Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-22T22:11:07.547Z Has data issue: false hasContentIssue false
  • English
  • Français

Probing inner retinal circuits in the rod pathway: A comparison of c-fos activation in mutant mice

Published online by Cambridge University Press:  25 February 2005

BRETT W. HANZLICEK ,
NEAL S. PEACHEY ,
CHRISTIAN GRIMM ,
STEPHANIE A. HAGSTROM  and
SHERRY L. BALL
BRETT W. HANZLICEK
Affiliation:
Cleveland Department of Veterans Affairs Medical Center, Cleveland
NEAL S. PEACHEY
Affiliation:
Cleveland Department of Veterans Affairs Medical Center, Cleveland Cole Eye Institute, Cleveland Clinic Foundation, Cleveland
CHRISTIAN GRIMM
Affiliation:
Department of Ophthalmology, University Eye Clinic, University Hospital, Zurich, Switzerland
STEPHANIE A. HAGSTROM
Affiliation:
Cole Eye Institute, Cleveland Clinic Foundation, Cleveland
SHERRY L. BALL
Affiliation:
Cleveland Department of Veterans Affairs Medical Center, Cleveland Cole Eye Institute, Cleveland Clinic Foundation, Cleveland Department of Psychology, Case Western Reserve University, Cleveland
Get access Rights & Permissions [Opens in a new window]

Abstract

We have used wild-type mice and mice possessing defects in specific retinal circuits in order to more clearly define functional circuits of the inner retina. The retina of the nob mouse lacks communication between photoreceptors and depolarizing bipolar cells (DBCs). Thus, all light driven activity in the nob mouse is mediated via remaining hyperpolarizing bipolar cell (HBC) circuits. Transducin null (Trα−/−) mice lack rod photoreceptor activity and thus remaining retinal circuits are solely generated via cone photoreceptor activity. Activation in inner retinal circuits in each of these mice was identified by monitoring light-induced expression of an immediate early gene, c-fos. The number of cells expressing c-fos in the inner retina was dependent upon stimulus intensity and was altered in a systematic fashion in mice with known retinal mutations. To determine whether c-fos is activated via circuits other than photoreceptors in the outer retina, we examined c-fos expression in tulp1−/− mice that lack photoreceptors in the outer retina; these mice showed virtually no c-fos activity following light exposure. Double-labeling immunohistochemical studies were carried out to more clearly define the population of c-fos expressing amacrine cells. Our results indicate that c-fos may be used to map functional circuits in the retina.

Keywords

Amacrine cellMouse retinac-fos immunohistochemistryInner retinal circuits
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 6 , November 2004 , pp. 873 - 881
Copyright
© 2004 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

Araki, C.M. & Hamassaki-Britto, D.E. (1998). Motion-sensitive neurons in the chick retina: A study using Fos immunohistochemistry. Brain Research 794, 333–337.Google Scholar
Ball, S.L., Pardue, M.T., McCall, M.A., Gregg, R.G., & Peachey, N.S. (2003). Immunohistochemical analysis of the outer plexiform layer in the nob mouse shows no abnormalities. Visual Neuroscience 20, 267–272.Google Scholar
Batterham, R.L., Cowley, M.A., Small, C.J., Herzog, H., Cohen, M.A., Dakin, C.L., Wren, A.M., Brynes, A.E., Low, M.J., Ghatei, M.A., Cone, R.D., & Bloom, S.R. (2002). Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 418, 650–654.Google Scholar
Boldogkoi, Z., Sik, A., Denes, A., Reichart, A., Toldi, J., Gerendai, I., Kovacs, K.J., & Palkovits, M. (2004). Novel tracing paradigms-genetically engineered herpesviruses as tools for mapping functional circuits within the CNS: Present status and future prospects. Progress in Neurobiology 72, 417–445.Google Scholar
Boycott, B.D. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions: Royal Society of London B Biological Sciences 225, 109–184.Google Scholar
Bussolino, D.F., de Arriba Zerpa, G.A., Grabois, V.R., Conde, C.B., Guido, M.E., & Caputto, B.L. (1998). Light affects c-fos expression and phospholipid synthesis in both retinal ganglion cells and photoreceptor cells in an opposite way for each cell type. Molecular Brain Research 58, 10–15.Google Scholar
Buzsaki, G. (2004). Large-scale recording of neuronal ensembles. Nature Neuroscience 7, 446–451.Google Scholar
Calvert, P.D., Krasnoperova, N.V., Lyubarsky, A.L., Isayama, T., Nicolo, M., Kosaras, B., Wong, G., Gannon, K.S., Margolskee, R.F., Sidman, R.L., Pugh, E.N., Jr., Makino, C.L., & Lem, J. (2000). Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha-subunit. Proceedings of the National Academy of Sciences of the U.S.A. 97, 13913–13918.Google Scholar
Casagrande, V.A., Xu, X., & Sary, G. (2002). Static and dynamic views of visual cortical organization. Progress in Brain Research 136, 389–408.Google Scholar
Cook, J.E. & Becker, D.L. (1995). Gap junctions in the vertebrate retina. Microscopy Research Technique 31, 408–419.Google Scholar
Curran, T. & Morgan, J.L. (1995). Fos: An immediate-early transcription factor in neurons. Journal of Neurobiology 26, 403–412.Google Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.Google Scholar
Deans, M.R., Volgyi, B., Goodenough, D.A., Bloomfield, S.A., & Paul, D.L. (2002). Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36, 703–712.Google Scholar
de Arriba Zerpa, G.A., Guido, M.E., Bussolino, D.F., Pasquare, S.J., Castagnet, P.I., Giusto, N.M., & Caputto, B.L. (1999). Light exposure activates retina ganglion cell lysophosphatidic acid acyl transferase and phosphatidic acid phosphatase by a c-fos-dependent mechanism. Journal of Neurochemistry 73, 1228–1235.Google Scholar
DeVries, S.H. & Baylor, D.A. (1995). An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. Proceeding of the National Academy of Sciences of the U.S.A. 92, 10658–10662.Google Scholar
Field, G.D. & Rieke, F. (2002). Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 34, 773–785.Google Scholar
Foster, R.G. & Hankins, M.W. (2002). Non-rod, non-cone photoreception in the vertebrates. Progress in Retinal and Eye Research 21, 507–527.Google Scholar
Gregg, R.G., Mukhopadhyay, S., Candille, S.I., Ball, S.L., Pardue, M.T., McCall, M.A., & Peachey, N.S. (2003). Identification of the gene and the mutation responsible for the mouse nob phenotype. Investigative Ophthalmology and Visual Science 44, 378–384.Google Scholar
Grimm, C., Wenzel, A., Williams, T., Rol, P., Hafezi, F., & Reme, C. (2001). Rhodopsin-mediated blue-light damage to the rat retina: Effect of photoreversal of bleaching. Investigative Ophthalmolology and Visual Science 42, 497–505.Google Scholar
Guldenagel, M., Ammermuller, J., Feigenspan, A., Teubner, B., Degen, J., Sohl, G., Willecke, K., & Weiler, R. (2001). Visual transmission deficits in mice with targeted disruption of the gap junction gene connexin36. Journal of Neuroscience 21, 6036–6044.Google Scholar
Gunhan, E., Choudary, P.V., Landerholm, T.E., & Chalupa, L.M. (2002). Depletion of cholinergic amacrine cells by a novel immunotoxin does not perturb the formation of segregated on and off cone bipolar cell projections. Journal of Neuroscience 22, 2265–2273.Google Scholar
Hack, I., Peichl, L., & Brandstatter, J.H. (1999). An alternative pathway for rod signals in the rodent retina: Rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proceedings of the National Academy of Sciences of the U.S.A. 96, 14130–14135.Google Scholar
Hagstrom, S.A., Duyao, M., North, M.A., & Li, T. (1999). Retinal degeneration in tulp1−/− mice: Vesicular accumulation in the interphotoreceptor matrix. Investigative Ophthalmology Visual Science 40, 2795–2802.Google Scholar
Haverkamp, S. & Wässle, H. (2000). Immunocytochemical analysis of the mouse retina. Journal of Comparative Neurology 424, 1–23.Google Scholar
Huerta, J.J., Llamosas, M.M., Cernuda-Cernuda, R., & Garcia-Fernandez, J.M. (1997). Fos expression in the retina of rd/rd mice during the light/dark cycle. Neuroscience Letters 232, 143–146.Google Scholar
Ikeda, S., Shiva, N., Ikeda, A., Smith, R.S., Nusinowitz, S., Yan, G., Lin, T.R., Chu, S., Heckenlively, J.R., North, M.A., Naggert, J.K., Nishina, P.M., & Duyao, M.P. (2000). Retinal degeneration but not obesity is observed in null mutants of the tubby-like protein 1 gene. Human Molecular Genetics 9, 155–163.Google Scholar
Kim, I.B., Lee, E.J., Kim, K.Y., Ju, W.K., Oh, S.J., Joo, C.K., & Chun, M.H. (1999). Immunocytochemical localization of nitric oxide synthase in the mammalian retina. Neuroscience Letters 267, 193–196.Google Scholar
Koistinaho, J. & Sagar, S.M. (1995). Light-induced c-fos expression in amacrine cells in the rabbit retina. Molecular Brain Research 29, 53–63.Google Scholar
Lu, B., Coffey, P., Wang, S., Ferrari, R., & Lund, R. (2004). Abnormal c-fos-like immunoreactivity in the superior colliculus and other subcortical visual centers of pigmented royal college of surgeons rats. Journal of Comparative Neurology 472, 100–112.Google Scholar
Marc, R.E., Jones, B.W., Watt, C.B., & Strettoie, E. (2003). Neural remodeling in retinal degeneration. Progress in Retinal and Eye Research 22, 607–655.Google Scholar
Mills, S.L., O'Brien, J.J., Li, W., O'Brien, J., & Massey, S.C. (2001). Rod pathways in the mammalian retina use connexin 36. Journal of Comparative Neurology 436, 336–350.Google Scholar
Nelson, L.E., Guo, T.Z., Lu, J., Saper, C.B., Franks, N.P., & Maze, M. (2002). The sedative component of anesthesia is mediated by GABA(A) receptors in an endogenous sleep pathway. Nature Neuroscience 5, 979–984.Google Scholar
Pardue, M.T., McCall, M.A., LaVail, M.M., Gregg, R.G., & Peachey, N.S. (1998). A naturally occurring mouse model of X-linked congenital stationary night blindness. Investigative Ophthalmology and Visual Science 39, 2443–2449.Google Scholar
Pennesi, M.E., Lyubarsky, A.L., & Pugh, E.N. (1998). Extreme responsiveness of the pupil of the dark-adapted mouse to steady retinal illumination. Investigative Ophthalmology and Visual Science 39, 2148–2156.Google Scholar
Provencio, I., Rodriguez, I.R., Jiang, G., Hayes, W.P., Moreira, E.F., & Rollag, M.D. (2000). A novel human opsin in the inner retina. Journal of Neuroscience 20, 600–605.Google Scholar
Raviola, E. & Gilula, N.B. (1973). Gap junctions between photoreceptor cells in the vertebrate retina. Proceeding of the National Academy of Sciences of the U.S.A. 70, 1677–1681.Google Scholar
Rice, D.S. & Curran, T. (2000). Disabled-1 is expressed in type AII amacrine cells in the mouse retina. Journal of Comparative Neurology 424, 327–338.Google Scholar
Saszik, S.M., Robson, J.G., & Frishman, L.J. (2002). The scotopic threshold response of the dark-adapted electroretinogram of the mouse. Journal of Physiology 543, 899–916.Google Scholar
Semo, M., Lupi, D., Peirson, S.N., Butler, J.N., & Foster, R.G. (2003). Light-induced c-fos in melanopsin retinal ganglion cells of young and aged rodless/coneless (rd/rd cl) mice. European Journal of Neuroscience 18, 3007–3017.Google Scholar
Sheng, M. & Greenberg, M.E. (1990). The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4, 477–485.Google Scholar
Soucy, E., Wang, Y., Nirenberg, S., Nathans, J., & Meister, M. (1998). A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron 21, 481–493.Google Scholar
Strettoi, E., Porciatti, V., Falsini, B., Pignatelli, V., & Rossi, C. (2002). Morphological and functional abnormalities in the inner retina of the rd/rd mouse. Journal of Neuroscience 22, 5492–5504.Google Scholar
Truitt, W.A., Shipley, M.T., Veening, J.G., & Coolen, L.M. (2003). Activation of a subset of lumbar spinothalamic neurons after copulatory behavior in male but not female rats. Journal of Neuroscience 23, 325–331.Google Scholar
Tsukamoto, Y., Morigiwa, K., Ueda, M., & Sterling, P. (2001). Microcircuits for night vision in mouse retina. Journal of Neuroscience 21, 8616–8623Google Scholar
Wu, J., Peachey, N.S., & Marmorstein, A.D. (2004). Light-evoked responses of the mouse retinal pigment epithelium. Journal of Neurophysiology 91, 1134–1142.Google Scholar
Wyszecki, G. & Stiles, W.S. (1982). Color Science. Concepts and Methods. Quantitative Data and Formulae (2nd edition). New York: Wiley.