Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-19T22:49:22.866Z Has data issue: false hasContentIssue false
  • English
  • Français

Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey

Published online by Cambridge University Press:  02 June 2009

Edgar A. Deyoe ,
Susan Hockfield ,
Hideki Garren  and
David C. Van Essen
Edgar A. Deyoe
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee
Susan Hockfield
Affiliation:
Section of Neuroanatomy, Yale University School of Medicine, New Haven
Hideki Garren
Affiliation:
Biology Division 216-76, California Institute of Technology, Pasadena
David C. Van Essen
Affiliation:
Biology Division 216-76, California Institute of Technology, Pasadena
Get access Rights & Permissions [Opens in a new window]

Abstract

We have examined the distribution of immunoreactivity for the monoclonal antibody Cat-301 in visual cortex of the macaque monkey. Remarkably, those portions of striate cortex (V1) and extrastriate cortex that are most immunoreactive for Cat-301 are anatomically interconnected and are dominated by inputs arising from the magnocellular layers of the LGN (which are themselves highly immunoreactive). In particular, we found that a band of Cat-301 labeled neurons known to exist in layer 4 of V1 is centered on the boundary between layers 4Cα and 4B and thus includes portions of both the primary target of the magnocellular LGN and its subsequent relay through layer 4B. We also demonstrated consistently strong Cat-301 immunoreactivity in all three extrastriate targets of layer 4B: areas V3, MT, and the cytochrome-oxidase (CO) enriched thick stripes of V2. In V2, there was a close correlation between Cat-301 labeling and clusters of cells projecting to MT but not to V4. This was true even in regions where the CO pattern was equivocal or irregular, indicating that Cat-301 is a more reliable marker than CO for the thick-stripe subregions of V2. Finally, we found strong Cat-301 immunoreactivity in at least parts of areas V3A, the MST complex, and the posterior parietal complex, but not in area V4 or inferotemporal cortex. The molecular specificity revealed by this single marker thus correlates with functionally specific subdivisions at each hierarchical level over nearly the entire known extent of the visual pathway in macaques. This supports the notion that these subdivisions form an anatomically, physiologically, and now molecularly distinct pathway known as the M-stream.

Keywords

Cat-301 antibodyVisual cortexMacaqueM-stream
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 1 , July 1990 , pp. 67 - 81
Copyright
Copyright © Cambridge University Press 1990

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

Anderson, R.A. (1987). Inferior parietal lobule function in spatial perception and visuomotor integration. In Handbook of Physiology: The Nervous System, Vol. 5., ed. Mountcastle, F.P. & Geiger, S.R., pp. 483–518. Bethesda, Maryland: American Physiological Society.Google Scholar
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. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 1389–1413.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
Burkhalter, A., Felleman, D.J., Newsome, W.T. & Van, Essen D.C. (1986). Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex. Vision Research 26, 63–80.CrossRefGoogle ScholarPubMed
Colby, C.L., Gattass, R., Olson, C.R. & Gross, C.G. (1988). Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. Journal of Comparative Neurology 269, 392–413.CrossRefGoogle ScholarPubMed
De Lima, A.D., Bloom, F.E. & Morrison, J.H. (1988). Synaptic organization of serotonin-immunoreactive fibers in primary visual cortex of the macaque monkey. Journal of Comparative Neurology 274, 280–294.CrossRefGoogle ScholarPubMed
Desimone, R. & Ungerleider, L.G. (1986). Multiple visual areas in the caudal superior temporal sulcus of the macaque. Journal of Comparative Neurology 248, 164–189.CrossRefGoogle ScholarPubMed
Desimone, R. & Ungerleider, L.G. (1989). Neural mechanisms of visual processing in monkey. In Handbook of Neuropsychology, ed. Boller, F. & Grafman, J., pp. 267–299. Elsevier.Google Scholar
DeYoe, E. A. & Van Essen, D.C. (1985). Segregation of efferent connections and receptive-field properties in visual area V2 of the macaque. Nature 317, 58–61.CrossRefGoogle ScholarPubMed
DeYoe, E. A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219–226.CrossRefGoogle ScholarPubMed
DeYoe, E.A., Felleman, D.J., Knierim, J.J., Olavarria, J. & Van Essen, D.C. (1988). Heterogeneous subregions of macaque visual area V4 receive selective projections from V2 thin-Stripe and interstripe subregions. Investigative Ophthalmology and Visual Science (Suppl.) 29, 115.Google Scholar
DeYoe, E.A., Garren, H., Hockfield, S. & Van Essen, D.C. (1986). Cat-301 antibody identifies distinct areas and subdivisions in macaque extrastriate cortex. Society for Neuroscience Abstracts 12, 130.Google Scholar
Felleman, D.J. & Van Essen, D.C. (1990). Distributed hierarchical processing in the primate visual cortex (submitted).CrossRefGoogle Scholar
Felleman, D.J., Burkhalter, A. & Van Essen, D.C. (1987). Visual area PIP: an extrastriate cortical area in the posterior intra-parietal sulcus of macaque monkeys. Society for Neuroscience Abstracts 13, 626.Google Scholar
Felleman, D.J., DeYoe, E.A., Knierim, J.J., Olavarria, J. & Van Essen, D.C. (1988). Compartmental organization of projections from V2 to extrastnate areas V3, V3A, and V4t in macaque monkeys. Investigative Ophthalmology and Visual Science (Supp.) 29, 115.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., Lund, J.S., Schmechel, D.E. & Towles, A.C. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. Journal of Comparative Neurology 264, 73–91.CrossRefGoogle ScholarPubMed
Gallyas, F. (1979). Silver Staining of myelin by means of physical development. Neurological Research 1, 203–209.CrossRefGoogle ScholarPubMed
Hawken, M.J. & Parker, A.J. (1984). Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of Old World monkeys. Experimental Brain Research 54, 367–372.CrossRefGoogle ScholarPubMed
Hawken, M.J. & Parker, A.J. & Lund, J.S. (1988). Laminar organization and contrast sensitivity of direction-selective cells in the striate cortex of the Old World monkey. Journal of Neuroscience 8, 3541–3548.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuroanatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. Journal of Comparative Neurology 182, 123–186.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Hockfield, S., Jones, E.G. & McKay, R.D.G. (1984). Monoclonal antibody that identifies subsets of neurons in the central visual system of monkey and cat. Nature 307, 267–269.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G., Hockfield, S. & Mckay, R.D.G. (1988). Neuronal populations stained with the monoclonal antibody Cat-301 in the mammalian cerebral cortex and thalamus. Journal of Neuroscience 8, 518–542.CrossRefGoogle ScholarPubMed
Hockfield, S. & McKay, R.D.G. (1983). A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proceedings of the National Academy of Sciences of the U.S.A. 80, 5758–5761.CrossRefGoogle ScholarPubMed
Hockfield, S., McKay, R.D.G., Hendry, S.H.C. & Jones, E.G. (1983). A surface antigen that identifies ocular dominance columns in the visual cortex and laminar features of the lateral gemculate nucleus. Cold Spring Harbor Symposium on Quantitative Biology 48, 877–889.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Livingstone, M.S. (1987). Segregation of form, color, and stereopsis in primate area 18. Journal of Neuroscience 7(11), 3378–3415.CrossRefGoogle ScholarPubMed
Kalb, R.G. & Hockfield, S. (1988). Molecular evidence for early activity-dependent development of hamster motor neurons. Journal of Neuroscience 8, 2350–2360.CrossRefGoogle ScholarPubMed
Kalb, R.G. & Hockfield, S. (1989). Large-diameter primary afferent input is required for expression of the Cat-301 proteoglycan on the surface of motor neurons. Neuroscience (in press).Google Scholar
Komatsu, H. & Wurtz, R.H. (1988). Relation of cortical areas MT and MST to pursuit eye movements, I: Localization and visual properties of neurons. Journal of Neurophysiology 60, 580–603.CrossRefGoogle ScholarPubMed
Levitt, P. (1984). A monoclonal antibody to limbic system neurons. Science 223, 299–301.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). 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. (1987). Connections between layer 4B of area 17 and thick cytochrome-oxidase stripes of area 18 in the squirrel monkey. Journal of Neuroscience 7, 3371–3377.CrossRefGoogle ScholarPubMed
Lund, J.S. (1973). Organization of neurons in the visual cortex, area 17, of the monkey (Macacca 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., Henry, G.H., Macqueen, C.L. & Harvey, A.R. (1979). Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey. Journal of Comparative Neurology 184, 599–618.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, 287–304.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Newsome, W.T. (1987). Visual processing in monkey extrastriate cortex. Annual Review of Neuroscience 10, 363–401.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, 2563–2586.CrossRefGoogle ScholarPubMed
McGuire, P.K., & Hockfield, S. & Goldman-Rakic, P.S. (1989). The distribution of Cat-301 immunoreactivity in the frontal and parietal lobes of the macaque monkey. Journal of Comparative Neurology 288, 280–296.CrossRefGoogle ScholarPubMed
McKay, R.D.G. & Hockfield, S.J. (1982). Monoclonal antibodies distinguish antigenically discrete neuronal types in the vertebrate central nervous system. Proceedings of the National Academy of Sciences of the U.S.A. 79, 6747–6751.CrossRefGoogle ScholarPubMed
Mesulam, M.M. (1978). Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 105–117.CrossRefGoogle ScholarPubMed
Mrrzdorf, U. & Singer, W. (1979). Excitatory synaptic ensemble properties in the visual cortex of the macaque monkey: a current source density analysis of electrically evoked potentials. Journal of Comparative Neurology 187, 71–84.Google Scholar
Morrison, J.H. & Foote, S.L. (1986). Noradrenergic and serotonergic innervation of cortical, thalamic, and tectal visual structures in Old and New World monkeys. Journal of Comparative Neurology 243, 117–138.CrossRefGoogle Scholar
Newsome, W.T., Maunsell, J.H.R. & Van Essen, D.C. (1986). Ventral posterior visual area of the macaque: visual topography and areal boundaries. Journal of Comparative Neurology 252, 139–153.CrossRefGoogle ScholarPubMed
Olavarria, J., DeYoe, E.A. & Van Essen, D.C.(1989). Pattern of cytochrome-oxidase staining in the unfolded and flattened V2 of the macaque monkey. Investigative Ophthalmology and Visual Science (Supp.) 30, 298.Google Scholar
Olavarria, J. & Van Sluyters, R.C. (1985). Unfolding and flattening the cortex of gyrencephalic brains. Journal of Neuroscience Methods 15, 191–202.CrossRefGoogle ScholarPubMed
Rockland, K.S. (1989). Bistratified distribution of terminal arbors of individual axons projecting from area Vl to MT in the macaque monkey. Visual Neuroscience (submitted).CrossRefGoogle Scholar
Rockland, K.S. & Virga, A. (1989). Organization of individual cortical axons projecting from area V1 (area 17) to V2 (area 18) in the macaque monkey (submitted).CrossRefGoogle Scholar
Shipp, S. & Zeki, S. (1985) Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315, 322–324.CrossRefGoogle ScholarPubMed
Stephenson, D.T. & Kushner, P.D. (1988). An Atlas of a rare neuronal surface antigen in the rat central nervous system. Journal of Neuroscience 8, 3035–3056.CrossRefGoogle ScholarPubMed
Sur, M., Frost, D.O. & Hockfield, S. (1988). Expression of a surface-associated antigen on Y cells in the cat lateral geniculate nucleus is regulated by visual experience. Journal of Neuroscience 8(3), 874–882.CrossRefGoogle Scholar
Tootell, R.B.H. & Silverman, M.S. (1985). Two methods for flat-mounting cortical tissue. Journal of Neuroscience Methods 15, 177–190.CrossRefGoogle ScholarPubMed
Tootell, R.B.H. & Hamilton, S.L. (1989). Functional anatomy of the second cortical visual area (V2) in the macaque. Journal of Neuroscience 9, 2620–2644.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Hamilton, S.L. & Switkes, E. (1988). Functional anatomy of macaque striate cortex, IV: Contrast and magno-parvo streams. Journal of Neuroscience 8, 1594–1609.CrossRefGoogle ScholarPubMed
Ts'o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate striate cortex. Journal of Neuroscience 8(5), 1712–1727.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190–222.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two cortical visual systems. In Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W., pp. 549–586. Cambridge, Massachusetts: MIT Press.Google Scholar
Van Essen, D.C., Newsome, W.T., Maunsell, J.H.R. & Bixby, J.L. (1986). The projections from striate cortex (VI) to areas V2 and V3 in the macaque monkey: asymmetries, areal boundaries, and patchy connections. Journal of Comparative Neurology 244, 451–480.CrossRefGoogle Scholar
Van Essen, D.C. & Zeki, S.M. (1978). The topographical organization of rhesus monkey prestriate cortex. Journal of Physiology 277, 193–226.CrossRefGoogle Scholar
Wong-Riley, M.T.T. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome-oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Zaremba, S., Guimaraes, A., Kalb, R.G. & Hockfield, S. (1989). Characterization of an activity-dependent neuronal surface proteoglycan identified with monoclonal antibody Cat-301. Neuron 2, 1207–1219.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1978). The third visual complex of rhesus monkey prestriate cortex. Journal of Physiology 277, 245–272.CrossRefGoogle ScholarPubMed
Zeki, S. & Shipp, S. (1988). The functional logic of cortical connections. Nature 335, 311–317.CrossRefGoogle ScholarPubMed