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June, 2006
Electrical Synapses
(a brief bibliography)
Barry Connors
Brown University
[email protected]
I. Introduction and history
50 mV
Presynaptic axon
Postsynaptic axon
5 ms
(Furshpan and Potter, 1957)
Bennett MV. 1997. Gap junctions as electrical synapses. J Neurocytol. 26:349-366.
Bennett MVL, Crain SM, Grundfest H. 1959. Electrophysiology of supramedullary neurons in Spheroides
maculates: I. Orthodromic and antidromic responses. J. Gen. Physiol. 43:159-188
Baker R, Llinás R. 1971. Electrotonic coupling between neurones in the rat mesencephalic nucleus. J.
Physiol. 212:45-63
Cowan WM, Kandel ER. 2001. A brief history of synapses and synaptic transmission. In Synapses, ed.
WM Cowan, TC Südhof, CF Stevens, 1-88. Baltimore: Johns Hopkins University Press.
Furshpan EJ, Potter DD. 1957. Mechanism of nerve-impulse transmission at a crayfish synapse. Nature
180:342-3
Watanabe A. 1958. The interaction of electrical activity among neurons of lobster cardiac ganglion.
Jpn. J. Physiol. 8:305-18
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II. Structure and biophysics of gap junctions
Connexon
(hemichannel)
Gap junction
channel
Connexin
(White & Paul, 1999)
Bennett MVL. 1977. Electrical transmission: a functional analysis and comparison with chemical
transmission. In Cellular Biology of Neurons, Handbook of Physiology, The Nervous System, ed.
ER Kandel, 1(1):357-416. Baltimore: Williams and Wilkins Co. 717 pp.
Harris AL. 2001. Emerging issues of connexin channels: biophysics fills the gap. Q. Rev. Biophys.
34:325-472
Herve J-C. 2005. The Connexins Part II (special issue). Biochim Biophys Acta. 1711: 97-246
Saez JC, Retamal MA, Basilio D, Bukauskas FF, Bennett MV. 2005. Connexin-based gap junction
hemichannels: gating mechanisms. Biochim Biophys Acta. 1711:215-24.
Sosinsky GE, Nicholson BJ. 2005. Structural organization of gap junction channels. Biochim Biophys
Acta. 1711:99-125.
Unger VM, Kumar NM, Gilula NB, Yeager M. 1999. Three-dimensional structure of a recombinant gap
junction membrane channel. Science. 283:1176-80.
June, 2006
III. Distribution of electrical synapses
electrical
synapses
chemical
synapses
Tamás et al., Nature Neurosci, 2000
Christie MJ, Williams JT, North RA. 1989. Electrical coupling synchronizes subthreshold activity in
locus coeruleus neurons in vitro from neonatal rats. J. Neurosci. 9:3584-9
Connors BW, Long MA. 2004. Electrical synapses in the mammalian brain. Annu Rev Neurosci. 27:393418.
Fukuda T, Kosaka T, Singer W, Galuske RA. 2006. Gap junctions among dendrites of cortical
GABAergic neurons establish a dense and widespread intercolumnar network. J Neurosci.
26:3434-43.
Fulton BP, Miledi R, Takahashi T. 1980. Electrical synapses between motoneurons in the spinal cord of
the newborn rat. Proc R Soc Lond B Biol Sci. 208:115-120.
Galarreta M, Hestrin S. 1999. A network of fast-spiking cells in the neocortex connected by electrical
synapses. Nature 402:72-5
Gibson JR, Beierlein M, Connors BW. 1999. Two networks of electrically coupled inhibitory neurons in
neocortex. Nature 402:75-9
Hinrichsen CF. 1970. Coupling between cells of the trigeminal mesencephalic nucleus. J. Dent. Res.
49:1369-73
Llinás RR, Baker, Sotelo C. 1974. Electrotonic coupling between neurons in cat inferior olive. J.
Neurophysiol. 37:560-71
Marder E. 1984. Roles for electrical coupling in neural circuits as revealed by selective neuronal
deletions. J Exp Biol. 112:147-67.
Vaney DI. 2002. Retinal neurons: cell types and coupled networks. Prog Brain Res. 136:239-54.
June, 2006
IV. Molecular basis
(Rash et al., 2001)
Bruzzone R, Hormuzdi SG, Barbe M, Herb A, Monyer H. 2003. Pannexins, a novel family of gap
junction proteins expressed in the brain. Proc. Natl. Acad. Sci. USA. 100:13644-9.
Condorelli DF, Belluardo N, Trovato-Salinaro A, Mudo G. 2000. Expression of Cx36 in mammalian
neurons. Brain Res. Brain Res. Rev. 32:72-85
Herve JC, Bourmeyster N, Sarrouilhe D. 2004. Diversity in protein-protein interactions of connexins:
emerging roles. Biochim Biophys Acta. 1662:22-41
Kamermans M, Fahrenfort I. 2004. Ephaptic interactions within a chemical synapse: hemichannelmediated ephaptic inhibition in the retina. Curr Opin Neurobiol. 14:531-41.
Panchin YV. 2005. Evolution of gap junction proteins--the pannexin alternative. J Exp Biol. 208:1415-9.
Panchin Y, Kelmanson I, Matz M, Lukyanov K, Usman N, Lukyanov S. 2000. A ubiquitous family of
putative gap junction molecules. Curr. Biol. 10:R473-4
Rash JE, Yasumura T, Dudek FE, Nagy JI. 2001. Cell-specific expression of connexins and evidence of
restricted gap junctional coupling between glial cells and between neurons. J. Neurosci. 21:19832000
Sohl G, Maxeiner S, Willecke K. 2005. Expression and functions of neuronal gap junctions. Nat Rev
Neurosci. 6:191-200.
Stout C, Goodenough DA, Paul DL. 2004. Connexins: functions without junctions. Curr Opin Cell Biol.
16:507-12.
White TW, Paul DL. 1999. Genetic diseases and gene knockouts reveal diverse connexin functions. Annu
Rev Physiol. 61:283-310.
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V. Pharmacology and modulation
halothane
heptanol
enflurane
18-glycyrrhetinic acid (R=H)
carbenoxolone R=NaOOC(CH2)2CO)
mefloquine
quinine
(Rozental et al., 2001; Cruikshank et al., 2004)
Arumugam H, Liu X, Colombo PJ, Corriveau RA, Belousov AB. 2005. NMDA receptors regulate
developmental gap junction uncoupling via CREB signaling. Nat Neurosci. 8:1720-6.
Cruikshank SJ, Hopperstad M, Younger M, Connors BW, Spray DC, Srinivas M. 2004. Potent block of
Cx36 and Cx50 gap junction channels by mefloquine. Proc Natl Acad Sci USA. 101:12364-9.
McMahon DG, Knapp AG, Dowling JE. 1989. Horizontal cell gap junctions: single-channel
conductance and modulation by dopamine. Proc. Natl. Acad. Sci. 86:7639-43
Pereda AE, Bell TD, Chang BH, Czernik AJ, Nairn AC, et al. 1998. Ca2+/calmodulin-dependent kinase
II mediates simultaneous enhancement of gap-junctional conductance and glutamatergic
transmission. Proc. Natl. Acad. Sci. 95:13272-7
Peracchia C. 2004. Chemical gating of gap junction channels; roles of calcium, pH and calmodulin.
Biochim Biophys Acta. 1662:61-80.
Rozental R, Srinivas M, Spray DC. 2001. How to close a gap junction channel: Efficacies and potencies
of uncoupling agents. In Methods in Molecular Biology, Connexin Methods and Protocols, eds.
R Bruzzone, C Giaume, Totwa, 154:447-76. New Jersey: Humana Press.
Smith M, Pereda AE. 2003. Chemical synaptic activity modulates nearby electrical synapses. Proc.
Natl. Acad. Sci. 100:4849-54
Spray DC, Harris AL, Bennett MV. 1979. Voltage dependence of junctional conductance in early
amphibian embryos. Science 204:432-4
Spray DC, Harris AL, Bennett MV. 1981. Gap junctional conductance is a simple and sensitive function
of intracellular pH. Science 211:712-5
June, 2006
VI. Functions of electrical synapses
WT
Cx36 KO
(Long et al., 2002)
Bennett MV, Zukin RS. 2004. Electrical coupling and neuronal synchronization in the mammalian brain.
Neuron. 41:495-511.
Christie JM, Bark C, Hormuzdi SG, Helbig I, Monyer H, Westbrook GL. 2005. Connexin36 mediates
spike synchrony in olfactory bulb glomeruli. Neuron. 46:761-72.
Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL. 2001. Synchronous activity of inhibitory
networks in neocortex requires electrical synapses containing connexin 36. Neuron 31:477-85
Hormuzdi SG, Filippov MA, Mitropoulou G, Monyer H, Bruzzone R. 2004. Electrical synapses: a
dynamic signaling system that shapes the activity of neuronal networks. Biochim Biophys Acta.
1662:113-37.
Lewis TJ, Rinzel J. 2003. Dynamics of spiking neurons connected by both inhibitory and electrical
coupling. J Comput Neurosci. 14:283-309.
Long MA, Cruikshank SJ, Jutras MJ, Connors BW. 2005. Abrupt maturation of a spike-synchronizing
mechanism in neocortex. J Neurosci. 25:7309-16.
Long MA, Deans MR, Paul DL, Connors BW. 2002. Rhythmicity without synchrony in the electrically
uncoupled inferior olive. J. Neurosci. 22:10898-905
Marder E. 1998. Electrical synapses: beyond speed and synchrony to computation. Curr Biol. 8:R795-7.
Pereda AE, Rash JE, Nagy JI, Bennett MV. 2004. Dynamics of electrical transmission at club endings on
the Mauthner cells. Brain Res Brain Res Rev. 47:227-44
Pfeuty B, Mato G, Golomb D, Hansel D. 2003. Electrical synapses and synchrony: the role of intrinsic
currents. J Neurosci. 23:6280-94.
Thompson RJ, Zhou N, MacVicar BA. 2006. Ischemia opens neuronal gap junction hemichannels.
Science. 312:924-7.