Intrinsic bursting of AII amacrine cells underlies oscillations in the rd1 mouse retina

Journal of Neurophysiology

Volumn 112, Issue 6, 2014, Pages 1491-1504

  Choi, Hannah ^a   Zhang, Lei ^b   Cembrowski, Mark S ^c   Sabottke, Carl F ^b   Markowitz, Alexander L ^b   Butts, Daniel A ^b   Kath, William L ^a   Singer, Joshua H ^b   Riecke, Hermann ^a  

^a Northwestern University   (United States)

^b University of Maryland   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

AII amacrine cell; Bursting; Oscillation; Retinal degeneration

Indexed keywords

FLUPIRTINE; PDE6B PROTEIN, MOUSE; PHOSPHODIESTERASE VI; POTASSIUM; SODIUM;

ANIMAL CELL; ARTICLE; BLINDNESS; COMPARTMENT MODEL; CONTROLLED STUDY; GAP JUNCTION; INTRACELLULAR RECORDING; MEMBRANE POTENTIAL; MOUSE; NERVE POTENTIAL; NONHUMAN; OSCILLATION; POTASSIUM CONDUCTANCE; POTASSIUM CURRENT; PREDICTIVE VALUE; RETINA AMACRINE CELL; RETINA DISEASE; RETINA GANGLION CELL; SODIUM CONDUCTANCE; SYNAPTIC POTENTIAL; WILD TYPE; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA CONE; RETINA DEGENERATION;

ACTION POTENTIALS; AMACRINE CELLS; ANIMALS; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 6; EXCITATORY POSTSYNAPTIC POTENTIALS; MEMBRANE POTENTIALS; MICE; MODELS, NEUROLOGICAL; POTASSIUM; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL DEGENERATION; RETINAL GANGLION CELLS; SODIUM;

EID: 84907257185     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00437.2014     Document Type: Article

References (37)

1. Adams NA, Awadein A, Toma HS. The retinal ciliopathies. Ophthalmic Genet 28: 113–125, 2007.
2. Apollo N, Grayden DB, Burkitt AN, Meffin H, Kameneva T. Modeling intrinsic electrophysiology of AII amacrine cells: preliminary results. Conf Proc IEEE Eng Med Biol Soc 2013: 6551–6554, 2013.
3. Borowska J, Trenholm S, Awatramani GB. An intrinsic neural oscillator in the degenerating mouse retina. J Neurosci 31: 5000–5012, 2011.
4. Carter-Dawson LD, LaVail MM, Sidman RL. Differential effect of the rd mutation on rods and cones in the mouse retina. Invest Ophthalmol Vis Sci 17: 489–498, 1978.
5. Cembrowski MS, Logan SM, Tian M, Jia L, Li W, Kath WL, Riecke H, Singer JH. The mechanisms of repetitive spike generation in an axonless retinal interneuron. Cell Rep 1: 155–166, 2012.
6. Chang B, Hawes NL, Hurd RE, Davisson MT, Nusinowitz S, Heckenlively JR. Retinal degeneration mutants in the mouse. Vision Res 42: 517–525, 2002.
7. Chang B, Hawes NL, Pardue MT, German AM, Hurd RE, Davisson MT, Nusinowitz S, Rengarajan K, Boyd AP, Sidney SS, Phillips MJ, Stewart RE, Chaudhury R, Nickerson JM, Heckenlively JR, Boatright JH. Two mouse retinal degenerations caused by missense mutations in the betasubunit of rod cGMP phosphodiesterase gene. Vision Res 47: 624–633, 2007.
8. Choi H. Modeling of Oscillations and Bursting in Retinal AII Amacrine Cells (PhD thesis). Evanston, IL: Northwestern Univ., 2014.
9. Demb JB, Singer JH. Intrinsic properties, and functional circuitry of the AII amacrine cell. Vis Neurosci 29: 51–60, 2012.
10. Doroudchi MM, Greenberg KP, Liu J, Silka KA, Boyden ES, Lockridge JA, Arman AC, Janani R, Boye SE, Boye SL, Gordon GM, Matteo BC, Sampath AP, Hauswirth WW, Horsager A. Virally delivered channel-rhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness. Mol Ther 19: 1220–1229, 2011.
11. Fine I, Wade A, Brewer A, May M, Goodman D, Boynton G, Wandell B, MacLeod D. Long-term deprivation affects visual perception and cortex. Nat Neurosci 6: 915–916, 2003.
12. Fitzhugh R. Impulses and physiological states in theoretical models of nerve membrane. Biophys J 1: 445–466, 1961.
13. Habermann C, O’Brien B, Wassle H, Protti D. AII amacrine cells express L-type calcium channels at their output synapses. J Neurosci 23: 6904–6913, 2003.
14. Harris KD, Hirase H, Leinekugel X, Henze DA, Buzsaki G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32: 141–149, 2001.
15. Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet 368: 1795–1809, 2006.
16. Jimenez AJ, Garcia-Fernandez JM, Gonzalez B, Foster RG. The spatiotemporal pattern of photoreceptor degeneration in the aged rd/rd mouse retina. Cell Tissue Res 284: 193–202, 1996.
17. Lagali P, Balya D, Awatramani G, Munch T, Kim D, Busskamp V, Cepko C, Roska B. Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat Neurosci 11: 667–675, 2008.
18. 2+ channels. Vis Neurosci 20: 131–139, 2003.
19. Marc RE, Jones BW, Anderson JR, Kinard K, Marshak DW, Wilson JH, Wensel T, Lucas RJ. Neural reprogramming in retinal degeneration. Invest Ophthalmol Vis Sci 48: 3364–3371, 2007.
20. Margolis DJ, Gartland AJ, Singer JH, Detwiler PB. Network oscillations drive correlated spiking of ON and OFF ganglion cells in the rd1 mouse model of retinal degeneration. PLoS One 9: e86253, 2014.
21. Margolis DJ, Newkirk G, Euler T, Detwiler PB. Functional stability of retinal ganglion cells after degeneration-induced changes in synaptic input. J Neurosci 28: 6526–6536, 2008.
22. Menzler J, Zeck G. Network oscillations in rod-degenerated mouse retinas. J Neurosci 31: 2280–2291, 2011.
23. Murphy G, Rieke F. Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 52: 511–524, 2006.
24. Pan F, Mills SL, Massey SC. Screening of gap junction antagonists on dye coupling in the rabbit retina. Vis Neurosci 24: 609–618, 2007.
25. Quiroga RQ, Nadasdy Z, Ben-Shaul Y. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16: 1661–1687, 2004.
26. Schmitzer-Torbert N, Jackson J, Henze D, Harris K, Redish AD. Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131: 1–11, 2005.
27. Schmitzer-Torbert N, Redish AD. Neuronal activity in the rodent dorsal striatum in sequential navigation: separation of spatial, and reward responses on the multiple T task. J Neurophysiol 91: 2259–2272, 2004.
28. Stasheff SF. 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, 2008.
29. Stingl K, Bartz-Schmidt K, Besch D, Braun A, Bruckmann A, Gekeler F, Greppmaier U, Hipp S, Hortdorfer G, Kernstock C, Koitschev A, Kusnyerik A, Sachs H, Schatz A, Stingl K, Peters T, Wilhelm B, Zrenner E. Artificial vision with wirelessly powered subretinal electronic implant alpha-IMS. Proc Biol Sci 280: 20130077, 2013.
30. Tian M, Jarsky T, Murphy GJ, Rieke F, Singer JH. Voltage-gated Na channels in AII amacrine cells accelerate scotopic light responses mediated by the rod bipolar cell pathway. J Neurosci 30: 4650–4659, 2010.
31. Toychiev AH, Ivanova E, Yee CW, Sagdullaev BT. Block of gap junctions eliminates aberrant activity and restores light responses during retinal degeneration. J Neurosci 33: 13972–13977, 2013.
32. + channels. J Physiol 590: 2501–2517, 2012.
33. Veruki ML, Hartveit E. Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. J Neurosci 22: 10558–10566, 2002.
34. + currents in motor neuron-like cells. Evid Based Complement Alternat Med 2012: 148403, 2012.
35. Ye JH, Goo YS. The slow wave component of retinal activity in rd/rd mice recorded with a multi-electrode array. Physiol Meas 28: 1079–1088, 2007.
36. Yee CW, Toychiev AH, Sagdullaev BT. Network deficiency exacerbates impairment in a mouse model of retinal degeneration. Front Syst Neurosci 6: 8, 2012.
37. Zenisek D, Matthews G. Calcium action potentials in retinal bipolar neurons. Vis Neurosci 15: 69–75, 1998.