Gap junctions in developing thalamic and neocortical neuronal networks

Cerebral Cortex

Volumn 24, Issue 12, 2014, Pages 3097-3106

  Niculescu, Dragos ^a   Lohmann, Christian ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Connexin; Electrical synapse; Gap junctions; Neocortex; Thalamus

Indexed keywords

GAP JUNCTION PROTEIN;

ARTICLE; ASTROCYTE; BIOCHEMICAL COMPOSITION; BRAIN DEVELOPMENT; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL MEMBRANE; CELL MIGRATION; CEREBELLUM; DEUTEROSTOMIA; ELECTRICAL SYNAPSE; ELECTROENCEPHALOGRAM; EXTRACELLULAR CALCIUM; GAP JUNCTION; HIPPOCAMPUS; HUMAN; INTERNEURON; NEOCORTEX; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; THALAMUS; VISUAL CORTEX; ANIMAL; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; CONNEXINS; GAP JUNCTIONS; NEOCORTEX; NERVE NET; NEURONS; THALAMUS;

EID: 84891371834     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht175     Document Type: Article

References (75)

1. Alev C, Urschel S, Sonntag S, Zoidl G, Fort AG, Hoher T, Matsubara M, Willecke K, Spray DC, Dermietzel R. 2008. The neuronal connexin36 interacts with and is phosphorylated by CaMKII in a way similar to CaMKII interaction with glutamate receptors. Proc Natl Acad Sci USA. 105(52):20964-9.
2. Amitai Y, Gibson JR, Beierlein M, Patrick SL, Ho AM, Connors BW, Golomb D. 2002. The spatial dimensions of electrically coupled networks of interneurons in the neocortex. J Neurosci. 22(10):4142-4152.
3. Bittman K, Becker DL, Cicirata F, Parnavelas JG. 2002. Connexin expression in homotypic and heterotypic cell coupling in the developing cerebral cortex. J Comp Neurol. 443(3):201-212.
4. Bittman K, Owens DF, Kriegstein AR, Lo Turco JJ. 1997. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J Neurosci. 17(18):7037-7044.
5. Bittman KS, Lo Turco JJ. 1999. Differential regulation of connexin 26 and 43 in murine neocortical precursors. Cereb Cortex. 9(2):188-195.
6. Blethyn KL, Hughes SW, Crunelli V. 2008. Evidence for electrical synapses between neurons of the nucleus reticularis thalami in the adult brain in vitro. Thalamus Relat Syst. 4(1):13-20.
7. Bloomfield SA, Volgyi B. 2009. The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat Rev Neurosci. 10(7):495-506.
8. Bruzzone R, Dermietzel R. 2006. Structure and function of gap junctions in the developing brain. Cell Tissue Res. 326(2):239-248.
9. Condorelli DF, Parenti R, Spinella F, Trovato SA, 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(3):1202-1208.
10. Condorelli DF, Trovato-Salinaro A, Mudo G, Mirone MB, Belluardo N. 2003. Cellular expression of connexins in the rat brain: neuronal localization, effects of kainate-induced seizures and expression in apoptotic neuronal cells. Eur J Neurosci. 18(7):1807-1827.
11. Connors BW, Long MA. 2004. Electrical synapses in the mammalian brain. Annu Rev Neurosci. 27:393-418.
12. Cruikshank SJ, Landisman CE, Mancilla JG, Connors BW. 2005. Connexon connexions in the thalamocortical system. Prog Brain Res. 149:41-57.
13. Del CC, Iglesias R, Zoidl G, Dermietzel R, Spray DC. 2012. Calmodulin dependent protein kinase increases conductance at gap junctions formed by the neuronal gap junction protein connexin36. Brain Res. 1487:69-77.
14. Dupont E, Hanganu IL, Kilb W, Hirsch S, Luhmann HJ. 2006. Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature. 439(7072):79-83.
15. Elfgang C, Eckert R, Lichtenberg-Frate H, Butterweck A, Traub O, Klein RA, Hulser DF, Willecke K. 1995. Specific permeability and selective formation of gap junction channels in connexintransfected HeLa cells. J Cell Biol. 129(3):805-817.
16. Elias LA, Kriegstein AR. 2008. Gap junctions: multifaceted regulators of embryonic cortical development. Trends Neurosci. 31(5):243-250.
17. Elias LA, Wang DD, Kriegstein AR. 2007. Gap junction adhesion is necessary for radial migration in the neocortex. Nature. 448(7156):901-907.
18. Foote CI, Zhou L, Zhu X, Nicholson BJ. 1998. The pattern of disulfide linkages in the extracellular loop regions of connexin 32 suggests a model for the docking interface of gap junctions. J Cell Biol. 140(5):1187-1197.
19. Fuentealba P, Crochet S, Timofeev I, Bazhenov M, Sejnowski TJ, Steriade M. 2004. Experimental evidence and modeling studies support a synchronizing role for electrical coupling in the cat thalamic reticular neurons in vivo. Eur J Neurosci. 20(1):111-119.
20. Fukuda T. 2007. Structural organization of the gap junction network in the cerebral cortex. Neuroscientist. 13(3):199-207.
21. Galarreta M, Hestrin S. 2001. Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci. 2(6):425-433.
22. Galarreta M, Hestrin S. 1999. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature. 402(6757):72-75.
23. Garaschuk O, Linn J, Eilers J, Konnerth A. 2000. Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci. 3(5):452-459.
24. Gibson JR, Beierlein M, Connors BW. 2005. Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4. J Neurophysiol. 93(1):467-480.
25. Gibson JR, Beierlein M, Connors BW. 1999. Two networks of electrically coupled inhibitory neurons in neocortex. Nature. 402(6757):75-79.
26. Gonzalez D, Gomez-Hernandez JM, Barrio LC. 2007. Molecular basis of voltage dependence of connexin channels: an integrative appraisal. Prog Biophys Mol Biol. 94(1-2):66-106.
27. Haas JS, Zavala B, Landisman CE. 2011. Activity-dependent long-term depression of electrical synapses. Science. 334(6054):389-393.
28. Hartfield EM, Rinaldi F, Glover CP, Wong LF, Caldwell MA, Uney JB. 2011. Connexin 36 expression regulates neuronal differentiation from neural progenitor cells. PLoS One. 6(3):e14746.
29. Hensch TK. 2004. Critical period regulation. Annu Rev Neurosci. 27:549-579.
30. Hestrin S, Galarreta M. 2005. Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci. 28(6):304-309.
31. Hombach S, Janssen-Bienhold U, Sohl G, Schubert T, Bussow H, Ott T, Weiler R, Willecke K. 2004. Functional expression of connexin57 in horizontal cells of the mouse retina. Eur J Neurosci. 19(10):2633-2640.
32. 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(1-2):113-137.
33. Jezierski A, Rennie K, Tremblay R, Zurakowski B, Gruslin A, Sikorska M, Bani-Yaghoub M. 2012. Human amniotic fluid cells form functional gap junctions with cortical cells. Stem Cells Int. 2012:607161.
34. Kandler K, Katz LC. 1998. Coordination of neuronal activity in developing visual cortex by gap junction-mediated biochemical communication. J Neurosci. 18(4):1419-1427.
35. Kokarovtseva L, Jaciw-Zurakiwsky T, Mendizabal AR, Frantseva MV, Perez Velazquez JL. 2009. Excitability and gap junction-mediated mechanisms in nucleus accumbens regulate self-stimulation reward in rats. Neuroscience. 159(4):1257-1263.
36. Kumar NM, Gilula NB. 1996. The gap junction communication channel. Cell. 84(3):381-388.
37. Kunze A, Congreso MR, Hartmann C, Wallraff-Beck A, Huttmann K, Bedner P, Requardt R, Seifert G, Redecker C, Willecke K et al. 2009. Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA. 106(27):11336-11341.
38. Landisman CE, Connors BW. 2005. Long-term modulation of electrical synapses in the mammalian thalamus. Science. 310(5755):1809-1813.
39. Landisman CE, Long MA, Beierlein M, Deans MR, Paul DL, Connors BW. 2002. Electrical synapses in the thalamic reticular nucleus. J Neurosci. 22(3):1002-1009.
40. Lee SC, Cruikshank SJ, Connors BW. 2010. Electrical and chemical synapses between relay neurons in developing thalamus. J Physiol. 588(Pt 13):2403-2415.
41. Li Y, Lu H, Cheng PL, Ge S, Xu H, Shi SH, Dan Y. 2012. Clonally related visual cortical neurons show similar stimulus feature selectivity. Nature. 486(7401):118-121.
42. Liu X, Sun L, Torii M, Rakic P. 2012. Connexin 43 controls the multipolar phase of neuronal migration to the cerebral cortex. Proc Natl Acad Sci USA. 109(21):8280-8285.
43. Long MA, Landisman CE, Connors BW. 2004. Small clusters of electrically coupled neurons generate synchronous rhythms in the thalamic reticular nucleus. J Neurosci. 24(2):341-349.
44. Lubke J, Egger V, Sakmann B, Feldmeyer D. 2000. Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. J Neurosci. 20(14):5300-5311.
45. MacVicar BA, Dudek FE. 1980. Dye-coupling betwen CA3 pyramidal cells in slices of rat hippocampus. Brain Res. 196(2):494-497.
46. Marins M, Xavier AL, Viana NB, Fortes FS, Froes MM, Menezes JR. 2009. Gap junctions are involved in cell migration in the early postnatal subventricular zone. Dev Neurobiol. 69(11):715-730.
47. Maxeiner S, Kruger O, Schilling K, Traub O, Urschel S, Willecke K. 2003. Spatiotemporal transcription of connexin45 during brain development results in neuronal expression in adult mice. Neuroscience. 119(3):689-700.
48. Mercer A, Bannister AP, Thomson AM. 2006. Electrical coupling between pyramidal cells in adult cortical regions. Brain Cell Biol. 35(1):13-27.
49. Meyer AH, Katona I, Blatow M, Rozov A, Monyer H. 2002. In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci. 22(16):7055-7064.
50. Montoro RJ, Yuste R. 2004. Gap junctions in developing neocortex: a review. Brain Res Brain Res Rev. 47(1-3):216-226.
51. Nadarajah B, Jones AM, Evans WH, Parnavelas JG. 1997. Differential expression of connexins during neocortical development and neuronal circuit formation. J Neurosci. 17(9):3096-3111.
52. Nadarajah B, Thomaidou D, Evans WH, Parnavelas JG. 1996. Gap junctions in the adult cerebral cortex: regional differences in their distribution and cellular expression of connexins. J Comp Neurol. 376(2):326-342.
53. Nagy JI, Rash JE. 2000. Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res Brain Res Rev. 32(1):29-44.
54. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature. 409(6821):714-720.
55. Oviedo NJ, Levin M. 2007. Gap junctions provide new links in left-right patterning. Cell. 129(4):645-647.
56. Pangratz-Fuehrer S, Hestrin S. 2011. Synaptogenesis of electrical and GABAergic synapses of fast-spiking inhibitory neurons in the neocortex. J Neurosci. 31(30):10767-10775.
57. Park WM, Wang Y, Park S, Denisova JV, Fontes JD, Belousov AB. 2011. Interplay of chemical neurotransmitters regulates developmental increase in electrical synapses. J Neurosci. 31(16):5909-5920.
58. Parker PR, Cruikshank SJ, Connors BW. 2009. Stability of electrical coupling despite massive developmental changes of intrinsic neuronal physiology. J Neurosci. 29(31):9761-9770.
59. Peinado A. 2001. Immature neocortical neurons exist as extensive syncitial networks linked by dendrodendritic electrical connections. J Neurophysiol. 85(2):620-629.
60. Peinado A, Yuste R, Katz LC. 1993. Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron. 10(1):103-114.
61. Postma F, Liu CH, Dietsche C, Khan M, Lee HK, Paul D, Kanold PO. 2011. Electrical synapses formed by connexin36 regulate inhibition- and experience-dependent plasticity. Proc Natl Acad Sci USA. 108(33):13770-5.
62. Prime G, Horn G, Sutor B. 2000. Time-related changes in connexin mRNA abundance in the rat neocortex during postnatal development. Brain Res Dev Brain Res. 119(1):111-125.
63. Rackauskas M, Neverauskas V, Skeberdis VA. 2010. Diversity and properties of connexin gap junction channels. Medicina (Kaunas). 46(1):1-12.
64. Rouach N, Segal M, Koulakoff A, Giaume C, Avignone E. 2003. Carbenoxolone blockade of neuronal network activity in culture is not mediated by an action on gap junctions. J Physiol. 553(Pt 3):729-745.
65. Siegel F, Heimel JA, Peters J, Lohmann C. 2012. Peripheral and central inputs shape network dynamics in the developing visual cortex in vivo. Curr Biol. 22(3):253-258.
66. Sohl G, Maxeiner S, Willecke K. 2005. Expression and functions of neuronal gap junctions. Nat Rev Neurosci. 6(3):191-200.
67. Sohl G, Willecke K. 2004. Gap junctions and the connexin protein family. Cardiovasc Res. 62(2):228-232.
68. Sutor B, Hagerty T. 2005. Involvement of gap junctions in the development of the neocortex. Biochim Biophys Acta. 1719(1-2):59-68.
69. Venance L, Rozov A, Blatow M, Burnashev N, Feldmeyer D, Monyer H. 2000. Connexin expression in electrically coupled postnatal rat brain neurons. Proc Natl Acad Sci USA. 97(18):10260-5.
70. Vervaeke K, Lorincz A, Nusser Z, Silver RA. 2012. Gap junctions compensate for sublinear dendritic integration in an inhibitory network. Science. 335(6076):1624-1628.
71. Wang Y, Barakat A, Zhou H. 2010. Electrotonic coupling between pyramidal neurons in the neocortex. PLoS One. 5(4):e10253.
72. Warren RA, Jones EG. 1997. Maturation of neuronal form and function in a mouse thalamo-cortical circuit. J Neurosci. 17(1):277-295.
73. Yeager M, Gilula NB. 1992. Membrane topology and quaternary structure of cardiac gap junction ion channels. J Mol Biol. 223(4):929-948.
74. Yu YC, He S, Chen S, Fu Y, Brown KN, Yao XH, Ma J, Gao KP, Sosinsky GE, Huang K et al. 2012. Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly. Nature. 486(7401):113-117.
75. Zhang XL, Zhang L, Carlen PL. 2004. Electrotonic coupling between stratum oriens interneurones in the intact in vitro mouse juvenile hippocampus. J Physiol. 558(Pt 3):825-839.