Olfactory Stimulation Selectively Modulates the OFF Pathway in the Retina of Zebrafish

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2013 Jul 16

PMID 23849198

Citations 20

Authors

Federico Esposti

Jamie Johnston

Juliana M Rosa

Kin-Mei Leung

Leon Lagnado

Affiliations

Soon will be listed here.

Abstract

Cross-modal regulation of visual performance by olfactory stimuli begins in the retina, where dopaminergic interneurons receive projections from the olfactory bulb. However, we do not understand how olfactory stimuli alter the processing of visual signals within the retina. We investigated this question by in vivo imaging activity in transgenic zebrafish expressing SyGCaMP2 in bipolar cell terminals and GCaMP3.5 in ganglion cells. The food-related amino acid methionine reduced the gain and increased sensitivity of responses to luminance and contrast transmitted through OFF bipolar cells but not ON. The effects of olfactory stimulus were blocked by inhibiting dopamine uptake and release. Activation of dopamine receptors increased the gain of synaptic transmission in vivo and potentiated synaptic calcium currents in isolated bipolar cells. These results indicate that olfactory stimuli alter the sensitivity of the retina through the dopaminergic regulation of presynaptic calcium channels that control the gain of synaptic transmission through OFF bipolar cells.

Citing Articles

Update on central factors in myopia development beyond intraocular mechanisms.

Tian R, Tian X, Yang H, Wu Y Front Neurol. 2024; 15:1486139.

PMID: 39624669 PMC: 11609075. DOI: 10.3389/fneur.2024.1486139.

Study of a precise treatment protocol for patients with consciousness disorders based on the brain network analysis of functional magnetic resonance imaging.

Wang P, Xiang J, Niu Y, Wei J, Lan C, Li X Front Neurosci. 2024; 18:1443478.

PMID: 39351395 PMC: 11439825. DOI: 10.3389/fnins.2024.1443478.

A Novel Cre Recombinase Mouse Strain for Cell-Specific Deletion of Floxed Genes in Ribbon Synapse-Forming Retinal Neurons.

Suiwal S, Wartenberg P, Boehm U, Schmitz F, Schwarz K Int J Mol Sci. 2024; 25(3).

PMID: 38339191 PMC: 10856425. DOI: 10.3390/ijms25031916.

Awake responses suggest inefficient dense coding in the mouse retina.

Boissonnet T, Tripodi M, Asari H Elife. 2023; 12.

PMID: 37922200 PMC: 10624425. DOI: 10.7554/eLife.78005.

Altered whole-brain gray matter volume in form-deprivation myopia rats based on voxel-based morphometry: A pilot study.

Liu J, Lei Y, Diao Y, Lu Y, Teng X, Chen Q Front Neurosci. 2023; 17:1113578.

PMID: 37144093 PMC: 10151753. DOI: 10.3389/fnins.2023.1113578.

References

Dorostkar M, Dreosti E, Odermatt B, Lagnado L . Computational processing of optical measurements of neuronal and synaptic activity in networks. J Neurosci Methods. 2010; 188(1):141-50. PMC: 2849931. DOI: 10.1016/j.jneumeth.2010.01.033. View

Yu C, Li L . Dopamine modulates voltage-activated potassium currents in zebrafish retinal on bipolar cells. J Neurosci Res. 2005; 82(3):368-76. DOI: 10.1002/jnr.20637. View

Maguire G, Werblin F . Dopamine enhances a glutamate-gated ionic current in OFF bipolar cells of the tiger salamander retina. J Neurosci. 1994; 14(10):6094-101. PMC: 6576970. View

Schlicker E, Timm J, Gothert M . Cannabinoid receptor-mediated inhibition of dopamine release in the retina. Naunyn Schmiedebergs Arch Pharmacol. 1996; 354(6):791-5. DOI: 10.1007/BF00166907. View

Bai Q, Garver J, Hukriede N, Burton E . Generation of a transgenic zebrafish model of Tauopathy using a novel promoter element derived from the zebrafish eno2 gene. Nucleic Acids Res. 2007; 35(19):6501-16. PMC: 2095798. DOI: 10.1093/nar/gkm608. View

Li L, Dowling J . Effects of dopamine depletion on visual sensitivity of zebrafish. J Neurosci. 2000; 20(5):1893-903. PMC: 6772905. View

Yamamoto N, Ito H . Afferent sources to the ganglion of the terminal nerve in teleosts. J Comp Neurol. 2000; 428(2):355-75. DOI: 10.1002/1096-9861(20001211)428:2<355::aid-cne12>3.0.co;2-w. View

Lima L, Schmeer C, Urbina M . 8-[3H]hydroxy-2-(di-n-propylamino) tetralin binding sites in goldfish retina. Neurochem Res. 1994; 19(3):249-55. DOI: 10.1007/BF00971572. View

Kubrusly R, Panizzutti R, Gardino P, Stutz B, Reis R, Ventura A . Expression of functional dopaminergic phenotype in purified cultured Müller cells from vertebrate retina. Neurochem Int. 2008; 53(3-4):63-70. DOI: 10.1016/j.neuint.2008.05.002. View

10.

Knapp A, Dowling J . Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature. 1987; 325(6103):437-9. DOI: 10.1038/325437a0. View

11.

Odermatt B, Nikolaev A, Lagnado L . Encoding of luminance and contrast by linear and nonlinear synapses in the retina. Neuron. 2012; 73(4):758-73. PMC: 3314971. DOI: 10.1016/j.neuron.2011.12.023. View

12.

Burgess H, Schoch H, Granato M . Distinct retinal pathways drive spatial orientation behaviors in zebrafish navigation. Curr Biol. 2010; 20(4):381-6. PMC: 3412192. DOI: 10.1016/j.cub.2010.01.022. View

13.

Reith M, Coffey L, Xu C, Chen N . GBR 12909 and 12935 block dopamine uptake into brain synaptic vesicles as well as nerve endings. Eur J Pharmacol. 1994; 253(1-2):175-8. DOI: 10.1016/0014-2999(94)90774-9. View

14.

Ribelayga C, Wang Y, Mangel S . Dopamine mediates circadian clock regulation of rod and cone input to fish retinal horizontal cells. J Physiol. 2002; 544(3):801-16. PMC: 2290614. DOI: 10.1113/jphysiol.2002.023671. View

15.

Dowling J . Retinal neuromodulation: the role of dopamine. Vis Neurosci. 1991; 7(1-2):87-97. DOI: 10.1017/s0952523800010968. View

16.

Connaughton V, Nelson R . Axonal stratification patterns and glutamate-gated conductance mechanisms in zebrafish retinal bipolar cells. J Physiol. 2000; 524 Pt 1:135-46. PMC: 2269842. DOI: 10.1111/j.1469-7793.2000.t01-1-00135.x. View

17.

Catterall W, Striessnig J, Snutch T, Perez-Reyes E . International Union of Pharmacology. XL. Compendium of voltage-gated ion channels: calcium channels. Pharmacol Rev. 2003; 55(4):579-81. DOI: 10.1124/pr.55.4.8. View

18.

Feigenspan A, Bormann J . Facilitation of GABAergic signaling in the retina by receptors stimulating adenylate cyclase. Proc Natl Acad Sci U S A. 1994; 91(23):10893-7. PMC: 45132. DOI: 10.1073/pnas.91.23.10893. View

19.

Demski L . Terminal nerve complex. Acta Anat (Basel). 1993; 148(2-3):81-95. DOI: 10.1159/000147528. View

20.

Huang L, Maaswinkel H, Li L . Olfactoretinal centrifugal input modulates zebrafish retinal ganglion cell activity: a possible role for dopamine-mediated Ca2+ signalling pathways. J Physiol. 2005; 569(Pt 3):939-48. PMC: 1464265. DOI: 10.1113/jphysiol.2005.099531. View