Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter July 22, 2014

Wiring prior to firing: the evolutionary rise of electrical and chemical modes of synaptic transmission

  • Saak V. Ovsepian EMAIL logo and Nikolai P. Vesselkin EMAIL logo

Abstract

Paracrine signaling and coupling via intercellular conduits are widely utilized for cell-cell interactions from primitive eukaryotes to advanced metazoa. Here, we review the functional and molecular data suggestive of a phylogenic continuum between these primeval forms of communication with the chemical and electrical synaptic transmission of neurons. We discuss selective evidence for the essential role played by the shift of function in early cellular morphologies and protosynaptic scaffolds, with their co-optation for new functionality, which ultimately lead to the rise of the chemical synapse. It is proposed that, rather than representing a transitional element, mixed electrochemical synapses exemplify an exaptive effect. The nonadaptive model of the synaptic origin described herein supports the pluralistic hypothesis of evolutionary change.


Corresponding authors: Saak V. Ovsepian, Department of Translational Brain Research, German Center for Neurodegenerative Diseases (DZNE), 81377 Munich, Germany; and Department of Biotechnology and International Centre for Neurotherapeutics, Dublin City University, Dublin 9, Ireland, e-mail: ; and Nikolai P. Vesselkin, Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, 194021 St. Petersburg, Russia; and Faculty of Medicine, The State University of Saint Petersburg, 199034 St. Petersburg, Russia, e-mail:

Acknowledgments

The authors thank Drs. Valerie O’Leary and Hovik Panosyan and Prof. J. Oliver Dolly for insightful discussions and critical reading of the manuscript. This work was supported by the Neuroscience Section of the Programme for Research in Third Level Institutions (PRTLI) Cycle 4 (to S.V.O.) and RFFI-Grant N10098 (to N.P.V.). The PRTLI is cofunded through the European Regional Development Fund (ERDF), part of the European Union Structural Funds Programme 2007 to 2013.

References

Abascal, F. and Zardoya, R. (2013). Evolutionary analyses of gap junction protein families. Biochim. Biophys. Acta 1828, 4–14.10.1016/j.bbamem.2012.02.007Search in Google Scholar

Abedin, M. and King, N. (2010). Diverse evolutionary paths to cell adhesion. Trends Cell. Biol. 20, 734–742.10.1016/j.tcb.2010.08.002Search in Google Scholar

Abraham, V., Chou, M.L., George, P., Pooler, P., Zaman, A., Savani, R.C., and Koval, M. (2001). Heterocellular gap junctional communication between alveolar epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L1085–L1093.10.1152/ajplung.2001.280.6.L1085Search in Google Scholar

Agricola, H.J. and Braunig, P. (2011). Comparative Aspect of Peptidergic Signaling Pathways in Nervous System of Arthropoda (Basel: Birkhauser Vergal).Search in Google Scholar

Arendt, D. (2008). The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 9, 868–882.10.1038/nrg2416Search in Google Scholar

Arumugam, H., Liu, X., Colombo, P.J., Corriveau, R.A., and Belousov, A.B. (2005). NMDA receptors regulate developmental gap junction uncoupling via CREB signaling. Nat. Neurosci. 8, 1720–1726.10.1038/nn1588Search in Google Scholar

Belluardo, N., Mudo, G., Trovato-Salinaro, A., Le Gurun, S., Charollais, A., Serre-Beinier, V., Amato, G., Haefliger, J.A., Meda, P., and Condorelli, D.F. (2000). Expression of connexin36 in the adult and developing rat brain. Brain Res. 865, 121–138.10.1016/S0006-8993(00)02300-3Search in Google Scholar

Belousov, A.B. and Fontes, J.D. (2013). Neuronal gap junctions: making and breaking connections during development and injury. Trends Neurosci. 36, 227–236.10.1016/j.tins.2012.11.001Search in Google Scholar

Bennett, M.V.L. (1972). A comparison of electrically and chemically mediated transmission (New York: Raven Press).Search in Google Scholar

Bennett, M.V. (2000a). Electrical synapses, a personal perspective (or history). Brain Res. Brain Res. Rev. 32, 16–28.10.1016/S0165-0173(99)00065-XSearch in Google Scholar

Bennett, M.V. (2000b). Seeing is relieving: electrical synapses between visualized neurons. Nat. Neurosci. 3, 7–9.10.1038/71082Search in Google Scholar

Bennett, M.V. and Zukin, R.S. (2004). Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41, 495–511.10.1016/S0896-6273(04)00043-1Search in Google Scholar

Bittman, K., Owens, D.F., Kriegstein, A.R., and LoTurco, J.J. (1997). Cell coupling and uncoupling in the ventricular zone of developing neocortex. J. Neurosci. 17, 7037–7044.10.1523/JNEUROSCI.17-18-07037.1997Search in Google Scholar

Bloomfield, S.A. and Volgyi, B. (2009). The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat. Rev. Neurosci. 10, 495–506.10.1038/nrn2636Search in Google Scholar

Bonner, J.T. (2000). First Signal: The Evolution of Multicellular Development (Princeton/Oxford: Princeton University Press).Search in Google Scholar

Bonner, J.T. (2003). On the origin of differentiation. J. Biosci. 28, 523–528.10.1007/BF02705126Search in Google Scholar

Butler, A.B. and Hodos, W. (2005). Neurons and Sensory Receptors (Hoboken, NJ: Wiley-Intersciencce).Search in Google Scholar

Carroll, S.B. (2001). Chance and necessity: the evolution of morphological complexity and diversity. Nature 409, 1102–1109.10.1038/35059227Search in Google Scholar

Cohen-Cory, S. (2002). The developing synapse: construction and modulation of synaptic structures and circuits. Science 298, 770–776.10.1126/science.1075510Search in Google Scholar

Condorelli, D.F., Parenti, R., Spinella, F., Trovato Salinaro, A., Belluardo, N., Cardile, V., and Cicirata, F. (1998). Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur. J. Neurosci. 10, 1202–1208.10.1046/j.1460-9568.1998.00163.xSearch in Google Scholar

Connors, B.W. and Long, M.A. (2004). Electrical synapses in the mammalian brain. Annu. Rev. Neurosci. 27, 393–418.10.1146/annurev.neuro.26.041002.131128Search in Google Scholar

Cowan, W.M. and Kandel, E.R. (2001). A Brief History of Synapses and Synaptic Transmission (Baltimore/London: The Johns Hopkins University Press).Search in Google Scholar

Darwin, C.R. (1862). On the Various Contrivances by Which British and Foreign Orchids Are Fertilised by Insects, and on the Good Effects of Intercrossing (London: John Murray).Search in Google Scholar

Dbouk, H.A., Mroue, R.M., El-Sabban, M.E., and Talhouk, R.S. (2009). Connexins: a myriad of functions extending beyond assembly of gap junction channels. Cell Commun. Signal. 7, 4.10.1186/1478-811X-7-4Search in Google Scholar

De Camilli, P., Haucke, V., Takei, K., and Mugnaini, E. (2001). The Structure of Synapse (Baltimore/London: The Johns Hopkins University Press).Search in Google Scholar

Demarque, M., Represa, A., Becq, H., Khalilov, I., Ben-Ari, Y., and Aniksztejn, L. (2002). Paracrine intercellular communication by a Ca2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36, 1051–1061.10.1016/S0896-6273(02)01053-XSearch in Google Scholar

Dermietzel, R. (1998). Gap junction wiring: a ‘new’ principle in cell-to-cell communication in the nervous system? Brain Res. Brain Res. Rev. 26, 176–183.10.1016/S0165-0173(97)00031-3Search in Google Scholar

Eccles, J.C. (1964). The Physiology of Synapses (New York: Academic Press).10.1007/978-3-642-64950-9Search in Google Scholar

Eccles, J.C. (1982). The synapse: from electrical to chemical transmission. Annu. Rev. Neurosci. 5, 325–339.10.1146/annurev.ne.05.030182.001545Search in Google Scholar

Elias, L.A. and Kriegstein, A.R. (2008). Gap junctions: multifaceted regulators of embryonic cortical development. Trends Neurosci. 31, 243–250.10.1016/j.tins.2008.02.007Search in Google Scholar

Emes, R.D. and Grant, S.G. (2012). Evolution of synapse complexity and diversity. Annu. Rev. Neurosci. 35, 111–131.10.1146/annurev-neuro-062111-150433Search in Google Scholar

Fatt, P. and Katz, B. (1951). An analysis of the end-plate potential recorded with an intracellular electrode. J. Physiol. 115, 320–370.10.1113/jphysiol.1951.sp004675Search in Google Scholar

Fischbach, G.D. (1972). Synapse formation between dissociated nerve and muscle cells in low density cell cultures. Dev. Biol. 28, 407–429.10.1016/0012-1606(72)90023-1Search in Google Scholar

Furshpan, E.J. and Potter, D.D. (1957). Mechanism of nerve-impulse transmission at a crayfish synapse. Nature 180, 342–343.10.1038/180342a0Search in Google Scholar PubMed

Fuxe, K., Borroto-Escuela, D.O., Romero-Fernandez, W., Zhang, W.B., and Agnati, L.F. (2013). Volume transmission and its different forms in the central nervous system. Chin. J. Integr. Med. 19, 323–329.10.1007/s11655-013-1455-1Search in Google Scholar PubMed

Gajda, Z., Gyengesi, E., Hermesz, E., Ali, K.S., and Szente, M. (2003). Involvement of gap junctions in the manifestation and control of the duration of seizures in rats in vivo. Epilepsia 44, 1596–1600.10.1111/j.0013-9580.2003.25803.xSearch in Google Scholar PubMed

Gerst, J.E., Rodgers, L., Riggs, M., and Wigler, M. (1992). SNC1, a yeast homolog of the synaptic vesicle-associated membrane protein/synaptobrevin gene family: genetic interactions with the RAS and CAP genes. Proc. Natl. Acad. Sci. USA 89, 4338–4342.10.1073/pnas.89.10.4338Search in Google Scholar PubMed PubMed Central

Goodenough, D.A. and Paul, D.L. (2009). Gap junctions. Cold Spring Harb. Perspect. Biol. 1, a002576.10.1101/cshperspect.a002576Search in Google Scholar

Gotow, T. and Sotelo, C. (1987). Postnatal development of the inferior olivary complex in the rat: IV. Synaptogenesis of GABAergic afferents, analyzed by glutamic acid decarboxylase immunocytochemistry. J. Comp. Neurol. 263, 526–552.10.1002/cne.902630406Search in Google Scholar

Gould, S.J. (2006). The Reachnes of the Life (London: Vintage Books).Search in Google Scholar

Grant, S.G. (2009). A general basis for cognition in the evolution of synapse signaling complexes. Cold Spring Harb. Symp. Quant. Biol. 74, 249–257.10.1101/sqb.2009.74.033Search in Google Scholar

Grosberg, R.K. and Strathmann, R.R. (2007). The evolution of multicellularity: a minor major transition? Annu. Rev. Ecol. Evol. Syst. 38, 621–654.10.1146/annurev.ecolsys.36.102403.114735Search in Google Scholar

Hatton, G.I. (1998) Synaptic modulation of neuronal coupling. Cell. Biol. Int. 22, 765–780.Search in Google Scholar

Hormuzdi, S.G., Filippov, M.A., Mitropoulou, G., Monyer, H., and Bruzzone, R. (2004). Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks. Biochim. Biophys. Acta 1662, 113–137.10.1016/j.bbamem.2003.10.023Search in Google Scholar

Hoyle, C.H. (2011). Evolution of neuronal signalling: transmitters and receptors. Auton. Neurosci. 165, 28–53.10.1016/j.autneu.2010.05.007Search in Google Scholar

Hyman, L. (1940). The Invertebrates: Protozoa Through Ctenophora (New York: McGraw-Hill).Search in Google Scholar

Iball, J. and Ali, A.B. (2011). Endocannabinoid release modulates electrical coupling between CCK cells connected via chemical and electrical synapses in CA1. Front. Neural Circuits 5, 17.10.3389/fncir.2011.00017Search in Google Scholar

Kandler, K. and Katz, L.C. (1995). Neuronal coupling and uncoupling in the developing nervous system. Curr. Opin. Neurobiol. 5, 98–105.10.1016/0959-4388(95)80093-XSearch in Google Scholar

Kandler, K. and Katz, L.C. (1998). Coordination of neuronal activity in developing visual cortex by gap junction-mediated biochemical communication. J. Neurosci. 18, 1419–1427.10.1523/JNEUROSCI.18-04-01419.1998Search in Google Scholar

Katz, B. (1969). The Release of Neural Transmitter Substances. The Xth Sherrington Lecture (Springfield, IL: Charles C. Thomas).Search in Google Scholar

Kienle, N., Kloepper, T.H., and Fasshauer, D. (2009a). Phylogeny of the SNARE vesicle fusion machinery yields insights into the conservation of the secretory pathway in fungi. BMC Evol. Biol. 9, 19.10.1186/1471-2148-9-19Search in Google Scholar PubMed PubMed Central

Kienle, N., Kloepper, T.H., and Fasshauer, D. (2009b). Differences in the SNARE evolution of fungi and metazoa. Biochem. Soc. Trans. 37, 787–791.10.1042/BST0370787Search in Google Scholar

King, N. (2004). The unicellular ancestry of animal development. Dev. Cell 7, 313–325.10.1016/j.devcel.2004.08.010Search in Google Scholar

Kloepper, T.H., Kienle, C.N., and Fasshauer, D. (2007). An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol. Biol. Cell. 18, 3463–3471.10.1091/mbc.e07-03-0193Search in Google Scholar

Koenig, J.H. and Ikeda, K. (2005). Relationship of the reserve vesicle population to synaptic depression in the tergotrochanteral and dorsal longitudinal muscles of Drosophila. J. Neurophysiol. 94, 2111–2119.10.1152/jn.00323.2005Search in Google Scholar

Korn, H., Triller, A., and Faber, D.S. (1978). Structural correlates of recurrent collateral interneurons producing both electrical and chemical inhibitions of the Mauthner cell. Proc. R. Soc. Lond. B Biol. Sci. 202, 533–538.10.1098/rspb.1978.0085Search in Google Scholar

Kosik, K.S. (2009). Exploring the early origins of the synapse by comparative genomics. Biol. Lett. 5, 108–111.10.1098/rsbl.2008.0594Search in Google Scholar

Lehmenkuhler, A., Sykova, E., Svoboda, J., Zilles, K., and Nicholson, C. (1993). Extracellular space parameters in the rat neocortex and subcortical white matter during postnatal development determined by diffusion analysis. Neuroscience 55, 339–351.10.1016/0306-4522(93)90503-8Search in Google Scholar

Lo Turco, J.J. and Kriegstein, A.R. (1991). Clusters of coupled neuroblasts in embryonic neocortex. Science 252, 563–566.10.1126/science.1850552Search in Google Scholar PubMed

Mackie, G.O. (1970). Neuroid conduction and the evolution of conducting tissues. Q. Rev. Biol. 45, 319–332.10.1086/406645Search in Google Scholar PubMed

Maher, B.J., McGinley, M.J., and Westbrook, G.L. (2009). Experience-dependent maturation of the glomerular microcircuit. Proc. Natl. Acad. Sci. USA 106, 16865–16870.10.1073/pnas.0808946106Search in Google Scholar PubMed PubMed Central

Manent, J.B., Demarque, M., Jorquera, I., Pellegrino, C., Ben-Ari, Y., Aniksztejn, L., and Represa, A. (2005). A noncanonical release of GABA and glutamate modulates neuronal migration. J. Neurosci. 25, 4755–4765.10.1523/JNEUROSCI.0553-05.2005Search in Google Scholar PubMed PubMed Central

Martinez, A.D., Acuna, R., Figueroa, V., Maripillan, J., and Nicholson, B. (2009). Gap-junction channels dysfunction in deafness and hearing loss. Antioxid. Redox Signal. 11, 309–322.10.1089/ars.2008.2138Search in Google Scholar PubMed PubMed Central

McMahon, D.G. and Brown, D.R. (1994). Modulation of gap-junction channel gating at zebrafish retinal electrical synapses. J. Neurophysiol. 72, 2257–2268.10.1152/jn.1994.72.5.2257Search in Google Scholar PubMed

McMahon, D.G., Knapp, A.G., and Dowling, J.E. (1989). Horizontal cell gap junctions: single-channel conductance and modulation by dopamine. Proc. Natl. Acad. Sci. USA 86, 7639–7643.10.1073/pnas.86.19.7639Search in Google Scholar PubMed PubMed Central

Mian, I.S. and Rose, C. (2011). Communication theory and multicellular biology. Integr. Biol. (Camb.) 3, 350–367.10.1039/c0ib00117aSearch in Google Scholar PubMed

Missler, M., Sudhof, T., and Biederer, T. (2012). Synaptic Cell Adhesion (New York: Cold Spring Harbor Laboratory Press).10.1101/cshperspect.a005694Search in Google Scholar PubMed PubMed Central

Moody, W.J. and Bosma, M.M. (2005). Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol. Rev. 85, 883–941.10.1152/physrev.00017.2004Search in Google Scholar PubMed

Moroz, L.L. (2009). On the independent origins of complex brains and neurons. Brain Behav. Evol. 74, 177–190.10.1159/000258665Search in Google Scholar PubMed PubMed Central

Nagy, J.I., Dudek, F.E., and Rash, J.E. (2004). Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res. Brain Res. Rev. 47, 191–215.10.1016/j.brainresrev.2004.05.005Search in Google Scholar PubMed

Nagy, J.I., Bautista, W., Blakley, B., and Rash, J.E. (2013). 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 252, 468–488.10.1016/j.neuroscience.2013.07.056Search in Google Scholar PubMed PubMed Central

Nicholson, B., Dermietzel, R., Teplow, D., Traub, O., Willecke, K., and Revel, J.P. (1987). Two homologous protein components of hepatic gap junctions. Nature 329, 732–734.10.1038/329732a0Search in Google Scholar

Niculescu, D. and Lohmann, C. (2013). Gap junctions in developing thalamic and neocortical neuronal networks. Cereb. Cortex.Search in Google Scholar

O’Lague, P.H., Potter, D.D., and Furshpan, E.J. (1978). Studies on rat sympathetic neurons developing in cell culture. I. Growth characteristics and electrophysiological properties. Dev. Biol. 67, 384–403.10.1016/0012-1606(78)90208-7Search in Google Scholar

Oguro, K., Jover, T., Tanaka, H., Lin, Y., Kojima, T., Oguro, N., Grooms, S.Y., Bennett, M.V., and Zukin, R.S. (2001). Global ischemia-induced increases in the gap junctional proteins connexin 32 (Cx32) and Cx36 in hippocampus and enhanced vulnerability of Cx32 knock-out mice. J. Neurosci. 21, 7534–7542.10.1523/JNEUROSCI.21-19-07534.2001Search in Google Scholar

Oh, S., Rubin, J.B., Bennett, M.V., Verselis, V.K., and Bargiello, T.A. (1999). Molecular determinants of electrical rectification of single channel conductance in gap junctions formed by connexins 26 and 32. J. Gen. Physiol. 114, 339–364.10.1085/jgp.114.3.339Search in Google Scholar PubMed PubMed Central

Ovsepian, S.V. and Dolly, J.O. (2011). Dendritic SNAREs add a new twist to the old neuron theory. Proc. Natl. Acad. Sci. USA 108, 19113–19120.10.1073/pnas.1017235108Search in Google Scholar PubMed PubMed Central

Pappas, G.D. and Bennett, M.V. (1966). Specialized junctions involved in electrical transmission between neurons. Ann. N. Y. Acad. Sci. 137, 495–508.10.1111/j.1749-6632.1966.tb50177.xSearch in Google Scholar PubMed

Park, W.M., Wang, Y., Park, S., Denisova, J.V., Fontes, J.D., and Belousov, A.B. (2011). Interplay of chemical neurotransmitters regulates developmental increase in electrical synapses. J. Neurosci. 31, 5909–5920.10.1523/JNEUROSCI.6787-10.2011Search in Google Scholar PubMed PubMed Central

Paul, D.L. (1986). Molecular cloning of cDNA for rat liver gap junction protein. J. Cell. Biol. 103, 123–134.10.1083/jcb.103.1.123Search in Google Scholar PubMed PubMed Central

Pereda, A.E. (2014). Electrical synapses and their functional interactions with chemical synapses. Nat. Rev. Neurosci. 15, 250–263.10.1038/nrn3708Search in Google Scholar PubMed PubMed Central

Personius, K.E., Chang, Q., Mentis, G.Z., O’Donovan, M.J., and Balice-Gordon, R.J. (2007). Reduced gap junctional coupling leads to uncorrelated motor neuron firing and precocious neuromuscular synapse elimination. Proc. Natl. Acad. Sci. USA 104, 11808–11813.10.1073/pnas.0703357104Search in Google Scholar PubMed PubMed Central

Prokopova, S., Vargova, L., and Sykova, E. (1997). Heterogeneous and anisotropic diffusion in the developing rat spinal cord. Neuroreport 8, 3527–3532.10.1097/00001756-199711100-00022Search in Google Scholar

Putnam, N.H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V.V., et al. (2007). Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86–94.10.1126/science.1139158Search in Google Scholar

Rash, J.E., Dillman, R.K., Bilhartz, B.L., Duffy, H.S., Whalen, L.R., and Yasumura, T. (1996). Mixed synapses discovered and mapped throughout mammalian spinal cord. Proc. Natl. Acad. Sci. USA 93, 4235–4239.10.1073/pnas.93.9.4235Search in Google Scholar

Ratcliff, W.C., Denison, R.F., Borrello, M., and Travisano, M. (2012). Experimental evolution of multicellularity. Proc. Natl. Acad. Sci. USA 109, 1595–1600.10.1073/pnas.1115323109Search in Google Scholar

Rela, L. and Szczupak, L. (2004). Gap junctions: their importance for the dynamics of neural circuits. Mol. Neurobiol. 30, 341–357.10.1385/MN:30:3:341Search in Google Scholar

Revel, J.P. and Karnovsky, M.J. (1967). Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell. Biol. 33, C7–C12.10.1083/jcb.33.3.C7Search in Google Scholar

Rokas, A. (2008). The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 42, 235–251.10.1146/annurev.genet.42.110807.091513Search in Google Scholar

Ryan, T.J. and Grant, S.G. (2009). The origin and evolution of synapses. Nat. Rev. Neurosci. 10, 701–712.10.1038/nrn2717Search in Google Scholar

Sakarya, O., Armstrong, K.A., Adamska, M., Adamski, M., Wang, I.F., Tidor, B., Degnan, B.M., Oakley, T.H., and Kosik, K.S. (2007). A post-synaptic scaffold at the origin of the Animal Kingdom. PLoS One 2, e506.10.1371/journal.pone.0000506Search in Google Scholar

Sanes, D.H., Thomas, R.A., and Harris, W.A. (2006). Development of the Nervous System. 2nd ed. (Amsterdam: Elsevier).Search in Google Scholar

Shapovalov, A.I. (1980). Interneuronal synapses with electrical, dual and chemical mode of transmission in vertebrates. Neuroscience 5, 1113–1124.10.1016/0306-4522(80)90190-6Search in Google Scholar

Shepherd, G.M. (1988). Neurobiology (New York: Oxford Univ. Press).Search in Google Scholar

Sherrington, C.S. (1897). The Central Nervous System. 7th ed. (London: Macmillan).Search in Google Scholar

Shestopalov, V.I. and Panchin, Y. (2008). Pannexins and gap junction protein diversity. Cell. Mol. Life Sci. 65, 376–394.10.1007/s00018-007-7200-1Search in Google Scholar

Simpson, I., Rose, B., and Loewenstein, W.R. (1977). Size limit of molecules permeating the junctional membrane channels. Science 195, 294–296.10.1126/science.831276Search in Google Scholar

Sotelo, C. and Palay, S.L. (1970). The fine structure of the later vestibular nucleus in the rat. II. Synaptic organization. Brain Res. 18, 93–115.Search in Google Scholar

Sotelo, C. and Korn, H. (1978). Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system. Int. Rev. Cytol. 55, 67–107.10.1016/S0074-7696(08)61887-2Search in Google Scholar

Spitzer, N.C. (2006). Electrical activity in early neuronal development. Nature 444, 707–712.10.1038/nature05300Search in Google Scholar

Stanley, S.M. (1973). An ecological theory for the sudden origin of multicellular life in the late Precambrian. Proc. Natl. Acad. Sci. USA 70, 1486–1489.10.1073/pnas.70.5.1486Search in Google Scholar

Stoka, A.M. (1999). Phylogeny and evolution of chemical communication: an endocrine approach. J. Mol. Endocrinol. 22, 207–225.10.1677/jme.0.0220207Search in Google Scholar

Sudhof, T.C. (2013). Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80, 675–690.10.1016/j.neuron.2013.10.022Search in Google Scholar

Szabo, T.M., Faber, D.S., and Zoran, M.J. (2004). Transient electrical coupling delays the onset of chemical neurotransmission at developing synapses. J. Neurosci. 24, 112–120.10.1523/JNEUROSCI.4336-03.2004Search in Google Scholar

Takaku, Y., Hwang, J.S., Wolf, A., Bottger, A., Shimizu, H., David, C.N., and Gojobori, T. (2013). Innexin gap junctions in nerve cells coordinate spontaneous contractile behavior in Hydra polyps. Sci. Rep. 4, 3573.10.1038/srep03573Search in Google Scholar

Tierney, A.J. (1996). Evolutionary implications of neural circuit structure and function. Behav. Processes 35, 173–182.10.1016/0376-6357(95)00041-0Search in Google Scholar

Todd, K.L., Kristan, W.B., Jr., and French, K.A. (2010). Gap junction expression is required for normal chemical synapse formation. J. Neurosci. 30, 15277–15285.10.1523/JNEUROSCI.2331-10.2010Search in Google Scholar

Trosko, J.E. (2011). The gap junction as a “Biological Rosetta Stone”: implications of evolution, stem cells to homeostatic regulation of health and disease in the Barker hypothesis. J. Cell. Commun. Signal. 5, 53–66.10.1007/s12079-010-0108-9Search in Google Scholar

Trosko, J.E., Chang, C.C., Wilson, M.R., Upham, B., Hayashi, T., and Wade, M. (2000). Gap junctions and the regulation of cellular functions of stem cells during development and differentiation. Methods 20, 245–264.10.1006/meth.1999.0941Search in Google Scholar

Veenstra, R.D., Wang, H.Z., Beblo, D.A., Chilton, M.G., Harris, A.L., Beyer, E.C., and Brink, P.R. (1995). Selectivity of connexin-specific gap junctions does not correlate with channel conductance. Circ. Res. 77, 1156–1165.10.1161/01.RES.77.6.1156Search in Google Scholar

Wang, Y., Song, J.H., Denisova, J.V., Park, W.M., Fontes, J.D., and Belousov, A.B. (2012). Neuronal gap junction coupling is regulated by glutamate and plays critical role in cell death during neuronal injury. J. Neurosci. 32, 713–725.10.1523/JNEUROSCI.3872-11.2012Search in Google Scholar

Westfall, I.A. (1996). Ultrastructure of synapses in the first-evolved nervous systems. J. Neurocytol. 25, 735–746.10.1007/BF02284838Search in Google Scholar

Yu, Y.C., He, S., Chen, S., Fu, Y., Brown, K.N., Yao, X.H., Ma, J., Gao, K.P., Sosinsky, G.E., Huang, K., et al. (2012). Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly. Nature 486, 113–117.10.1038/nature10958Search in Google Scholar

Yuste, R., Peinado, A., and Katz, L.C. (1992). Neuronal domains in developing neocortex. Science 257, 665–669.10.1126/science.1496379Search in Google Scholar

Yuste, R., Nelson, D.A., Rubin, W.W., and Katz, L.C. (1995). Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron 14, 7–17.10.1016/0896-6273(95)90236-8Search in Google Scholar

Zhang, J.T. and Nicholson, B.J. (1989). Sequence and tissue distribution of a second protein of hepatic gap junctions, Cx26, as deduced from its cDNA. J. Cell. Biol. 109, 3391–3401.10.1083/jcb.109.6.3391Search in Google Scholar PubMed PubMed Central

Received: 2014-5-22
Accepted: 2014-6-16
Published Online: 2014-7-22
Published in Print: 2014-12-1

©2014 by De Gruyter

Downloaded on 30.3.2023 from https://www.degruyter.com/document/doi/10.1515/revneuro-2014-0037/html
Scroll Up Arrow