A mammalian retinal bipolar cell uses both graded changes in membrane voltage and all-or-nothing Na + spikes to encode light

Journal of Neuroscience

Volumn 32, Issue 1, 2012, Pages 297-307

  Saszik, Shannon ^a   Devries, Steven H ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHANNEL;

ACTION POTENTIAL; ANIMAL; ARTICLE; CELL MEMBRANE; COMPARATIVE STUDY; FEMALE; LIGHT; MALE; MAMMAL; METHODOLOGY; ORGAN CULTURE TECHNIQUE; PHOTOSTIMULATION; PHYSIOLOGY; RADIATION EXPOSURE; RETINA BIPOLAR GANGLION CELL; SCIURIDAE; VISION;

ACTION POTENTIALS; ANIMALS; CELL MEMBRANE; FEMALE; LIGHT; MALE; MAMMALS; ORGAN CULTURE TECHNIQUES; PHOTIC STIMULATION; RETINAL BIPOLAR CELLS; SCIURIDAE; SODIUM CHANNELS; VISION, OCULAR;

EID: 84855943040     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2739-08.2012     Document Type: Article

References (45)

1. Akaike N (1996) Gramicidin perforated patch recording and intracellular chloride activity in excitable cells. Prog Biophys Mol Biol 65:251-264.
2. Barlow HB (1953) Summation and inhibition in the frog's retina. J Physiol 119:69-88.
3. Baylor DA, Fettiplace R (1977) Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina. J Physiol 271:425-448.
4. Baylor DA, Fuortes MG (1970) Electrical responses of single cones in the retina of the turtle. J Physiol 207:77-92.
5. Cuenca N, Deng P, Linberg KA, Lewis GP, Fisher SK, Kolb H (2002) The neurons of the ground squirrel retina as revealed by immunostains for calcium binding proteins and neurotransmitters. J Neurocytol 31:649-666.
6. Cui J, Pan ZH (2008) Two types of cone bipolar cells express voltage-gated Na_ channels in the rat retina. Vis Neurosci 25:635-645.
7. Dawis SM (1981) Polynomial expressions of pigment nomograms. Vision Res 21:1427-1430.
8. de Ruyter van Steveninck RR, Laughlin SB (1996) Light adaptation and reliability in blowfly photoreceptors. Int J Neural Syst 7:437-444.
9. Demb JB, Haarsma L, Freed MA, Sterling P (1999) Functional circuitry of the retinal ganglion cell's nonlinear receptive field. J Neurosci 19:9756-9767.
10. Demb JB, Zaghloul K, Haarsma L, Sterling P (2001) Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. J Neurosci 21:7447-7454.
11. DeVries SH (2000) Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28:847-856.
12. DeVries SH, Li W, Saszik S (2006) Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50:735-748.
13. Dowling JE, Ripps H (1973) Effect of magnesium on horizontal cell activity in the skate retina. Nature 242:101-103.
14. Dreosti E, Esposti F, Baden T, Lagnado L (2011) In vivo evidence that retinal bipolar cells generate spikes modulated by light. Nat Neurosci 14:951-952.
15. Helgen KM, Cole FR, Helgen LE, Wilson DE (2009) Generic revision in the holarctic ground squirrel genus Spermophilus. J Mammalogy 90:270-305.
16. Hille B (2001) Ion channels of excitable membranes, Ed 3. Sunderland, MA: Sinauer Associates, Inc.
17. Hof RP, Scholtysik G, Loutzenhiser R, Vuorela HJ, Neumann P (1984) PN 200-110, a new calcium antagonist: electrophysiological, inotropic, and chronotropic effects on guinea pig myocardial tissue and effects on contraction and calcium uptake of rabbit aorta. J Cardiovasc Pharmacol 6:399-406.
18. Hu C, Bi A, Pan ZH (2009) Differential expression of three T-type calcium channels in retinal bipolar cells in rats. Vis Neurosci 26:177-187.
19. Ichinose T, Lukasiewicz PD (2007) Ambient light regulates sodium channel activity to dynamically control retinal signaling. J Neurosci 27:4756-4764.
20. Ichinose T, Shields CR, Lukasiewicz PD (2005) Sodium channels in transient retinal bipolar cells enhance visual responses in ganglion cells. J Neurosci 25:1856-1865.
21. Juusola M, French AS (1997) The efficiency of sensory information coding by mechanoreceptor neurons. Neuron 18:959-968.
22. Kaneko A (1970) Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. J Physiol 207:623-633.
23. 2+ current boost graded depolarization of rat retinal amacrine cells in culture. J Neurophysiol 86:1006-1016.
24. Kraft TW (1988) Photocurrents of cone photoreceptors of the goldenmantled ground squirrel. J Physiol 404:199-213.
25. Lasater EM (1986) Ionic currents of cultured horizontal cells isolated from white perch retina. J Neurophysiol 55:499-513.
26. Li W, DeVries SH (2006) Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nat Neurosci 9:669-675.
27. Light AC (2009) Transient and sustained off bipolar cells in the ground squirrel retina. PhD thesis, Northwestern University.
28. Linberg KA, Suemune S, Fisher SK (1996) Retinal neurons of the California ground squirrel, Spermophilus beecheyi: a Golgi study. J Comp Neurol 365:173-216.
29. + channels in mammalian retinal bipolar cells. Vis Neurosci 22:119-133.
30. Mennerick S, Matthews G (1996) Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17:1241-1249.
31. Mennerick S, Matthews G (1998) Rapid calcium-current kinetics in synaptic terminals of goldfish retinal bipolar neurons. Vis Neurosci 15:1051-1056.
32. Pan ZH, Hu HJ (2000) Voltage-dependent Na(+) currents in mammalian retinal cone bipolar cells. J Neurophysiol 84:2564-2571.
33. Pan ZH, Hu HJ, Perring P, Andrade R (2001) T-type Ca(2+) channels mediate neurotransmitter release in retinal bipolar cells. Neuron 32:89-98.
34. 2+ spikes in the axon terminal of a retinal bipolar cell. Neuron 25:215-227.
35. Puller C, Ondreka K, Haverkamp S (2011) Bipolar cells of the ground squirrel retina. J Comp Neurol 519:759-774.
36. Reid RC, Victor JD, Shapley RM (1997) The use of m-sequences in the analysis of visual neurons: linear receptive field properties. Vis Neurosci 14:1015-1027.
37. Schroeder MR (2009) Number theory in science and communication: with applications in cryptography, physics, digital information, computing, and self-similarity, 5th Ed. Berlin: Springer.
38. Shingai R, Christensen BN (1983) Sodium and calcium currents measured in isolated catfish horizontal cells under voltage clamp. Neuroscience 10:893-897.
39. Shingai R, Christensen BN (1986) Excitable properties and voltage-sensitive ion conductances of horizontal cells isolated from catfish (Ictalurus punctatus) retina. J Neurophysiol 56:32-49.
40. 2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. J Neurosci 23:10923-10933.
41. Szmajda BA, DeVries SH (2011) Glutamate spillover between mammalian cone photoreceptors. J Neurosci 31:13431-13441.
42. Tian M, Jarsky T, Murphy GJ, Rieke F, Singer JH (2010) Voltage-gated Na channels in AII amacrine cells accelerate scotopic light responses mediated by the rod bipolar cell pathway. J Neurosci 30:4650-4659.
43. Werblin FS, Dowling JE (1969) Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol 32:339-355.
44. West RW (1976) Light and electron microscopy of the ground squirrel retina: functional considerations. J Comp Neurol 168:355-377.
45. Zenisek D, Henry D, Studholme K, Yazulla S, Matthews G (2001) Voltagedependent sodium channels are expressed in nonspiking retinal bipolar neurons. J Neurosci 21:4543-4550.