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The sublaminar organization of corticogeniculate neurons in layer 6 of macaque striate cortex

Published online by Cambridge University Press:  02 June 2009

David Fitzpatrick
Affiliation:
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina
W. Martin Usrey
Affiliation:
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina
Brett R. Schofield
Affiliation:
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina
Gillian Einstein
Affiliation:
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina

Abstract

We examined the laminar distribution of corticogeniculate neurons in the macaque striate cortex labeled by axonal transport following injections of retrograde tracers into the lateral geniculate nucleus (LGN). Large injections of retrograde tracers involving all layers of the LGN resulted in a distinctive bilaminar distribution of labeled cells in cortical layer 6. One tier of labeled neurons was located along the layer 5–6 border and a second was located near the bottom of the layer, leaving the middle of layer 6 largely free of labeled neurons. Following injections of tracers that were restricted to the magnocellular layers of the LGN, almost all of the labeled neurons were located in the lower tier. In contrast, following injections of retrograde tracers confined to the parvocellular layers of the LGN, labeled cells were found in both tiers, with the greatest number in the upper tier. Thus, layer 6 of macaque striate cortex consists of three distinct sublayers only two of which are the source of descending projections to the LGN: an upper tier that projects exclusively to the parvocellular layers and a lower tier that projects to both magnocellular and parvocellular layers.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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References

Blasdel, G. & Lund, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 13891413.CrossRefGoogle ScholarPubMed
Carey, R.G., Bear, M.F. & Diamomd, I.T. (1980). The laminar organization of the reciprocal projections between the claustrum and striate cortex in the tree shrew, Tupaia glis. Brain Research 184, 193198.CrossRefGoogle ScholarPubMed
Conley, M. & Raczkowski, D. (1990). Sublaminar organization within layer VI of the striate cortex in Galago. Journal of Comparative Neurology 302, 425436.CrossRefGoogle ScholarPubMed
Deyoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219226.CrossRefGoogle ScholarPubMed
Diamond, I.T., Conley, M., Itoh, K. & Fitzpatrick, D. (1985). Laminar organization of geniculocortical projections in Galago senegal-ensis and Aotus trivirgatus. Journal of Comparative Neurology 242, 584610.CrossRefGoogle ScholarPubMed
Fitzpatrick, D. & Einstein, G. (1989). Laminar distribution and morphology of area 17 neurons projecting to the lateral geniculate nucleus in the macaque. Society for Neuroscience Abstracts 15, 1398.Google Scholar
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, 673702.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Lund, J.S. & Blasdel, G.G. (1985). Intrinsic connections of macaque striate cortex. Afferent and efferent connections of lamina 4C Journal of Neuroscience 5, 33293349.Google ScholarPubMed
Fries, W., Keizer, K. & Kuypers, H.G.J.M. (1985). Large layer VI cells in macaque striate cortex project to both superior colliculus and prestriate visual area V5. Experimental Brain Research 58, 613616.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Kelly, J.P. (1975). The projections of cells in different layers of the cat’s visual cortex. Journal of Comparative Neurology 163, 81106.CrossRefGoogle ScholarPubMed
Guillery, R.W. & Colonnier, M. (1970). Synaptic patterns in the dorsal lateral geniculate nucleus of the monkey. Zeitschrift für Zellforschung 103, 90108.CrossRefGoogle ScholarPubMed
Hadley, R.T. & Trachtenberg, M. C (1978). Poly-l-ornithine enhances the uptake of horseradish peroxidase. Brain Research 158, 114.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuro-anatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. Journal of Comparative Neurology 182, 123136.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421450.CrossRefGoogle ScholarPubMed
Itoh, K., Conley, M. & Diamond, I.T. (1982). Retinal ganglion cell projections to different layers of the lateral geniculate body in Galago crassicaudatus. Journal of Comparative Neurology 205, 282290.CrossRefGoogle ScholarPubMed
Kaas, J.H., Huerta, M.F., Weber, J.T. & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. Journal of Comparative Neurology 182, 517554.CrossRefGoogle ScholarPubMed
Katz, L.C. (1987). Local circuitry of identified projection neurons in cat visual cortex brain slices. Journal of Neuroscience 7, 12231249.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, 28152830.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, 141158.CrossRefGoogle Scholar
Levay, S. & Sherk, H. (1981). The visual claustrum of the cat. I. Structure and connections. Journal of Neuroscience 1, 956980.CrossRefGoogle ScholarPubMed
Lin, C.S. & Kaas, J.H. (1977). Projections from cortical visual areas 17, 18, and MT onto the dorsal lateral geniculate nucleus in owl monkeys. Journal of Comparative Neurology 173, 457474.CrossRefGoogle Scholar
Livingstone, M. & Hubel, D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740749.CrossRefGoogle ScholarPubMed
Lund, J.S. (1988). Anatomical organization of macaque monkey striate visual cortex. Annual Review of Neuroscience 11, 253288.CrossRefGoogle ScholarPubMed
Lund, J.S. & Boothe, R. (1975). Interlaminar connections and pyramidal neuron organization in the visual cortex, area 17, of the macaque monkey. Journal of Comparative Neurology 159, 305334.CrossRefGoogle Scholar
Lund, J.S., Lund, R.D., Hendrickson, A.E., Bunt, A.H. & Fuchs, A.F. (1975). The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey. Journal of Comparative Neurology 164, 287304.CrossRefGoogle ScholarPubMed
Martin, K.A.C. & Whitteridge, D. (1984). Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. Journal of Physiology 353, 463504.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Van Essen, D.C. (1983). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 25632586.CrossRefGoogle ScholarPubMed
Merigan, W.H. & Maunsell, J.H.R. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience 16, 369402.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. (1977). Differential sensitivity between blue and brown reaction products of HRP neurohistochemistry. Neuroscience Letters 5, 714.CrossRefGoogle Scholar
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in the lateral geniculate nucleus of bush-baby (Galago crassicaudatus). Journal of Neurophysiology 47, 715741.CrossRefGoogle ScholarPubMed
Symonds, L.L. & Kaas, J.H. (1978). Connections of striate cortex in the prosimian Galago senegalensis. Journal of Comparative Neurology 181, 477512.CrossRefGoogle ScholarPubMed
Usrey, W.M. & Fttzpatrick, D. (1992). Intrinsic and extrinsic projections of neurons in layer VI of striate cortex: Anatomical evidence for selective influence on parallel geniculocortical pathways. Society for Neuroscience Abstracts 18, 297.Google Scholar
Usrey, W.M. & Fttzpatrick, D. (1993 a). The sublaminar organization of layer VI projections to layer IV in tree shrew striate cortex. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1175.Google Scholar
Usrey, W.M. & Fttzpatrick, D. (1993 b). Parallel streams in the corticogeniculate pathway: Intrinsic and extrinsic projections of neurons in layer VI of striate cortex. In Thalamic Networks for Relay and Modulation, ed. Minciacchi, D., Molinari, M., Macchi, G. & Jones, E.G.New York: Pergamon Press (in press).Google 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, 135145.CrossRefGoogle ScholarPubMed
Wilson, J.R. & Hendrickson, A.E. (1981). Neuronal and synaptic structure of the dorsal lateral geniculate nucleus in normal and monocularly deprived Macaca monkeys. Journal of Comparative Neurology 197, 517539.CrossRefGoogle ScholarPubMed