Hostname: page-component-745bb68f8f-cphqk Total loading time: 0 Render date: 2025-02-03T03:39:30.809Z Has data issue: false hasContentIssue false
  • English
  • Français

The distribution and morphology of LGN K pathway axons within the layers and CO blobs of owl monkey V1

Published online by Cambridge University Press:  02 June 2009

Y. Ding  and
V.A. Casagrande
Y. Ding
Affiliation:
Department of Cell Biology, Vanderbilt University, Nashville
V.A. Casagrande
Affiliation:
Department of Cell Biology, Vanderbilt University, Nashville Department of Psychology, Vanderbilt University, Nashville
Get access Rights & Permissions [Opens in a new window]

Abstract

The lateral geniculate nucleus (LGN) of primates contains three classes of relay cells, the magnocellular (M), parvocellular (P), and koniocellular (K) cells. At present, very little is known about either the structure or function of the K relay cells in New or Old World monkeys (simian primates). In monkeys, K cells are located between the main LGN layers and adjacent to the optic tract. For convenience, these intercalated cell layers are numbered K1-K4 starting closest to the optic tract with K1. The objective of this study was to examine the details of K axon morphology in the primary visual cortex (V1) of owl monkeys and to determine if different K layers give rise to distinct axon types. For this purpose, injections of WGA-HRP or PHA-L were made into specific K LGN layers and the distribution and morphology of the resulting labeled axons were analyzed. Injections of fluorescent tracers also were made within the superficial layers of V1 to further document connections via analysis of the patterns of retrogradely labeled cells in the LGN. Our main finding is that K axons in owl monkeys terminate as delicate focused arbors within single cytochrome oxidase (CO) blob columns in cortical layer III and within cortical layer I. Overall, the morphology of the K axons in these monkeys is quite similar to what we described previously for K geniculocortical axons in the distantly related bush baby (prosimian primate), suggesting that the basic features of this pathway are common to all primates. Our results also provide evidence that the axon arbors from different K layers are morphologically distinct; axons from LGN layer K1 project mainly to cortical layer I, while axons from LGN layer K3 chiefly terminate in cortical layer III. Taken together, these results imply that the basic features of axons within the K pathway are conserved across primates, and that the K axons from different K layers are likely to differ in function based upon their different morphologies.

Keywords

Striate cortexParallel pathwaysPHA-LPrimateVision
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 4 , July 1997 , pp. 691 - 704
Copyright
Copyright © Cambridge University Press 1997

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

Allman, J.M. & Kaas, J.H. (1971). Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). Brain Research 35, 89–106.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Yoshida, K. (1981). The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. Journal of Comparative Neurology 203, 455–474.CrossRefGoogle ScholarPubMed
Boyd, J.D., Mavity-Hudson, J.A. & Casagrande, V.A. (1997). Projection of layer IV to layer III in striate cortex of owl monkey (in preparation).Google Scholar
Brodmann, K. (1909). Vergleichende Lokalisationlehre der Grosshimrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. J.A. Barth, Leipzig.Google Scholar
Bullier, J. & Kennedy, H. (1983). Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Experimental Brain Research 53, 168–172.CrossRefGoogle ScholarPubMed
Campos-Ortega, J.A. & Hayhow, W.A. (1970). A new lamination pattern in the lateral geniculate nucleus of primates. Brain Research 20, 335–339.CrossRefGoogle ScholarPubMed
Casagrande, V.A. (1994). A third parallel visual pathway to primate area VI. (Review). Trends in Neuroscience 17, 305–310.CrossRefGoogle Scholar
Casagrande, V.A. & DeBruyn, E.J. (1982). The galago visual system: Aspects of normal organization and developmental plasticity. In The Lesser Bush Baby (Galago) An Animal Model: Selected Topics, ed. Haines, D.E., pp! 138–162. Boca Raton, Florida: CRC Press.Google Scholar
Casagrande, V.A. & Kaas, J.H. (1994). The afferent, intrinsic, and efferent connections of primary visual cortex. In Cerebral Cortex, Vol. 10, Primary Visual Cortex of Primates, ed. Peters, A. & Rockland, K., pp. 201–259. New York: Plenum Press.CrossRefGoogle Scholar
Chacko, L.W. (1955). The lateral geniculate body in gibbon (Hylobates hoolock). Journal of the Anatomical Society of India 4, 69–81.Google Scholar
Conley, M. & Fitzpatrick, D. (1989). Morphology of retinogeniculate axons in the macaque. Visual Neuroscience 2, 287–296.CrossRefGoogle ScholarPubMed
Diamond, I.T., Conley, M., Itoh, K. & Fitzpatrick, D. (1985). Laminar organization of geniculocortical projections in Galago senegalensis and Aotus trivirgatus. Journal of Comparative Neurology 242, 584–610.CrossRefGoogle ScholarPubMed
Diamond, I.T., Fitzpatrick, D. & Schmechel, D. (1993). Calcium binding proteins distinguish large and small cells of the ventral posterior and lateral geniculate nuclei of the prosimian galago and the tree shrew (Tupaia balangeri). Proceedings of the National Academy of Sciences of the U.S.A. 90, 1425–1429.CrossRefGoogle Scholar
Feig, S. & Harting, J.K. (1994). Ultrastructural studies of the primate lateral geniculate nucleus: Morphology and spatial relationships of axon terminals arising from the retina, visual cortex (area 17), superior colliculus, parabigeminal nucleus, and pretectum of Galago crassicaudatus. Journal of Comparative Neurology 343, 17–34.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Itoh, K. & Diamond, I.T. (1983). The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). Journal of Neuroscience 3, 673–702.CrossRefGoogle ScholarPubMed
Gibson, A.R., Hansma, D.I., Houk, J.C. & Robinson, F.R. (1984). A sensitive low artifact TMB procedure of the demonstration of WGAHRP in the CNS. Brain Research 298, 235–241.CrossRefGoogle ScholarPubMed
Giolli, R.A. & Tigges, J. (1970). The primary optic pathways and nuclei in primates. In Advances in Primatology, Vol. 1, ed. Noback, C.R. & Montagna, W., pp. 29–54. New York: Appleton-Century-Crofts.Google Scholar
Harting, J.K., Huerta, M.F., Hashikawa, T. & van Lieshout, D.P. (1991 a). Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: Organization of tectogeniculate pathways in nineteen species. (Review). Journal of Comparative Neurology 304, 275–306.CrossRefGoogle Scholar
Harting, J.K., Van Lieshout, D.P., Hashikawa, T. & Weber, J.T. (1991 b). The parabigeminogeniculate projection: Connectional studies in eight mammals. Journal of Comparative Neurology 305, 559–581.CrossRefGoogle ScholarPubMed
Hässler, R. (1967). Comparative anatomy of central visual systems in day- and night-active primates. In Evolution of the Forebrain, ed. Hässler, R. & Stephan, H., pp. 419–434. New York: Plenum Press.Google Scholar
Hendry, S.H.C. (1995). A neurochemically distinct pathway. In Thalamic Networks for Relay and Modulation, ed. Minciacchi, M., Molinari, M., Macchi, G. & Jones, E.G., pp. 251–267. New York: Pergamon Press.Google Scholar
Hendry, S.H.C. & Casagrande, V.A. (1996). A common pattern for a third visual channel in the primate LGN. Society for Neuroscience Abstracts 22, 1605.Google Scholar
Hendry, S.H. & Yoshioka, T. (1994). A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264, 575–577.CrossRefGoogle ScholarPubMed
Hernandez-Gonzalez, A., Cavada, C. & Reinoso-Suarez, F. (1994). The lateral geniculate nucleus projects to the inferior temporal cortex in the macaque monkey. Neuroreport 5, 2993–2996.CrossRefGoogle Scholar
Irvin, G.E., Norton, T.T., Sesma, M.A. & Casagrande, V.A. (1986). W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Research 362, 254–270.CrossRefGoogle ScholarPubMed
Itoh, K., Conley, M. & Diamond, I.T. (1982). Retinal ganglion cell projections to individual layers of the lateral geniculate body in Galago crassicaudatus. Journal of Comparative Neurology 205, 282–290.CrossRefGoogle ScholarPubMed
Johnson, J.K. & Casagrande, V.A. (1993). Calcium-binding protein expression correlates with primate visual parallel pathways. Society for Neuroscience Abstracts 19, 425.Google Scholar
Johnson, J.K. & Casagrande, V.A. (1995). Distribution of calciumbinding proteins within the parallel visual pathways of a primate (Galago crassicaudatus). Journal of Comparative Neurology 356, 238–260.CrossRefGoogle ScholarPubMed
Jones, E.G. & Hendry, S.H.C. (1989). Differential calcium-binding protein immunoreactivity distinguishes classes of relay neurons in the monkey thalamic nuclei. European Journal of Neuroscience 1, 222–246.CrossRefGoogle ScholarPubMed
Kaas, J.H., Lin, C.S. & Casagrande, V.A. (1976). The relay of ipsilateral and contralateral retinal input from the lateral geniculate nucleus to striate cortex in the owl monkey: A transneuronal transport study. Brain Research 106, 371–378.CrossRefGoogle ScholarPubMed
Kaas, J.H. & Morel, A. (1993). Connections of visual areas of the upper temporal lobe of owl monkeys: The MT crescent and dorsal and ventral subdivisions of FST. Journal of Neuroscience 13, 534–546.CrossRefGoogle Scholar
Kaas, J.H., Huerta, M.F., Weber, J.J., & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. Journal of Comparative Neurology 182, 517–554.CrossRefGoogle ScholarPubMed
Kennedy, H. & Bullier, J. (1985). A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey. Journal of Neuroscience 5, 2815–2830.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1989). Cortical integration of parallel pathways in the visual system of primates. Brain Research 478, 161–165.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1990). Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns. (Review). Visual Neuroscience 5, 165–204.CrossRefGoogle Scholar
Krubitzer, L.A. & Kaas, J.H. (1993). The dorsomedial visual area of owl monkeys: Connections, myeloarchitecture, and homologies in other primates. Journal of Comparative Neurology 334, 497–528.CrossRefGoogle ScholarPubMed
Lachica, E.A. & Casagrande, V.A. (1992). Direct W-like geniculate projections to the cytochrome oxidase (CO) blobs in primate visual cortex: Axon morphology. Journal of Comparative Neurology 319, 141–158.CrossRefGoogle Scholar
Lachica, E.A. & Casagrande, V.A. (1993). The morphology of collicular and retinal axons ending on small relay (W-like) cells of the primate lateral geniculate nucleus. Visual Neuroscience 10, 403–418.CrossRefGoogle ScholarPubMed
Lal, R. & Friedlander, M.J. (1990). Effect of passive eye movement on retinogeniculate transmission in the cat. Journal of Neurophysiology 63, 523–38.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in the Old World monkey: Morphology and central projections. Science 213, 1139–1142.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 79, 6098–6101.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740–749.CrossRefGoogle ScholarPubMed
Lund, J.S. (1988). Anatomical organization of macaque monkey striate visual cortex. (Review). Annual Review of Neuroscience 11, 253–288.CrossRefGoogle Scholar
Lysakowski, A., Standage, G.P. & Benevento, L.A. (1988). An investigation of collateral projections of the dorsal lateral geniculate nucleus and other subcortical structures to cortical areas V1 and V4 in the macaque monkey: A double label retrograde tracer study. Experimental Brain Research 69, 651–661.CrossRefGoogle ScholarPubMed
Merigan, W.H. & Maunsell, J.H. (1993). How parallel are the primate visual pathways? (Review). Annual Review of Neuroscience 16, 369–402.CrossRefGoogle Scholar
Newsome, W.T. & Pare, E.B. (1988). A selective impairment of motion perception following lesions of the middle temporal visual area (MT). Journal of Neuroscience 8, 2201–2211.CrossRefGoogle ScholarPubMed
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in lateral geniculate nucleus of bush baby (Galago crassicaudatus). Journal of Neurophysiology 47, 715–741.CrossRefGoogle ScholarPubMed
Norton, T.T., Casagrande, V.A., Irvin, G.E., Sesma, M.A. & Petry, H.M. (1988). Contrast-sensitivity functions of W-, X-, and Y-like relay cells in the lateral geniculate nucleus of bush baby, Galago crassicaudatus. Journal of Neurophysiology 59, 1639–1656.CrossRefGoogle Scholar
Perry, V.H. & Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12, 1125–1137.CrossRefGoogle Scholar
Sawchenko, P.E., Cunningham, E.T. Jr., Mortrud, M.T., Pfeiffer, S.W. & Gerfen, C.R. (1990). Phaseolus vulgaris leucoagglutinin anterograde axonal transport technique. In Methods in Neuroscience, Vol. 3, ed. Conn, M., pp. 247–260. San Diego, California: Academic Press.Google Scholar
Stone, J. (1983). Parallel Processing in the Visual System: The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision. New York: Plenum Press.CrossRefGoogle Scholar
Vogt, B.A. (1991). The role of layer I in cortical function. In Cerebral Cortex: Normal and Altered States of Function, Vol. 9, ed. Peters, A. & Jones, E.G., pp. 49–80. New York and London: Plenum Press.CrossRefGoogle Scholar
Weber, J.T., Huerta, M.F., Kaas, J.H. & Harting, J.K. (1983). The projections of the lateral geniculate nucleus of the squirrel monkey: Studies of the interlaminar zones and the S layers. Journal of Comparative Neurology 213, 135–145.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T. (1979). Projections from the dorsal lateral geniculate nucleus to prestriate cortex in the squirrel monkey as demonstrated by retrograde transport of horseradish peroxidase. Brain Research 109, 595–600.CrossRefGoogle Scholar
Wurtz, R.H. & Goldberg, M.E. (1972). Activity of superior colliculus in behaving monkey. IV. Effects of lesions on eye movements. Journal of Neurophysiology 35, 587–596.CrossRefGoogle ScholarPubMed
Xue, J.T., Kim, C.B., Moore, R.J. & Spear, P.D. (1994). Influence of the superior colliculus on responses of lateral geniculate neurons in the cat. Visual Neuroscience 11, 1059–1076.CrossRefGoogle ScholarPubMed