Electrical coupling and passive membrane properties of AII amacrine cells

Journal of Neurophysiology

Volumn 103, Issue 3, 2010, Pages 1456-1466

  Veruki, Margaret Lin ^a   Oltedal, Leif ^a   Hartveit, Espen ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; AMPA RECEPTOR; BICUCULLINE; GLYCINE RECEPTOR; MECLOFENAMIC ACID; STRYCHNINE; TETRODOTOXIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTRICAL SYNAPSE; HISTOLOGY; MEMBRANE CONDUCTANCE; MEMBRANE ELECTROPHYSIOLOGY; MEMBRANE RESISTANCE; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA AMACRINE CELL; RETINA CELL; VOLTAGE CLAMP;

AMACRINE CELLS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL POLARITY; DATA INTERPRETATION, STATISTICAL; ELECTROPHYSIOLOGY; GAP JUNCTIONS; MECLOFENAMIC ACID; MEMBRANES; MODELS, NEUROLOGICAL; NERVE NET; PATCH-CLAMP TECHNIQUES; RATS;

EID: 77949686101     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01105.2009     Document Type: Article

References (59)

1. Bennett MVL. Physiology of electrotonic junctions. Ann NY Acad Sci 137: 509-539, 1966.
2. Bennett MVL. Electrical transmission: a functional analysis and comparison to chemical transmission. In: Handbook of Physiology. The Nervous System. Cellular Biology of Neurons. Bethesda, MD: Am. Physiol. Soc, 1977, sect. 1, vol. I, pt. 1, p. 357-416.
3. Bloomfield SA, Dacheux RF. Rod vision: pathways and processing in the mammalian retina. Prog Ret Eye Res 20: 351-384, 2001.
4. Bloomfield SA, Völgyi B. The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat Rev Neurosci 10: 495-506, 2009.
5. Chun MH, Han SH, Chung JW, Wässle H. Electron microscopic analysis of the rod pathway of the rat retina. J Comp Neurol 332: 421-432, 1993.
6. Deans MR, Völgyi B, Goodenough DA, Bloomfield SA, Paul DL. Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36: 703-712, 2002.
7. Dedek K, Schultz K, Pieper M, Dirks P, Maxeiner S, Willecke K, Weiler R, Janssen-Bienhold U. Localization of heterotypic gap junctions composed of connexin45 and connexin36 in the rod pathway of the mouse retina. Eur J Neurosci 24: 1675-1686, 2006.
8. De Zeeuw CI, Chorev E, Devor A, Manor Y, Van Der Giessen RS, De Jeu MT, Hoogenraad CC, Bijman J, Ruigrok TJH, 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 23: 4700-4711, 2003.
9. Dodt H-U, Frick A, Kampe K, Zieglgänsberger W. NMDA and AMPA receptors on neocortical neurons are differentially distributed. Eur J Neurosci 10: 3351-3357, 1998.
10. Gentet LJ, Stuart GJ, Clements JD. Direct measurement of specific membrane capacitance in neurons. Biophys J 79: 314-320, 2000.
11. Gill SB, Veruki ML, Hartveit E. Functional properties of spontaneous IPSCs and glycine receptors in rod amacrine (AII) cells in the rat retina. J Physiol 575: 739-759, 2006.
12. Goaillard J-M, Marder E. Dynamic clamp analysis of cardiac, endocrine, and neural function. Physiology 21: 197-207, 2006.
13. Golding NL, Mickus TJ, Katz Y, Kath WL, Spruston N. Factors mediating powerful attenuation along CA1 pyramidal neuron dendrites. J Physiol 568: 69-82, 2005.
14. Halliwell JV, Plant TD, Robbins J, Standen NB. Voltage clamp techniques. In: Microelectrode Techniques. The Plymouth Workshop Handbook (2nd ed.), edited by Ogden D. Cambridge, UK: The Company of Biologists, 1994, p. 17-35.
15. Hampson EC, Vaney DI, Weiler R. Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J Neurosci 12: 4911-4922, 1992.
16. Han Y, Massey SC. Electrical synapses in retinal ON cone bipolar cells: subtype-specific expression of connexins. Proc Natl Acad Sci USA 102: 13313-13318, 2005.
17. Hartveit E, Veruki ML. Accurate measurement of junctional conductance between electrically coupled cells with dual whole-cell voltage-clamp under conditions of high series resistance. J Neurosci Methods doi:10.1016/ j.jneumeth.2009.12.003, 2010.
18. Hille B. Ion Channels of Excitable Membranes (3rd ed.) Sunderland: Sinauer, 2001.
19. Kolb H. The inner plexiform layer in the retina of the cat: electron microscopic observations. J Neurocytol 8: 295-329, 1979.
20. Kolb H, Famiglietti EV. Rod and cone pathways in the inner plexiform layer of cat retina. Science 186: 47-49, 1974.
21. Kothmann WW, Massey SC, O'Brien J. Dopamine-stimulated dephosphorylation of connexin 36 mediates AII amacrine cell uncoupling. J Neurosci 29: 14903-14911, 2009.
22. + channel, by meclofenamic acid. Eur J Pharmacol 378: 349-356, 1999.
23. Lin B, Jakobs TC, Masland RH. Different functional types of bipolar cells use different gap-junctional proteins. J Neurosci 25: 6696-6701, 2005.
24. Major G. Passive cable modeling - a practical introduction. In: Computational Neuroscience. Realistic Modeling for Experimentalists, edited by De Schutter E. Boca Raton, FL: CRC, 2001, p. 209-232.
25. Manookin MB, Beaudoin DL, Ernst ZR, Flagel LJ, Demb JB. Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. J Neurosci 28: 4136-4150, 2008.
26. Maxeiner S, Dedek K, Janssen-Bienhold U, Ammermü ller J, Brune H, Kirsch T, Pieper M, Degen J, Krüger O, Willecke K, Weiler R. Deletion of connexin45 in mouse retinal neurons disrupts the rod/cone signaling pathway between AII amacrine cells and ON cone bipolar cells and leads to impaired visual transmission. J Neurosci 25: 566-576, 2005.
27. McGuire BA, Stevens JK, Sterling P. Microcircuitry of bipolar cells in rat retina. J Neurosci 4: 2920-2938, 1984.
28. Mills SL, Massey SC. Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377: 734-737, 1995.
29. Mü ller A, Lauven M, Berkels R, Dhein S, Polder H-R, Klaus W. Switched single-electrode voltage-clamp amplifiers allow precise measurement of gap junction conductance. Am J Physiol 276, Cell Physiol 45:C980-C987, 1999.
30. Münch TA, da Silveira RA, Siegert S, Viney TJ, Awatramani GB, Roska B. Approach sensitivity in the retina processed by a multifunctional neural circuit. Nat Neurosci 12: 1308-1316, 2009.
31. Oltedal L, Mørkve SH, Veruki ML, Hartveit E. Patch-clamp investigations and compartmental modeling of rod bipolar axon terminals in an in vitro thin-slice preparation of the mammalian retina. J Neurophysiol 97: 1171-1187, 2007.
32. Oltedal L, Veruki ML, Hartveit E. Passive membrane properties and electrotonic signal processing in retinal rod bipolar cells. J Physiol 587: 829-849, 2009.
33. Pan F, Mills SL, Massey SC. Screening of gap junction antagonists on dye coupling in the rabbit retina. Vis Neurosci 24: 609-618, 2007.
34. Peretz A, Degani N, Nachman R, Uziyel Y, Gibor G, Shabat D, Attali B. Meclofenamic acid and diclofenac, novel templates of KCNQ2/Q3 potassium channel openers, depress cortical neuron activity and exhibit anticonvulsant properties. Mol Pharmacol 67: 1053-1066, 2005.
35. Pourcho RG, Goebel DJ. A combined Golgi and autoradiographic study of (3H)glycine-accumulating amacrine cells in the cat retina. J Comp Neurol 233: 473-480, 1985.
36. Robinson HPC. A scriptable DSP-based system for dynamic conductance injection. J Neurosci Methods 169: 271-281, 2008.
37. Robinson HPC, Kawai N. Injection of digitally synthesized conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49: 157-165, 1993.
38. Roth A, Häusser M. Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch-clamp recordings. J Physiol 535: 445-472, 2001.
39. Sassoè-Pognetto M, Grünert U, Wässle H. Glycinergic synapses in the rod pathway of the rat retina: cone bipolar cells express the α 1 subunit of the glycine receptor. J Neurosci 14: 5131-5146, 1994.
40. Schmidt-Hieber C, Jonas P, Bischofberger J. Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J Neurosci 27: 8430-8441, 2007.
41. Sharp AA, O'Neil MB, Abbott LF, Marder E. Dynamic clamp: computer-generated conductances in real neurons. J Neurophysiol 69: 992-995, 1993.
42. 2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. J Neurosci 23: 10923-10933, 2003.
43. Smith RG, Vardi N. Simulation of the AII amacrine cell of mammalian retina: functional consequences of electrical coupling and regenerative membrane properties. Visual Neurosci 12: 851-860, 1995.
44. Spruston N, Stuart G, Häusser MN. Dendritic integration. In: Dendrites (2nd ed.), edited by Stuart G, Spruston N, Häusser M. Oxford, UK: Oxford Univ. Press, 2008, p. 351-399.
45. Strettoi E, Raviola E, Dacheux RF. Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. J Comp Neurol 325: 152-168, 1992.
46. Strettoi E, Dacheux RF, Raviola E. Cone bipolar cells as interneurons in the rod pathway of the rabbit retina. J Comp Neurol 347: 139-149, 1994.
47. Stuart G, Spruston N. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J Neurosci 18: 3501-3510, 1998.
48. Trexler EB, Li W, Massey SC. Simultaneous contribution of two rod pathways to AII amacrine and cone bipolar cell light responses. J Neurophysiol 93: 1476-1485, 2005.
49. Urschel S, Höher T, Schubert T, Alev C, Söhl G, Wörsdörfer P, Asahara T, Dermietzel R, Weiler R, Willecke K. Protein kinase A-mediated phosphorylation of connexin36 in mouse retina results in decreased gap junctional communication between AII amacrine cells. J Biol Chem 281: 33163-33171, 2006.
50. Vaney DI. Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci Lett 125: 187-190, 1991.
51. van Rijen HVM, Wilders R, van Ginneken ACG, Jongsma HJ. Quantitative analysis of dual whole-cell voltage-clamp determination of gap junctional conductance. Pfluegers 436: 141-151, 1998.
52. Vardi N, Smith RG. The AII amacrine network: coupling can increase correlated activity. Vision Res 36: 3743-3757, 1996.
53. Veruki ML, Hartveit E. AII (rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 33: 935-946, 2002a.
54. Veruki ML, Hartveit E. Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. J Neurosci 22: 10558-10566, 2002b.
55. Veruki ML, Hartveit E. Meclofenamic acid blocks electrical synapses of retinal AII amacrine and ON-cone bipolar cells. J Neurophysiol 101: 2339-2347, 2009.
56. Veruki ML, Mørkve SH, Hartveit E. Functional properties of spontaneous EPSCs and non-NMDA receptors in rod amacrine (AII) cells in the rat retina. J Physiol 549: 759-774, 2003.
57. Veruki ML, Oltedal L, Hartveit E. Electrical synapses between AII amacrine cells: dynamic range and functional consequences of variation in junctional conductance. J Neurophysiol 100: 3305-3322, 2008.
58. Weiss J, O'Sullivan GA, Heinze L, Chen H-X, Betz H, Wässle H. Glycinergic input of small-field amacrine cells in the retinas of wildtype and glycine receptor deficient mice. Mol Cell Neurosci 37: 40-55, 2008.
59. Wu S-N, Jan C-R, Chiang H-T. Fenamates stimulate BKCa channel activity in the human osteoblast-like MG-63 cells. J Investig Med 49: 522-533, 2001.