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Contributions of individual layer 2–5 spiny neurons to local circuits in macaque primary visual cortex

Published online by Cambridge University Press:  02 June 2009

Edward M. Callaway  and
Anne K. Wiser
Edward M. Callaway
Affiliation:
Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla
Anne K. Wiser
Affiliation:
Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla
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Abstract

We studied excitatory local circuits in the macaque primary visual cortex (V1) to investigate their relationships to the magnocellular (M) and parvocellular (P) streams. Sixty-two intracellularly labeled spiny neurons in layers 2–5 were analyzed. We made detailed observations of the laminar and columnar specificity of axonal arbors and noted correlations with dendritic arbors. We find evidence for considerable mixing of M and P streams by the local circuitry in V1. Such mixing is provided by neurons in the primary geniculate recipient layer 4C, as well as by neurons in both the supragranular and infragranular layers. We were also interested in possible differences in the axonal projections of neurons with different dendritic morphologies. We found that layer 4B spiny stellate and pyramidal neurons have similar axonal arbors. However, we identified two types of layer 5 pyramidal neuron. The majority have a conventional pyramidal dendritic morphology, a dense axonal arbor in layers 2–4B, and do not project to the white matter. Layer 5 projection neurons have an unusual “backbranching” dendritic morphology (apical dendritic branches arc downward rather than upward) and weak or no axonal arborization in layers 2–4B, but have long horizontal axonal projections in layer 5B. We find no strong projection from layer 5 pyramidal neurons to layer 6. In macaque V1 there appears to be no single source of strong local input to layer 6; only a minority of cells in layers 2–5 have axonal branches in layer 6 and these are sparse. Our results suggest that local circuits in V1 mediate interactions between M and P input that are complex and not easily incorporated into a simple framework.

Keywords

MacaqueV1Striate cortexLocal circuitsFunctional streams

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Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 5 , September 1996 , pp. 907 - 922
Copyright
Copyright © Cambridge University Press 1996

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References

Anderson, J.C., Martin, K.A.C. & Whitteridge, D. (1993). Form, function, and intracortical projections of neurons in the striate cortex of the monkey Macacus nemestrinus. Cerebral Cortex 3, 412–420.CrossRefGoogle ScholarPubMed
Blanton, M.G., Lo Turco, J.J. & Kriegstein, A.R. (1989). Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. Journal of Neuroscience Methods 30, 203–210.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.CrossRefGoogle ScholarPubMed
Callaway, E.M. & Katz, L.C. (1992). Development of axonal arbors of layer 4 spiny neurons in cat striate cortex. Journal of Neuroscience 12, 570–582.CrossRefGoogle ScholarPubMed
Callaway, E.M. (1993). Organization of functional stream specific local circuits in the primary visual cortex of newborn macaque monkeys. Society for Neuroscience Abstracts 19, 240.Google Scholar
Casagrande, V.A. & Kaas, J.H. (1995). The afferent, intrinsic, and efferent connections of primary visual cortex in primates. In Cerebral Cortex, Vol. 10, ed. Peters, A. & Rockland, K.S., pp. 201–259. New York: Plenum Press.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.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Usrey, W.M., Schofield, B.R. & Einstein, G. (1994). The sublaminar organization of corticogeniculate neurons in layer 6 of macaque striate cortex. Visual Neuroscience 11, 307–315.CrossRefGoogle ScholarPubMed
Gilbert, C.D. (1983). Microcircuitry of the visual cortex. Annual Review of Neuroscience 6, 217–247.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Wiesel, T.N. (1979). Morphology and intracortical projections of functionally characterized neurones in the cat visual cortex. Nature 280, 120–125.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Wiesel, T.N. (1983). Clustered intrinsic connections in cat visual cortex. Journal of Neuroscience 3, 1116–1133.CrossRefGoogle ScholarPubMed
Horton, J.C. (1984). Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philosophic Transcript of the Royal Society B (London) 304, 199–253.Google ScholarPubMed
Horton, J.C. & Hocking, D.R. (1996). An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. Journal of Neuroscience 16, 1791–1807.CrossRefGoogle ScholarPubMed
Hubener, 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
Katz, L.C. (1987). Local circuitry of identified projection neurons in cat visual cortex brain slices. Journal of Neuroscience 7, 1223–1249.CrossRefGoogle ScholarPubMed
Katz, L.C., Gilbert, C.D. & Wiesel, T.N. (1989). Local circuits and ocular dominance columns in monkey striate cortex. Journal of Neuroscience 9, 1389–1399.CrossRefGoogle ScholarPubMed
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1992). Parallel pathways in macaque monkey striate cortex: Anatomically defined columns in layer III. Proceeding of the National Academy of Sciences of the U.S.A. 89, 3566–3570.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Specificity of intrinsic connections in primate primary visual cortex. Journal of Neuroscience 4, 2830–2835.CrossRefGoogle ScholarPubMed
Lund, J.S. (1973). Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta). Journal of Comparative Neurology 147, 455–496.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lund, J.S. (1988). Anatomical organization of macaque monkey striate visual cortex. Annual Review of Neuroscience 11, 253–288.CrossRefGoogle ScholarPubMed
Lund, J.S. & Boothe, R.G. (1975). Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17, of the macaque monkey. Journal of Comparative Neurology 159, 305–334.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 as shown by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 164, 287–303.CrossRefGoogle ScholarPubMed
Lund, J.S., Boothe, R.G. & Lund, R.D. (1977). Development of neurons in the visual cortex of the monkey (Macaca nemestrina): A Golgi study from fetal day 127 to postnatal maturity. Journal of Comparative Neurology 176, 149–188.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
Martin, K.A.C. (1984). Neuronal circuits in cat striate cortex. In Cerebral Cortex, Vol. 2, ed. Jones, E.G. & Peters, A., pp. 241–284. New York: Plenum Press.CrossRefGoogle Scholar
Martin, K.A.C. & Whitteridge, D. (1984). Form, function and intracortical projections of spiny neurons in the striate cortex of the cat. Journal of Physiology 353, 463–504.CrossRefGoogle ScholarPubMed
Mates, S.L. & Lund, J.S. (1983). Neuronal composition and development in lamina 4C of monkey striate cortex. Journal of Comparative Neurology 221, 60–90.CrossRefGoogle ScholarPubMed
McGuire, B.A., Gilbert, C.D., Rivlin, P.K. & Wiesel, T.N. (1991). Targets of horizontal connections in macaque primary visual cortex. Journal of Comparative Neurology 305, 370–392.CrossRefGoogle ScholarPubMed
Merigan, W.H. & Maunsell, J.H.R. (1993). How parallel are the visual pathways? Annual Review of Neuroscience 16, 369–402.CrossRefGoogle ScholarPubMed
Nealey, T.A. & Maunsell, J.H.R. (1994). Magnocellular and parvo-cellular contributions to the responses of neurons in macaque striate cortex. Journal of Neuroscience 14, 2069–2079.CrossRefGoogle Scholar
Saint Marie, R.L. & Peters, A. (1985). The morphology and synaptic connections of spiny stellate neurons in monkey visual cortex (area 17): A Golgi-electron microscopic study. Journal of Comparative Neurology 233, 213–235.CrossRefGoogle ScholarPubMed
Sawatari, A. & Callaway, E.M. (1996). Convergence of magno- and parvocellular pathways in layer 4B of macaque primary visual cortex. Nature 380, 442–446.CrossRefGoogle ScholarPubMed
Shipp, S. & Zeki, S. (1989). The organization of connections between areas V5 and V1 in macaque monkey visual cortex. European Journal of Neuroscience 1, 309–332.CrossRefGoogle ScholarPubMed
Usrey, W.M. & Fitzpatrick, D. (1994). Laminar specificity in the relay of magnocellular and parvocellular streams to the superficial and deep layers of macaque striate cortex. Society for Neuroscience Abstracts 20, 1578.Google Scholar
Valverde, F. (1985). The organizing principles of the primary visual cortex in the monkey. In Cerebral Cortex, Vol. 3, ed. Jones, E.G. & Peters, A., pp. 207–257. New York: Plenum Press.Google Scholar
Wiser, A.K. & Callaway, E.M. (1996). Contributions of individual layer 6 pyramidal neurons to local circuitry in macaque primary visual cortex. Journal of Neuroscience 16, 2724–2739.CrossRefGoogle ScholarPubMed
Yoshioka, T., Levitt, J.B. & Lund, J.S. (1994). Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: Anatomy of interlaminar projections. Visual Neuroscience 11, 467–489.CrossRefGoogle ScholarPubMed