Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-20T02:12:42.492Z Has data issue: false hasContentIssue false

Spatial receptive field properties of rat retinal ganglion cells

Published online by Cambridge University Press:  23 September 2011

WALTER F. HEINE
Affiliation:
Department of Biomedical Engineering, Boston University, Boston, Massachusetts
CHRISTOPHER L. PASSAGLIA*
Affiliation:
Department of Biomedical Engineering, Boston University, Boston, Massachusetts
*
*Address correspondence and reprint requests to: Dr. Christopher L. Passaglia, Department of Biomedical Engineering, Boston University, 24 Cummington Street, Boston, MA 02215. E-mail: psagls@bu.edu

Abstract

The rat is a popular animal model for vision research, yet there is little quantitative information about the physiological properties of the cells that provide its brain with visual input, the retinal ganglion cells. It is not clear whether rats even possess the full complement of ganglion cell types found in other mammals. Since such information is important for evaluating rodent models of visual disease and elucidating the function of homologous and heterologous cells in different animals, we recorded from rat ganglion cells in vivo and systematically measured their spatial receptive field (RF) properties using spot, annulus, and grating patterns. Most of the recorded cells bore likeness to cat X and Y cells, exhibiting brisk responses, center-surround RFs, and linear or nonlinear spatial summation. The others resembled various types of mammalian W cell, including local-edge-detector cells, suppressed-by-contrast cells, and an unusual type with an ON–OFF surround. They generally exhibited sluggish responses, larger RFs, and lower responsiveness. The peak responsivity of brisk-nonlinear (Y-type) cells was around twice that of brisk-linear (X-type) cells and several fold that of sluggish cells. The RF size of brisk-linear and brisk-nonlinear cells was indistinguishable, with average center and surround diameters of 5.6 ± 1.3 and 26.4 ± 11.3 deg, respectively. In contrast, the center diameter of recorded sluggish cells averaged 12.8 ± 7.9 deg. The homogeneous RF size of rat brisk cells is unlike that of cat X and Y cells, and its implication regarding the putative roles of these two ganglion cell types in visual signaling is discussed.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2011

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

Anishchenko, A., Greschner, M., Elstrott, J., Sher, A., Litke, A.M., Feller, M.B. & Chichilnisky, E.J. (2010). Receptive field mosaics of retinal ganglion cells are established without visual experience. Journal of Neurophysiology 103, 18561864.CrossRefGoogle ScholarPubMed
Artal, P., Herreros de Tejada, P., Redó, C.M. & Green, D.G. (1998). Retinal image quality in the rodent eye. Visual Neuroscience 15, 597605.CrossRefGoogle ScholarPubMed
Barlow, H.B. (1965). Visual resolution and the diffraction limit. Science 149, 553555.CrossRefGoogle ScholarPubMed
Brown, J.E. & Rojas, J.A. (1965). Rat retinal ganglion cells: Receptive field organization and maintained activity. Journal of Neurophysiology 28, 10731090.CrossRefGoogle ScholarPubMed
Calderone, L., Grimes, P. & Shalev, M. (1986). Acute reversible cataract induced by xylazine and by ketamine-xylazine anesthesia in rats and mice. Experimental Eye Research 42, 331337.CrossRefGoogle ScholarPubMed
Caldwell, J.H. & Daw, N.W. (1978). New properties of rabbit retinal ganglion cells. The Journal of Physiology 276, 257276.CrossRefGoogle ScholarPubMed
Campbell, F.W., Carpenter, R.H. & Levinson, J.Z. (1969). Visibility of aperiodic patterns compared with that of sinusoidal gratings. The Journal of Physiology 204, 283298.CrossRefGoogle ScholarPubMed
Carcieri, S.M., Jacobs, A.L. & Nirenberg, S. (2003). Classification of retinal ganglion cells: A statistical approach. Journal of Neurophysiology 90, 17041713.CrossRefGoogle ScholarPubMed
Chader, G.J. (2002). Animal models in research on retinal degenerations: Past progress and future hope. Vision Research 42, 393399.CrossRefGoogle ScholarPubMed
Cleland, B.G., Dubin, M.W. & Levick, W.R. (1971). Sustained and transient neurones in the cat’s retina and lateral geniculate nucleus. The Journal of Physiology 217, 473496.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Levick, W.R. (1974). Brisk and sluggish concentrically organized ganglion cells in the cat’s retina. The Journal of Physiology 2(40), 421456.CrossRefGoogle Scholar
Cowey, A., Henken, D.B. & Perry, V.H. (1982). Effects on visual acuity of neonatal or adult tectal ablation in rats. Experimental Brain Research 48, 149152.CrossRefGoogle ScholarPubMed
Dean, P. (1978). Visual acuity in hooded rats: Effects of superior collicular or posterior neocortical lesions. Brain Research 156, 1731.CrossRefGoogle ScholarPubMed
Demb, J.B., Zaghloul, K., Haarsma, L. & Sterling, P. (2001). Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. The Journal of Neuroscience 21, 74477454.CrossRefGoogle ScholarPubMed
Dreher, B., Sefton, A.J., Ni, S.Y. & Nisbett, G. (1985). The morphology, number, distribution and central projections of class I retinal ganglion cells in albino and hooded rats. Brain, Behavior and Evolution 26, 1048.CrossRefGoogle Scholar
Enroth-Cugell, C. & Freeman, A.W. (1987). The receptive-field spatial structure of cat retinal Y cells. The Journal of Physiology 384, 4979.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology 187, 517552.CrossRefGoogle ScholarPubMed
Freeman, D.K., Heine, W.F. & Passaglia, C.L. (2008). The maintained discharge of rat retinal ganglion cells. Visual Neuroscience 25, 535548.CrossRefGoogle ScholarPubMed
Freeman, D.K., Heine, W.F. & Passaglia, C.L. (2010). Single-unit in vivo recordings from the optic chiasm of rat. Journal of Visualized Experiments 38, pii:1887. doi:10.3791/1887.Google Scholar
Friedman, L.J. & Green, D.G. (1982). Ganglion cell acuity in hooded rats. Vision Research 22, 441444.CrossRefGoogle ScholarPubMed
Frishman, L.J., Freeman, A.W., Troy, J.B., Schweitzer-Tong, D.E. & Enroth-Cugell, C. (1987). Spatiotemporal frequency response of cat retinal ganglion cells. The Journal of General Physiology 89, 599628.CrossRefGoogle ScholarPubMed
Fukuda, Y. (1977). A three-group classification of rat retinal ganglion cells: Histological and physiological studies. Brain Research 119, 327334.CrossRefGoogle ScholarPubMed
Fukuda, Y., Sumitomo, I., Sugitani, M. & Iwama, K. (1979). Receptive-field properties of cells in the dorsal part of the albino rat’s lateral geniculate nucleus. The Japanese Journal of Physiology 29, 283307.CrossRefGoogle ScholarPubMed
Girman, S.V. & Lund, R.D. (2010). Orientation-specific modulation of rat retinal ganglion cell responses and its dependence on relative orientations of the center and surround gratings. Journal of Neurophysiology 104, 29512962.CrossRefGoogle Scholar
Girman, S.V., Sauve, Y. & Lund, R.D. (1999). Receptive field properties of single neurons in rat primary visual cortex. Journal of Neurophysiology 82, 301311.CrossRefGoogle ScholarPubMed
Grieve, K.L. (2005). Binocular visual responses in cells of the rat LGN. The Journal of Physiology 566, 119124.CrossRefGoogle Scholar
Grubb, M.S. & Thompson, I.D. (2003). Quantitative characterization of visual response properties in the mouse dorsal lateral geniculate nucleus. Journal of Neurophysiology 90, 35943607.CrossRefGoogle ScholarPubMed
Hale, P.T., Sefton, A.J. & Dreher, B. (1979). A correlation of receptive field properties with conduction velocity of cells in the rat’s retino-geniculo-cortical pathway. Experimental Brain Research 35, 425442.CrossRefGoogle ScholarPubMed
Hammond, P. (1974). Cat retinal ganglion cells: Size and shape of receptive field centres. The Journal of Physiology 242, 99118.CrossRefGoogle ScholarPubMed
Hartigan, J.A. & Hartigan, P.M. (1985). The dip test of unimodality. Annals of Statistics 13, 7084.CrossRefGoogle Scholar
Hochstein, S. & Shapley, R.M. (1976). Quantitative analysis of retinal ganglion cell classifications. The Journal of Physiology 262, 237264.CrossRefGoogle ScholarPubMed
Huxlin, K.R. & Goodchild, A.K. (1997). Retinal ganglion cells in the albino rat: Revised morphological classification. The Journal of Comparative Neurology 385, 309323.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Jakiela, H.G. & Enroth-Cugell, C. (1976). Adaptation and dynamics in X-cells and Y-cells of the cat retina. Experimental Brain Research 24, 335342.CrossRefGoogle ScholarPubMed
Kitada, K., Ishishita, S., Tosaka, K., Takahashi, R., Ueda, M., Keng, V.W., Horie, K. & Takeda, J. (2007). Transposon-tagged mutagenesis in the rat. Nature Methods 4, 131133.CrossRefGoogle ScholarPubMed
Lashley, K.S. (1938). The mechanism of vision. XV: Preliminary studies of the rat’s capacity for detailed vision. Journal of Comparative Psychology 18, 123193.Google Scholar
Lee, B.B., Kremers, J. & Yeh, T. (1998). Receptive fields of primate retinal ganglion cells studied with a novel technique. Visual Neuroscience 15, 161175.CrossRefGoogle ScholarPubMed
Lennie, P. & Perry, V.H. (1981). Spatial contrast sensitivity of cells in the lateral geniculate nucleus of the rat. The Journal of Physiology 315, 6979.CrossRefGoogle ScholarPubMed
Levick, W.R. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit’s retina. The Journal of Physiology 188, 285307.CrossRefGoogle Scholar
Levick, W.R. (1996). Receptive fields of cat retinal ganglion cells with special reference to the alpha cells. Progress in Retinal and Eye Research 15, 457500.CrossRefGoogle Scholar
Levick, W.R. & Thibos, L.N. (1982). Analysis of orientation bias in cat retina. The Journal of Physiology 329, 243261.CrossRefGoogle ScholarPubMed
Lin, B., Wang, S.W. & Masland, R.H. (2004). Retinal ganglion cell type, size, and spacing can be specified independent of homotypic dendritic contacts. Neuron 43, 475485.CrossRefGoogle ScholarPubMed
Linden, R., Cowey, A. & Perry, V.H. (1983). Tectal ablation at different ages in developing rats has different effects on retinal ganglion cell density but not on visual acuity. Experimental Brain Research 51, 368376.CrossRefGoogle Scholar
Linsenmeier, R.A., Frishman, L.J., Jakiela, H.G. & Enroth-Cugell, C. (1982). Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 11731183.CrossRefGoogle ScholarPubMed
Martin, P.R. (1986). The projection of different retinal ganglion cell classes to the dorsal lateral geniculate nucleus in the hooded rat. Experimental Brain Research 62, 7788.CrossRefGoogle Scholar
McCourt, M.E. & Jacobs, G.H. (1984). Spatial filter characteristics of optic nerve fibers in California ground squirrel (Spermophilus beecheyi). Journal of Neurophysiology 52, 11811199.CrossRefGoogle ScholarPubMed
Mechler, F. & Ringach, D.L. (2002). On the classification of simple and complex cells. Vision Research 42, 10171033.CrossRefGoogle ScholarPubMed
Merwine, D.K., Amthor, F.R. & Grzywacz, N.M. (1995). Interaction between center and surround in rabbit retinal ganglion cells. Journal of Neurophysiology 73, 15471567.CrossRefGoogle ScholarPubMed
Morrison, J.C., Moore, C.G., Deppmeier, L.M., Gold, B.G., Meshul, C.K. & Johnson, E.C. (1997). A rat model of chronic pressure-induced optic nerve damage. Experimental Eye Research 64, 8596.CrossRefGoogle ScholarPubMed
Partridge, L.D. & Brown, J.E. (1970). Receptive fields of rat retinal ganglion cells. Vision Research 10, 455460.CrossRefGoogle ScholarPubMed
Passaglia, C.L., Enroth-Cugell, C. & Troy, J.B. (2001). Effects of remote stimulation on the mean firing rate of cat retinal ganglion cells. The Journal of Neuroscience 21, 57945803.CrossRefGoogle ScholarPubMed
Passaglia, C.L., Troy, J.B., Ruttiger, L. & Lee, B.B. (2002). Orientation sensitivity of ganglion cells in primate retina. Vision Research 42, 683694.CrossRefGoogle ScholarPubMed
Peichl, L. & Wassle, H. (1979). Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. The Journal of Physiology 291, 117141.CrossRefGoogle ScholarPubMed
Perry, V.H. (1979). The ganglion cell layer of the retina of the rat: A Golgi study. Proceedings of the Royal Society of London. Series B, Biological Sciences 204, 363375.Google Scholar
Powers, M.K. & Green, D.G. (1978). Single retinal ganglion cell responses in the dark-reared rat: Grating acuity, contrast sensitivity, and defocusing. Vision Research 18, 15331539.CrossRefGoogle ScholarPubMed
Prévost, F., Lepore, F. & Guillemot, J.P. (2007). Spatiotemporal receptive field properties of cells in the rat superior colliculus. Brain Research 1142, 8091.CrossRefGoogle ScholarPubMed
Reese, B.E. & Cowey, A. (1986). Large retinal ganglion cells in the rat: Their distribution and laterality of projection. Experimental Brain Research 61, 375385.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1967). Receptive fields in the cat retina: A new type. Science 157, 9092.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Stone, J. (1965). Analysis of receptive fields of cat retinal ganglion cells. Journal of Neurophysiology 28, 832849.CrossRefGoogle ScholarPubMed
Rowe, M.H. & Cox, J.F. (1993). Spatial receptive-field structure of cat retinal W cells. Visual Neuroscience 10, 765779.CrossRefGoogle ScholarPubMed
Sagdullaev, B.T. & McCall, M.A. (2005). Stimulus size and intensity alter fundamental receptive field properties of mouse retinal ganglion cells in vivo. Visual Neuroscience 22, 649659.CrossRefGoogle ScholarPubMed
Schall, J.D., Perry, V.H. & Leventhal, A.G. (1987). Ganglion cell dendritic structure and retinal topography in the rat. The Journal of Comparative Neurology 257, 160165.CrossRefGoogle ScholarPubMed
Sefton, A.J. & Swinburn, M. (1964). Electrical activity of lateral geniculate nucleus and optic tract of the rat. Vision Research 4, 315328.CrossRefGoogle ScholarPubMed
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neuroscience 9, 229235.CrossRefGoogle Scholar
Silveira, L.C., Heywood, C.A. & Cowey, A. (1987). Contrast sensitivity and visual acuity of the pigmented rat determined electrophysiologically. Vision Research 27, 17191731.CrossRefGoogle ScholarPubMed
Stone, J. & Fukuda, Y. (1974). Properties of cat retinal ganglion cells: A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 37, 722748.CrossRefGoogle ScholarPubMed
Stone, C. & Pinto, L.H. (1993). Response properties of ganglion cells in the isolated mouse retina. Visual Neuroscience 10, 3139.CrossRefGoogle ScholarPubMed
Sumitomo, I., Sugitani, M., Fukuda, Y. & Iwama, K. (1979). Properties of cells responding to visual stimuli in the rat ventral lateral geniculate nucleus. Experimental Neurology 66, 721736.CrossRefGoogle ScholarPubMed
Sun, W., Li, N. & He, S. (2002). Large-scale morphological survey of rat retinal ganglion cells. Visual Neuroscience 19, 483493.CrossRefGoogle ScholarPubMed
Tailby, C., Solomon, S.G., Dhruv, N.T., Majaj, N.J., Sokol, S.H. & Lennie, P. (2007). A new code for contrast in the primate visual pathway. The Journal of Neuroscience 27, 39043909.CrossRefGoogle ScholarPubMed
Trejo, L.J. & Cicerone, C.M. (1984). Cells in the pretectal olivary nucleus are in the pathway for the direct light reflex of the pupil in the rat. Brain Research 300, 4962.CrossRefGoogle ScholarPubMed
Troy, J.B., Einstein, G., Schuurmans, R.P., Robson, J.G. & Enroth-Cugell, C. (1989). Responses to sinusoidal gratings of two types of very nonlinear retinal ganglion cells of cat. Visual Neuroscience 3, 213223.CrossRefGoogle ScholarPubMed
Troy, J.B., Schweitzer-Tong, D.E. & Enroth-Cugell, C. (1995). Receptive field properties of Q retinal ganglion cells of the cat. Visual Neuroscience 12, 285300.CrossRefGoogle ScholarPubMed
Troy, J.B. & Shou, T. (2002). The receptive fields of cat retinal ganglion cells in physiological and pathological states: Where we are after half a century of research. Progress in Retinal and Eye Research 21, 263302.CrossRefGoogle ScholarPubMed
van Dongen, P.A., ter Laak, H.J., Thijssen, J.M. & Vendrik, A.J. (1976). Functional classification of cells in the optic tract of a tree shrew (Tupaia chinensis). Experimental Brain Research 24, 441446.CrossRefGoogle ScholarPubMed
Vaney, D.I., Levick, W.R. & Thibos, L.N. (1981). Rabbit retinal ganglion cells. Receptive field classification and axonal conduction properties. Experimental Brain Research 44, 2733.Google ScholarPubMed
van Hooser, S.D., Heimel, J.A. & Nelson, S.B. (2003). Receptive field properties and laminar organization of lateral geniculate nucleus in the gray squirrel (Sciurus carolinensis). Journal of Neurophysiology 90, 33983418.CrossRefGoogle ScholarPubMed
van Wyk, M., Taylor, W.R. & Vaney, D.I. (2006). Local edge detectors: A substrate for fine spatial vision at low temporal frequencies in rabbit retina. The Journal of Neuroscience 26, 1325013263.CrossRefGoogle ScholarPubMed
Wiesenfeld, Z. & Branchek, T. (1976). Refractive state and visual acuity in the hooded rat. Vision Research 16, 823827.CrossRefGoogle ScholarPubMed
Winters, R.W., Hickey, T.L. & Pollack, J.G. (1973). Effect of variations of target location upon the peripheral responses of on-center retinal ganglion cells in the cat. Vision Research 13, 14871498.CrossRefGoogle ScholarPubMed
Yu, D.Y., Cringle, S.J., Su, E.N., Yu, P.K., Jerums, G. & Cooper, M.E. (2001). Pathogenesis and intervention strategies in diabetic retinopathy. Clinical and Experimental Ophthalmology 29, 164166.Google ScholarPubMed
Zeck, G.M., Xiao, Q. & Masland, R.H. (2005). The spatial filtering properties of local edge detectors and brisk-sustained retinal ganglion cells. The European Journal of Neuroscience 22, 20162026.CrossRefGoogle ScholarPubMed