Rods in daylight act as relay cells for cone-driven horizontal cell-mediated surround inhibition

Nature Neuroscience

Volumn 17, Issue 12, 2014, Pages 1728-1735

  Szikra, Tamas ^a   Trenholm, Stuart ^a,b   Drinnenberg, Antonia ^a,c   Jüttner, Josephine ^a   Raics, Zoltan ^a   Farrow, Karl ^a,l   Biel, Martin ^d   Awatramani, Gautam ^b   Clark, Damon A ^e   Sahel, José Alain ^f,g,h,i,j   Da Silveira, Rava Azeredo ^h,k   Roska, Botond ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF VICTORIA   (Canada)

^c UNIVERSITY OF BASEL   (Switzerland)

^d UNIVERSITY OF MUNICH   (Germany)

^e YALE UNIVERSITY   (United States)

^f SORBONNE UNIVERSITÉ   (France)

^g INSERM   (France)

^h CNRS   (France)

ⁱ CENTRE HOSPITALIER NATIONAL D OPHTALMOLOGIE DES QUINZE VINGTS   (France)

^j FONDATION OPHTALMOLOGIQUE ADOLPHE DE ROTHSCHILD   (France)

^k ECOLE NORMALE SUPÉRIEURE   (France)

^l Belgium   (Belgium)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CONE DRIVEN HORIZONTAL CELL MEDIATED SURROUND INHIBITION; DEPOLARIZATION; HYPERPOLARIZATION; ILLUMINATION; LIGHT INTENSITY; MOUSE; NEGATIVE FEEDBACK; NERVE ENDING; NONHUMAN; PERFORATED PATCH CLAMP; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRIORITY JOURNAL; RECEPTIVE FIELD; SUNLIGHT; ANIMAL; C57BL MOUSE; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; NERVE CELL INHIBITION; NERVE CELL NETWORK; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; RETINA CONE; RETINA HORIZONTAL NERVE CELL; RETINA ROD;

ANIMALS; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE NET; NEURAL INHIBITION; PHOTIC STIMULATION; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL HORIZONTAL CELLS; RETINAL ROD PHOTORECEPTOR CELLS;

EID: 84925222740     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3852     Document Type: Article

References (43)

1. Yau, K.-W. & Hardie, R.C. Phototransduction motifs and variations. Cell 139, 246-264 (2009).
2. Wässle, H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5, 747-757 (2004).
3. Peichl, L. & González-Soriano, J. Morphological types of horizontal cell in rodent retinae: a comparison of rat, mouse, gerbil, and guinea pig. Vis. Neurosci. 11, 501-517 (1994).
4. Kolb, H. The connections between horizontal cells and photoreceptors in the retina of the cat: electron microscopy of Golgi preparations. J. Comp. Neurol. 155, 1-14 (1974).
5. Kolb, H. Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells. Phil. Trans. R. Soc. Lond. B 258, 261-283 (1970).
6. Babai, N. & Thoreson, W.B. Horizontal cell feedback regulates calcium currents and intracellular calcium levels in rod photoreceptors of salamander and mouse retina. J. Physiol. (Lond.) 587, 2353-2364 (2009).
7. Baylor, D.A., Fuortes, M.G. & O'Bryan, P.M. Receptive fields of cones in the retina of the turtle. J. Physiol. (Lond.) 214, 265-294 (1971).
8. Davenport, C.M., Detwiler, P.B. & Dacey, D.M. Effects of pH buffering on horizontal and ganglion cell light responses in primate retina: evidence for the proton hypothesis of surround formation. J. Neurosci. 28, 456-464 (2008).
9. Nelson, R., von Litzow, A., Kolb, H. & Gouras, P. Horizontal cells in cat retina with independent dendritic systems. Science 189, 137-139 (1975).
10. Pan, F. & Massey, S.C. Rod and cone input to horizontal cells in the rabbit retina. J. Comp. Neurol. 500, 815-831 (2007).
11. Thoreson, W.B., Babai, N. & Bartoletti, T.M. Feedback from horizontal cells to rod photoreceptors in vertebrate retina. J. Neurosci. 28, 5691-5695 (2008).
12. Trümpler, J. et al. Rod and cone contributions to horizontal cell light responses in the mouse retina. J. Neurosci. 28, 6818-6825 (2008).
13. Thoreson, W.B. & Mangel, S.C. Lateral interactions in the outer retina. Prog. Retin. Eye Res. 31, 407-441 (2012).
14. Bloomfield, S.A. & Völgyi, B. The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat. Rev. Neurosci. 10, 495-506 (2009).
15. Asteriti, S., Gargini, C. & Cangiano, L. Mouse rods signal through gap junctions with cones. Elife 3, e01386 (2014).
16. Ribelayga, C., Cao, Y. & Mangel, S.C. The circadian clock in the retina controls rod-cone coupling. Neuron 59, 790-801 (2008).
17. Yau, K.W. Phototransduction mechanism in retinal rods and cones. The Friedenwald Lecture. Invest. Ophthalmol. Vis. Sci. 35, 9-32 (1994).
18. Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. Microcircuits for night vision in mouse retina. J. Neurosci. 21, 8616-8623 (2001).
19. Li, P.H., Verweij, J., Long, J.H. & Schnapf, J.L. Gap-junctional coupling of mammalian rod photoreceptors and its effect on visual detection. J. Neurosci. 32, 3552-3562 (2012).
20. Biel, M. et al. Selective loss of cone function in mice lacking the cyclic nucleotide-gated channel CNG3. Proc. Natl. Acad. Sci. USA 96, 7553-7557 (1999).
21. Chang, B. et al. Cone photoreceptor function loss-3, a novel mouse model of achromatopsia due to a mutation in Gnat2. Invest. Ophthalmol. Vis. Sci. 47, 5017-5021 (2006).
22. Altimus, C.M. et al. Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat. Neurosci. 13, 1107-1112 (2010).
23. Lyubarsky, A.L., Falsini, B., Pennesi, M.E., Valentini, P. & Pugh, E.N. Jr. UV-and midwave-sensitive cone-driven retinal responses of the mouse: a possible phenotype for coexpression of cone photopigments. J. Neurosci. 19, 442-455 (1999).
24. Siegert, S. et al. Transcriptional code and disease map for adult retinal cell types. Nat. Neurosci. 15, 487-495, S1-S2 (2012).
25. Berndt, A., Yizhar, O., Gunaydin, L.A., Hegemann, P. & Deisseroth, K. Bi-stable neural state switches. Nat. Neurosci. 12, 229-234 (2009).
26. Vroman, R., Klaassen, L.J. & Kamermans, M. Ephaptic communication in the vertebrate retina. Front. Hum. Neurosci. 7, 612 (2013).
27. Vessey, J.P. et al. Proton-mediated feedback inhibition of presynaptic calcium channels at the cone photoreceptor synapse. J. Neurosci. 25, 4108-4117 (2005).
28. Guo, C., Hirano, A.A., Stella, S.L. Jr., Bitzer, M. & Brecha, N.C. Guinea pig horizontal cells express GABA, the GABA-synthesizing enzyme GAD 65, and the GABA vesicular transporter. J. Comp. Neurol. 518, 1647-1669 (2010).
29. Hirasawa, H. & Kaneko, A. pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2 channels. J. Gen. Physiol. 122, 657-671 (2003).
30. Kamermans, M. et al. Hemichannel-mediated inhibition in the outer retina. Science 292, 1178-1180 (2001).
31. Wang, T.-M., Holzhausen, L.C. & Kramer, R.H. Imaging an optogenetic pH sensor reveals that protons mediate lateral inhibition in the retina. Nat. Neurosci. 17, 262-268 (2014).
32. Liu, X., Hirano, A.A., Sun, X., Brecha, N.C. & Barnes, S. Calcium channels in rat horizontal cells regulate feedback inhibition of photoreceptors through an unconventional GABA-and pH-sensitive mechanism. J. Physiol. (Lond.) 591, 3309-3324 (2013).
33. Clark, D.A., Benichou, R., Meister, M. & Azeredo da Silveira, R. Dynamical adaptation in photoreceptors. PLoS Comput. Biol. 9, e1003289 (2013).
34. Tomomura, M., Rice, D.S., Morgan, J.I. & Yuzaki, M. Purification of Purkinje cells by fluorescence-activated cell sorting from transgenic mice that express green fluorescent protein. Eur. J. Neurosci. 14, 57-63 (2001).
35. Münch, T.A. et al. Approach sensitivity in the retina processed by a multifunctional neural circuit. Nat. Neurosci. 12, 1308-1316 (2009).
36. Deans, M.R., Volgyi, B., Goodenough, D.A., Bloomfield, S.A. & Paul, D.L. Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36, 703-712 (2002).
37. Ke, J.-B. et al. Adaptation to background light enables contrast coding at rod bipolar cell synapses. Neuron 81, 388-401 (2014).
38. Naarendorp, F. et al. Dark light, rod saturation, and the absolute and incremental sensitivity of mouse cone vision. J. Neurosci. 30, 12495-12507 (2010).
39. Grimes, W.N., Schwartz, G.W. & Rieke, F. The synaptic and circuit mechanisms underlying a change in spatial encoding in the retina. Neuron 82, 460-473 (2014).
40. Farrow, K. et al. Ambient illumination toggles a neuronal circuit switch in the retina and visual perception at cone threshold. Neuron 78, 325-338 (2013).
41. Siegert, S. et al. Genetic address book for retinal cell types. Nat. Neurosci. 12, 1197-1204 (2009).
42. Grieger, J.C., Choi, V.W. & Samulski, R.J. Production and characterization of adeno-associated viral vectors. Nat. Protoc. 1, 1412-1428 (2006).
43. Rae, J., Cooper, K., Gates, P. & Watsky, M. Low access resistance perforated patch recordings using amphotericin B. J. Neurosci. Methods 37, 15-26 (1991).