Electrical synapses in basal ganglia

Reviews in the Neurosciences

Volumn 18, Issue 1, 2007, Pages 15-35

  Vandecasteele, Marie ^a   Deniau, Jean Michel ^a   Glowinski, Jacques ^a   Venance, Laurent ^a,b  

^a INSERM   (France)

^b l'alimentation et l'Environnement   (France)

Author keywords

Basal ganglia; Connexin; Electrical synapses; Gap junction; Striatum; Substantia nigra pars compacta; Synchronization

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; DYE; GAP JUNCTION PROTEIN; PANNEXIN; PROTEIN DERIVATIVE; TRACER; UNCLASSIFIED DRUG;

BASAL GANGLION; BRAIN NERVE CELL; BRAIN NUCLEUS; CELL COMMUNICATION; CELL FUNCTION; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CELL ULTRASTRUCTURE; CORPUS STRIATUM; EPHAPSE; HUMAN; NONHUMAN; PATHOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SUBSTANTIA NIGRA; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; NERVE CELL NETWORK; SYNAPTIC TRANSMISSION; ULTRASTRUCTURE;

ANIMALS; BASAL GANGLIA; GAP JUNCTIONS; HUMANS; MODELS, NEUROLOGICAL; NERVE NET; SYNAPTIC TRANSMISSION;

EID: 34248567884     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/REVNEURO.2007.18.1.15     Document Type: Review

References (155)

1. Amitai Y, Gibson JR, Beierlein M, Patrick SL, Ho AM, Connors BW, Golomb D. The spatial dimensions of electrically coupled networks of interneurons in the neocortex. J Neurosci 2002; 22: 4142-4152.
2. Andrade-Rozental AF, Rozental R, Hopperstad MG, Wu JK, Vrionis FD, Spray DC. Gap junctions: the "kiss of death" and the "kiss of life". Brain Res Brain Res Rev 2000; 32: 308-315.
3. Audesirk G, Audesirk T, Bowsher P. Variability and frequent failure of lucifer yellow to pass between two electrically coupled neurons in Lymnaea stagnalis. J Neurobiol 1982; 13: 369-375.
4. Ballantyne D, Andrzejewski M, Muckenhoff K, Scheid P. Rhythms, synchrony and electrical coupling in the locus coeruleus. Respir Physiol Neurobiol 2004; 143: 199-214.
5. Bamford NS, Robinson S, Palmiter RD, Joyce JA, Moore C, Meshul CK. Dopamine modulates release from corticostriatal terminals. J Neurosci 2004; 24: 9541-9552.
6. Bamford NS, Zhang H, Schmitz Y, Wu NP, Cepeda C, Levine MS, Schmauss C, Zakharenko SS, Zablow L, Sulzer D. Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 2004; 42: 653-663.
7. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P. Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 2001; 21: 2687-2698.
8. Bayer VE, Pickel VM. Ultrastructural localization of tyrosine hydroxylase in the rat ventral tegmental area: relationship between immunolabeling density and heuronal associations. J Neurosci 1990; 10: 2996-3013.
9. Beierlein M, Gibson JR, Connors BW. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 2000; 3: 904-910.
10. Belluardo N, Mudo G, Trovato-Salinaro A, Le Gurun S, Charollais A, Serre-Beinier V, Amato G, Haefliger JA, Meda P, Condorelli DF. Expression of connexin36 in the adult and developing rat brain. Brain Res 2000; 865: 121-38.
11. Bennett MV, Zukin RS. Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 2004; 41: 495-511.
12. Berger B, Thierry AM, Tassin JP, Moyne MA. Dopaminergic innervation of the rat prefrontal cortex: a fluorescence histochemical study. Brain Res 1976; 106: 133-145.
13. Berke JD, Okatan M, Skurski J, Eichenbaum HB. Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 2004; 43: 883-896.
14. Bishop GA, Chang HT, Kitai ST. Morphological and physiological properties of neostriatal neurons: an intracellular horseradish peroxidase study in the rat. Neuroscience 1982; 7: 179-191.
15. Bou-Flores C, Berger AJ. Gap junctions and inhibitory synapses modulate inspiratory motoneuron synchronization. J Neurophysiol 2001; 85: 1543-1551.
16. Bruzzone R, White TW, Paul DL. Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem 1996; 238: 1-27.
17. Bruzzone R, Hormuzdi SG, Barbe MT, Herb A, Monyer H. Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci USA 2003; 100: 13644-13649.
18. Buhl DL, Harris KD, Hormuzdi SG, Monyer H, Buzsaki G. Selective impairment of hippocampal gamma oscillations in connexin-36 knock-out mouse in vivo. J Neurosci 2003; 23: 1013-1018.
19. Bukauskas FF, Verselis VK. Gap junction channel gating. Biochim Biophys Acta 2004; 1662: 42-60.
20. Burke RE. Postnatal developmental programmed cell death in dopamine neurons. Ann NY Acad Sci 2003; 991: 69-79.
21. Calabresi P, Misgeld U, Dodt HU. Intrinsic membrane properties of neostriatal neurons can account for their low level of spontaneous activity. Neuroscience 1987; 20: 293-303.
22. Calabresi P, Centonze D, Bernardi G. Electrophysiology of dopamine in normal and denervated striatal neurons. Trends Neurosci 2000; 23: S57-63.
23. Cepeda C, Walsh JP, Hull CD, Howard SG, Buchwald NA, Levine MS. Dye-coupling in the neostriatum of the rat: I. Modulation by dopamine-depleting lesions. Synapse 1989; 4: 229-237.
24. Cepeda C, Walsh JP, Buchwald NA, Levine MS. Neurophysiological maturation of cat caudate neurons: evidence from in vitro studies. Synapse 1991; 7: 278-290.
25. Chang HT, Wilson CJ, Kitai ST. A Golgi study of rat neostriatal neurons: light microscopic analysis. J Comp Neurol 1982; 208: 107-126.
26. Chang HT, Kita H, Kitai ST. The fine structure of the rat subthalamic nucleus: an electron microscopic study. J Comp Neurol 1983; 221: 113-123.
27. Chen LW, Wei LC, Lang B, Ju G, Chan YS. Differential expression of AMPA receptor subunits in dopamine neurons of the rat brain: a double immunocytochemical study. Neuroscience 2001; 106: 149-160.
28. Christie JM, Bark C, Hormuzdi SG, Helbig I, Monyer H, Westbrook GL. Connexin36 mediates spike synchrony in olfactory bulb glomeruli. Neuron 2005; 46: 761-772.
29. Christie MJ, Williams JT, North RA. Electrical coupling synchronizes subthreshold activity in locus coeruleus neurons in vitro from neonatal rats. J Neurosci 1989; 9: 3584-3589.
30. Condorelli DF, Parenti R, Spinella F, Trovato Salinaro A, 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.
31. Condorelli DF, Belluardo N, Trovato-Salinaro A, Mudo G. Expression of Cx36 in mammalian neurons. Brain Res Brain Res Rev 2000; 32: 72-85.
32. Condorelli DF, Trovato-Salinaro A, Mudo G, Mirone MB, Belluardo N. Cellular expression of connexins in the rat brain: neuronal localization, effects of kainate-induced seizures and expression in apoptotic neuronal cells. Eur J Neurosci 2003; 18: 1807-1827.
33. Connors BW, Long MA. Electrical synapses in the mammalian brain. Annu Rev Neurosci 2004; 27: 393-418.
34. Czubayko U, Plenz D. Fast synaptic transmission between striatal spiny projection neurons. Proc Natl Acad Sci USA 2002; 99: 15764-15769.
35. De Zeeuw CI, Chorev E, Devor A, Manor Y, Van Der Giessen RS, De Jeu MT, Hoogenraad CC, Bijman J, Ruigrok TJ, French P, Jaarsma D, Kistler WM, Meier C, Petrasch-Parwez E, Dermietzel R, Sohl G, Gueldenagel M, Willecke K, Yarom Y. Deformation of network connectivity in the inferior olive of connexin 36-deficient mice is compensated by morphological and electrophysiological changes at the single neuron level. J Neurosci 2003; 23: 4700-4711.
36. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 2001; 31: 477-485.
37. Degen J, Meier C, Van Der Giessen RS, Sohl G, Petrasch-Parwez E, Urschel S, Dermietzel R, Schilling K, De Zeeuw CI, Willecke K. Expression pattern of lacZ reporter gene representing connexin36 in transgenic mice. J Comp Neurol 2004; 473: 511-525.
38. Dermietzel R, Spray DC. Gap junctions in the brain: where, what type, how many and why? Trends Neurosci 1993; 16: 186-192.
39. Devor A, Yarom Y. Electrotonic coupling in the inferior olivary nucleus revealed by simultaneous double patch recordings. J Neurophysiol 2002; 87: 3048-3058.
40. Fallon JH, Moore RY. Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J Comp Neurol 1978; 180: 545-580.
41. Fallon JH. Collateralization of monoamine neurons: mesotelencephalic dopamine projections to caudate, septum, and frontal cortex. J Neurosci 1981; 1: 1361-1368.
42. Fricker D, Miles R. Interneurons, spike timing, and perception. Neuron 2001; 32: 771-774.
43. Gajda Z, Szupera Z, Blazso G, Szente M. Quinine, a blocker of neuronal cx36 channels, suppresses seizure activity in rat neocortex in vivo. Epilepsia 2005; 46: 1581-1591.
44. Galarreta M, Hestrin S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 1999; 402: 72-75.
45. Galarreta M, Hestrin S. Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2001; 2: 425-433.
46. Galarreta M, Hestrin S. Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc Natl Acad Sci USA 2002; 99: 12438-12443.
47. Gauthier J, Parent M, Levesque M, Parent A. The axonal arborization of single nigrostriatal neurons in rats. Brain Res 1999; 834: 228-232.
48. Gerfen CR. The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 1984; 311: 461-464.
49. Gerfen CR. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 1992; 15: 133-139.
50. Gibson JR, Beierlein M, Connors BW. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 1999; 402: 75-79.
51. Gibson JR, Beierlein M, Connors BW. Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4. J Neurophysiol 2005; 93: 467-480.
52. Gonon FG. Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 1988; 24: 19-28.
53. Grace AA, Bunney BS. Intracellular and extracellular electrophysiology of nigral dopaminergic neurons-3. Evidence for electrotonic coupling. Neuroscience 1983; 10: 333-348.
54. Grace AA, Onn SP. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 1989; 9: 3463-3481.
55. Graybiel AM, Ragsdale CW Jr. Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining. Proc Natl Acad Sci USA 1978; 75: 5723-5726.
56. Graybiel AM, Aosaki T, Flaherty AW, Kimura M. The basal ganglia and adaptive motor control. Science 1994; 265: 1826-1831.
57. Guldenagel M, Ammermuller J, Feigenspan A, Teubner B, Degen J, Sohl G, Willecke K, Weiler R. Visual transmission deficits in mice with targeted disruption of the gap junction gene connexin36. J Neurosci 2001; 21: 6036-6044.
58. Guzman JN, Hernandez A, Galarraga E, Tapia D, Laville A, Vergara R, Aceves J, Bargas J. Dopaminergic modulation of axon collaterals interconnecting spiny neurons of the rat striatum. J Neurosci 2003; 23: 8931-8940.
59. Hajos M, Greenfield SA. Topographic heterogeneity of substantia nigra neurons: diversity in intrinsic membrane properties and synaptic inputs. Neuroscience 1993; 55: 919-934.
60. Harris AL. Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 2001; 34: 325-472.
61. Herkenham M, Pert CB. Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature 1981; 291: 415-418.
62. Hormuzdi SG, Pais I, LeBeau FE, Towers SK, Rozov A, Buhl EH, Whittington MA, Monyer H. Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 2001; 31: 487-495.
63. Hormuzdi SG, Filippov MA, Mitropoulou G, Monyer H, Bruzzone R. Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks. Biochim Biophys Acta 2004; 1662: 113-137.
64. Hutchison WD, Dostrovsky JO, Walters JR, Courtemanche R, Boraud T, Goldberg J, Brown P. Neuronal oscillations in the basal ganglia and movement disorders: evidence from whole animal and human recordings. J Neurosci 2004; 24: 9240-9243.
65. Kawaguchi Y. Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 1993; 13: 4908-4923.
66. Kita H, Kita T, Kitai ST. Active membrane properties of rat neostriatal neurons in an in vitro slice preparation. Exp Brain Res 1985; 60: 54-62.
67. Kita H, Kosaka T, Heizmann CW. Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 1990; 536: 1-15.
68. Kita H. Glutamatergic and GABAergic postsynaptic responses of striatal spiny neurons to intrastriatal and cortical stimulation recorded in slice preparations. Neuroscience 1996; 70: 925-940.
69. Klink R, de Kerchove d'Exaerde A, Zoli M, Changeux JP. Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 2001; 21: 1452-1463.
70. Komendantov AO, Canavier CC. Electrical coupling between model midbrain dopamine neurons: effects on firing pattern and synchrony. J Neurophysiol 2002; 87: 1526-1541.
71. Koos T, Tepper JM. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 1999; 2: 467-472.
72. Koos T, Tepper JM, Wilson CJ. Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum. J Neurosci 2004; 24: 7916-7922.
73. Kopell N, Ermentrout B. Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks. Proc Natl Acad Sci USA 2004; 101: 15482-15487.
74. Landisman CE, Long MA, Beierlein M, Deans MR, Paul DL, Connors BW. Electrical synapses in the thalamic reticular nucleus. J Neurosci 2002; 22: 1002-1009.
75. Leung DS, Unsicker K, Reuss B. Expression and developmental regulation of gap junction connexins cx26, cx32, cx43 and cx45 in the rat midbrain-floor. Int J Dev Neurosci 2002; 20: 63-75.
76. Lin JY, van Wyk M, Bowala TK, Teo MY, Lipski J. Dendritic projections and dye-coupling in dopaminergic neurons of the substantia nigra examined in horizontal brain slices from young rats. J Neurophysiol 2003; 90: 2531-2535.
77. Ljungberg T, Apicella P, Schultz W. Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 1992; 67: 145-163.
78. Long MA, Deans MR, Paul DL, Connors BW. Rhythmicity without synchrony in the electrically uncoupled inferior olive. J Neurosci 2002; 22: 10898-10905.
79. Long MA, Landisman CE, Connors BW. Small clusters of electrically coupled neurons generate synchronous rhythms in the thalamic reticular nucleus. J Neurosci 2004; 24: 341-349.
80. Long MA, Jutras MJ, Connors BW, Burwell RD. Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat Neurosci 2005; 8: 61-66.
81. Loughlin SE, Fallon JH. Dopaminergic and non-dopaminergic projections to amygdala from substantia nigra and ventral tegmental area. Brain Res 1983; 262: 334-338.
82. Mahon S, Deniau JM, Charpier S. Relationship between EEG potentials and intracellular activity of striatal and cortico-striatal neurons: an in vivo study under different anesthetics. Cereb Cortex 2001; 11: 360-373.
83. Maier N, Guldenagel M, Sohl G, Siegmund H, Willecke K, Draguhn A. Reduction of high-frequency network oscillations (ripples) and pathological network discharges in hippocampal slices from connexin 36-deficient mice. J Physiol 2002; 541: 521-528.
84. Mallet N, Le Moine C, Charpier S, Gonon F. Feed-forward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J Neurosci 2005; 25: 3857-3869.
85. Mann-Metzer P, Yarom Y. Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J Neurosci 1999; 19: 3298-3306.
86. Marti MJ, James CJ, Oo TF, Kelly WJ, Burke RE. Early developmental destruction of terminals in the striatal target induces apoptosis in dopamine neurons of the substantia nigra. J Neurosci 1997; 17: 2030-2039.
87. Maxeiner S, Kruger O, Schilling K, Traub O, Urschel S, Willecke K. Spatiotemporal transcription of connexin45 during brain development results in neuronal expression in adult mice. Neuroscience 2003; 119: 689-700.
88. McCracken CB, Hamby SM, Patel KM, Morgan D, Vrana KE, Roberts DC. Extended cocaine self-administration and deprivation produces region-specific and time-dependent changes in connexin36 expression in rat brain. Synapse 2005; 58: 141-150.
89. McCracken CB, Patel KM, Vrana KE, Paul DL, Roberts DC. Amphetamine withdrawal produces region-specific and time-dependent changes in connexin36 expression in rat brain. Synapse 2005; 56: 39-44.
90. Meyer AH, Katona I, Blatow M, Rozov A, Monyer H. In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci 2002; 22: 7055-7064.
91. Micevych PE, Abelson L. Distribution of mRNAs coding for liver and heart gap junction proteins in the rat central nervous system. J Comp Neurol 1991; 305: 96-118.
92. Moreno AP. Biophysical properties of homomeric and heteromultimeric channels formed by cardiac connexins. Cardiovasc Res 2004; 62: 276-286.
93. Morris G, Arkadir D, Nevet A, Vaadia E, Bergman H. Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons. Neuron 2004; 43: 133-143.
94. Nakase T, Naus CC. Gap junctions and neurological disorders of the central nervous system. Biochim Biophys Acta 2004; 1662: 149-158.
95. Neuhoff H, Neu A, Liss B, Roeper J. I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 2002; 22: 1290-1302.
96. Nicola SM, Surmeier J, Malenka RC. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 2000; 23: 185-215.
97. Nisenbaum ES, Xu ZC, Wilson CJ. Contribution of a slowly inactivating potassium current to the transition to firing of neostriatal spiny projection neurons. J Neurophysiol 1994; 71: 1174-1189.
98. Nisenbaum ES, Wilson CJ. Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J Neurosci 1995; 15: 4449-4463.
99. O'Donnell P, Grace AA. Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens. J Neurosci 1993; 13: 3456-3471.
100. O'Donnell P, Grace AA. Different effects of subchronic clozapine and Haloperidol on dye-coupling between neurons in the rat striatal complex. Neuroscience 1995; 66: 763-767
101. O'Donnell P, Grace AA. Dopaminergic reduction of excitability in nucleus accumbens neurons recorded in vitro. Neuropsychopharmacology 1996; 15: 87-97.
102. O'Donnell P, Grace AA. Cortical afferents modulate striatal gap junction permeability via nitric oxide. Neuroscience 1997; 76: 1-5.
103. Oades RD, Halliday GM. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res 1987; 434: 117-165.
104. Obeso JA, Rodriguez-Oroz MC, Rodriguez M, Lanciego JL, Artieda J, Gonzalo N, Olanow CW. Pathophysiology of the basal ganglia in Parkinson's disease. Trends Neurosci 2000; 23: S8-19.
105. Odermatt B, Weilershaus K, Wallraff A, Seifert G, Degen J, Euwens C, Fuss B, Bussow H, Schilling K, Steinhauser C, Willecke K. Connexin 47 (Cx47)-deficient mice with enhanced green fluorescent protein reporter gene reveal predominant oligodendrocytic expression of Cx47 and display vacuolized myelin in the CNS. J Neurosci 2003; 23: 4549-4559.
106. Onn SP, Grace AA. Dye coupling between rat striatal neurons recorded in vivo: compartmental organization and modulation by dopamine. J Neurophysiol 1994; 71: 1917-1934.
107. Onn SP, Grace AA. Repeated treatment with haloperidol and clozapine exerts differential effects on dye coupling between neurons in subregions of striatum and nucleus accumbens. J Neurosci 1995; 15: 7024-7036.
108. Onn SP, Grace AA. Amphetamine withdrawal alters bistable states and cellular coupling in rat prefrontal cortex and nucleus accumbens neurons recorded in vivo. J Neurosci 2000; 20: 2332-2345.
109. Onn SP, West AR, Grace AA. Dopamine-mediated regulation of striatal neuronal and network interactions. Trends Neurosci 2000; 23: S48-56.
110. Parenti R, Gulisano M, Zappala A, Cicirata F. Expression of connexin36 mRNA in adult rodent brain. NeuroReport 2000; 11: 1497-1502.
111. Parthasarathy HB, Graybiel AM. Cortically driven immediate-early gene expression reflects modular influence of sensorimotor cortex on identified striatal neurons in the squirrel monkey. J Neurosci 1997; 17: 2477-2491.
112. Pereda A, Triller A, Korn H, Faber DS. Dopamine enhances both electrotonic coupling and chemical excitatory postsynaptic potentials at mixed synapses. Proc Natl Acad Sci USA 1992; 89: 12088-12092.
113. Pfeuty B, Mato G, Golomb D, Hansel D. Electrical synapses and synchrony: the role of intrinsic currents. J Neurosci 2003; 23: 6280-6294.
114. Pfeuty B, Mato G, Golomb D, Hansel D. The combined effects of inhibitory and electrical synapses in synchrony. Neural Comput 2005; 17: 633-670.
115. Prinz AA, Fromherz P. Effect of neuritic cables on conductance estimates for remote electrical synapses. J Neurophysiol 2003; 89: 2215-2224.
116. Rabbah P, Golowasch J, Nadim F. Effect of electrical coupling on ionic current and synaptic potential measurements. J Neurophysiol 2005; 94: 519-530.
117. Ray A, Zoidl G, Weickert S, Wahle P, Dermietzel R. Site-specific and developmental expression of pannexin1 in the mouse nervous system. Eur J Neurosci 2005; 21: 3277-3290.
118. Reyes A, Galarraga E, Flores-Hernandez J, Tapia D, Bargas J. Passive properties of neostriatal neurons during potassium conductance blockade. Exp Brain Res 1998; 120: 70-84.
119. Reynolds JN, Wickens JR. Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw 2002; 15: 507-521.
120. Romo R, Schultz W. Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements. J Neurophysiol 1990; 63: 592-606.
121. Rorig B, Klausa G, Sutor B. Beta-adrenoreceptor activation reduces dye-coupling between immature rat neocortical neurones. NeuroReport 1995; 6: 1811-1815.
122. Rorig B, Klausa G, Sutor B. Dye coupling between pyramidal neurons in developing rat prefrontal and frontal cortex is reduced by protein kinase A activation and dopamine. J Neurosci 1995; 15: 7386-7400.
123. Rorig B, Sutor B. Serotonin regulates gap junction coupling in the developing rat somatosensory cortex. Eur J Neurosci 1996; 8: 1685-1695.
124. Rouach N, Avignone E, Meme W, Koulakoff A, Venance L, Blomstrand F, Giaume C. Gap junctions and connexin expression in the normal and pathological central nervous system. Biol Cell 2002; 94: 457-475.
125. Rouach N, Koulakoff A, Giaume C. Neurons set the tone of gap junctional communication in astrocytic networks. Neurochem Int 2004; 45: 265-272.
126. Saez JC, Berthoud VM, Branes MC, Martinez AD, Beyer EC. Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 2003; 83: 1359-1400.
127. Scatton B, Simon H, Le Moal M, Bischoff S. Origin of dopaminergic innervation of the rat hippocampal formation. Neurosci Lett 1980; 18: 125-131.
128. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD. Axo-axonal coupling. A novel mechanism for ultrafast neuronal communication. Neuron 2001; 31: 831-840.
129. Schnitzler A, Gross J. Normal and pathological oscillatory communication in the brain. Nat Rev Neurosci 2005; 6: 285-296.
130. Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science 1997; 275: 1593-1599.
131. Seroogy K, Tsuruo Y, Hokfelt T, Walsh J, Fahrenkrug J, Emson PC, Goldstein M. Further analysis of presence of peptides in dopamine neurons. Cholecystokinin, peptide histidine-isoleucine/vasoactive intestinal polypeptide and substance P in rat supramammillary region and mesencephalon. Exp Brain Res 1988; 72: 523-534.
132. Shinohara K, Hiruma H, Funabashi T, Kimura F. GABAergic modulation of gap junction communication in slice cultures of the rat suprachiasmatic nucleus. Neuroscience 2000; 96: 591-596.
133. Sloper JJ. Gap junctions between dendrites in the primate neocortex. Brain Res 1972; 44: 641-646.
134. Sloper JJ, Powell TP. Gap junctions between dendrites and somata of neurons in the primate sensori-motor cortex. Proc R Soc Lond B Biol Sci 1978; 203: 39-47.
135. Smith Y, Kieval JZ. Anatomy of the dopamine system in the basal ganglia. Trends Neurosci 2000; 23: S28-33.
136. Sotelo C, Llinas R. Specialized membrane junctions between neurons in the vertebrate cerebellar cortex. J Cell Biol 1972; 53: 271-289.
137. Stern EA, Jaeger D, Wilson CJ. Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo. Nature 1998; 394: 475-478.
138. Surmeier DJ, Song WJ, Yan Z. Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci 1996; 16: 6579-6591.
139. Vandecasteele M, Glowinski J, Venance L. Electrical synapses between dopaminergic neurons of the substantia nigra pars compacta. J Neurosci 2005; 25: 291-298.
140. Vandecasteele M, Glowinski J, Venance L. Connexin mRNA expression in single dopaminergic neurons of substatia nigra pars compacta. Neurosci Res 2006; 56: 419-426.
141. Venance L, Premont J, Glowinski J, Giaume C. Gap junctional communication and pharmacological heterogeneity in astrocytes cultured from the rat striatum. J Physiol 1998; 510: 429-240.
142. Venance L, Rozov A, Blatow M, Burnashev N, Feldmeyer D, Monyer H. Connexin expression in electrically coupled postnatal rat brain neurons. Proc Natl Acad Sci USA 2000; 97: 10260-10265.
143. Venance L, Glowinski J. Heterogeneity of spike frequency adaptation among medium spiny neurones from the rat striatum. Neuroscience 2003; 122: 77-92.
144. Venance L, Glowinski J, Giaume C. Electrical and chemical transmission between striatal GABAergic output neurones in rat brain slices. J Physiol 2004; 559: 215-230.
145. Veruki ML, Hartveit E. AII (rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 2002; 33: 935-946.
146. Veruki ML, Hartveit E. Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. J Neurosci 2002; 22: 10558-10566.
147. Vis JC, Nicholson LF, Faull RL, Evans WH, Severs NJ, Green CR. Connexin expression in Huntington's diseased human brain. Cell Biol Int 1998; 22: 837-847.
148. Volterra A, Meldolesi J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 2005; 6: 626-640.
149. Walsh JP, Cepeda C, Hull CD, Fisher RS, Levine MS, Buchwald NA. Dye-coupling in the neostriatum of the rat: II. Decreased coupling between neurons during development. Synapse 1989; 4: 238-247.
150. Walsh JP, Cepeda C, Buchwald NA, Levine MS. Neurophysiological maturation of cat substantia nigra neurons: evidence from in vitro studies. Synapse 1991; 7: 291-300.
151. Watanabe M, Ito H, Ikushima M. Cytoarchitecture and ultrastructure of the avian ectostriatum: afferent terminals from the dorsal telencephalon and some nuclei in the thalamus. J Comp Neurol 1985; 236: 241-257.
152. Wickens JR, Arbuthnott GW. The corticostriatal system on computer simulation: an intermediate mechanism for sequencing of actions. Prog Brain Res 1993; 99: 325-339.
153. Willecke K, Eiberger J, Degen J, Eckardt D, Romualdi A, Guldenagel M, Deutsch U, Sohl G. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem 2002; 383: 725-737.
154. Wilson CJ. The contribution of cortical neurons to the firing pattern of striatal spiny neurons. In: Houk JC, David JL, Beiser DG, eds. Model of Information Processing in Basal Ganglia. Cambridge, MA: MIT Press, 1995; 29-50.
155. Wilson CJ, Kawaguchi Y. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 1996; 16: 2397-2410.