PH Changes in the Invaginating Synaptic Cleft Mediate Feedback from Horizontal Cells to Cone Photoreceptors by Modulating Ca2+ Channels

Overview

Journal J Gen Physiol

Specialty Physiology

Date 2003 Nov 12

PMID 14610018

Citations 112

Authors

Hajime Hirasawa

Akimichi Kaneko

Affiliations

Soon will be listed here.

Abstract

Feedback from horizontal cells (HCs) to cone photoreceptors plays a key role in the center-surround-receptive field organization of retinal neurons. Recordings from cone photoreceptors in newt retinal slices were obtained by the whole-cell patch-clamp technique, using a superfusate containing a GABA antagonist (100 microM picrotoxin). Surround illumination of the receptive field increased the voltage-dependent calcium current (ICa) in the cones, and shifted the activation voltage of ICa to negative voltages. External alkalinization also increased cone ICa and shifted its activation voltage toward negative voltages. Enrichment of the pH buffering capacity of the extracellular solution increased cone ICa, and blocked any additional increase in cone ICa by surround illumination. Hyperpolarization of the HCs by a glutamate receptor antagonist-augmented cone ICa, whereas depolarization of the HCs by kainate suppressed cone ICa. From these results, we propose the hypothesis that pH changes in the synaptic clefts, which are intimately related to the membrane voltage of the HCs, mediate the feedback from the HCs to cone photoreceptors. The feedback mediated by pH changes in the synaptic cleft may serve as an additional mechanism for the center-surround organization of the receptive field in the outer retina.

Citing Articles

pH in the vertebrate retina and its naturally occurring and pathological changes.

Dmitriev A, Linsenmeier R Prog Retin Eye Res. 2024; 104():101321.

PMID: 39608565 PMC: 11711014. DOI: 10.1016/j.preteyeres.2024.101321.

Rod inputs arrive at horizontal cell somas in mouse retina solely via rod-cone coupling.

Thoreson W, Sladek A, Barta C, Townsend L bioRxiv. 2024; .

PMID: 39554062 PMC: 11565799. DOI: 10.1101/2024.10.30.621116.

The sodium-bicarbonate cotransporter Slc4a5 mediates feedback at the first synapse of vision.

Morikawa R, Rodrigues T, Schreyer H, Cowan C, Nadeau S, Graff-Meyer A Neuron. 2024; 112(22):3715-3733.e9.

PMID: 39317184 PMC: 11602199. DOI: 10.1016/j.neuron.2024.08.015.

Dye coupling of horizontal cells in the primate retina.

Pan F, Massey S Front Ophthalmol (Lausanne). 2024; 3:1173706.

PMID: 38983052 PMC: 11182241. DOI: 10.3389/fopht.2023.1173706.

Presynaptic Proteins and Their Roles in Visual Processing by the Retina.

Thoreson W, Zenisek D Annu Rev Vis Sci. 2024; 10(1):347-375.

PMID: 38621251 PMC: 11536687. DOI: 10.1146/annurev-vision-101322-111204.

References

Nakatani K, Yau K . Calcium and light adaptation in retinal rods and cones. Nature. 1988; 334(6177):69-71. DOI: 10.1038/334069a0. View

Krafte D, Kass R . Hydrogen ion modulation of Ca channel current in cardiac ventricular cells. Evidence for multiple mechanisms. J Gen Physiol. 1988; 91(5):641-57. PMC: 2216148. DOI: 10.1085/jgp.91.5.641. View

St Jules R . L-type calcium channels in the photoreceptor ribbon synapse: localization and role in plasticity. J Comp Neurol. 1999; 415(1):1-16. View

Kraaij D, Spekreijse H, Kamermans M . The nature of surround-induced depolarizing responses in goldfish cones. J Gen Physiol. 1999; 115(1):3-16. PMC: 1887777. DOI: 10.1085/jgp.115.1.3. View

Pattnaik B, Jellali A, Sahel J, Dreyfus H, Picaud S . GABAC receptors are localized with microtubule-associated protein 1B in mammalian cone photoreceptors. J Neurosci. 2000; 20(18):6789-96. PMC: 6772813. View

Molina A, Smith P, Malchow R . Hydrogen ion fluxes from isolated retinal horizontal cells: modulation by glutamate. Biol Bull. 2000; 199(2):168-70. DOI: 10.2307/1542879. View

Ihle E, Patneau D . Modulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor desensitization by extracellular protons. Mol Pharmacol. 2000; 58(6):1204-12. DOI: 10.1124/mol.58.6.1204. View

Ransom B . Glial modulation of neural excitability mediated by extracellular pH: a hypothesis revisited. Prog Brain Res. 2000; 125:217-28. DOI: 10.1016/S0079-6123(00)25012-7. View

Kamermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T, Weiler R . Hemichannel-mediated inhibition in the outer retina. Science. 2001; 292(5519):1178-80. DOI: 10.1126/science.1060101. View

10.

DeVries S . Exocytosed protons feedback to suppress the Ca2+ current in mammalian cone photoreceptors. Neuron. 2002; 32(6):1107-17. DOI: 10.1016/s0896-6273(01)00535-9. View

11.

Cueva J, Haverkamp S, Reimer R, Edwards R, Wassle H, Brecha N . Vesicular gamma-aminobutyric acid transporter expression in amacrine and horizontal cells. J Comp Neurol. 2002; 445(3):227-37. PMC: 3696019. DOI: 10.1002/cne.10166. View

12.

Sakakibara S, Hiramatsu H, Takahashi Y, Hisatomi O, Kobayashi Y, Sakami S . Opsin expression in adult, developing, and regenerating newt retinas. Brain Res Mol Brain Res. 2002; 103(1-2):28-35. DOI: 10.1016/s0169-328x(02)00164-x. View

13.

DeVries S, Qi X, Smith R, Makous W, Sterling P . Electrical coupling between mammalian cones. Curr Biol. 2002; 12(22):1900-7. DOI: 10.1016/s0960-9822(02)01261-7. View

14.

Kaneko A . Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. J Physiol. 1970; 207(3):623-33. PMC: 1348731. DOI: 10.1113/jphysiol.1970.sp009084. View

15.

Baylor D, FUORTES M, OBryan P . Receptive fields of cones in the retina of the turtle. J Physiol. 1971; 214(2):265-94. PMC: 1331836. DOI: 10.1113/jphysiol.1971.sp009432. View

16.

Lam D, Steinman L . The uptake of ( - 3 H) aminobutyric acid in the goldfish retina. Proc Natl Acad Sci U S A. 1971; 68(11):2777-81. PMC: 389523. DOI: 10.1073/pnas.68.11.2777. View

17.

Piccolino M, GERSCHENFELD H . Activation of a regenerative calcium conductance in turtle cones by peripheral stimulation. Proc R Soc Lond B Biol Sci. 1978; 201(1144):309-15. DOI: 10.1098/rspb.1978.0048. View

18.

KUFFLER S . Discharge patterns and functional organization of mammalian retina. J Neurophysiol. 1953; 16(1):37-68. DOI: 10.1152/jn.1953.16.1.37. View

19.

Marc R, Stell W, Bok D, Lam D . GABA-ergic pathways in the goldfish retina. J Comp Neurol. 1978; 182(2):221-44. DOI: 10.1002/cne.901820204. View

20.

Lam D, Su Y, Swain L, Marc R, Brandon C, Wu J . Immunocytochemical localisation of L-glutamic acid decarboxylase in the goldfish retina. Nature. 1979; 278(5704):565-7. DOI: 10.1038/278565a0. View