Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-18T18:33:35.840Z Has data issue: false hasContentIssue false
  • English
  • Français

Diurnal and circadian retinomotor movements in zebrafish

Published online by Cambridge University Press:  02 June 2005

GUS J. MENGER ,
JOSEPH R. KOKE  and
GREGORY M. CAHILL
GUS J. MENGER
Affiliation:
Department of Biology and Biochemistry, University of Houston, Science and Research Building 2, Houston Current address: Department of Biology and Center for Biological Clocks Research, Texas A&M University, College Station, TX 77843-3258, USA.
JOSEPH R. KOKE
Affiliation:
Department of Biology, Texas State University–San Marcos, 431 New Science Building, San Marcos
GREGORY M. CAHILL
Affiliation:
Department of Biology and Biochemistry, University of Houston, Science and Research Building 2, Houston Current address: Department of Biology and Center for Biological Clocks Research, Texas A&M University, College Station, TX 77843-3258, USA.
Get access Rights & Permissions [Opens in a new window]

Abstract

Key indicators of circadian regulation include the persistence of physiological rhythmicity in the absence of environmental time cues and entrainment of this rhythmicity by the ambient light cycle. In some teleosts, the inner segments of rod and cone photoreceptors contract and elongate according to changes in ambient lighting and the circadian cycle. Pigment granules in the retinal pigment epithelium (RPE) disperse and aggregate in a similar manner. Collectively, these movements are known as retinomotor movements. We report the histological characterization of diurnal and circadian retinomotor movements in zebrafish, Danio rerio. Adult fish subjected to a 14:10 light:dark (LD) cycle, constant darkness (DD), or constant light (LL) were sacrificed at 1–13 h intervals and processed for semithin sectioning of the retina. Using bright-field microscopy, 15 measurements of pigment granule position and the inner segment lengths of 30 rods and 30–45 cones were collected from the central third of the dorso-optic retina per time point. In LD, rods and cones followed a clear diurnal rhythm in their inner segment movements. Short-single, UV-sensitive cones were found to contract significantly 1 h before light onset in LD conditions. In DD conditions, the inner segments movements of short-single and double cones displayed statistically significant rhythms. RPE pigment granule movements are rhythmically regulated in both LD and DD although fluctuations are damped in the absence of photic cues. No significant retinomotor movements were observed in LL. These findings indicate retinomotor movements in zebrafish are differentially regulated by an endogenous oscillator and by light-dependent mechanisms.

Keywords

RetinaCircadianClockOscillationPhotoreceptorsRetinal pigment epithelium
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 2 , March 2005 , pp. 203 - 209
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bruenner, U. & Burnside, B. (1986). Pigment granule migration in isolated cells of the teleost retinal pigment epithelium. Investigative Ophthalmology and Visual Science 27(11), 1634–1643.Google Scholar
Burnside, B. & Ackland, N. (1984). Effects of circadian rhythm and cAMP on retinomotor movements in the green sunfish, Lepomis cyanellus. Investigative Ophthalmology and Visual Science 25(5), 539–545.Google Scholar
Burnside, B., Evans, M., Fletcher, R.T., & Chader, G.J. (1982). Induction of dark-adaptive retinomotor movement (cell elongation) in teleost retinal cones by cyclic adenosine 3′, ′5-monophosphate. Journal of General Physiology 79(5), 759–774.CrossRefGoogle Scholar
Cahill, G.M. (1997). Circadian melatonin rhythms in cultured zebrafish pineals are not affected by catecholamine receptor agonists. General Comparative Endocrinology 105, 270–275.CrossRefGoogle Scholar
Cahill, G.M. (2002). Clock mechanisms in zebrafish. Cell Tissue Research 309, 27–34.CrossRefGoogle Scholar
Cahill, G.M. & Besharse, J.C. (1995). Circadian rhythmicity in vertebrate retinas: regulation by a photoreceptor oscillator. Progress in Retinal Eye Research 14 (1), 267–291.CrossRefGoogle Scholar
Cahill, G.M., Straume, M., & Batchelor, M.M. (1998). Circadian rhythmicity in the locomotor activity of larval zebrafish. Neuroreport 9(15), 3445–3449.CrossRefGoogle Scholar
Cermakian, N., Whitmore, D., Foulkes, N.S., & Sassone-Corsi, P. (2000). Asynchronous oscillations of two zebrafish CLOCK partners reveal differential clock control and function. Proceedings of the National Academy of Sciences of the U.S.A. 97(8), 4339–4344.CrossRefGoogle Scholar
Dearry, A. & Barlow, R.B. (1987). Circadian rhythms in the green sunfish. Journal of General Physiology 89, 745–770.CrossRefGoogle Scholar
Dearry, A. & Burnside, B. (1984). Effects of extracellular Ca2+, K+, and Na+ on cone and retinal pigment epithelium retinomotor movements in isolated teleost retinas. Journal of General Physiology 83, 589–611.CrossRefGoogle Scholar
Douglas, R.H. (1981a). The function of photomechanical movements in the retina of the rainbow trout (Salmo gairdneri). Journal of Experimental Biology 96, 389–403.Google Scholar
Douglas, R.H. (1981b). An endogenous crespuscular rhythm of rainbow trout (Salmo gairdneri) photomechanical movements. Journal of Experimental Biology 96, 377–388.Google Scholar
Douglas, R.H. & Wagner, H.-J. (1982). Endogenous patterns of photomechanical movements in teleosts and their relation to activity rhythms. Cell Tissue Research 226, 133–144.Google Scholar
García, D. & Burnside, B. (1994). Suppression of cAMP-induced pigment granule aggregation in RPE by organic anion transport inhibitors. Investigative Ophthalmology and Visual Science 35 (1), 178–188.Google Scholar
Gothilf, Y., Coon, S.L., Toyama, R., Chitnis, A., Namboodiri, M.A., & Klein, D.C. (1999). Zebrafish serotonin N-acetyltransferase-2: Marker for development of pineal photoreceptors and circadian clock function. Endocrinology 140(10), 4895–4903.CrossRefGoogle Scholar
Ishikawa, T., Hirayama, J., Kobayashi, Y., & Todo, T. (2002). Zebrafish CRY represses transcription mediated by CLOCK-BMAL heterodimer without inhibiting its binding to DNA. Genes to Cells 7: 1073–1086.Google Scholar
Ivanova, T.N. & Iuvone, P.M. (2003). Circadian rhythm and photic control of cAMP level in chick retinal cell cultures: A mechanism for coupling the circadian oscillator to the melatonin-synthesizing enzyme, arylalkylamine N-acetyltransferase, in photoreceptor cells. Brain Research 991, 96–103.CrossRefGoogle Scholar
John, K.R. & Gring, D.M. (1968). Retinomotor rhythms in the bluegill, Lepomis macrochirus. Journal of the Fisheries Research Board of Canada 25 (2), 373–381.CrossRefGoogle Scholar
Levinson, G. & Burnside, B. (1981). Circadian rhythms in teleost retinomotor movements: A comparison of the effects of circadian rhythm and light condition on cone length. Investigative Ophthalmology & Visual Science 20, 294–303.Google Scholar
Li, L. & Dowling, J.E. (1998). Zebrafish visual sensitivity is regulated by a circadian clock. Visual Neuroscience 15, 851–857.Google Scholar
Lythgoe, J.N. & Partridge, J.C. (1989). Visual pigments and the acquisition of visual information. Journal of Experimental Biology 146, 1–20.Google Scholar
McCormack, C.A., Hayden, T.J., & Kunz, Y.W. (1989). Ontogenesis of diurnal rhythms of cAMP concentration, outer segment disc shedding and retinomotor movements in the eye of the brown trout, Salmo trutta. Brain and Behavioral Evolution 34(1), 65–72.CrossRefGoogle Scholar
McCormack, C. & McDonnell, M. (1994). Circadian regulation of teleost retinal cone movements in vitro. Journal of General Physiology 103, 487–499.CrossRefGoogle Scholar
McCormack, C.A. & Burnside, B. (1991). Effects of circadian phase on cone retinomotor movements in the midas cichlid. Experimental Eye Research 52(4), 431–438.CrossRefGoogle Scholar
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retinomotor movements. Journal of General Physiology 86, 671–689.CrossRefGoogle Scholar
Rajendran, R.R., Van Niel, E.E., Stenkamp, D.L., Cunningham, L.L., Raymond, P.A., & Gonzalez-Fernandez, F. (1996). Zebrafish interphotoreceptor retinoid-binding protein: Differential circadian expression among cone subtypes. Journal of Experimental Biology 199, 2775–2787.Google Scholar
Reppert, S.M. & Weaver, D.R. (2000). Comparing clockworks: Mouse verses fly. Journal of Biological Rhythms 15(5), 357–364.CrossRefGoogle Scholar
Robinson, J., Schmitt, E.A., Harosi, F.I., Reece, R.J., & Dowling, J.E. (1993). Zebrafish ultraviolet visual pigment: Absorption spectrum, sequence, and localization. Proceedings of the National Academy of Sciences of the U.S.A. 90, 6009–6012.CrossRefGoogle Scholar
Schmitt, E.A. & Dowling, J.E. (1999). Early retinal development in the zebrafish, Danio rerio: Light and electron microscopic analyses. Journal of Comparative Neurobiology 404(4), 515–536.3.0.CO;2-A>CrossRefGoogle Scholar
Stenkamp, D.L., Iuvone, P.M., & Adler, R. (1994). Photomechanical movements of cultured embryonic photoreceptors: regulation by exogenous neuromodulators and by regulable source of endogenous dopamine. Journal of Neuroscience 14(5), 3083–3096.Google Scholar
Troutt, L.L. & Burnside, B. (1989). Role of microtubules in pigment granule migration in teleost retinal pigment epithelial cells. Experimental Eye Research 48(3), 433–443.CrossRefGoogle Scholar
Westerfield, M. (2000). General methods for zebrafish care. In The Zebrafish Book (4th edition), ed. Westerfield, M. Eugene, Oregon: University of Oregon Press, retrieved from the Zebrafish Information Network (ZFIN), the Zebrafish International Resource Center, University of Oregon, Eugene, OR 97403; World Wide Web URL: http://zfin.org/; January 2, 2005.
Zinn, K.M. & Marmor, M.F. (1979). The Retinal Pigment Epithelium. Cambridge, Massachusetts: Harvard University Press.