Skip to main content
×
×
Home

The squirrel as a rodent model of the human visual system

  • STEPHEN D. VAN HOOSER (a1) and SACHA B. NELSON (a1)
Abstract

Over the last 50 years, studies of receptive fields in the early mammalian visual system have identified many classes of response properties in brain areas such as retina, lateral geniculate nucleus (LGN), and primary visual cortex (V1). Recently, there has been significant interest in understanding the cellular and network mechanisms that underlie these visual responses and their functional architecture. Small mammals like rodents offer many advantages for such studies, because they are appropriate for a wide variety of experimental techniques. However, the traditional rodent models, mice and rats, do not rely heavily on vision and have small visual brain areas. Squirrels are highly visual rodents that may be excellent model preparations for understanding mechanisms of function and disease in the human visual system. They use vision for navigating in their environment, predator avoidance, and foraging for food. Visual brain areas such as LGN, V1, superior colliculus, and pulvinar are particularly large and well elaborated in the squirrel, and the squirrel has several extrastriate cortical areas lateral to V1. Unlike many mammals, most squirrel species are diurnal with cone-dominated retinas, similar to the primate fovea, and have excellent dichromatic color vision that is mediated by green and blue cones. Owing to their larger size, squirrels are physiologically more robust than mice and rats under anesthesia, and some hibernating species are particularly tolerant of hypoxia that occurs during procedures such as brain slicing. Finally, many basic anatomical and physiological properties in the early visual system of squirrel have now been described, permitting investigations of cellular mechanisms. In this article, we review four decades of anatomical, behavioral, and physiological studies in squirrel and make comparisons with other species.

Copyright
Corresponding author
Address correspondence and reprint requests to: Stephen D. Van Hooser, Duke University, Department of Neurobiology, Box 3209, Durham, NC 27710. E-mail: vanhooser@neuro.duke.edu
References
Hide All

REFERENCES

Abplanalp, P. (1970). Some subcortical connections of the visual system in tree shrews and squirrels. Brain, Behavior and Evolution 3, 155168.
Adams, D.L. & Horton, J.C. (2003). Capricious expression of cortical columns in the primate brain. Brain, Behavior and Evolution 6, 113114.
Adler, B. (1996). Outwitting squirrels: 101 cunning stratagems to reduce dramatically the egregious misappropriation of seed from your birdfeeder by squirrels. Chicago, IL: Chicago Review Press, Inc.
Agmon, A. & Connors, B.W. (1991). Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41, 365379.
Arenz, C.L. & Leger, D.W. (1999). Thirteen-lined ground squirrel (Sciuridae: Spermophilus tridecemlineatus) Antipredator vigilance: Monitoring the sky for aerial predators. Ethology 105, 807816.
Baker, J.F., Petersen, S.E., Newsome, W.T., & Allman, J.M. (1981). Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus): A quantitative comparison of medial, dorsomedial, dorsolateral, and middle temporal areas. Journal of Neurophysiology 45, 397416.
Birch, D. & Jacobs, G.H. (1979). Spatial contrast sensitivity in albino and pigmented rats. Vision Research 19, 933937.
Blake, R., Cool, S.J., & Crawford, M.L. (1974). Visual resolution in the cat. Vision Research 14, 12111217.
Blakeslee, B., Jacobs, G.H., & McCourt, M.E. (1985). Anisotropy in the preferred directions and visual field location of directionally-selective optic nerve fibers in the gray squirrel. Vision Research 25, 615618.
Blakeslee, B., Jacobs, G.H., & Neitz, J. (1988). Spectral mechanisms in the tree squirrel retina. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 162, 773780.
Blasdel, G.G. & Salama, G. (1986). Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579585.
Bosking, W.H., Zhang, Y., Schofield, B., & Fitzpatrick, D. (1997). Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. Journal of Neuroscience 17, 21122127.
Bullier, J. & Norton, T.T. (1979). Comparison of receptive-field properties of X and Y ganglion cells with X and Y lateral geniculate cells in the cat. Journal of Neurophysiology 42, 274291.
Casagrande, V.A. & Diamond, I.T. (1974). Ablation study of the superior colliculus in the tree shrew (Tupaia glis). Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 156, 207237.
Casagrande, V.A. & Norton, T.T. (1991). Lateral geniculate nucleus: A review of its physiology and function. In The Neural Basis of Visual Function, ed. Leventhal, A.G., pp. 4184. Basingstoke, UK: Macmillan Press.
Chapman, B. & Stryker, M.P. (1993). Development of orientation selectivity in ferret visual cortex and effects of deprivation. Journal of Neuroscience 13, 52515262.
Chisum, H.J., Mooser, F., & Fitzpatrick, D. (2003). Emergent properties of layer 2/3 neurons reflect the collinear arrangement of horizontal connections in tree shrew visual cortex. Journal of Neuroscience 23, 29472960.
Clarke, P.G., Donaldson, I.M., & Whitteridge, D. (1976). Binocular visual mechanisms in cortical areas I and II of the sheep. Journal of Physiology 256, 509526.
Clarke, P.G. & Whitteridge, D. (1976). The cortical visual areas of the sheep. Journal of Physiology 256, 497508.
Cleland, B.G., Dubin, M.W., & Levick, W.R. (1971). Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. Journal of Physiology 217, 473496.
Crewther, D.P., Crewther, S.G., & Sanderson, K.J. (1984). Primary visual cortex in the brushtailed possum: Receptive field properties and corticocortical connections. Brain, Behavior and Evolution 24, 184197.
Cuenca, N.Deng, P.Linberg, K.A., Fisher, S.K., & Kolb, H. (2003). Choline acetyltransferase is expressed by non-starburst amacrine cells in the ground squirrel retina. Brain Research 964, 2130.
Cuenca, N., Deng, P., Linberg, K.A., Lewis, G.P., Fisher, S.K., & Kolb, H. (2002). The neurons of the ground squirrel retina as revealed by immunostains for calcium binding proteins and neurotransmitters. Journal of Neurocytology 31, 649666.
Cusick, C.G. & Kaas, J.H. (1982). Retinal projections in adult and newborn grey squirrels. Brain Research 256, 275284.
DeBruyn, E.J., Wise, V.L., & Casagrande, V.A. (1980). The size and topographic arrangement of retinal ganglion cells in the galago. Vision Research 20, 315327.
Dec, K. & Harutiunian-Kozak, B. (1972). Columnar organization of visually driven neurons in the superior colliculus of the cat. Acta Neurobiologiae Experimentalis (Wars) 32, 3542.
DeValois, R.L., Morgan, H., & Snodderly, D.M. (1974). Psychophysical studies of monkey vision: III. Spatial luminance contrast sensitivity tests of macaque and human observers. Vision Research 14, 7581.
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847856.
DeVries, S.H., Qi, X., Smith, R., Makous, W., & Sterling, P. (2002). Electrical coupling between mammalian cones. Current Biology 12, 19001907.
DeVries, S.H. & Schwartz, E.A. (1999). Kainate receptors mediate synaptic transmission between cones and “Off” bipolar cells in a mammalian retina. Nature 397, 157160.
Diamond, I.T. (1976). Organization of the visual cortex: Comparative anatomical and behavioral studies. Federation Proceedings 35, 6067.
Dräger, U.C. (1974). Autoradiography of tritiated proline and fucose transported transneuronally from the eye to the visual cortex in pigmented and albino mice. Brain Research 82, 284292.
Dräger, U.C. & Olsen, J.F. (1981). Ganglion cell distribution in the retina of the mouse. Investigative Ophthalmology and Visual Science 20, 285293.
Duncan, R.D. & Jenkins, S.H. (1998). Use of visual cues in foraging by a diurnal herbivore, Belding's ground squirrel. Canadian Journal of Zoology-Revue Canadienne De Zoologie 76, 17661770.
Enroth-Cugell, C. & Robson, J.G. (1966). Contrast sensitivity of retinal ganglion cells of cat. Journal of Physiology 187, 517552.
Fagiolini, M., Fritschy, J.M., Low, K., Mohler, H., Rudolph, U., & Hensch, T.K. (2004). Specific GABAA circuits for visual cortical plasticity. Science 303, 16811683.
Fisher, S.K., Lewis, G.P., Linberg, K.A., & Verardo, M.R. (2005). Cellular remodeling in mammalian retina: Results from studies of experimental retinal detachment. Progress in Retinal and Eye Research 24, 395431.
Fitch, H.S. (1948). Ecology of the California ground squirrel on grazing lands. American Midland Naturalist 39, 513596.
Fukuda, Y. (1977). A three-group classification of rat retinal ganglion cells: Histological and physiological studies. Brain Research 119, 327334.
Fukuda, Y., Takatsuji, K., Sawai, H., Wakakuwa, K., Watanabe, M., & Mitani-Yamanishi, Y. (1986). Ipsilateral retinal projections and laminations of the dorsal lateral geniculate nucleus in the eastern chipmunk (Tamias sibiricus asiaticus). Brain Research 384, 373378.
Giolli, R.A. & Guthrie, M.D. (1969). The primary optic projections in the rabbit. An experimental degeneration study. Journal of Comparative Neurology 136, 99126.
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.
Godement, P., Saillour, P., & Imbert, M. (1980). The ipsilateral optic pathway to the dorsal lateral geniculate nucleus and superior colliculus in mice with prenatal or postnatal loss of one eye. Journal of Comparative Neurology 190, 611626.
Gordon, J.A. & Stryker, M.P. (1996). Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. Journal of Neuroscience 16, 32743286.
Gould, H.J., 3rd. (1984). Interhemispheric connections of the visual cortex in the grey squirrel (Sciurus carolinensis). Journal of Comparative Neurology 223, 259301.
Green, D.G., Powers, M.K., & Banks, M.S. (1980). Depth of focus, eye size and visual acuity. Vision Research 20, 827835.
Grinvald, A., Lieke, E., Frostig, R.D., Gilbert, C.D., & Wiesel, T.N. (1986). Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324, 361364.
Gur, M. & Purple, R.L. (1978). Retinal ganglion cell activity in the ground squirrel under halothane anesthesia. Vision Research 18, 114.
Gur, M. & Sivak, J.G. (1979). Refractive state of the eye of a small diurnal mammal: The ground squirrel. Journal of the Optical Society of America B 56, 689695.
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.
Hall, W.C., Kaas, J.H., Killackey, H., & Diamond, I.T. (1971). Cortical visual areas in the grey squirrel (Sciurus carolinensis): A correlation between cortical evoked potential maps and architectonic subdivisions. Journal of Neurophysiology 34, 437452.
Harting, J.K. & Huerta, M.F. (1983). The geniculostriate projection in the grey squirrel: Preliminary autoradiographic data. Brain Research 272, 341349.
Harting, J.K., Huerta, M.F., Hashikawa, T., & van Lieshout, D.P. (1991). Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: Organization of tectogeniculate pathways in nineteen species. Journal of Comparative Neurology 304, 275306.
Hollander, H. & Halbig, W. (1980). Topography of retinal representation in the rabbit cortex: An experimental study using transneuronal and retrograde tracing techniques. Journal of Comparative Neurology 193, 701710.
Horton, J.C. & Adams, D.L. (2005). The cortical column: A structure without a function. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 837862.
Hubel, D.H. (1975). An autoradiographic study of the retino-cortical projections in the tree shrew (Tupaia glis). Brain Research 96, 4150.
Hubel, D.H., LeVay, S., & Wiesel, T.N. (1975). Mode of termination of retinotectal fibers in macaque monkey: An autoradiographic study. Brain Research 96, 2540.
Hubel, D.H. & Wiesel, T.N. (1959). Receptive fields of single neurones in the cat's striate cortex. Journal of Physiology 148, 574591.
Hubel, D.H. & Wiesel, T.N. (1960). Receptive fields of optic nerve fibres in the spider monkey. Journal of Physiology 154, 572580.
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106154.
Hubel, D.H. & Wiesel, T.N. (1963). Shape and arrangement of columns in cat's striate cortex. Journal of Physiology 165, 559568.
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215243.
Hubel, D.H., Wiesel, T.N., & Stryker, M.P. (1978). Anatomical demonstration of orientation columns in macaque monkey. Journal of Comparative Neurology 177, 361380.
Hughes, A. (1975). A quantitative analysis of the cat retinal ganglion cell topography. Journal of Comparative Neurology 163, 107128.
Humphrey, A.L. & Norton, T.T. (1980). Topographic organization of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). I. Microelectrode recording. Journal of Comparative Neurology 192, 531547.
Ibbotson, M.R. & Mark, R.F. (2003). Orientation and spatiotemporal tuning of cells in the primary visual cortex of an Australian marsupial, the wallaby Macropus eugenii. Journal of Physiology 189, 115123.
Immel, J.H. & Fisher, S.K. (1985). Cone photoreceptor shedding in the tree shrew (Tupaia belangerii). Cell Tissue Research 239, 667675.
Jacobs, G.H. (1975). Scotopic and photopic visual capacities of an arboreal squirrel (sciurus niger). Brain, Behavior and Evolution 10, 307321.
Jacobs, G.H. (1977). Visual capacities of the owl monkey (Aotus trivirgatus)–II. Spatial contrast sensitivity. Vision Research 17, 821825.
Jacobs, G.H., Birch, D.G., & Blakeslee, B. (1982). Visual acuity and spatial contrast sensitivity in tree squirrels. Behavioural Processes 7, 367375.
Jacobs, G.H., Blakeslee, B., McCourt, M.E., & Tootell, R.H. (1980a). Visual sensitivity of ground squirrels to spatial and temporal luminance variations. Journal of Comparative Physiology 136, 291299.
Jacobs, G.H., Calderone, J.B., Sakai, T., Lewis, G.P., & Fisher, S.K. (2002). An animal model for studying cone function in retinal detachment. Documenta Ophthalmologica. Advances in Ophthalmology 104, 119132.
Jacobs, G.H. & Neitz, J. (1985). Color vision in squirrel monkeys: Sex-related differences suggest the mode of inheritance. Vision Research 25, 141143.
Jacobs, G.H. & Tootell, R.B. (1980). Spectrally-opponent responses in ground squirrel optic nerve. Vision Research 20, 913.
Jacobs, G.H. & Tootell, R.B. (1981). Spectral-response properties of optic-nerve fibers in the ground squirrel. Journal of Neurophysiology 45, 891902.
Jacobs, G.H., Tootell, R.B., Fisher, S.K., & Anderson, D.H. (1980b). Rod photoreceptors and scotopic vision in ground squirrels. Journal of Comparative Neurology 189, 113125.
Jacobs, G.H. & Yolton, R.L. (1969). Dichromacy in the ground squirrel. Nature 223, 414415.
Jacobs, G.H. & Yolton, R.L. (1971). Visual sensitivity and color vision in ground squirrels. Vision Research 11, 511537.
Johnson, P.T., Geller, S.F., & Reese, B.E. (1998). Distribution, size and number of axons in the optic pathway of ground squirrels. Experimental Brain Research 118, 93104.
Kaas, J.H. (1996). What comparative studies of neocortex tell us about the human brain. Revista Brasileira de Biologia 56, 315322.
Kaas, J.H. (1997). Topographic maps are fundamental to sensory processing. Brain Research Bulletin 44, 107112.
Kaas, J.H., Guillery, R.W., & Allman, J.M. (1972a). Some principles of organization in the dorsal lateral geniculate nucleus. Brain, Behavior and Evolution 6, 253299.
Kaas, J.H., Hall, W.C., & Diamond, I.T. (1972b). Visual cortex of the grey squirrel (Sciurus carolinensis): Architectonic subdivisions and connections from the visual thalamus. Journal of Comparative Neurology 145, 273305.
Kaas, J.H., Harting, J.K., & Guillery, R.W. (1974). Representation of the complete retina in the contralateral superior colliculus of some mammals. Brain Research 65, 343346.
Kaas, J.H., Krubitzer, L.A., & Johanson, K.L. (1989). Cortical connections of areas 17 (V-I) and 18 (V-II) of squirrels. Journal of Comparative Neurology 281, 426446.
Kicliter, E., Loop, M.S., & Jane, J.A. (1977). Effects of posterior neocortical lesions on wavelength, light/dark and stripe orientation discrimination in ground squirrels. Brain Research 122, 1531.
Kryger, Z., Galli-Resta, L., Jacobs, G.H., & Reese, B.E. (1998). The topography of rod and cone photoreceptors in the retina of the ground squirrel. Visual Neuroscience 15, 685691.
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768.
Lane, R.H., Allman, J.M., & Kaas, J.H. (1971). Representation of the visual field in the superior colliculus of the grey squirrel (Sciurus carolinensis) and the tree shrew (Tupaia glis). Brain Research 26, 277292.
Lane, R.H., Allman, J.M., Kaas, J.H., & Miezin, F.M. (1973). The visuotopic organization of the superior colliculus of the owl monkey (Aotus trivirgatus) and the bush baby (Galago senegalensis). Brain Research 60, 335349.
Law, M.I., Zahs, K.R., & Stryker, M.P. (1988). Organization of primary visual cortex (area 17) in the ferret. Journal of Comparative Neurology 278, 157180.
LeVay, S., McConnell, S.K., & Luskin, M.B. (1987). Functional organization of primary visual cortex in the mink (Mustela vison), and a comparison with the cat. Journal of Comparative Neurology 257, 422441.
Li, C., Cheng, M., Yang, H., Peachey, N.S., & Naash, M.I. (2001). Age-related changes in the mouse outer retina. Optometry & Vision Science 78, 425430.
Li, W. & DeVries, S.H. (2004). Separate blue and green cone networks in the mammalian retina. Brain, Behavior and Evolution 7, 751756.
Linberg, K.A., Sakai, T., Lewis, G.P., & Fisher, S.K. (2002). Experimental retinal detachment in the cone-dominant ground squirrel retina: Morphology and basic immunocytochemistry. Visual Neuroscience 19, 603619.
Linberg, K.A., Suemune, S., & Fisher, S.K. (1996). Retinal neurons of the California ground squirrel, Spermophilus beecheyi: A Golgi study. Journal of Comparative Neurology 365, 173216.
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.
Livingstone, M.S. (1996). Ocular dominance columns in New World monkeys. Journal of Neuroscience 16, 20862096.
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309356.
Long, K.O. & Fisher, S.K. (1983). The distributions of photoreceptors and ganglion cells in the California ground squirrel, Spermophilus beecheyi. Journal of Comparative Neurology 221, 329340.
Lugo-Garcia, N. & Blanco, R.E. (1993). Dopaminergic neurons in the cone-dominated ground squirrel retina: A light and electron microscopy study. Journal of Hirnforsch 34, 561569.
Lugo-Garcia, N. & Kicliter, E. (1988). Morphology of ganglion cells which project to the dorsal lateral geniculate and superior colliculus in the ground squirrel. Brain Research 454, 6777.
Lyon, D.C., Jain, N., & Kaas, J.H. (2003). The visual pulvinar in tree shrews II. Projections of four nuclei to areas of visual cortex. Journal of Comparative Neurology 467, 607627.
Major, D.E., Luksch, H., & Karten, H.J. (2000). Bottlebrush dendritic endings and large dendritic fields: Motion-detecting neurons in the mammalian tectum. Journal of Comparative Neurology 423, 243260.
Major, D.E., Rodman, H.R., Libedinsky, C., & Karten, H.J. (2003). Pattern of retinal projections in the California ground squirrel (Spermophilus beecheyi): Anterograde tracing study using cholera toxin. Journal of Comparative Neurology 463, 317340.
Martin, P.R., White, A.J., Goodchild, A.K., Wilder, H.D., & Sefton, A.E. (1997). Evidence that blue-on cells are part of the third geniculocortical pathway in primates. European Journal of Neuroscience 9, 15361541.
Maunsell, J.H. & Van Essen, D.C. (1983). Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. Journal of Neurophysiology 49, 11271147.
McBrien, N.A., Moghaddam, H.O., New, R., & Williams, L.R. (1993). Experimental myopia in a diurnal mammal (Sciurus carolinensis) with no accommodative ability. Journal of Physiology 469, 427441.
McConnell, S.K. & LeVay, S. (1986). Anatomical organization of the visual system of the mink, Mustela vison. Journal of Comparative Neurology 250, 109132.
McCourt, M.E. & Jacobs, G.H. (1984a). Directional filter characteristics of optic nerve fibers in California ground squirrel (Spermophilus beecheyi). Journal of Neurophysiology 52, 12001212.
McCourt, M.E. & Jacobs, G.H. (1984b). Refractive state, depth of focus and accommodation of the eye of the California ground squirrel (Spermophilus beecheyi). Vision Research 24, 12611266.
McCourt, M.E. & Jacobs, G.H. (1984c). Spatial filter characteristics of optic nerve fibers in California ground squirrel (Spermophilus beecheyi). Journal of Neurophysiology 52, 11811199.
Metín, C., Godement, P., & Imbert, M. (1988). The primary visual cortex in the mouse: Receptive field properties and functional organization. Experimental Brain Research 69, 594612.
Michael, C.R. (1968a). Receptive fields of single optic nerve fibers in a mammal with an all-cone retina. 3. Opponent color units. Journal of Neurophysiology 31, 268282.
Michael, C.R. (1968b). Receptive fields of single optic nerve fibers in a mammal with an all-cone retina. I: Contrast-sensitive units. Journal of Neurophysiology 31, 249256.
Michael, C.R. (1968c). Receptive fields of single optic nerve fibers in a mammal with an all-cone retina. II: Directionally selective units. Journal of Neurophysiology 31, 257267.
Michael, C.R. (1972a). Functional organization of cells in superior colliculus of the ground squirrel. Journal of Neurophysiology 35, 833846.
Michael, C.R. (1972b). Visual receptive fields of single neurons in superior colliculus of the ground squirrel. Journal of Neurophysiology 35, 815832.
Michael, C.R. (1973). Opponent-color and opponent-contrast cells in lateral geniculate nucleus of the ground squirrel. Journal of Neurophysiology 36, 536550.
Montero, V.M., Brugge, J.F., & Beitel, R.E. (1968). Relation of the visual field to the lateral geniculate body of the albino rat. Journal of Neurophysiology 31, 221236.
Moore, S. (2001). The anatomy of the visual system of the gray squirrel as revealed by histological and histochemical techniques. Waltham, MA: Brandeis University, Department of Biology.
Morigiwa, K., Sawai, H., Wakakuwa, K., Mitani-Yamanishi, Y., & Fukuda, Y. (1988). Retinal inputs and laminar distributions of the dorsal lateral geniculate nucleus relay cells in the eastern chipmunk (Tamias sibiricus asiaticus). Experimental Brain Research 71, 527540.
Murphy, E.H. & Berman, N. (1979). The rabbit and the cat: A comparison of some features of response properties of single cells in the primary visual cortex. Journal of Comparative Neurology 188, 401427.
Orban, G.A., Kennedy, H., & Bullier, J. (1986). Velocity sensitivity and direction selectivity of neurons in areas V1 and V2 of the monkey: Influence of eccentricity. Journal of Neurophysiology 56, 462480.
Owings, D.H., Coss, R.G., McKernon, D., Rowe, M.P., & Arrowood, P.C. (2001). Snake-directed antipredator behavior of rock squirrels (spermophilus variegatus): Population differences and snake-species discrimination. Behaviour 138, 575595.
Pakhotin, P.I., Belousov, A.B., & Otmakhov, N.A. (1990). Functional stability of the brain slices of ground squirrels, Citellus undulatus, kept in conditions of prolonged deep periodic hypothermia: Electrophysiological criteria. Neuroscience 38, 591598.
Paolini, M. & Sereno, M.I. (1998). Direction selectivity in the middle lateral and lateral (ML and L) visual areas in the California ground squirrel. Cerebral Cortex 8, 362371.
Pearlman, A.L. & Daw, N.W. (1970). Opponent color cells in the cat lateral geniculate nucleus. Science 167, 8486.
Perry, V.H., Oehler, R., & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 11011123.
Petry, H.M., Fox, R., & Casagrande, V.A. (1984). Spatial contrast sensitivity of the tree shrew. Vision Research 24, 10371042.
Pettigrew, J.D., Ramachandran, V.S., & Bravo, H. (1984). Some neural connections subserving binocular vision in ungulates. Brain, Behavior and Evolution 24, 6593.
Polkoshnikov, E. & Supin, A. (1988). Receptive field properties of neurons in the squirrel striate cortex. Acta Neurobiologiae Experimentalis (Wars) 48, 4969.
Prusky, G.T., West, P.W., & Douglas, R.M. (2000). Behavioral assessment of visual acuity in mice and rats. Vision Research 40, 22012209.
Rao, S.C., Toth, L.J., & Sur, M. (1997). Optically imaged maps of orientation preference in primary visual cortex of cats and ferrets. Journal of Comparative Neurology 387, 358370.
Rebrik, T.I. & Korenbrot, J.I. (2004). In intact mammalian photoreceptors, Ca2+-dependent modulation of cGMP-gated ion channels is detectable in cones but not in rods. Journal of General Physiology 123, 6375.
Reese, B.E. & Jeffery, G. (1983). Crossed and uncrossed visual topography in dorsal lateral geniculate nucleus of the pigmented rat. Journal of Neurophysiology 49, 877885.
Revishchin, A.V. & Polkoshnikov, E.V. (2000). Selectivity of squirrel parastriate cortical neurons for speed and direction of moving stimuli. Doklady Biological Sciences 372, 255257.
Rivera, N. & Lugo, N. (1998). Four retinal ganglion cell types that project to the superior colliculus in the thirteen-lined ground squirrel (Spermophilus tridecemlineatus). Journal of Comparative Neurology 396, 105120.
Robson, J.A. & Hall, W.C. (1976). Projections from the superior colliculus to the dorsal lateral geniculate nucleus of the grey squirrel (Sciurus carolinensis). Brain Research 113, 379385.
Robson, J.A. & Hall, W.C. (1977). The organization of the pulvinar in the grey squirrel (Sciurus carolinensis). I. Cytoarchitecture and connections. Journal of Comparative Neurology 173, 355388.
Rocha-Miranda, C.E., Linden, R., Volchan, E., Lent, R., & Bombar-Dieri, R.A., Jr. (1976). Receptive field properties of single units in the opossum striate cortex. Brain Research 104, 197219.
Rodman, H.R. & Dieguez, D. (2003). The koniocellular pathway and the thalamo-cortical projection in the ground squirrel. 701.8. In SFN Meeting.
Rosa, M.G. & Krubitzer, L.A. (1999). The evolution of visual cortex: Where is V2? Trends in Neuroscience 22, 242248.
Royce, G.J., Ward, J.P., & Harting, J.K. (1976). Retinofugal pathways in two marsupials. Journal of Comparative Neurology 170, 391413.
Ruthazer, E.S. & Stryker, M.P. (1996). The role of activity in the development of long-range horizontal connections in area 17 of the ferret. Journal of Neuroscience 16, 72537269.
Sakai, T., Calderone, J.B., Lewis, G.P., Linberg, K.A., Fisher, S.K., & Jacobs, G.H. (2003). Cone photoreceptor recovery after experimental detachment and reattachment: An immunocytochemical, morphological, and electrophysiological study. Investigative Ophthalmology & Visual Science 44, 416425.
Sanna, P.P., Keyser, K.T., Celio, M.R., Karten, H.J., & Bloom, F.E. (1993). Distribution of parvalbumin immunoreactivity in the vertebrate retina. Brain Research 600, 141150.
Schuett, S., Bonhoeffer, T., & Hubener, M. (2002). Mapping retinotopic structure in mouse visual cortex with optical imaging. Journal of Neuroscience 22, 65496559.
Shatz, C.J. & Stryker, M.P. (1978). Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. Journal of Physiology 281, 267283.
Sherman, S.M. & Guillery, R.W. (2002). The role of the thalamus in the flow of information to the cortex. Philosophical Transactions of the Royal Society B: Biological Sciences 357, 16951708.
Shorten, M. (1954). Squirrels. London: Collins.
Sinclair, J.R., Jacobs, A.L., & Nirenberg, S. (2004). Selective ablation of a class of amacrine cells alters spatial processing in the retina. Journal of Neuroscience 24, 14591467.
Snyder, M. & Diamond, I.T. (1968). Organization and Function of Visual Cortex in Tree Shrew. Brain Behavior and Evolution 1, 244288.
Spear, P.D. & Baumann, T.P. (1975). Receptive-field characteristics of single neurons in lateral suprasylvian visual area of the cat. Journal of Neurophysiology 38, 14031420.
Sterling, P. (1990). Retina. In The synaptic organization of the brain, ed. Shepherd, G.M., pp. 170213. New York: Oxford University Press.
Stone, J. & Dreher, B. (1973). Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex. Journal of Neurophysiology 36, 551567.
Swadlow, H.A. & Weyand, T.G. (1985). Receptive-field and axonal properties of neurons in the dorsal lateral geniculate nucleus of awake unparalyzed rabbits. Journal of Neurophysiology 54, 168183.
Szel, A. & Rohlich, P. (1988). Four photoreceptor types in the ground squirrel retina as evidenced by immunocytochemistry. Vision Research 28, 12971302.
Tiao, Y.C. & Blakemore, C. (1976). Functional organization in the visual cortex of the golden hamster. Journal of Comparative Neurology 168, 459481.
Tigges, J. (1970). Retinal projections to subcortical optic nuclei in diurnal and nocturnal squirrels. Brain, Behavior and Evolution 3, 121134.
Tigges, J. & Tigges, M. (1969). The accessory optic system and other optic fibers of the squirrel monkey. Folia Primatologica 10, 245262.
Usrey, W.M. & Reid, R.C. (2000). Visual physiology of the lateral geniculate nucleus in two species of new world monkey: Saimiri sciureus and Aotus trivirgatis. Journal of Physiology 523 Pt 3, 755769.
Van Hooser, S.D., Heimel, J.A., Chung, S., & Nelson, S.B. (2006). Horizontal connectivity in primary visual cortex of a highly visual mammal lacking orientation maps. Journal of Neuroscience 26, 76807692.
Van Hooser, S.D., Heimel, J.A., Chung, S., & Nelson, S.B. (2006). Lack of patchy horizontal connectivity in primary visual cortex of a highly visual mammal without orientation maps. Journal of Neuroscience 26, 76807692.
Van Hooser, S.D., Heimel, J.A., Chung, S., Nelson, S.B., & Toth, L.J. (2005). Orientation selectivity without orientation maps in visual cortex of a highly visual mammal. Journal of Neuroscience 25, 1928.
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.
Vaughan, D.K., Gruber, A.R., Michalski, M.L., Seidling, J., & Schlink, S. (2006). Capture, care, and captive breeding of 13-lined ground squirrels, Spermophilus tridecemlineatus. Lab Animal (NY) 35, 3340.
Walls, G.L. (1942). The vertebrate eye and its adaptive radiation. Bloomfield Hills, MI: The Cranbook Press.
Ward, J.P. & Masterton, B. (1970). Encephalization and visual cortex in tree shrew (Tupaia-Glis). Brain Behavior and Evolution 3, 421469.
Ware, C.B., Casagrande, V.A., & Diamond, I.T. (1972). Does the acuity of the tree shrew suffer from removal of striate cortex? A commentary on the paper by ward and Masterton. Brain, Behavior and Evolution 5, 1829.
Webb, S.V. & Kaas, J.H. (1976). The sizes and distribution of ganglion cells in the retina of the owl monkey. Aotus trivirgatus. Vision Research 16, 12471254.
Weber, J.T., Casagrande, V.A., & Harting, J.K. (1977). Transneuronal transport of [3H]proline within the visual system of the grey squirrel. Brain Research 129, 346352.
Weiss, E.R., Raman, D., Shirakawa, S., Ducceschi, M.H., Bertram, P.T., Wong, F., Kraft, T.W., & Osawa, S. (1998). The cloning of GRK7, a candidate cone opsin kinase, from cone- and rod-dominant mammalian retinas. Molecular Vision 4, 27.
West, R.W. (1976). Light and electron microscopy of the ground squirrel retina: Functional considerations. Journal of Comparative Neurology 168, 355377.
West, R.W. (1978). Bipolar and horizontal cells of the gray squirrel retina: Golgi morphology and receptor connections. Vision Research 18, 129136.
West, R.W. & Dowling, J.E. (1975). Anatomical evidence for cone and rod-like receptors in the gray squirrel, ground squirrel, and prairie dog retinas. Journal of Comparative Neurology 159, 439460.
White, A.J., Wilder, H.D., Goodchild, A.K., Sefton, A.J., & Martin, P.R. (1998). Segregation of receptive field properties in the lateral geniculate nucleus of a New-World monkey, the marmoset Callithrix jacchus. Journal of Neurophysiology 80, 20632076.
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 11151156.
Wilson, M. (2000). A new labor agreement for the retina? Neuron 28, 628629.
Wong-Riley, M.T. & Norton, T.T.. (1988). Histochemical localization of cytochrome oxidase activity in the visual system of the tree shrew: Normal patterns and the effect of retinal impulse blockage. Journal of Comparative Neurology 272, 562578.
Wässle, H., Levick, W.R., & Cleland, B.G. (1975). The distribution of the alpha type of ganglion cells in the cat's retina. Journal of Comparative Neurology 159, 419438.
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society of London Series B, Biological Sciences 200, 441461.
Yolton, R.L., Yolton, D.P., Renz, J., & Jacobs, G.H. (1974). Preretinal absorbance in sciurid eyes. Journal of Mammal 55, 1420.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed