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Spatial, temporal, and intensive determinants of dopamine release in the chick retina

Published online by Cambridge University Press:  01 July 2004

W.A. LUFT ,
P.M. IUVONE  and
W.K. STELL
W.A. LUFT
Affiliation:
Department of Cell Biology and Anatomy, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada
P.M. IUVONE
Affiliation:
Department of Pharmacology, Emory University, Atlanta
W.K. STELL
Affiliation:
Department of Cell Biology and Anatomy, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada
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Abstract

The retinal dopaminergic system is a global regulator of retinal function. Apart from the fact that the rates of dopamine synthesis and release are increased by increasing illumination, the visual image parameters that influence dopaminergic function are mostly unknown. Roles for spatial and temporal frequency and image contrast are suggested by the effects of form-deprivation with a diffusing goggle. Form-deprivation reduces the rates of dopamine synthesis and release, and induces myopia, which is prevented by dopamine agonists. Our purpose here was to identify visual stimulus parameters that activate dopaminergic amacrine cells and elicit dopamine release. White Leghorn cockerels 4–7 days old were exposed to 2 h of form-deprivation, reduced light intensity, or stimuli of varied temporal or spatial frequency. Activation of dopaminergic neurons, labeled for tyrosine hydroxylase (TH), was assessed with immunocytochemistry for c-Fos, and dopamine release was measured by HPLC analysis of dopamine metabolite accumulation in the vitreous body. Form-deprivation did not reduce TH+ cell activation or vitreal dopamine metabolite accumulation any more than did neutral-density filters of approximately equal transmittance. TH+ cell activation and vitreal metabolite accumulation were not affected significantly by exposure to 2, 5, 10, 15, or 20 Hz stroboscopic stimulation on a dark background, or by sine-wave gratings of 0.089, 0.44, 0.89, 1.04, or 3.13 cycles/deg compared to a uniform gray target of equal mean luminance. These data indicate that the retinal dopaminergic system does not respond readily to short-term changes in visual stimulus parameters, other than light intensity, under the conditions of these experiments.

Keywords

DopamineSpatial frequencyFlickerAmacrine cellc-Fos
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 4 , July 2004 , pp. 627 - 635
Copyright
2004 Cambridge University Press

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References

REFERENCES

Boatright, J.H., Gordon, J.R., & Iuvone, P.M. (1994). Inhibition of endogenous dopamine release in amphibian retina by L-2-amino-4-phosphonobutyric acid (L-AP4) and trans-2-aminocyclopentane-1,3,-dicarboxylate (ACPD). Brain Research 649, 339–342.CrossRefGoogle Scholar
Boatright, J.H., Hoel, M.J., & Iuvone, P.M. (1989). Stimulation of endogenous dopamine release and metabolism in amphibian retina by light and K+-evoked depolarization. Brain Research 482, 164–168.CrossRefGoogle Scholar
Bodis-Wollner. (1990). Visual deficits related to dopamine deficiency in experimental animals and Parkinson's disease patients. Trends in Neuroscience 13, 296–302.CrossRefGoogle Scholar
Bodis-Wollner, I. & Tzelepi, A. (1998). The push–pull action of dopamine on spatial tuning of the monkey retina: The effects of dopaminergic deficiency and selective D1 and D2 receptor ligands on the pattern electroretinogram. Vision Research 38, 1479–1487.CrossRefGoogle Scholar
Dacey, D.M. (1990). The dopaminergic amacrine cell. Journal of Comparative Neurology 301, 461–489.CrossRefGoogle Scholar
Dearry, A. (1991). Light onset stimulates tyrosine hydroxylase activity in isolated teleost retinas. Vision Research 31, 395–399.CrossRefGoogle Scholar
Djamgoz, M.B.A., Usai, C., & Vallerga, S. (1991). An interplexiform cell in the goldfish retina: Light-evoked response pattern and intracellular staining with horseradish peroxidase. Cell and Tissue Research 264, 111–116.CrossRefGoogle Scholar
Feldkaemper, M., Diether, S., Kleine, G., & Schaeffel, F. (1999). Interactions of spatial and luminance information in the retina of chickens during myopia development. Experimental Eye Research 68, 105–115.CrossRefGoogle Scholar
Fischer, A.J., McGuire, J., Schaeffel, F., & Stell, W.K. (1999). Light- and focus-dependent expression of the transcription factor ZENK in the chick retina. Nature Neuroscience 2, 706–712.CrossRefGoogle Scholar
Hunt, S.P., Pini, A., & Evan, G. (1987). Induction of the c-Fos-like protein in spinal cord neurons following sensory stimulation. Nature 328, 632–634.CrossRefGoogle Scholar
Iuvone, P.M., Galli, C.L., Garrison-Gund, C.K., & Neff, N.H. (1978a). Light stimulates tyrosine hydroxylase activity and dopamine synthesis in retinal amacrine cells. Science 202, 901–902.Google Scholar
Iuvone, P.M., Galli, C.L., & Neff, N.H. (1978b). Retinal tyrosine hydroxylase: Comparison of short-term and long-term stimulation by light. Molecular Pharmacology 14, 1212–1219.Google Scholar
Iuvone, P.M. & Marshburn, P.B. (1982). Regulation of tyrosine hydroxylase activity in retinal cell suspensions: Effects of potassium and 8-bromo cyclic AMP. Life Sciences 30, 85–91.CrossRefGoogle Scholar
Iuvone, P.M., Rauch, A.L., Marshburn, P.B., Glass, D.B., & Neff, N.H. (1982). Activation of retinal tyrosine hydroxylase in vitro by cyclic AMP-dependent protein kinase: Characterization and comparison to activation in vivo by photic stimulation. Journal of Neurochemistry 39, 1632–1640.CrossRefGoogle Scholar
Iuvone, P.M., Tigges, M., Stone, R.A., Lambert, S., & Laties, A.M. (1991). Effects of apomorphine, a dopamine receptor agonist, on ocular refraction and axial elongation in a primate model of myopia. Investigative Ophthalmology and Visual Science 32, 1674–1677.Google Scholar
Keesey, U.T. (1969). Visibility of a stabilized target as a function of frequency and amplitude of luminance variation. Journal of the Optical Society of America 59, 604–610.CrossRefGoogle Scholar
Kohler, K., Kolbinger, W., Kurz-Isler, G., & Weiler, R. (1990). Endogenous dopamine and cyclic events in the fish retina, II: Correlation of retinomotor movement, spinule formation, and connexon density of gap junctions with dopamine activity during light/dark cycles. Visual Neuroscience 5, 417–428.CrossRefGoogle Scholar
Koistinaho, J., Swanson, R.A., de Vente, J., & Sagar, S.M. (1993). NADPH-diaphorase (nitric oxide synthase)-reactive amacrine cells of the rabbit retina: Putative target cells and stimulation by light. Neuroscience 57, 587–597.CrossRefGoogle Scholar
Kolb, H., Cuenca, N., Wang, H.-H., & Dekorver, L. (1990). The synaptic organization of the dopaminergic amacrine cell in the cat retina. Journal of Neurocytology 19, 343–366.CrossRefGoogle Scholar
Kolb, H., Netzer, E., & Ammermüller, J. (1997). Neural circuitry and light responses of the dopamine amacrine cell of the turtle retina. Molecular Vision 3(6): 〈http://www.molvis.org/molvis/v3/a6/〉.Google Scholar
Kolbinger, W. & Weiler, R. (1993). Modulation of endogenous dopamine release in the turtle retina: Effects of light, calcium, and neurotransmitters. Visual Neuroscience 10, 1035–1041.CrossRefGoogle Scholar
Kumer, S.C. & Vrana, K.E. (1996). Intricate regulation of tyrosine hydroxylase activity and gene expression. Journal of Neurochemistry 67, 443–462.Google Scholar
Manglapus, M.K., Iuvone, P.M., Underwood, H., Pierce, M.E., & Barlow, R.B. (1999). Dopamine mediates circadian rhythms of rod–cone dominance in the Japanese quail retina. Journal of Neuroscience 19, 4132–4141.Google Scholar
McNeil, M.A. & Masland, R.H. (1998). Extreme diversity among amacrine cells: Implications for function. Neuron 20, 971–982.CrossRefGoogle Scholar
Megaw, P. (1998). The Neurological Control of Eye-Growth. Ph.D. Thesis, La Trobe University, Bendigo, Australia.
Megaw, P., Morgan, I.G., & Boelen, M.K. (1997). Dopaminergic behaviour in chicken retina and the effect of form deprivation. Australian and New Zealand Journal of Ophthalmology 25 (Suppl. 1), S76–S78.CrossRefGoogle Scholar
Megaw, P., Morgan, I., & Boelen, M. (2001). Vitreal dihydroxyphenylacetic acid (DOPAC) as an index of retinal dopamine release. Journal of Neurochemistry 76, 1636–1644.CrossRefGoogle Scholar
Morgan, J.I. & Curran, T. (1989). Stimulus-transcription coupling in neurons: Role of cellular immediate-early genes. Trends in Neuroscience 12, 459–462.CrossRefGoogle Scholar
Mustonen, J., Rovamo, J., & Nasanen, R. (1993). The effects of grating area and spatial frequency on contrast sensitivity as a function of light level. Vision Research 33, 2065–2072.CrossRefGoogle Scholar
Ohngemach, S., Hagel, G., & Schaeffel, F. (1997). Concentrations of biogenic amines in fundal layers in chickens with normal visual experience, deprivation, and after reserpine application. Visual Neuroscience 14, 493–505.CrossRefGoogle Scholar
Pendrak, K., Nguyen, T., Lin, T., Capehart, C., Zhu, X., & Stone, R.A. (1996). Retinal dopamine in the recovery from experimental myopia. Current Eye Research 16, 152–157.Google Scholar
Peppe, A., Antal, A., Tagliati, M., Stanzione, P., & Bodis-Wollner, I. (1998). D1 agonist CY208-243 attenuates the pattern electroretinogram to low spatial frequency stimuli in the monkey. Neuroscience Letters 243, 5–8.CrossRefGoogle Scholar
Prusky, G.T., West, P.W., & Douglas, R.M. (2000) Behavioral assessment of visual acuity in mice and rats. Vision Research 40, 2201–2209.CrossRefGoogle Scholar
Rohrer, B., Spira, A., & Stell, W.K. (1993). Apomorphine blocks form-deprivation myopia in chickens by a dopamine D2-receptor mechanism acting in retina or pigment epithelium. Visual Neuroscience 10, 447–453.CrossRefGoogle Scholar
Rohrer, B., Iuvone, P.M., & Stell, W.K. (1995). Stimulation of dopaminergic amacrine cells by stroboscopic illumination or fibroblast growth factor (bFGF, FGF-2) injections: Possible roles in prevention of form-deprivation myopia in the chick. Brain Research 686, 169–181.CrossRefGoogle Scholar
Sagar, S.M. & Sharp, F.R. (1990). Light induces a Fos-like nuclear antigen in retinal neurons. Molecular Brain Research 7, 17–21.CrossRefGoogle Scholar
Sagar, S.M., Sharp, F.R., & Curran, T. (1988). Expression of the c-fos protein in brain: metabolic mapping at the cellular level. Science 240, 1328–1331.CrossRefGoogle Scholar
Schaeffel, F., Bartmann, M., Hagel, G., & Zrenner, E. (1995). Studies on the role of the retinal dopamine/melatonin system in experimental refractive errors in chickens. Vision Research 35, 1247–1264.CrossRefGoogle Scholar
Stone, R.A., Lin, T., Laties, A.M., & Iuvone, P.M. (1989). Retinal dopamine and form-deprivation myopia. Proceedings of the National Academy of Sciences of the U.S.A. 86, 704–706.CrossRefGoogle Scholar
Tagliati, M., Bodis-Wollner, I., Kovanecz, I., & Stanzione, P. (1994). Spatial frequency tuning of the monkey pattern ERG depends on D2 receptor-linked action of dopamine. Vision Research 34, 2051–2057.Google Scholar
Teakle, E.M., Wildsoet, C.F., & Vaney, D.I. (1993). The spatial organization of tyrosine hydroxylase-immunoreactive amacrine cells in the chicken retina and the consequences of myopia. Vision Research 33, 2383–2396.Google Scholar
Teranishi, T., Negishi, K., & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301, 243–246.Google Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of AII amacrine cells in mammalian retina. Journal of Neuroscience 7, 4115–4128.Google Scholar
Witkovsky, P., Stone, S., & Tranchina, D. (1989). Photoreceptor to horizontal cell synaptic transfer in the Xenopus retina: Modulation by dopamine ligands and a circuit model for interactions of rod and cone inputs. Journal of Neurophysiology 62, 864–881.Google Scholar
Witkovsky, P., Gabriel, R., Haycock, J.W., & Meller, E. (2000). Influence of light and neural circuitry on tyrosine hydroxylase phosphorylation in the rat retina. Journal of Chemical Neuroanatomy 19, 105–116.Google Scholar
Wülle, I., Kirsch, M., & Wagner, H.-J. (1990). Cyclic changes in dopamine and DOPAC content, and tyrosine hydroxylase activity in the retina of a cichlid fish. Brain Research 515, 163–167.Google Scholar