Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-08T11:29:27.648Z Has data issue: false hasContentIssue false
  • English
  • Français

Cone and rod inputs to murine retinal ganglion cells: Evidence of cone opsin specific channels

Published online by Cambridge University Press:  03 February 2006

BJORN EKESTEN  and
PETER GOURAS
BJORN EKESTEN
Affiliation:
Department of Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden
PETER GOURAS
Affiliation:
Department of Ophthalmology, Columbia University, New York, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

To identify ultraviolet (UV) and middle- (M) wavelength-sensitive cone and rod signals in murine retinal ganglion cells, single ganglion cell responses were studied in anesthetized, light-adapted C57/BL6 mice with tungsten microelectrodes driven through the sclera and vitreous to the neural retina. One hundred fifty-four ganglion cells were examined in 43 retinas of 34 mice. The retina was stimulated with diffuse flashes and/or pulses of ultraviolet (360 nm) or green (520 nm) light in the presence and absence of a strong steady orange adapting light. Twelve ganglion cells were studied in the dark-adapted retina in order to identify the signals of rods. Three functionally different types of ganglion cells were found: (1) phasic responding cells (31%) with no spontaneous activity and large impulse amplitudes; (2) tonic responding cells (60%) with irregular, low frequency (5–10 Hz) spontaneous activity and smaller impulse amplitudes; and (3) metronome-like cells (9%) with regular, relatively high-frequency (20–40 Hz) spontaneous activity. A few cells (1%) had habituating responses. Every cell encountered was affected by diffuse stimulation. The more common two types were excited at either the ON or OFF or at both the ON and OFF phases of stimulation. Type III cells had weaker responses, sometimes only inhibited by turning off a light. In the light-adapted state, most cells received signals of the same polarity from UV- and M-cones but UV-cone inputs were usually more dominant, especially in ventral retina. A fraction of cells received signals from only UV- (18%) or only M- (3%) cones. In rare cases (2%) these cone inputs had an opposite polarity on the same cell. In the dark-adapted state, all cells were at least four or five logarithmic units more sensitive and more to green than ultraviolet light. The results indicate that co-expression of both UV-and M-cone opsins cannot be ubiquitous in murine retina. Some cones, especially UV cones, exist without the presence of any functional M-cone opsin. This must be the case to explain the presence of ganglion cells that receive inputs only from UV-cones and others that receive inputs of opposite polarity from UV- and M-cones. The results support the hypothesis that murine retina has the physiological capacity to relay signals to the brain that allow the sensing of chromatic contrast and color vision.

Keywords

Mouse retinaGanglion cellsRodsCones
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 6 , November 2005 , pp. 893 - 903
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

Applebury, M.L., Antoch, M.P., Baxter, L.C., Chun, L.L., Falk, J.D., Farhangfar, F., Kage, K., Krzystolik, M.G., Lyass, L.A., & Robbins, J.T. (2000). The murine cone photoreceptor: A single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513–523.CrossRefGoogle Scholar
Arden, G.B. (1963). Complex receptive fields and responses to moving objects in cells of the rabbit's lateral geniculate body. Journal of Physiology 166, 468–488.CrossRefGoogle Scholar
Balkema, Jr., G.W. & Pinto, L.H. (1982). Electrophysiology of retinal ganglion cells in the mouse: A study of a normally pigmented mouse and a congenic hypopigmentation mutant, pearl. Journal of Neurophysiology 48, 968–980.Google Scholar
Barlow, H.B., Hill, R.M., & Levick, W.R. (1964). Retinal ganglion cells responding selectively to direction and speed of motion in the rabbit. Journal of Physiology 178, 377–407.CrossRefGoogle Scholar
Bova, L.M., Wood, A.M., Jamie, J.F., & Truscott, R.J. (1999). UV filter compounds in human lenses: The origin of 4-(2-amino-3-hydroxyphenyl)-4-oxobutanoic acie O-beta-D-glucoside. Investigative Ophthalmology and Visual Science 40, 3237–3244.Google Scholar
Cleland, B.G. & Levick, W.R. (1974). Properties of rarely encountered types of ganglion cells in the cat's retina and an overall classification. Journal of Physiology 240, 457–492.CrossRefGoogle Scholar
Cooper, G.F. & Robson, J.G. (1969a). The yellow colour of the lens of the grey squirrel (sciurus carolinensis leucotis) Journal of Physiology 203, 403–410.Google Scholar
Cooper, G.F. & Robson, J.G. (1969b). The yellow colour of the lens of man and other primates. Journal of Physiology 203, 411–417.Google Scholar
Daw, N.W. & Pearlman, A.L. (1970). Cat colour vision: Evidence for more than one cone process. Journal of Physiology 211, 125–135CrossRefGoogle Scholar
Deans, M.R., Volgyi, B., Goodenough, D.A., Bloomfield, S.A., & Paul, D.L. (2002). Connexin 36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36, 703–712.CrossRefGoogle Scholar
Doi, M., Uji, Y., & Yamamura, H. (1995). Morphological classification of retinal ganglion cells in mice. Journal of Comparative Neurology 356, 368–386.CrossRefGoogle Scholar
Dräger, U.C. & Hubel, D.H. (1978). Studies of visual function and its decay in mice with hereditary retinal degeneration. Journal of Comparative Neurology 180, 85–114.CrossRefGoogle Scholar
Dräger, U.C. & Olsen, J.F. (1981). Ganglion cell distribution in the retina of the mouse. Investigative Ophthalmology and Visual Science 20, 285–293.Google Scholar
Ekesten, B. & Gouras, P. (2005). Cone inputs and interactions in murine retinal ganglion cells (Abstract). Investigative Ophthalmology and Visual Sciences S2236.Google Scholar
Ekesten, B., Gouras, P., & Yamamoto, S. (2000). Cone inputs to murine retinal ganglion cells. Vision Research 40, 2573–2577.CrossRefGoogle Scholar
Freedman, M.S., Lucas, R.J., Soni, B., von Schantz, M., Munoz, M., David-Gray, Z.K., & Foster, R.G. (1999). Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284, 502–504.CrossRefGoogle Scholar
Fukuda, Y. (1977). A three-group classification of rat retinal ganglion cells: Histological and physiological studies. Brain Research 119, 327–344.CrossRefGoogle Scholar
Glösmann, M. & Ahnelt, P.K. (1998). Co-expression of M- and S-opsin extends over the entire inferior mouse retina. [Abstract]. Investigative Ophthalmology and Visual Science 39, S1059.Google Scholar
Håstad, O. (2003). Plumage colors and the eye of the beholder. Dissertation of the Faculty of Science and Technology, Uppsala University.
Haverkamp, S., Wässle, H., Duebel, J., Kuner, T., Augustine, G.J., Feng, G., & Euler, T. (2005). The primordial, blue-cone color system of the mouse retina. Journal of Neuroscience 25, 5438–5445.CrossRefGoogle Scholar
Horn, G. & Hill, R.M. (1966). Responsiveness to sensory stimulation of units in the superior colliculus and subjacent tectosegmental regions of the rabbit. Experimental Neurology 14, 199–233.CrossRefGoogle Scholar
Hughes, A. (1971). Topographic relationships between the anatomy and physiology of the rabbit visual system. Documenta Ophthalmologica 30, 33–59.CrossRefGoogle Scholar
Jacobs, G.H., Neitz, J., & Deagan, J.F. (1991). Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature 353, 644–656.Google Scholar
Jacobs, G.H., Fenwick, J.A., & Williams, G.A. (2002). Evaluating the prospects for color vision in the mouse. Investigative Ophthalmology and Visual Science ARVO Abstracts B790.Google Scholar
Jeon, C.J., Stretta, E., & Masland, R.H. (1998). The major cell populations of the mouse retina. Journal of Neuroscience 18, 8936–8946.Google Scholar
Le Grande, Y. (1957). Light, Colour and Vision. New York: John Wiley & Sons, Inc.
Lettvin, J.Y., Maturana, H.R., Pitts, W.H., & McCulloch, W.S. (1961). Two remarks on the visual system of the frog. In Sensory Communication, ed. Rosenblith, W.A., pp. 21–23. New York: Wiley.
Lucas, R.J., Douglas, R.H., & Foster, R.G. (2001). Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nature Neuroscience 4, 621–626.CrossRefGoogle Scholar
Lythgoe, J.N. (1979). The Ecology of Vision. Oxford: Clarendon.
Lyubarsky, A.L., Falsini, B., Pennesi, M.E., Valentini, P., & Pugh, Jr., E.N. (1999). UV- and midwave-sensitive cone-driven retinal responses of the mouse: A possible phenotype for coexpression of cone photopigments. Journal of Neuroscience 19, 442–455.Google Scholar
Masland, R.H., Chow, K.L., & Stewart, D.L. (1971). Receptive-field characteristics of superior colliculus neurons in the rabbit. Journal of Neurophysiology 34, 148–156.Google Scholar
Michael, C.R. (1968). Receptive fields of single optic nerve fibers in a mammal with an all-cone retina. III. Color opponent units. Journal of Neurophysiology 31, 268–282.Google Scholar
Oyster, C. & Takahashi, E.S. (1975). Responses of rabbit superior colliculus neurons to repeated visual stimuli. Journal of Neurophysiology 38, 301–312.Google Scholar
Remtulla, S. & Hallett, P.E. (1985). A schematic eye for the mouse, and comparisons with the rat. Vision Research 25, 21–31.CrossRefGoogle Scholar
Ridder, W.H., Nusinowitz, S., & Heckenlively, J.R. (2002). Causes of cataract development in anesthetized mice. Experimental Eye Research 75, 365–370.CrossRefGoogle Scholar
Röhlich, P., van Veen, T., & Szel, A. (1994). Two different visual pigments in one retinal cone cell. Neuron 13, 1159–1166.CrossRefGoogle Scholar
Sagdullaev, M.A. & McCall, M.A. (2003). Effects of stimulus size on ganglion cell responses in the light adapted murine retina. Investigative Ophthalmology and Visual Science Abstract 5193.Google Scholar
Schaeffer, K.P. (1966). Mikroableitungen im Tectum opticum des frei beweglichen wachen kaninchens. Ein experimenteller Beitrag zum Problem des Bewegungssehens Arch Psych Nervenkranh 208, 120–146.Google Scholar
Semo, M., Peirson, S., Lupi, D., Lucas, R.J., Jeffrey, G., & Foster, R.G. (2003). Melanopsin retinal ganglion cells and the maintenance of circadian and papillary responses to light in aged rodless/coneless (rd/rd cl) mice. European Journal of Neuroscience 17, 1793–1801.CrossRefGoogle Scholar
Shi, Y. & Yokoyama, S. (2003). Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proceedings of the National Academy of Sciences of the U.S.A. 100, 8308–8313.CrossRefGoogle Scholar
Steinberg, R.H. (1969). High intensity effects on slow potentials and ganglion cell activity in the area centralis of cat retina. Vision Research 9, 333–350.CrossRefGoogle Scholar
Stone, C. & Pinto, L.H. (1993). Response properties of ganglion cells in the isolated mouse retina. Visual Neuroscience 10, 31–39.CrossRefGoogle Scholar
Szel, A., Röhlich, P., Caffe, A.R., Juliusson, B., Aguirre, G., & van Veen, T. (1992). Unique topographic separation of two spectral classes of cones in the mouse retina. Journal of Comparative Neurology 325, 327–342.CrossRefGoogle Scholar
Szel, A., Röhlich, P., Mieziewska, K., Aguirre, G., & van Veen, T. (1993). Spatial and temporal differences between the expression of short- and middle-wavelength cone pigments in the mouse retina: A developmental study. Journal of Comparative Neurology 331, 564–577.CrossRefGoogle Scholar
Tiao, Y.C. & Blakemore, C. (1976). Regional specialization in the golden hamster's retina. Journal of Comparative Neurology 168, 439–450.Google Scholar
Varju, D. & Pickering, S.G. (1969). Delayed responses of retinal ganglion cells: The influence of stimulus parameters upon the discharge frequency. Kybernetik 6, 112–119.CrossRefGoogle Scholar
Volgyi, B., Abdekalimi, J., & Bloomfield, S.A. (2003). A physiological/morphological study of alpha ganglion cells in the mouse retina. Investigative Ophthalmology and Visual Science Abstract 5191.Google Scholar
Yoshida, K., Watanabe, D., Ishikane, H., Tachibana, M., Pastan, I., & Nakanishi, S. (2001). A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movements. Neuron 30, 771–780.CrossRefGoogle Scholar