Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T11:45:58.977Z Has data issue: false hasContentIssue false

Retinal projections in the ground squirrel (Citellus tridecemlineatus)

Published online by Cambridge University Press:  02 June 2009

Seema Agarwala
Affiliation:
Department of Psychology, State University of New York at Stony Brook, Stony Brook
Heywood M. Petry
Affiliation:
Department of Psychology, State University of New York at Stony Brook, Stony Brook
Jack G. May III
Affiliation:
Department of Psychology, State University of New York at Stony Brook, Stony Brook

Abstract

The retinal projections of the thirteen-lined ground squirrel were determined by tracing anterograde transport of intravitreally injected horseradish peroxidase (HRP) or wheat-germ conjugated horseradish peroxidase (WGA-HRP). Label was seen in the suprachiasmatic nucleus and adjacent anterior hypothalamic area, the accessory optic system (the medial, dorsal, and lateral terminal nuclei), the dorsal and ventral lateral geniculate nuclei, the intergeniculate leaflet, the pretectal nuclei (the anterior, posterior, and olivary pretectal nuclei and the nucleus of optic tract), and the superior colliculus. Most of these structures were labeled bilaterally, with dense contralateral label and sparse ipsilateral label, a pattern typical for animals with laterally placed eyes. However, the suprachiasmatic nucleus and the nucleus of the optic tract received input only from the contralateral eye. In contrast to previous degeneration studies, the sensitive HRP tracers (in conjunction with cytochrome-oxidase reactivity) revealed an elaborate organization within the lateral geniculate nucleus (dorsal LGN, ventral LGN, and intergeniculate leaflet) that is consistent with existing organizational schemes for other mammalian species.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1989

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

Abplanalp, P. (1974). Topography of retinal efferent connections in sciurids. Brain, Behavior and Evolution 9, 333375.CrossRefGoogle ScholarPubMed
Beckstead, R.M. & Frankfurter, A. (1983). A direct projection from the retina to the intermediate gray layer of the superior colliculus demonstrated by anterograde transport of horseradish peroxidase in monkey, cat, and rat. Experimental Brain Research 52, 261268.CrossRefGoogle Scholar
Berson, D.M. & Mcilwain, J.T. (1982). Retinal Y-cell activation of deep-layer cells in superior colliculus of the cat. Journal of Neurophysiology 47, 700714.CrossRefGoogle ScholarPubMed
Bruce, L.L. & Kicliter, E. (1984). A study of retinal projections in the ground squirrel, (Spermophilus tridecemlineatus) using anterograde transport techniques. Puerto Rico Health Sciences Journal 3, 97106.Google Scholar
Card, P.J. & Moore, R.Y. (1982). Ventral lateral geniculate nucleus efferents to the rat suprachiasmatic nucleus exhibit avian pancreatic polypeptide-like immunoreactivity. Journal of Comparative Neurology 206, 390396.CrossRefGoogle Scholar
Casagrande, V.A. & Harting, J.K. (1975). Transneuronal transport of tritiated proline in the visual pathways of the tree shrew (Tupaia glis). Brain Research 96, 367372.CrossRefGoogle ScholarPubMed
Crain, B.J. & Hall, W.C. (1980). The normal organization of the lateral posterior nucleus of the golden hamster. Journal of Comparative Neurology 193, 351370.CrossRefGoogle ScholarPubMed
Crognale, M. & Jacobs, G.H. (1988). Temporal properties of the short-wavelength cone mechanism: comparison of receptor and post-receptor signals in the ground squirrel. Vision Research 28, 10771082.CrossRefGoogle Scholar
Cusick, C.G. & Kaas, J.H. (1982). Retinal projections in adult and newborn grey squirrels. Developmental + Brain Research 4, 275284.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Gibson, A.R., Hansma, D.I., Houk, J.C. & Robinson, F.R. (1984). A sensitive method for visualizing the HRP reaction product using tetramethyl benzidine histochemistry. Experimental Brain Research 298, 235241.CrossRefGoogle Scholar
Gur, M. (1987). Intensity coding and luxotonic activity in the ground squirrel lateral geniculate nucleus. Vision Research 27, 20732079.CrossRefGoogle ScholarPubMed
Gur, M. & Purple, R.L. (1978). Retinal ganglion cell activity in the ground squirrel under halothane anesthesia. Vision Research 18, 114.CrossRefGoogle ScholarPubMed
Hall, W.C. & May, P.J. (1984). The anatomical basis for sensorimotor transformations in the superior colliculus. Contributions to Sensory Physiology 8, 140.CrossRefGoogle Scholar
Harrington, M.E., Nance, D.M. & Rusak, B. (1985). Neuropeptide Y immunoreactivity in the hamster geniculo-suprachiasmatic tract. Brain Research Bulletin 15, 465472.CrossRefGoogle ScholarPubMed
Harrington, M.E. & Rusak, B. (1986). Lesions of the thalamic intergeniculate leaflet alter hamster circadian rhythms. Journal of Biological Rhythms 1, 309325.CrossRefGoogle ScholarPubMed
Hickey, T.L. & Spear, P.D. (1976). Retinogeniculate projections in hooded and albino rats: an autoradiographic study. Experimental Brain Research 24, 523529.CrossRefGoogle ScholarPubMed
Holcombe, V. & Guillery, R.W. (1984). The organization of retinal maps within the dorsal and ventral lateral geniculate nuclei of the rabbit. Journal of Comparative Neurology 225, 469491.CrossRefGoogle ScholarPubMed
Hubel, D.H. (1975). An autoradiographic study of the retino-cortical projections in the tree shrew (Tupaia glis). Brain Research 96, 4150.CrossRefGoogle ScholarPubMed
Hutchins, B. & Weber, J.T. (1985). The pretectal complex of the monkey: a reinvestigation of the morphology and retinal terminations. Journal of Comparative Neurology 232, 425442.CrossRefGoogle ScholarPubMed
Jacobs, G.H., Neitz, J. & Crognale, M. (1985). Spectral sensitivity of ground squirrel cones measured with ERG flicker photometry. Journal of Comparative Physiology A 156, 503509.CrossRefGoogle Scholar
Jacobs, G. H., Fisher, S.K., Anderson, D.H. & Silverman, M.S. (1976). Scotopic and photopic vision in the California ground squirrel: physiological and anatomical evidence. Journal of Comparative Neurology 165, 209228.CrossRefGoogle ScholarPubMed
Johnson, R.F., Moore, R.Y. & Morin, L.P. (1989). Lateral geniculate lesions alter circadian activity rhythms in the hamster. Brain Research Bulletin 22, 411422.CrossRefGoogle ScholarPubMed
Johnston, J.P. & Gardener, E. (1959). Central connections of the optic nerves in mammals with pure-cone retinae. Anatomical Record 134, 205216.CrossRefGoogle ScholarPubMed
Kaas, J.H., Guillery, R.W. & Allman, J.M. (1972). Some principles of organization in the dorsal lateral geniculate nucleus. Brain, Behavior, and Evolution 6, 253299.CrossRefGoogle ScholarPubMed
Kaas, J.H., Guillery, R.W. & Allman, J.M. (1973). Discontinuities in the dorsal lateral geniculate nucleus corresponding to the optic disc: a comparative study. Journal of Comparative Neurology 147, 163180.CrossRefGoogle Scholar
Kageyama, G.H. & Wong-Riley, M.T.T. (1984). The histochemical localization of cytochrome oxidase in the retina and lateral geniculate nucleus of the ferret, cat, and monkey, with particular reference to retinal mosaics and ON/OFF center visual channels. Journal of Neuroscience 4, 24452459.CrossRefGoogle Scholar
Kageyama, G.H. & Wong-Riley, M.T.T. (1985). An analysis of the cellular localization of cytochrome oxidase in the lateral geniculate nucleus of the adult cat. Journal of Comparative Neurology 242, 338357.CrossRefGoogle ScholarPubMed
Kanaseki, T. & Sprague, J.M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 158, 319338.CrossRefGoogle ScholarPubMed
Kicliter, E. & Bruce, L.L. (1983). Ground squirrel ventral lateral geniculate receives laminated retinal projections. Brain Research 267, 340344.CrossRefGoogle ScholarPubMed
Lachica, E.A., Condo, G.J. & Casagrande, V.A. (1987). Development of cytochrome-oxidase staining in the retina and lateral genieulate nucleus: a possible correlate of ON- and OFF-center channel maturation. Developmental Brain Research 34, 298302.CrossRefGoogle Scholar
Laemle, L.K. (1968). Retinal projections of Tupaia glis. Brain, Behavior, and Evolution 1, 473499.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Lund, J.S., Remington, F.L. & Lund, R.D. (1976). Differential central distribution of optic nerve components in the rat. Brain Research 116, 83100.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. (1982). Tracing Neural Connections with Horseradish Peroxidase. New York: Wiley, 251 pp.Google Scholar
Michael, C.R. (1968). Receptive fields of single optic nerve fibers in a mammal with an all-cone retina, II: Directionally selective units. Journal of Neurophysiology 31, 257267.CrossRefGoogle Scholar
Micheal, C.R. (1972 a). Visual receptive fields of single neurons in superior colliculus of the ground squirrel. Journal of Neurophysiology 35, 815832.CrossRefGoogle Scholar
Michael, C.R. (1972 b). Functional organization of cells in the superior colliculus of the ground squirrel. Journal of Neurophysiology 35, 833846.CrossRefGoogle ScholarPubMed
Michael, C.R. (1973). Opponent-color and opponent-contrast cells in lateral geniculate nucleus of the ground squirrel. Journal of Neurophysiology 36, 536550.CrossRefGoogle Scholar
Moore, R.Y. (1973). Retinohypothalamic projection in mammals: a comparative study. Brain Research 49, 403409.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Niimi, K., Kanaseki, T. & Takimoto, T. (1963). The comparative anatomy of the ventral nucleus of the lateral geniculate body in mammals. Journal of Comparative Neurology 121, 313323.CrossRefGoogle ScholarPubMed
Paxinos, G. & Wilson, C. (1986). The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.Google Scholar
Perry, V.H. & Cowey, A. (1982). A sensitive period for ganglion cell degeneration and the formation of aberrant retino-fugal connections following tectal lesions in rats. Neuroscience 7, 583594.CrossRefGoogle ScholarPubMed
Petry, H.M., Agarwala, S. & May, J.G., III. (1989). Striped pattern of labeling in ground squirrel superior colliculus following intraocular HRP injections. Brain Research 489, 199203.CrossRefGoogle ScholarPubMed
Pickard, G.E., Ralph, M.R. & Menaker, M. (1987). The intergeniculate leaflet partially mediates effects of light on circadian rhythms. Journal of Biological Rhythms 2, 3556.CrossRefGoogle ScholarPubMed
Raisanen, J. & Dawis, S.M. (1983). A reweighting of receptor mechanisms in the ground squirrel retina: PIII and b-wave spectral sensitivity functions. Brain Research 270, 311318.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Rose, J.E. (1942). The thalamus of sheep: Cellular and fibrous structure and comparison with pig, rabbit and cat. Journal of Comparative Neurology 77, 469524.CrossRefGoogle Scholar
Sanderson, K.J. (1986). Evolution of the lateral geniculate nucleus. In Visual Neuroscience, ed. Pettigrew, J.D., Sanderson, K.J. & Levick, W.R., pp. 183195. Cambridge: Cambridge University Press.Google Scholar
Scalia, F. (1972). The termination of retinal axons in the pretectal region of mammals. Journal of Comparative Neurology 145, 223258.CrossRefGoogle ScholarPubMed
Scalia, F. & Arango, V. (1979). Topographic organization of the projection of the retina to the pretectal region in the rat. Journal of Comparative Neurology 186, 271292.CrossRefGoogle Scholar
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 1341.CrossRefGoogle ScholarPubMed
Takahashi, E.S., Hickey, T.L. & Oyster, C.W. (1977). Retinogeniculate projections in the rabbit: an autoradiographic study. Journal of Comparative Neurology 175, 112.CrossRefGoogle ScholarPubMed
Takatsuji, K. & Tohyama, M. (1989). The organization of the rat lateral geniculate body by immunohistochemical analysis of neuroactive substances. Brain Research 480, 198209.CrossRefGoogle ScholarPubMed
Tansley, K., Copenhaver, R.M. & Gunkel, R.D. (1961). Spectral sensitivity curves of diurnal squirrels. Vision Research 1, 154165.CrossRefGoogle Scholar
Terubayashi, H. & Fujisawa, H. (1988). The accessory optic system of the rabbit, cat, dog and monkey: A whole-mount study. Anatomy and Embryology 177, 285295.CrossRefGoogle Scholar
Tigges, J. (1970). Retinal projections to subcortical optic nuclei in diurnal and nocturnal squirrels. Brain, Behavior, and Evolution 3, 121134.CrossRefGoogle ScholarPubMed
Walls, G.L. (1942). The Vertebrate Eye and its Adaptive Radiation. Bloomfield Hills, Michigan: The Cranbrook Institute of Science.Google Scholar
Weber, J.T. (1985). Pretectal complex and accessory optic system of primates. Brain, Behavior, and Evolution 26, 117140.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome-oxidase histochemistry. Brain Research 7, 1128.CrossRefGoogle Scholar
Wong-Riley, M. & 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.CrossRefGoogle ScholarPubMed
Wooslsey, C.N., Carlton, T.G., Kaas, J.K. & Earls, F.J. (1971). Projections of visual field on the superior colliculus of ground squirrel (Citellus tridecemlineatus). Vision Research 11, 115127.CrossRefGoogle Scholar