Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-19T10:24:30.315Z Has data issue: false hasContentIssue false
  • English
  • Français

Age dependent modification of cytochrome oxidase activity in the cat dorsal lateral geniculate nucleus following removal of primary visual cortex

Published online by Cambridge University Press:  02 June 2009

Bertram R. Payne  and
Stephen G. Lomber
Bertram R. Payne
Affiliation:
Laboratory for Visual Perception and Cognition, Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston
Stephen G. Lomber
Affiliation:
Laboratory for Visual Perception and Cognition, Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston
Get access Rights & Permissions [Opens in a new window]

Abstract

The purpose of the present study was to assess changes in the levels of cytochrome oxidase (CO) activity in the dorsal lateral geniculate nucleus (dLGN) of the adult cat following removal of primary visual cortical areas 17 and 18 on the day of birth (P1), P28, or in adulthood (≫6 months). Cytochrome oxidase activity was measured in histological sections 9 or more months after the cortical ablation. Control measures obtained from intact cats show that CO activity is normally highest in the A-laminae of dLGN, and slightly lower in the C-complex. Following visual cortex ablations incurred at any age, CO activity levels are reduced in the A-laminae. This reduction is most profound following ablations incurred on P28 or in adulthood. In contrast, CO activity in the C-complex of dLGN is at nearly normal levels following ablations on P1 or P28, but not in adulthood. These findings contribute to our understanding of the role played by the dLGN in the transfer of visual signals along retino-geniculo-extrastriate pathways that expand following early removal of areas 17 and 18. Moreover, they have implications for our understanding of spared behavioral functions attributed to the extrastriate cortex in cats which incurred early damage of areas 17 and 18.

Keywords

Areas 17 and 18NeonatalExtrastriate cortexThalamusBrain damage
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 5 , September 1996 , pp. 805 - 816
Copyright
Copyright © Cambridge University Press 1996

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

Blakemore, C. & Zumbroich, T.J. (1987). Stimulus selectivity and functional organization in the lateral suprasylvian visual cortex of the cat. Journal of Physiology (London) 389, 569–603.CrossRefGoogle ScholarPubMed
Bowling, D. & Michael, C.R. (1984). Terminal patterns of single physiologically characterized optic tract fibers in the cat's lateral geniculate nucleus. Journal of Neuroscience 4, 198–216.CrossRefGoogle ScholarPubMed
Callahan, E.C., Tong, L. & Spear, P.D. (1984). Critical period for the loss of retinal X-cells following visual cortex damage in cats. Brain Research 323, 302–306.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Levick, W.R. (1974 a). Brisk and sluggish concentrically organized ganglion cells in the cat's retina. Journal of Physiology (London) 240, 421–456.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Levick, W.R. (1974 b). Properties of rarely encountered types of ganglion cells in the cat's retina and an overall classification. Journal of Physiology (London) 240, 457–492CrossRefGoogle Scholar
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 (London) 217, 473–496.CrossRefGoogle ScholarPubMed
Cleland, B.C., Morstyn, R., Wagner, H. & Levick, W.R. (1975). Long latency input to lateral geniculate neurones of the cat. Brain Research 91, 306–310.CrossRefGoogle ScholarPubMed
Cornwell, P. & Payne, B.R. (1989). Visual discrimination by cats with adult or one- or two-stage neonatal lesions of visual cortex. Behavioral Neuroscience 103, 1191–1199.CrossRefGoogle ScholarPubMed
Cornwell, P., Herbein, S., Corso, C., Eskew, R., Warren, J.M. & Payne, B.R. (1989). Selective sparing after lesions of visual cortex in newborn cats. Behavioral Neuroscience 103, 1176–1190.CrossRefGoogle Scholar
Cornwell, P., Overman, W.H. & Ross, C. (1978). Extent of recovery from neonatal damage to the cortical visual system in cats. Journal of Comparative and Physiological Psychology 90, 986–995.CrossRefGoogle Scholar
Friedlander, M.J. & Sherman, S.M. (1981). Morphology of physiologically identified neurons. Trends in Neuroscience 4, 211–214.CrossRefGoogle Scholar
Friedlander, M.J., Lin, C.-S., Stanford, L.R. & Sherman, S.M. (1981). Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. Journal of Neurophysiology 46, 80–129.CrossRefGoogle ScholarPubMed
Fukuda, Y., Hsiao, C.-F., Watanabe, M. & Ito, H. (1984). Morphological correlates of physiologically identified Y-, X- and W-cells in cat retina. Journal of Neurophysiology 52, 999–1013.CrossRefGoogle Scholar
Gizzi, M.S., Katz, E., Schumer, R.A. & Movshon, J.A. (1990). Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex. Journal of Neurophysiology 83, 1529–1543.CrossRefGoogle Scholar
Graham, J. (1977). An autoradiographic study of the efferent connections of the superior colliculus in the cat. Journal of Comparative Neurology 173, 629–654.CrossRefGoogle ScholarPubMed
Guido, W., Spear, P.D. & Tong, L. (1990). Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens. Experimental Brain Research 83, 219–224.CrossRefGoogle ScholarPubMed
Guido, W., Spear, P.D. & Tong, L. (1992). How complete is physiological compensation in extrastriate cortex after visual cortex damage in kittens? Experimental Brain Research 91, 455–466.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1966). A study of Golgi preparations from the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 128, 21–50.CrossRefGoogle Scholar
Guillery, R.W., Geisert, E.E., Polley, E.H. & Mason, C.A. (1980). An analysis of the retinal afferents to the cat's medial interlaminar nucleus and to its rostral extension the “geniculate wing”. Journal of Comparative Neurology 194, 117–142.CrossRefGoogle Scholar
Kageyama, G.H. & Wong-Riley, M. (1985). An analysis of the cellular localization of cytochrome oxidase in the lateral geniculate nucleus of the adult cat. Journal of Comparative Neurology 242, 338–357.CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Wong-Riley, M. (1986). The localization of cytochrome oxidase in the LGN and striate cortex of postnatal kittens. Journal of Comparative Neurology 243, 182–194.CrossRefGoogle ScholarPubMed
Kalil, R.E., Tong, L.L. & Spear, P.D. (1991). Thalamic projections to the lateral suprasylvian visual area in cats with neonatal or adult visual cortex damage. Journal of Comparative Neurology 314, 512–525.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1985). Central projections of cat retinal ganglion cells. Journal of Comparative Neurology 237, 216–226.CrossRefGoogle ScholarPubMed
Lomber, S.G., MacNeil, M.A. & Payne, B.R. (1995). Amplification of thalamic projections to middle suprasylvian cortex following ablation of immature primary visual cortex in the cat. Cerebral Cortex 5, 166–191.CrossRefGoogle ScholarPubMed
Lomber, S.G., Payne, B.R., Cornwell, P. & Pearson, H.E. (1993). Capacity of the retinogeniculate pathway to reorganize following ablation of visual cortical areas in developing and mature cats. Journal of Comparative Neurology 338, 432–457.CrossRefGoogle ScholarPubMed
MacNeil, M.A., Einstein, G.E. & Payne, B.R. (1997). Transgeniculate signal transmission to middle suprasylvian extrastriate cortex in intact cats and following early removal of areas 17 and 18: A morphological approach. Experimental Brain Research (submitted for publication).CrossRefGoogle Scholar
Mendola, J.D. & Payne, B.R. (1993). Direction selectivity and physiological compensation in the superior colliculus following removal of areas 17 and 18. Visual Neuroscience 10, 1019–1026.CrossRefGoogle Scholar
Otsuka, R. & Hassler, R. (1962). Uber Aufbau und Gliederung der corticalen Sehsphare bei der Katze. Archives für Psychialrie & Zeitsschrift fur gesammelte Neurologie 203, 212–234.CrossRefGoogle Scholar
Payne, B.R. (1990). The representation of the ipsilateral visual field in the transition zone between areas 17 and 18 of the cat's cerebral cortex. Visual Neuroscience 4, 445–474.CrossRefGoogle ScholarPubMed
Payne, B.R. & Cornwell, P. (1994). System-wide repercussions of immature visual cortex damage. Trends in Neuroscience 17, 126–130.CrossRefGoogle Scholar
Payne, B.R. & Peters, A. (1989). Cytochrome oxidase patches and Meynert cells in monkey visual cortex. Neuroscience 28, 353–363.CrossRefGoogle ScholarPubMed
Payne, B.R., Pearson, H.E. & Cornwell, P. (1984). Transneuronal degeneration of beta retinal ganglion cells in the cat. Proceedings of the Royal Society B (London) 222, 15–32.Google ScholarPubMed
Payne, B.R., Connors, C. & Cornwell, P. (1991). Survival and death of neurons in cortical area PMLS after removal of areas 17, 18 & 19 from cats & kittens. Cerebral Cortex 1, 469–491.CrossRefGoogle Scholar
Payne, B.R., Pearson, H.E. & Cornwell, P. (1992). Survival and death of retinal ganglion cells in the cat. Investigative Ophthalmology 33, 1132.Google Scholar
Payne, B.R., Lomber, S.G., Geeraerts, S., Van Der Gucht, E. & Van-Denbussche, E. (1996 a). Reversible visual hemineglect. Proceedings of the National Academy of Sciences of the U.S.A. 93, 290–294.CrossRefGoogle ScholarPubMed
Payne, B.R., Lomber, S.G., MacNeil, M.A. & Cornwell, P. (1996 b). Evidence for greater sight in blindsight following damage of primary visual cortex early in life. Neuropsychologia 34, 741–744.CrossRefGoogle ScholarPubMed
Pearson, H.E., Labar, D.R., Payne, B.R., Cornwell, P. & Aggarwal, N. (1981). Transneuronal retrograde degeneration in the cat retina following neonatal ablation of the visual cortex. Brain Research 212, 470–475.CrossRefGoogle ScholarPubMed
Price, D.J. (1985). Patterns of cytochrome oxidase activity in areas 17, 18 & 19 of the visual cortex of cats and kittens. Experimental Brain Research 58, 125–133.CrossRefGoogle Scholar
Rauscheker, J.P., Von Grunau, M.W. & Poulin, C. (1987). Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to flow field processing. Journal of Neuroscience 7, 943–958.CrossRefGoogle Scholar
Rosenquist, A.C. (1985). Connections of visual cortical areas in the cat. In Cerebral Cortex, Vol. 3, Visual Cortex, ed. Peters, A. & Jones, E.G., pp. 81–117. New York: Plenum Press.Google Scholar
Saito, H.-A. (1983). Morphology of physiologically identified X-, Y- & W-type retinal ganglion cells of the cat. Journal of Comparative Neurology 221, 279–288.CrossRefGoogle Scholar
Sanderson, K.J. (1971). The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. Journal of Comparative Neurology 143, 101–118.CrossRefGoogle Scholar
Sanides, F. & Hoffmann, J. (1969). Cyto- and myeloarchitecture of the visual cortex of the cat and the surrounding integration cortices. Journal fur Hirnforschung 1, 79–104.Google Scholar
Sherman, S.M. (1977). The effect of superior colliculus lesions upon the visual fields of cats with cortical lesions. Journal of Comparative Neurology 172, 211–230.CrossRefGoogle Scholar
Sherman, S.M. (1985). Functional organization of the W-, X- and Y-cell pathways in the cat: a review and hypothesis. In Progress in Psychobiology and Physiological Psychology, Vol. 11, ed. Sprague, J.M. & Epstein, A.N., pp. 233–314. New York: Academic Press.Google Scholar
Shupert, C., Cornwell, P. & Payne, B.R. (1993). Differential sparing of depth perception, orienting and optokinetic nystagmus after neonatal versus adult lesions of cortical areas 17, 18 & 19 in the cat. Behavioral Neuroscience 107, 633–650.CrossRefGoogle Scholar
Spear, P.D. & Baumann, T.P. (1975). Receptive field characteristics of single neurons in the lateral suprasylvian visual area of the cat. Journal of Neurophysiology 38, 1404–1420.CrossRefGoogle ScholarPubMed
Spear, P.D. & Baumann, T.P. (1979). Effects of visual cortex removal on the receptive field properties of neurons in lateral suprasylvian visual area of the cat. Journal of Neurophysiology 42, 31–56.CrossRefGoogle ScholarPubMed
Spear, P.D., Kalil, R.E. & Tong, L. (1980). Functional compensation in lateral suprasylvian visual area following neonatal visual cortex removal in cats. Journal of Neurophysiology 43, 851–869.CrossRefGoogle ScholarPubMed
Sprague, J.M. & Meikle, T.H. (1965). The role of the superior colliculus in visually guided behavior. Experimental Neurology 11, 115–146.CrossRefGoogle ScholarPubMed
Stanford, L.R. (1987). W-cells in the cat retina: Correlated morphological and physiological evidence for two distinct classes. Journal of Neurophysiology 57, 218–243.CrossRefGoogle ScholarPubMed
Stanford, L.R., Friedlander, M.J. & Sherman, S.M. (1981). Morphology of physiologically identified W-cells in the C laminae of the cat's lateral geniculate nucleus. Journal of Neuroscience 1, 578–584.CrossRefGoogle Scholar
Stanford, L.R., Friedlander, M.J. & Sherman, S.M. (1983). Morphological & physiological properties of geniculate W-cells of the cat: A comparison with X- & Y-cells. Journal of Neurophysiology 50, 582–608.CrossRefGoogle Scholar
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, 722–748.CrossRefGoogle ScholarPubMed
Sun, J.-S., Lomber, S.G. & Payne, B.R. (1994). Expansion of suprasylvian cortex projections into the superficial layers of the superior colliculus following damage of areas 17 and 18 in developing cats. Visual Neuroscience 11, 13–22.CrossRefGoogle ScholarPubMed
Sur, M., Esguerra, M., Garraghty, P.E., Kritzer, M.F. & Sherman, S.M. (1987). Morphology of physiologically identified retinogenic-ulate X- & Y-axons in the cat. Journal of Neurophysiology 58, 1–31.CrossRefGoogle ScholarPubMed
Tong, L., Kalil, R.E. & Spear, P.D. (1984). Critical periods for functional and anatomical compensation in the lateral suprasylvian visual area following removal of visual cortex in cats. Journal of Neurophysiology 52, 941–960.CrossRefGoogle ScholarPubMed
Tong, L., Spear, P.D., Kalil, R.E. & Callahan, E.C. (1982). Loss of retinal X-cells in cats with neonatal or adult visual cortex damage. Science 111, 72–75.CrossRefGoogle Scholar
Tumosa, N., McCall, M.A., Guido, W. & Spear, P.D. (1989). Responses of lateral geniculate neurons that survive long-term visual cortex damage in kittens and adult cats. Journal of Neuroscience 9, 280–298.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213–236.CrossRefGoogle ScholarPubMed
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of areas 18 & 19 in the cat. Journal of Comparative Neurology 185, 657–678.CrossRefGoogle Scholar
Von Grunau, M. & Frost, B.J. (1983). Double opponent process mechanism underlying RF-structure of directionally specific cells in cat lateral suprasylvian visual area. Experimental Brain Research 49, 84–92.CrossRefGoogle ScholarPubMed
Von Grunau, M.W., Zumbroich, T.J. & Poulin, C. (1987). Visual receptive field properties in the posterior suprasylvian cortex of the cat: A comparison between the areas PMLS & PLLS. Vision Research 27, 343–356.CrossRefGoogle Scholar
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neuroscience 12, 94–101.CrossRefGoogle ScholarPubMed
Zumbroich, T.J. & Blakemore, C. (1987). Spatial and temporal selectivity in the suprasylvian visual cortex of the cat. Journal of Neuroscience 7, 482–500.CrossRefGoogle ScholarPubMed