. Kothmann W.W., Trexler E.B., Whitaker C.M., Li W., Massey S.C., O'Brien J. Nonsynaptic NMDA receptors mediate activity-dependent plasticity of gap junctional coupling in the AII amacrine cell network. J Neurosci 2012, 32:6747-6759.
56. 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.
57. Kurz-Isler G., Wolburg H. Gap junctions between horizontal cells in the cyprinid fish alter rapidly their structure during light and dark adaptation. Neurosci Lett 1986, 67:7-12.
58. Landis D.M.D., Reese T.S. Differences in membrane structure between excitatory and inhibitory synapses in the cerebellar cortex. J Comp Neurol 1974, 155:93-126.
59. Landis D.M.D., Reese T.S., Raviola E. Differences in membrane structure between excitatory and inhibitory components of the reciprocal synapse in the olfactory bulb. J Comp Neurol 1974, 155:67-92.
60. Lee R.K.K., Eaton R.C., Zottoli S.J. Segmental arrangement of reticulospinal neurons in the goldfish hindbrain. J Comp Neurol 1993, 329:539-556.
61. Lefler Y., Yarom Y., Uusisaari M.Y. Cerebellar inhibitory input to the inferior olive decreases electrical coupling and blocks subthreshold oscillations. Neuron 2014, 81:1389-1400.
62. Legendre P. The glycinergic inhibitory synapse. Cell Mol Life Sci CMLS 2001, 58:760-793.
63. 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.
64. Li X., Lynn B.D., Nagy J.I. The effector and scaffolding proteins AF6 and MUPP1 interact with connexin36 and localize at gap junctions that form electrical synapses in rodent brain. Eur J Neurosci 2012, 35:166-181.
65. 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.
66. Lin J.W., Faber D.S. Synaptic transmission mediated by single Club Endings on the goldfish Mauthner cell. I. Characteristics of electrotonic and chemical postsynaptic potentials. J Neurosci 1988, 8:1302-1312.
67. Lynn B.D., Li X., Nagy J.I. Under construction: building the macromolecular superstructure and signaling components of an electrical synapse. J Membr Biol 2012, 245:303-317.
68. Maler L., Sas E.K.B., Rogers J. The cytology of the posterior lateral line lobe of high-frequency weakly electric fish (gymnotidae): dendritic differentiation and synaptic specificity in a simple cortex. J Comp Neurol 1981, 195:87-139.
69. Marc R.E., Liu W.L., Muller J.F. Gap junctions in the inner plexiform layer of the goldfish retina. Vision Res 1988, 28:9-24.
70. Masugi-Tokita M., Shigemoto R. High-resolution quantitative visualization of glutamate and GABA receptors at central synapses. Cur Opin Neurobiol 2007, 17:387-393.
71. Mathieson W.B., Heiligenberg W., Maler L. Ultrastructural studies of physiologically identified electrosensory afferent synapses in the gymnotiform fish, Eigenmannia. J Comp Neurol 1987, 255:526-537.
72. McLysaght A., Hokamp K., Wolfe K.H. Extensive genomic duplication during early chordate evolution. Nat Genet 2002, 31:200-204.
73. Metcalfe W.K., Mendelson B., Kimmel C.B. Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva. J Comp Neurol 1986, 251:147-159.
74. 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.
75. Nagy J.I., Bautista W., Blakley B., Rash J.E. 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 2013, 252:468-488.
76. Naka K.I., Christensen B.N. Direct electrical connections between transient amacrine cells in the catfish retina. Science 1981, 214:462-464.
77. Nakajima Y., Tuttle R., Masuko S., Betz H., Pfeiffer F. Synapses on the Mauthner cell of the goldfish: thin section, freeze-fracture, and immunocytochemical studies. J Electron Microsc Tech 1987, 6:143-153.
78. O'Brien J., Al-Ubaidi M.R., Ripps H. Connexin35: a gap junctional protein expressed preferentially in the skate retina. Mol Biol Cell 1996, 7:233-243.
79. O'Brien J., Bruzzone R., White T.W., Al-Ubaidi M.R., Ripps H. Cloning and expression of two related connexins from the perch retina define distinct subgroups of the connexin family. J Neurosci 1998, 18:7625-7637.
80. O'Brien J., Nguyen H.B., Mills S.L. Cone photoreceptors in bass retina use two connexins to mediate electrical coupling. J Neurosci 2004, 24:5632-5642.
81. Oh S., Rubin J.B., Bennett M.V.L., Verselis V.K., Bargiello T.A. Molecular determinants of electrical rectification of single channel conductance in gap junctions formed by connexins 26 and 32. J Gen Physiol 1999, 114:339-364.
82. Palacios-Prado N., Huetteroth W., Pereda A.E. Hemichannel composition and electrical synaptic transmission: molecular diversity and its implications for electrical rectification. Front Cell Neurosci 2014, 8(324):1-13.
83. Pappas G.D., Bennett M.V.L. Specialized junctions involved in electrical transmission between neurons. Ann N Y Acad Sci 1966, 166:495-508.
84. Payton B.W., Bennett M.V.L., Pappas G.D. Permeability and structure of junctional membranes at an electrotonic synapse. Science 1969, 166:1641.
85. Peracchia C. Low resistance junctions in crayfish. I. Two arrays of globules in junctional membranes. J Cell Biol 1973, 57:54-65.
86. Peracchia C. Low resistance junctions in crayfish. II. Structural details and further evidence for intercellular channels by freeze-fracture and negative staining. J Cell Biol 1973, 57:66-76.
87. Pereda A., O'Brien J., Nagy J.I., Bukauskas F., Davidson K.G.V., Kamasawa N., Yasumura T., Rash J.E. Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells. J Neurosci 2003, 23:7489-7503.
88. 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 Brain Res Rev 2004, 47:227-244.
89. Peters A (2014) The fine structure of the aging brain. http://www.bu.edu/agingbrain/chapter-9-synapses/.
90. Peters A., Palay S.L., Webster H.D. The fine structure of the nervous system. Neurons and their supporting cells 1991, Oxford University Press, New York.
91. Pfenninger K., Akert K., Moor H., Sandri C. The fine structure of freeze-fractured presynaptic membranes. J Neurocytol 1972, 1:129-149.
92. Rash J.E., Curti S., Vanderpool K.G., Kamasawa N., Nannapaneni S., Palacios-Prado N., Flores C.E., Yasumura T., O'Brien J., Lynn B.D., Bukauskas F.F., Nagy J.I., Pereda A.E. Molecular and functional asymmetry at a vertebrate electrical synapse. Neuron 2013, 79:957-969.
93. Rash J.E., Davidson K.G.V., Kamasawa N., Yasumura T., Kamasawa M., Zhang C., Michaels R., Restrepo D., Ottersen O.P., Olson C., Nagy J.I. Ultrastructural localization of connexins (Cx36, Cx43, Cx45), glutamate receptors and aquaporin-4 in rodent olfactory mucosa, olfactory nerve and olfactory bulb. J Neurocytol 2005, 34:307-341.
94. 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.
95. Rash JE, Johnson TJA, Dinchuk JE, Giddings FD, Kuenning W (1983) Labeling intramembrane particles and surface markers in freeze-etch replicas. In: Frontiers of Membrane Research in Agriculture (John JB, Berlin E, Jackson PC, eds), pp 7-22. Totowa, NJ: Rowman & Allenheld.
96. Rash J.E., Pereda A., Kamasawa N., Furman C.S., Yasumura T., Davidson K.G.V., Dudek F.E., Olson C., Nagy J.I. High-resolution proteomic mapping in the vertebrate central nervous system: close proximity of connexin35 to NMDA glutamate receptor clusters and co-localization of connexin36 with immunoreactivity for zonula occludens protein-1 (ZO-1). J Neurocytol 2004, 33:131-152.
97. Rash J.E., Pickard G.E., Davidson K.G.V., O'Brien J., Hartwick A.T.E., Kamasawa N., Yasumura T., Nagy J.I. Exposure to dopamine and its D1 receptor antagonist SCH23390 produces large-scale ultrastructural plasticity and changes in phosphorylation of connexin36 in neuronal gap junctions of adult rat retina. Mol Biol Cell 2007, 18. (supplement): Abstract #910.
98. Rash J.E., Yasumura T. Direct immunogold labeling of connexins and aquaporin4 in freeze-fracture replicas of liver, brain and spinal cord: factors limiting quantitative analysis. Cell Tissue Res 1999, 296:307-321.
99. 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, 21:1983-2001.
100. Robertson J.D., Bodenheimer T.S., Stage D.E. The ultrastructure of Mauthner cell synapses and nodes in goldfish brains. J Cell Biol 1963, 19:159-199.
101. Sato Y., Nishida M. Teleost fish with specific genome duplication as unique models of vertebrate evolution. Environ Biol Fish 2010, 88:169-188.
102. Schlörmann W., John M., Steiniger F., Westermann M., Richter W. Improved antigen retrieval in freeze-fracture cytochemistry by evaporation of carbon as first replication layer. Histochem Cell Biol 2007, 127:633-639.
103. Serrano-Vélez J.L., Rodriguez-Alvarado M., Torres-Vázquez I.I., Fraser S.E., Yasumura T., Vanderpool K.G., Rash J.E., Rosa-Molinar E. Abundance of gap junctions at glutamatergic mixed synapses in adult Mosquitofish spinal cord neurons. Front Neural Circuits 2014, 66:1-16. 8 Article.
104. Sotelo C., Korn H. Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system. Intern Rev Cytol 1978, 55:67-107.
105. Steere R.L., Erbe E.F. Supporting freeze-etch specimens with 'Lexan' while dissolving biological remains in acids. Microsc Soc Am Proc 1983, 41:618-619. (Published Abstract).
106. Steere R.L., Rash J.E. Use of double-tilt device (goniometer) to obtain optimum contrast in freeze-fracture replicas. Freeze fracture: Methods, artifacts, and interpretations 1979, 161-167. Raven Press, New York. J.E. Rash, C.S. Hudson (Eds.).
107. Trenholm S., McLaughlin A.J., Schwab D.J., Awatramani G.B. Dynamic tuning of electrical and chemical synaptic transmission in a network of motion coding retinal neurons. J Neurosci 2013, 33:14927-14938.
108. Tuttle R., Masuko S., Nakajima Y. Freeze-fracture study of the large myelinated club ending synapse on the goldfish Mauthner cell: specialized reference to the quantitative analysis of gap junctions. J Comp Neurol 1986, 246:202-211.
109. Uchiyama H., Ito H. Fiber connections and synaptic organization of the preoptic retinopetal nucleus in the filefish (Balistidae, Teleostei). Brain Res 1984, 298:11-24.
110. Witkovsky P., Shakib M., Ripps H. Interreceptoral junctions in the teleost retina. Invest Opthal Vis Sci 1974, 13:996-1009.
111. Wolburg H., Rohlmann A. Structure-function relationships in gap junctions. Intern Rev Cytol 1995, 157:315-373.
112. Yao C., Vanderpool K.G., Delfiner M., Eddy V., Lucaci A., Soto-Riveros C., Yasumura T., Rash J., Pereda A.E. Electrical synaptic transmission in developing zebrafish: properties and molecular composition of gap junctions at a central auditory synapse. J Neurophysiol 2014, 112:2102-2113. 10.1152/jn.00397.2014.
113. Zupanc G.K.H. Clustering of cell bodies, bundling of dendrites, and gap junctions: morphological substrate for electrical coupling in the prepacemaker nucleus. Neurosci Let 1991, 129:29-34.