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Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: Anatomy of interlaminar projections

Published online by Cambridge University Press:  02 June 2009

Takashi Yoshioka ,
Jonathan B. Levitt  and
Jennifer S. Lund
Takashi Yoshioka
Affiliation:
Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore
Jonathan B. Levitt
Affiliation:
Department of Visual Science, Institute of Ophthalmology, University of London, Bath St., London EC1V 9EL, England
Jennifer S. Lund
Affiliation:
Department of Visual Science, Institute of Ophthalmology, University of London, Bath St., London EC1V 9EL, England
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Abstract

An important issue in understanding the function of primary visual cortex in the macaque monkey is how the several efferent neuron groups projecting to extrastriate cortex acquire their different response properties. To assist our understanding of this issue, we have compared the anatomical distribution of VI intrinsic relays that carry information derived from magno- (M) and parvocellular (P) divisions of the dorsal lateral geniculate nucleus between thalamic recipient neurons and interareal efferent neuron groups within area VI. We used small, iontophoretic injections of biocytin placed in individual cortical laminae of area VI to trace orthograde and retrograde inter- and intralaminar projections. In either the same or adjacent sections, the tissue was reacted for cytochrome oxidase (CO), which provides important landmarks for different efferent neuron populations located in CO rich blobs and CO poor interblobs in laminae ⅔, as well as defining clear boundaries for the populations of efferent neurons in laminae 4A and 4B. This study shows that the interblobs, but not the blobs, receive direct input from thalamic recipient 4C neurons; the interblobs receive relays from mid 4C neurons (believed to receive convergent M and P inputs), while blobs receive indirect inputs from either M or P (or both) pathways through layers 4B (which receives M relays from layer 4Cα) and 4A (which receives P relays directly from the thalamus as well as from layer 4Cβ). The property of orientation selectivity, most prominent in the interblob regions and in layer 4B, may have a common origin from oriented lateral projections made by mid 4C spiny stellate neurons. While layer 4B efferents may emphasize M characteristics and layer 4A efferents emphasize P characteristics, the dendrites of their constituent pyramidal neurons may provide anatomical access to the other channel since both blob and interblob regions in layers ⅔ have anatomical access to M and P driven relays, despite functional differences in the way these properties may be expressed in the two compartments.

Keywords

Parallel pathwaysArea VIVisionBiocytinCytochrome oxidase
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 3 , May 1994 , pp. 467 - 489
Copyright
Copyright © Cambridge University Press 1994

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References

Blasdel, G.G. & Lund, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 1389–1413.CrossRefGoogle ScholarPubMed
Blasdel, G.G. & Fitzpatrick, D. (1984). Physiological organization of layer 4 in macaque striate cortex. Journal of Neuroscience 4, 880–895.CrossRefGoogle ScholarPubMed
Blasdel, G.G., Lund, J.S. & Fitzpatrick, D. (1985). Intrinsic connections of macaque striate cortex: Axonal projections of cells outside lamina 4C. Journal of Neuroscience 5, 3350–3369.Google Scholar
De Monasterio, F.M. (1978). Properties of concentrically organized X and Y ganglion cells of macaque retina. Journal of Neurophysiology 41, 1394–1417.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.Google Scholar
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, 3329–3349.Google Scholar
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, 123–136.Google 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, 421–450.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1977). Functional architecture of macaque monkey visual cortex. Proceedings of the Royal Society B (London) 198, 1–59.Google ScholarPubMed
Hübener, M. & Bolz, J. (1992). Relationships between dendritic morphology and cytochrome oxidase compartments in monkey striate cortex. Journal of Comparative Neurology 324, 67–80.CrossRefGoogle ScholarPubMed
Lachica, E.A., Mavity-Hudson, J. & Casagrande, V.A. (1991). Morphological details of primate axons and dendrites revealed by extracellular injection of biocytin: An economic and reliable alternative to PHA-L. Brain Research 564, 1–11.Google Scholar
Lachica, E.A., Beck, P. & Casagrande, V.A. (1992). Parallel pathways in macaque monkey striate cortex: Anatomically defined columns in layer 111. Proceedings of the National Academy of Science of the U.S.A. 89, 3566–3570.Google Scholar
Lennie, P., Krauskopf, J. & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. Journal of Neuroscience 10, 649–669.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.Google Scholar
Levitt, J.B., Yoshioka, T. & Lund, J.S. (1994). Intrinsic cortical connections in macaque visual area V2: Evidence for interaction between different functional streams. Journal of Comparative Neurology (in press).CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1982). Thalamic inputs to cyto- chrome oxidase-rich regions in monkey visual cortex. Proceedings of the National Academy of Science of the U.S.A. 79, 6098–6101.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1983). Specificity of cortico-cortical connections in monkey visual system. Nature 304, 531–534.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984 a). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984 b). Specificity of intrinsic connections in primate primary visual cortex. Journal of Neuroscience 4, 2830–2835.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1987 a). Connections between layer 4B of area 17 and the thick cytochrome oxidase stripes of area 18 in the squirrel monkey. Journal of Neuroscience 7, 3371–3377.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1987 b). Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. Journal of Neuroscience 7, 3416–3468.CrossRefGoogle ScholarPubMed
Lund, J.S. (1973). Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatto). Journal of Comparative Neurology 147, 455–496.Google Scholar
Lund, J.S. (1987). Local circuit neurons of macaque monkey striate cortex: I. Neurons of laminae 4C and 5A. Journal of Comparative Neurology 257, 60–92.Google Scholar
Lund, J.S. (1990). Excitatory and inhibitory circuitry and laminar mapping strategies in the primary visual cortex of the monkey. In Signal and Sense. Local and Global Order in Perceptual Maps, ed. Edelman, G.M., Gall, W.E. & Cowan, W.M., pp. 51–66. New York: John Wiley & Sons.Google Scholar
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, 305–334.Google Scholar
Lund, J.S., Hendrickson, A.E., Ogren, M.P. & Tobin, E.A. (1981). Anatomical organization of primate visual cortex, area VII. Journal of Comparative Neurology 202, 19–45.CrossRefGoogle ScholarPubMed
Lund, J.S., Hawken, M.J. & Parker, A.J. (1988). Local circuit neurons of macaque monkey striate cortex: II. Neurons of laminae 5 and 6. Journal of Comparative Neurology 276, 1–29.Google Scholar
Lund, J.S. & Yoshioka, T. (1991). Local circuit neurons of macaque monkey striate cortex: III. Neurons of laminae 4B, 4A, and 3B. Journal of Comparative Neurology 311, 234–258.CrossRefGoogle ScholarPubMed
Lund, J.S., Yoshioka, T. & Levitt, J.B. (1993). Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cerebral Cortex 3, 148–162.CrossRefGoogle ScholarPubMed
Malach, R. (1992). Dendritic sampling across processing streams in monkey striate cortex. Journal of Comparative Neurology 315, 303–312.Google Scholar
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, 1101–1123.Google Scholar
Purpura, K., Kaplan, E. & Shapley, R.M. (1988). Background light and the contrast gain of primate P and M retinal ganglion cells. Proceedings of the National Academy of Sciences of the U.S.A. 85, 4534–4537.Google Scholar
Rockland, K.S. (1992). Laminar distribution of neurons projecting from area VI to area V2 in macaque and squirrel monkeys. Cerebral Cortex 2, 38–47.Google Scholar
Rockland, K.S. & Pandya, D.N. (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Research 179, 3–20.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428–445Google Scholar
Ts'o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate striate cortex. Journal of Neuroscience 8, 1712–1728.CrossRefGoogle ScholarPubMed
Yoshioka, T, Levitt, J.B. & Lund, J.S. (1992 a). Intrinsic lattice connections of macaque monkey visual cortical area V4. Journal of Neuroscience 12, 2785–2802.Google Scholar
Yoshioka, T., Blasdel, G.G., Levitt, J.B. & Lund, J.S. (1992 b). Patterns of lateral connections in macaque visual area VI revealed by biocytin histochemistry and functional imaging. Society for Neuroscience Abstracts 18, 299.Google Scholar
Yoshioka, T., Levitt, J.B. & Lund, J.S. (1993). Anatomical basis for channel interactions in macaque conical visual area VI. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1173.Google Scholar