An intrinsic neural oscillator in the degenerating mouse retina

Journal of Neuroscience

Volumn 31, Issue 13, 2011, Pages 5000-5012

  Borowska, Joanna ^a   Trenholm, Stuart ^a   Awatramani, Gautam B ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NERVE CELL; NONHUMAN; OSCILLATION; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA DEGENERATION; RETINA GANGLION CELL; RETINA NERVE CELL; SYNAPSE;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; FEMALE; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE NET; NEURONS; RETINA; RETINAL DEGENERATION;

EID: 79955720528     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5800-10.2011     Document Type: Article

References (74)

1. Acland GM, Aguirre GD, Ray J, Zhang Q, Aleman TS, Cideciyan AV, Pearce-Kelling SE, Anand V, Zeng Y, Maguire AM, Jacobson SG, Hauswirth WW, Bennett J (2001) Gene therapy restores vision in a canine model of childhood blindness. Nat Genet 28:92-95.
2. Arai I, Tanaka M, Tachibana M (2010) Active roles of electrically coupled bipolar cell network in the adult retina. J Neurosci 30:9260-9270.
3. Awatramani GB, Slaughter MM (2000) Origin of transient and sustained responses in ganglion cells of the retina. J Neurosci 20:7087-7095.
4. Awatramani GB, Slaughter MM (2001) Intensity-dependent, rapid activation of presynaptic metabotropic glutamate receptors at a central synapse. J Neurosci 21:741-749.
5. Awatramani GB, Boyd JD, Delaney KR, Murphy TH (2007) Effective release rates at single rat Schaffer collateral-CAI synapses during sustained thetaburst activity revealed by optical imaging. J Physiol 582:583-595.
6. Barhoum R, Martínez-Navarrete G, Corrochano S, Germain F, Fernandez-Sanchez L, de la Rosa EJ, de la Villa P, Cuenca N (2008) Functional and structural modifications during retinal degeneration in the rd10 mouse. Neuroscience 155:698-713.
7. Berntson A, Taylor WR, Morgans CW (2003) Molecular identity, synaptic localization, and physiology of calcium channels in retinal bipolar cells. J Neurosci Res 71:146-151.
8. Berntson A, Smith RG, Taylor WR (2004) Postsynaptic calcium feedback between rods and rod bipolar cells in the mouse retina. Vis Neurosci 21:913-924.
9. Bi A, Cui J, Ma YP, Olshevskaya E, Pu M, Dizhoor AM, Pan ZH (2006) Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50:23-33.
10. Borowska JT, Trenholm S, Awatramani GB (2010) Intrinsic mechanisms in bipolar cells drive spontaneous network activity during retinal degeneration. ARVO Meet Abstr 46:2486.
11. Brenowitz S, David J, Trussell L (1998) Enhancement of synaptic efficacy by presynaptic GABA(B) receptors. Neuron 20:135-141.
12. + influx in the synaptic terminal of depolarizing bipolar cells from the goldfish retina. J Physiol 505:571-584.
13. Busskamp V, Duebel J, Balya D, Fradot M, Viney TJ, Siegert S, Groner AC, Cabuy E, Forster V, Seeliger M, Biel M, Humphries P, Paques M, Mohand-Said S, Trono D, Deisseroth K, Sahel JA, Picaud S, Roska B (2010) Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329:413-417.
14. Cangiano L, Gargini C, Della Santina L, Demontis GC, Cervetto L (2007) High-pass filtering of input signals by the Ih current in a non-spiking neuron, the retinal rod bipolar cell. PLoS One 2:e1327.
15. Carter-Dawson LD, LaVail MM, Sidman RL (1978) Differential effect of the rd mutation on rods and cones in the mouse retina. Invest Ophthalmol Vis Sci 17:489-498.
16. Chen M, Weng S, Deng Q, Xu Z, He S (2009) Physiological properties of direction-selective ganglion cells in early postnatal and adult mouse retina. J Physiol 587:819-828.
17. Deans MR, Volgyi B, Goodenough DA, Bloomfield SA, Paul DL (2002) Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36:703-712.
18. Diamond JS, Copenhagen DR (1993) The contribution of NMDA and non-NMDA receptors to the light-evoked input-output characteristics of retinal ganglion cells. Neuron 11:725-738.
19. Dunn FA, Rieke F (2008) Single-photon absorptions evoke synaptic depression in the retina to extend the operational range of rod vision. Neuron 57:894-904.
20. Ghosh KK, Bujan S, Haverkamp S, Feigenspan A, Wässle H (2004) Types of bipolar cells in the mouse retina. J Comp Neurol 469:70-82.
21. Hallum LE, Chen SC, Cloherty SL, Lovell NH (2006) Psychophysics of prosthetic vision. II. stochastic sampling, the phosphene image, and noise. Conf Proc IEEE Eng Med Biol Soc 1:1634-1637.
22. Hoelter SM, Dalke C, Kallnik M, Becker L, Horsch M, Schrewe A, Favor J, Klopstock T, Beckers J, Ivandic B, Gailus-Durner V, Fuchs H, Hrabéde Angelis M, Graw J, Wurst W (2008) "Sighted C3H" mice: a tool for analysing the influence of vision on mouse behaviour? Front Biosci 13:5810-5823.
23. + currents in mammalian retinal bipolar cells. Vis Neurosci 19:163-173.
24. Ivanova E, Müller F (2006) Retinal bipolar cell types differ in their inventory of ion channels. Vis Neurosci 23:143-154.
25. Jahr CE, Stevens CF (1990) Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. J Neurosci 10:3178-3182.
26. Kalbaugh TL, Zhang J, Diamond JS (2009) Coagonist release modulates NMDA receptor subtype contributions at synaptic inputs to retinal ganglion cells. J Neurosci 29:1469-1479.
27. Lagali PS, Balya D, Awatramani GB, Münch TA, Kim DS, Busskamp V, Cepko CL, Roska B (2008) Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat Neurosci 11:667-675.
28. Lee YT, Wang Q (1999) Inhibition of hKv2.1, a major human neuronal voltage-gated K_ channel, by meclofenamic acid. Eur J Pharmacol 378:349-356.
29. Lin B, Koizumi A, Tanaka N, Panda S, Masland RH (2008) Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc Natl Acad Sci USA 105:16009-16014.
30. Lin B, Masland RH, Strettoi E (2009) Remodeling of cone photoreceptor cells after rod degeneration in rd mice. Exp Eye Res 88:589-599.
31. Loewenstein Y, Yarom Y, Sompolinsky H (2001) The generation of oscillations in networks of electrically coupled cells. Proc Natl Acad Sci USA 98:8095-8100.
32. + channels. Vis Neurosci 20:131-139.
33. +currents (IKir) with a different distribution than that of Ih. J Neurophysiol 90:3479-3489.
34. MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE, Akimoto M, Swaroop A, Sowden JC, Ali RR (2006) Retinal repair by transplantation of photoreceptor precursors. Nature 444:203-207.
35. MacNeil MA, Masland RH (1998) Extreme diversity among amacrine cells: implications for function. Neuron 20:971-982.
36. Manookin MB, Beaudoin DL, Ernst ZR, Flagel LJ, Demb JB (2008) Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. J Neurosci 28:4136-4150.
37. Manookin MB, Weick M, Stafford BK, Demb JB (2010) NMDA receptor contributions to visual contrast coding. Neuron 67:280-293.
38. Marc RE, Jones BW, Watt CB, Strettoi E (2003) Neural remodeling in retinal degeneration. Prog Retin Eye Res 22:607-655.
39. Marc RE, Jones BW, Anderson JR, Kinard K, Marshak DW, Wilson JH, Wensel T, Lucas RJ (2007) Neural reprogramming in retinal degeneration. Invest Ophthalmol Vis Sci 48:3364-3371.
40. Margolis DJ, Detwiler PB (2011) Cellular origin of spontaneous ganglion cell spike activity in animal models of retinitis pigmentosa. J Ophthalmol pii:507037.
41. Margolis DJ, Newkirk G, Euler T, Detwiler PB (2008) Functional stability of retinal ganglion cells after degeneration-induced changes in synaptic input. J Neurosci 28:6526-6536.
42. Mazzoni F, Novelli E, Strettoi E (2008) Retinal ganglion cells survive and maintain normal dendritic morphology in a mouse model of inherited photoreceptor degeneration. J Neurosci 28:14282-14292.
43. Müller F, Scholten A, Ivanova E, Haverkamp S, Kremmer E, Kaupp UB (2003) HCN channels are expressed differentially in retinal bipolar cells and concentrated at synaptic terminals. Eur J Neurosci 17:2084-2096.
44. Münch TA, da Silveira RA, Siegert S, Viney TJ, Awatramani GB, Roska B (2009) Approach sensitivity in the retina processed by a multifunctional neural circuit. Nat Neurosci 12:1308-1316.
45. Murphy GJ, Rieke F (2008) Signals and noise in an inhibitory interneuron diverge to control activity in nearby retinal ganglion cells. Nat Neurosci 11:318-326.
46. Oesch N, Euler T, Taylor WR (2005) Direction-selective dendritic action potentials in rabbit retina. Neuron 47:739-750.
47. +- dependent action potentials by exocytosis in goldfish bipolar cell terminals. J Physiol 572:747-762.
48. Patel A, Kosko B (2005) Stochastic resonance in noisy spiking retinal and sensory neuron models. Neural Netw 18:467-478.
49. Peretz A, Degani N, Nachman R, Uziyel Y, Gibor G, Shabat D, Attali B (2005) Meclofenamic acid and diclofenac, novel templates of KCNQ2/Q3 potassium channel openers, depress cortial neuron activity and exhibit anticonvulsant properties. Mol Pharmacol 67:1053-1066.
50. Petit-Jacques J, Völgyi B, Rudy B, Bloomfield S (2005) Spontaneous oscillatory activity of starburst amacrine cells in the mouse retina. J Neurophysiol 94:1770-1780.
51. Powers NL, Salvi RJ, Wang J, Spongr V, Qiu CX (1995) Elevation of auditory thresholds by spontaneous cochlear oscillations. Nature 375:585-587.
52. Puthussery T, Taylor WR (2010) Functional changes in inner retinal neurons in animal models of photoreceptor degeneration. Adv Exp Med Biol 664:525-532.
53. Quraishi S, Gayet J, Morgans CW, Duvoisin RM (2007) Distribution of group-III metabotropic glutamate receptors in the retina. J Comp Neurol 501:931-943.
54. Sagdullaev BT, McCall MA, Lukasiewicz PD (2006) Presynaptic inhibition modulates spillover, creating distinct dynamic response ranges of sensory output. Neuron 50:923-935.
55. Singer JH, Diamond JS (2006) Vesicle depletion and synaptic depression at a mammalian ribbon synapse. J Neurophysiol 95:3191-3198.
56. Slaughter MM, Miller RF (1981) 2-amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science 211:182-185.
57. Solessio E, Vigh J, Cuenca N, Rapp K, Lasater EM (2002) Membrane prop-erties of an unusual intrinsically oscillating, wide-field teleost retinal amacrine cell. J Physiol 544:831-847.
58. Stasheff SF (2008) Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse. J Neurophysiol 99:1408-1421.
59. Stasheff SF, Andrews MP (2010) A subpopulation of retinal ganglion cells sustains spontaneous hyperactivity through non-synaptic mechanisms in mice with retinal degeneration. Abstract (5798) presented at the annual meeting of the Association for Research in Vision and Ophthalmology (ARVO), Fort Lauderdale, FL, May.
60. Strettoi E, Pignatelli V (2000) Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proc Natl Acad Sci USA 97:11020-11025.
61. Strettoi E, Porciatti V, Falsini B, Pignatelli V, Rossi C (2002) Morphological and functional abnormalities in the inner retina of the rd/rd mouse. J Neurosci 22:5492-5504.
62. Tropepe V, Coles BL, Chiasson BJ, Horsford DJ, Elia AJ, McInnes RR, van der Kooy D (2000) Retinal stem cells in the adult mammalian eye. Science 287:2032-2036.
63. Vaithianathan T, Sagdullaev BT (2010) Functional remodeling of inner retinal synaptic transmission during photoreceptor degeneration. ARVO Meet Abstr 51:2483.
64. Varela C, Igartua I, De la Rosa EJ, De la Villa P (2003) Functional modifications in rod bipolar cells in a mouse model of retinitis pigmentosa. Vision Res 43:879-885.
65. Veruki ML, Hartveit E (2002) AII (Rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 33:935-946.
66. Veruki ML, Hartveit E (2009) Meclofenamic acid blocks electrical synapses of retinal AII amacrine and on-cone bipolar cells. J Neurophysiol 101: 2339-2347.
67. Vigh J, Solessio E, Morgans CW, Lasater EM (2003) Ionic mechanisms mediating oscillatory membrane potentials in wide-field retinal amacrine cells. J Neurophysiol 90:431-443.
68. von Gersdorff H, Borst JG (2002) Short-term plasticity at the calyx of held. Nat Rev Neurosci 3:53-64.
69. Wässle H, Puller C, Müller F, Haverkamp S (2009) Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J Neurosci 29:106-117.
70. Weiland JD, Liu W, Humayun MS (2005) Retinal prosthesis. Annu Rev Biomed Eng 7:361-401.
71. Ye JH, Goo YS (2007) The slow wave component of retinal activity in rd/rd mice recorded with a multi-electrode array. Physiol Meas 28:1079-1088.
72. Ying SW, Jia F, Abbas SY, Hofmann F, Ludwig A, Goldstein PA (2007) Dendritic HCN2 channels constrain glutamate-driven excitability in reticular thalamic neurons. J Neurosci 27:8719-8732.
73. Zeck G, Menzler J (2010) Network oscillations in rod degenerated (rd1) retina. ARVO Meet Abstr 46:5799.
74. Zhang AJ, Wu SM (2009) Receptive fields of retinal bipolar cells are mediated by heterogeneous synaptic circuitry. J Neurosci 29:789-797.