Voltage-Dependent Enhancement of Electrical Coupling by a Subthreshold Sodium Current

Journal of Neuroscience

Volumn 24, Issue 16, 2004, Pages 3999-4010

  Curti, Sebastián ^a   Pereda, Alberto E ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Auditory; Electrical synapse; Gap junctions; Mauthner; Persistent sodium current; Synaptic plasticity; Synchronization

Indexed keywords

4 AMINOPYRIDINE; LIDOCAINE ETHOBROMIDE; SODIUM ION; TETRODOTOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GAP JUNCTION; GOLDFISH; MEMBRANE CONDUCTANCE; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SODIUM CURRENT; SYNAPSE;

ANIMALS; AUDITORY PATHWAYS; ESCAPE REACTION; EVOKED POTENTIALS; GOLDFISH; LIDOCAINE; MODELS, NEUROLOGICAL; NEURONS; POTASSIUM CHANNEL BLOCKERS; PRESYNAPTIC TERMINALS; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SYNAPTIC TRANSMISSION; TETRODOTOXIN; VESTIBULOCOCHLEAR NERVE;

EID: 2142815760     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0077-04.2004     Document Type: Article

References (65)

1. Auerbach AA, Bennett MVL (1969) A rectifying synapse in the central nervous system of a vertebrate. J Gen Physiol 53:183-210.
2. Barrio L, Schuyna T, Bargiello TA, Xian Hu L, Roginski R, Bennett MVL, Nicholson B (1991) Gap junctions formed by connexin 26 and 32 alone and in combination are differently affected by applied voltage. Proc Natl Acad Sci USA 88:8410-8414.
3. Bartelmez GW (1915) Mauthner's cell and the nucleus motorius tegmenti. J Comp Neurol 25:87-128.
4. Bennett MVL (1966) Physiology of electrotonic junctions. Ann NY Acad Sci 137:509-539.
5. Bennett MVL (1977) Electrical transmission: a functional analysis and comparison with chemical transmission. In: Cellular biology of neurons, Vol 1, Handbook of physiology. The nervous system (Kandel ER, ed) pp 357-416. Baltimore: Williams & Wilkins.
6. Bennett MVL, Verselis VK (1992) Biophysics of gap junctions. Semin Cell Biol 3:29-47.
7. Berman N, Dunn RJ, Maler L (2001) Function of NMDA receptors and persistent sodium channels in a feedback pathway of the electrosensory system. J Neurophysiol 86:1612-1621.
8. Bowe CM, Kocsis JD, Waxman SG (1985) Differences between mammalian ventral and dorsal spinal roots in response to blockade of potassium channels during maturation. Proc R Soc Lond B Biol Sci 224:355-366.
9. Bukauskas FF, Angele AB, Verselis VK, Bennett MV (2002) Coupling asymmetry of heterotypic connexin 45/connexin 43-EGFP gap junctions: properties of fast and slow gating mechanisms. Proc Natl Acad Sci USA 99:7113-7118.
10. Condorelli DF, Parenti R, Spinella F, Trovato Salinaro A, Belluardo N, Cardile V, Cicirata F (1998) Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur J Neurosci 10:1202-1208.
11. Crill WE (1996) Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58:349-362.
12. Curti S, Bennett MVL, Pereda A (2004) Co-activation of afferents facilitates transmitter release at mixed synapses on the Mauthner (M-) cell. Soc Neurosci Abstr, in press.
13. DeVries SH, Qi X, Smith R, Makous W, Sterling P (2002) Electrical coupling between mammalian cones. Curr Biol 12:1900-1907.
14. De Zeeuw CI, Hertzberg EL, Mugnaini E (1995) The dendritic lamellar body: a new neuronal organelle putatively associated with dendroden-dritic gap junctions. J Neurosci 5:1587-1604.
15. + current modifies burst discharge by regulating conditional backpropagation of dendritic spikes. J Neurophysiol 89:324-337.
16. Eaton RC, Lee RK, Foreman MB (2001) The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog Neurobiol 63:467-485.
17. Edwards DH, Heitler WJ, Leise EM, Fricke RA (1991) Postsynaptic modulation of rectifying electrical synaptic inputs to the LG escape command neuron in crayfish. J Neurosci 11:2117-2129.
18. el Manira A, Cattaert D, Wallen P, DiCaprio RA, Clarac F (1993) Electrical coupling of mechanoreceptor afferents in the crayfish: a possible mechanism for enhancement of sensory signal transmission. J Neurophysiol 69:2248-2251.
19. Faber DS, Korn H (1986) Instantaneous inward rectification in the Mauthner cell: a postsynaptic booster for excitatory inputs. Neuroscience 19:1037-1043.
20. Frank K, Fuortes MGF (1956) Stimulation of spinal motoneurones with intracellular electrodes. J Physiol (Lond) 134:451-470.
21. French CR, Gage PW (1985) A threshold sodium current in pyramidal cells in rat hippocampus. Neurosci Lett 56:289-293.
22. French CR, Sah P, Buckett KJ, Gage PW (1990) A voltage-dependent persistent sodium current in mammalian hippocampal neurons. J Gen Physiol 95:1139-1157.
23. Fukami Y, Furukawa T, Asada Y (1964) Excitability changes of the Mauthner cell during collateral inhibition. J Gen Physiol 48:581-600.
24. Fukuda T, Kosaka T (2000) Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J Neurosci 20:1519-1528.
25. Fukuda T, Kosaka T (2003) Ultrastructural study of gap junctions between dendrites of parvalbumin-containing GABAergic neurons in various neocortical areas of the adult rat. Neuroscience 120:5-20.
26. Furshpan EJ (1964) Electrical transmission at an excitatory synapse in a vertebrate brain. Science 144:878-880.
27. Furshpan EJ, Potter DD (1959) Transmission at the giant motor synapses of the crayfish. J Physiol (Lond) 145:289-325.
28. Giaume C, Korn H (1983) Bi-directional transmission at the rectifying electrotonic synapse: a voltage-dependent process. Science 220:84-87.
29. Herberholz J, Antonsen BL, Edwards DH (2002) A lateral excitatory network in the escape circuit of crayfish. J Neurosci 22:9078-9085.
30. Honmou O, Utzschneider D, Rizzo M, Bowe, C Waxman SG, Kocsis JD (1994) Delayed depolarization and slow sodium currents in cutaneous afferents. J Neurophysiol 71:1627-1637.
31. Hotson JR, Prince DA, Schwartzkroin PA (1979) Anomalous inward rectification in hippocampal neurons. J Neurophysiol 42:889-895.
32. Kandel E, Tauc L (1966) Anomalous rectification in the metacerebral giant cells and its consequence for synaptic transmission. J Physiol (Lond) 183:287-304.
33. Kocsis J, Waxman SG (1983) Long-term regenerated nerve fibers retain sensitivity to potassium channel blocking agents. Nature 304:640-642.
34. Lasater E, Dowling JE (1985) Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proc Natl Acad Sci USA 82:3025-3029.
35. Lin JW, Faber DS (1988) Synaptic transmission mediated by single club endings on the goldfish Mauthner cell. I. Characteristics of electrotonic and chemical postsynaptic potentials. J Neurosci 8:1302-1312.
36. Llinás R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol (Lond) 305:171-195.
37. Llinás R, Baker R, Sotelo C (1974) Electrotonic coupling between neurons in the cat inferior olive. J Neurophysiol 37:560-571.
38. Logan SD, Pickering AE, Gibson IC, Nolan MF, Spanswick D (1996) Electrotonic coupling between rat sympathetic preganglionic neurons in vitro. J Physiol (Lond) 495:491-502.
39. + dependent in CA1 pyramidal neurons. Brain Res 333:378-381.
40. Mann-Metzer P, Yarom Y (1999) Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J Neurosci 19:3298-3306.
41. Nakajima Y (1974) Fine structure of the synaptic endings on the Mauthner cell of the goldfish. J Comp Neurol 156:375-402.
42. O'Brien J, Bruzzone R, White TW, Al-Ubaidi MR, Ripps H (1998) Cloning and expression of two related connexins from the perch retina define a distinct subgroup of the connexin family. J Neurosci 18:7625-7637.
43. + channels. Jpn J Pharmacol 88:365-377.
44. Peinado A, Yuste R, Katz LC (1993) Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 10:103-114.
45. Pereda A, Faber D (1996) Activity-dependent short-term plasticity of intercellular coupling. J Neurosci 16:983-992.
46. Pereda A, Triller A, Korn H, Faber DS (1992) Dopamine enhances both electrotonic coupling and chemical excitatory postsynaptic potentials at mixed synapses. Proc Natl Acad Sci USA 89:12088-12092.
47. Pereda A, Nairn A, Wolzson L, Faber DS (1994) Postsynaptic modulation of synaptic efficacy at mixed synapses on the Mauthner cell. J Neurosci 14:3704-3712.
48. Pereda A, Bell T, Faber DS (1995) Retrograde synaptic communication via gap junctions coupling auditory afferents to the Mauthner cell. J Neurosci 15:5943-5955.
49. 2+/calmodulin-dependent kinase 11 mediates simultaneous enhancement of gap junctional conductance and glutamatergic transmission. Proc Natl Acad Sci USA 95:13272-13277.
50. Pereda A, O'Brien J, Nagy JI, Bukauskas F, Davidson KGV, Kamasawa N, Yasumura T, Rash JE (2003a) Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells. J Neurosci 23:7489-7503.
51. Pereda A, O'Brien J, Nagy JI, Smith M, Bukauskas F, Davidson KGV, Kamasawa N, Yasumura T, Rash JE (2003b) Short-range functional interaction between Connexin35 and neighboring chemical synapses. Cell Commun Adhesion 10:419-423.
52. Piccolino M, Neyton J, Gerschenfeld H (1982) Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3′:5′ -monophosphate in horizontal cells of turtle retina. J Neurosci 2:2477-2488.
53. Ringham GL (1975) Localization and electrical characteristics of a giant synapse in the spinal cord of the lamprey. J Physiol (Lond) 251:395-407.
54. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling. A novel mechanism for ultrafast neuronal communication. Neuron 31:831-834.
55. Slesinger P, Bell CC (1985) Primary afferent fibers conduct impulses in both directions under physiological stimulus conditions. J Comp Physiol 157:15-22.
56. Smith M, Pereda A (2003) Chemical synaptic activity modulates nearby electrical synapses. Proc Natl Acad Sci USA 100:4849-4854.
57. Spira ME, Spray DC, Bennett MV (1976) Electrotonic coupling: effective sign reversal by inhibitory neurons. Science 194:1065-1067.
58. Staftsrom CE, Schwindt PC, Crill WE (1982) Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro. Brain Res 236:221-226.
59. Staftsrom CE, Schwindt PC, Chubb MC, Crill WE (1985) Properties of a persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. J Neurophysiol 53:153-170.
60. Traub RD (1995) Model of synchronized population bursts in electrically coupled interneurons containing active dendritic conductances. J Comp Neurosci 2:283-289.
61. Trussell LO (1997) Cellular mechanisms for preservation of timing in central auditory pathways. Curr Opin Neurobiol 7:487-492.
62. Verselis VK, Ginter CS, Bargiello TA (1994) Opposite voltage gating polarities of two closely related connexins. Nature 368:348-351.
63. Watanabe S, Satoh H, Koizumi A, Takayanagi T, Kaneko A (2000) Tetrodotoxin-sensitive persistent current boosts the depolarization of retinal amacrine cells in goldfish. Neurosci Lett 278:97-100.
64. Yang XD, Korn H, Faber DS (1990) Long-term potentiation of electrotonic coupling at mixed synapses. Nature 348:542-545.
65. Zipser B (1979) Voltage-modulated membrane resistance in coupled leech neurons. J Neurophysiol 42:465-475.