Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T10:40:25.415Z Has data issue: false hasContentIssue false
  • English
  • Français

Cortical connections of area 18 and dorsolateral visual cortex in squirrel monkeys

Published online by Cambridge University Press:  02 June 2009

C. G. Cusick  and
J. H. Kaas
C. G. Cusick
Affiliation:
Department of Anatomy, Tulane University Medical Center, New Orleans
J. H. Kaas
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Get access Rights & Permissions [Opens in a new window]

Abstract

Cortical connections of area 18 (V-II) and part of the dorsolateral visual area (DL) were determined in squirrel monkeys with single and multiple injections of the sensitive bidirectional tracer, wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP). Injections were placed into portions of area 18 or DL on the dorsolateral surface of the brain, patterns of label were examined in brain sections cut parallel to the surface of physically flattened cortex, and comparisons were made with alternate brain sections reacted for cytochrome oxidase (CO) or stained for myelinated fibers. Major results are as follows. (1) Area 18 was identified by a characteristic alternation of dense and light CO bands crossing its width; the middle temporal visual area (MT) was CO dense; the dorsolateral area (DL) was less reactive, with rostral DL (DLR) lighter than caudal DL (DLC); area 17 had clear CO puffs in the supragranular layers. (2) Intrinsic connections revealed in area 18 included a narrow 100–200 μm fringe of less dense label around each injection core, label unevenly distributed in small clumps within 1–2 mm of injection sites, and clumps of transported label up to 6 mm from injection sites. (3) Single and multiple injections in area 18 produced patterns of labeled cells and terminations in area 17 that ranged from lattice- to puff-like in surface-view distribution. With multiple area 18 injections, regions of area 17 could be found where transported label was concentrated in CO puffs, avoided the CO puffs, or overlapped both puff and interpuff divisions of cortex. The labeled regions of area 17 were somewhat larger than the injection sites, suggesting some convergence from area 17 to area 18. (4) The major rostral connections of area 18 were with caudal DL (DLC). Rostral DL (DLR) was largely free of transported label. Single injection sites in area 18 resulted in several large clumps of label separated by regions of sparse or no label in DLC. Injections in lateral area 18 produced lateral foci of label in DL, while more medial injections produced more medial foci. However, following multiple injections into area 18 that included the representation of central vision, a continuous 2–3-mm-wide band of infragranular labeled cells extended from area 18 caudally to MT rostrally in the presumed location of central vision in DLC and DLR. (5) Injections in area 18 produced foci of label in MT. Label was more dorsal in MT with more dorsal injection sites in area 18. (6) Injections in area 18 resulted in sparse label in cortex within the inferior temporal sulcus and in cortex in the location of the frontal eye field. (7) Callosal connections of area 18 were with areas 17, 18, DL, and sparsely with MT. Multiple injections in area 18 produced a narrow, dense strip of label along the contralateral 17/18 border. Most of this label was in area 18, but small protrusions of label extended into area 17, and small separate foci of label were found displaced slightly into area 17. Fingers of callosal connections extended rostrally from the caudal border to cross up to half of the width of medial area 18 and the entire width of lateral area 18 where central vision is represented. Patchy callosal connections were found with DLC. (8) Injections in caudal DL confirmed the observation from area 18 injections that major connections of DLC are with area 18. Injections in DLR produced scattered, small foci of label in area 18 near the rostral border, as well as puffs of intrinsic connections, connections with MT, and with cortex rostral to area 18 medially.

The major conclusion stemming from the present results is that the DL region consists of at least two fields, with the caudal portion, DLC, receiving major inputs from area 18, and the rostral portion, DLR, having little input from area 18.

Keywords

Cortical visual areasArea 17Area 18Middle temporal areaPrimates
Type
Research Article
Information
Visual Neuroscience , Volume 1 , Issue 2 , March 1988 , pp. 211 - 237
Copyright
Copyright © Cambridge University Press 1988

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

Albright, T.P., Desimone, R., & Gross, C.G. (1984). Columnar organization of directionally selective cells in visual area MT of the macaque. Journal of Neurophysiology 51, 16–31.CrossRefGoogle ScholarPubMed
Allman, J.M. & Kaas, J.H. (1971). A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Research 31, 85–105.CrossRefGoogle ScholarPubMed
Allman, J.M. & Kaas, J.H. (1974 a). The organization of the second visual area (VII) in the owl monkey: a second order transformation of the visual hemifield. Brain Research 76, 247–265.CrossRefGoogle Scholar
Allman, J.M. & Kaas, J.H. (1974 b). A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatus). Brain Research 81, 199–213.CrossRefGoogle ScholarPubMed
Allman, J.M. & Kaas, J.H. (1976). Representation of the visual field on the medial wall of occipital-parietal cortex in the owl monkey. Science 191, 572–576.CrossRefGoogle ScholarPubMed
Allman, J.M., Kaas, J.H. & Lane, R.H. (1973). The middle temporal visual area (MT) in the bush baby (Galago senegalenis). Brain Research 57, 197–202.CrossRefGoogle ScholarPubMed
Allman, J., Miezin, F. & McGuinness, E. (1985). Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. Annual Review of Neuroscience 8, 407–430.CrossRefGoogle ScholarPubMed
Brodmann, K. (1909). Vergleichende Lokalisationslehre der Grosshirnrinde. Leipzig: Barth.Google Scholar
Colonnier, M. & Sas, E. (1978). An anterograde degeneration study of the tangential spread of axons in cortical areas 17 and 18 of the squirrel monkey (Saimiri sciureus). Journal of Comparative Neurology 179, 245–262.CrossRefGoogle ScholarPubMed
Cowey, A. (1964). Projections of the retina onto striate and prestriate cortex in the squirrel monkey (Saimiri sciureus). Journal of Neurophysiology 27, 366–393.CrossRefGoogle Scholar
Cragg, B.G. (1969). The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. Vision Research 9, 733–747.CrossRefGoogle ScholarPubMed
Cusick, C.G., Gould, H.J. III., & Kaas, J.H. (1984). Interhemispheric connections of visual cortex in owl monkeys (Aotus trivirgatus), marmosets (Callithrix jacchus), and galagos (Galago crassicaudatus). Journal of Comparative Neurology 230, 311–336.CrossRefGoogle ScholarPubMed
Cusick, C.G. & Kaas, J.H. (1986). Interhemispheric connections of cortical sensory and motor representations in primates. In Two Hemispheres-One Brain: Functions of the Corpus Callosum, ed. Lepore, F., Ptito, M. & Jasper, H.H. pp. 83–102. New York: Alan R. Liss, Inc.Google Scholar
Cusick, C.G. (1987). Evidence from patterns of cortical connections for subdivisions within the dorsolateral visual cortex of squirrel monkeys. Neuroscience 22, S122.Google Scholar
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
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
Felleman, D.J. & Kaas, J.H. (1984). Receptive-field properties of neurons in the middle temporal visual area (MT) of owl monkeys. Journal of Neurophysiology 52, 488–513.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1983). The connections of area V4 of macaque extrastriate cortex. Society for Neuroscience Abstracts 9, 153.Google Scholar
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurology Research 1, 203–209.CrossRefGoogle ScholarPubMed
Gattass, R. & Gross, C.G. (1981). Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. Journal of Neurophysiology 46, 621–638.CrossRefGoogle ScholarPubMed
Gattass, R., Sousa, A.P.B. & Covey, E. (1985). Cortical visual areas of the macaque: possible substrates for pattern recognition mechanisms. In Pattern Recognition Mechanisms, ed. Chagas, C., Gattass, R. & Gross, C., pp. 1–20. Vatican City: Pontifical Academy of Sciences.Google Scholar
Gould, H.J. III., Weber, J.T. & Rieck, R.W. (1987). Interhemispheric connections in the visual cortex of the squirrel monkey (Saimiri sciureus). Journal of Comparative Neurology 256, 14–28.CrossRefGoogle ScholarPubMed
Hassler, R. (1966). Comparative anatomy of the central visual systems in day- and night-active primates. In Evolution of the Forebrain, ed. Hassler, R. & Stephan, H., pp. 419–434. Stuttgart: Thieml Verlag.CrossRefGoogle Scholar
Horton, J.C. (1984). Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society of London B 304, 199–253.Google ScholarPubMed
Horton, J.C. & Hubel, D.H. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Livingstone, M.S. (1985). Complex-unoriented cells in a subregion of primate area 18. Nature 315, 325–327.CrossRefGoogle Scholar
Huerta, M.F., Krubitzer, L.A. & Kaas, J.H. (1987). The frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. Journal of Comparative Neurology 265, 332–361.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Hendrickson, A.E. (1983). Background and stimulus-induced patterns of high metabolic activity in the visual cortex (area 17) of the squirrel and macaque monkey. Journal of Neuroscience 3, 345–358.CrossRefGoogle ScholarPubMed
Kaas, J.H. & Cusick, C.G. (1984). Intrinsic and extrinsic cortical connections of area 17 of the prosimian primate (Galago). Society for Neuroscience Abstracts 10, 729.Google Scholar
Kaas, J.H. & Cusick, C.G. (1985). Cortical connections of area 18 in squirrel monkeys. Society for Neuroscience Abstracts 11, 1011.Google Scholar
Kaas, J.H. & Lin, C.-S. (1977). Cortical connections of area 18 in owl monkeys. Vision Research 17, 739–741.CrossRefGoogle Scholar
Kennedy, H. & Bullier, J. (1985). A double-labeling investigation of the afferent connectivity to cortical areas VI and V2 of the macaque monkey. Journal of Neuroscience 5, 2815–2830.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proceedings of the National Academy of Science (USA) 79, 6098–6101.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.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1987). 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.CrossRefGoogle ScholarPubMed
Lund, J.S., Hendrickson, A.E., Ogren, M.P. & Tobin, E.A. (1981). Anatomical organization of primate visual area V-II. Journal of Comparative Neurology 202, 19–45.CrossRefGoogle Scholar
Maguire, W.M. & Baizer, J.S. (1984). Visuotopic organization of the prelunate gyrus in rhesus monkey. Journal of Neuroscience 4, 1690–1704.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, 2563–2686.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. (1978). Tetramethylbenzidine for horseradish perox-idase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106–117.CrossRefGoogle Scholar
Moran, J., Desimone, R., Schein, S.J. & Mishkin, M. (1983). Suppression from ipsilateral visual field in area V4 of the macaque. Society for Neuroscience Abstracts 9, 957.Google Scholar
Newsome, W.T. & Allman, J.M. (1980). Interhemispheric connections of visual cortex in the owl monkey (Aotus trivirgatus) and the bushbaby (Galago senegalensis). Journal of Comparative Neurology 194, 209–233.CrossRefGoogle ScholarPubMed
Rockland, K.S. (1985). A reticulated pattern of intrinsic connections in primate area V2 (area 18). Journal of Comparative Neurology 235, 467–478.CrossRefGoogle Scholar
Rockland, K.S. & Lund, J.S. (1982). Widespread periodic intrinsic connections in tree shrew visual cortex (area 17). Science 215, 1532–1534.CrossRefGoogle Scholar
Rockland, K.S. & Lund, J.S. (1983). Intrinsic laminar lattice connections in primate visual cortex. Journal of Comparative Neurology 216, 303–318.CrossRefGoogle ScholarPubMed
Rockland, K.S., Lund, J.S. & Humphrey, A.L. (1982). Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis). Journal of Comparative Neurology 209, 41–58.CrossRefGoogle Scholar
Sereno, M.I., McDonald, C.T. & Allman, J.M. (1987). Multiple visual areas between V2 and MT in the owl monkey. Society for Neuroscience Abstracts 13, 625.Google Scholar
Sesma, M.A., Casagrande, V.A. & Kaas, J.H. (1984). Cortical connections of area 17 in tree shrew. Journal of Comparative Neurology 230, 337–351.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, 322–325.CrossRefGoogle ScholarPubMed
Staines, Wm. A., Kimura, H., Fibiger, H.C. & McGeer, E.G. (1980). Peroxidase-labeled lectin as a neuroanatomical tracer: evaluation in a CNS pathway. Brain Research 197, 485–490.CrossRefGoogle Scholar
Tigges, J., Spatz, W.B. & Tigges, M. (1973). Reciprocal point-to-point connections between parastriate and striate cortex in the squirrel monkey (Saimiri). Journal of Comparative Neurology 148, 481–490.CrossRefGoogle ScholarPubMed
Tigges, J., Spatz, W.B. & Tigges, M. (1974). Efferent cortico-cortical fiber connections of area 18 in the squirrel monkey (Saimiri). Journal of Comparative Neurology 158, 219–236.CrossRefGoogle ScholarPubMed
Tigges, J., Tigges, M., Anschel, S., Cross, N.A., Letbetter, W.D. & McBride, R.L. (1981). Areal and laminar distribution of neurons interconnecting the central visual cortical areas 17, 18, 19, and MT in squirrel monkey (Saimiri). Journal of Comparative Neurology 202, 539–560.CrossRefGoogle Scholar
Tigges, J., Tigges, M. & Perachio, A.A. (1977). Complementary laminar terminations of afferents to area 17 originating in area 18 and the LGN in squirrel monkey. Journal of Comparative Neurology 176, 87–100.CrossRefGoogle Scholar
Tigges, M., Tigges, J., Anschel, S., Cross, N.A., Letbetter, W.D. & McBride, R.L. (1980). Cell layers of origin for association and callosal neurons in visual cortical areas of squirrel monkey (Saimiri). Experimental Brain Research 41, A23.Google Scholar
Tootell, R.B.H., Hamilton, S.L. & Silverman, M.S. (1985). Topography of cytochrome oxidase activity in owl monkey cortex. Journal of Neuroscience 5, 2786–2800.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Silverman, M.S., De Valois, R.L. & Jacobs, G.H. (1983). Functional organization of the second cortical visual area in primates. Science 220, 737–739.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Desimone, R. (1986 a). Projections to the superior temporal sulcus from the central and peripheral field representations of VI and V2. Journal of Comparative Neurology 248, 147–163.CrossRefGoogle Scholar
Ungerleider, L.G. & Desimone, R. (1986 b). Cortical connections of area MT in the macaque. Journal of Comparative Neurology 248, 190–222.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1979). The striate projection zone in the superior temporal sulcus of Macaca mulatta: location and topographic organization. Journal of Comparative Neurology 188, 347–366.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two cortical visual systems. In Analysis of Visual Behavior, ed. Ingle, et al., pp. 549–586. Cambridge, Massachusetts: MIT Press.Google Scholar
Ungerleider, L.G., Gattass, R., Sousa, A.P.B. & Mishkin, M. (1983). Projections of area V2 in the macaque. Society for Neuroscience Abstracts 9, 152.Google Scholar
Van Essen, D.C. (1985). Functional organization of primate visual cortex. In Cerebral Cortex, Vol. 3, ed. Jones, E.G. & Peters, A.A., pp. 259–329. New York: Plenum Press.Google Scholar
Van Essen, D.C., Maunsell, J.H.R. & Blxby, J.L. (1981). The middle temporal visual area in the macaque: myeloarchitecture, connections, functional properties, and topographical organization. Journal of Comparative Neurology 199, 293–326.CrossRefGoogle Scholar
Van Essen, D.C., Newsome, W.T. & Bixby, J.L. (1982). The pattern of inter-hemispheric connections and its relationship to extrastriate visual areas in the macaque monkey. Journal of Neuroscience 2, 265–283.CrossRefGoogle Scholar
Van Essen, D.C. & Zeki, S.M. (1978). The topographic organization of prestriate cortex. Journal of Physiology (London) 277, 193–226.CrossRefGoogle Scholar
Weller, R.E. & Kaas, J.H. (1981). Cortical and subcortical connections of visual cortex in primates. In Cortical Sensory Organization, Vol. 2: Multiple Visual Areas, ed. Woolsey, C.N. pp. 121–125. Clifton, New Jersey: Humana Press.Google Scholar
Weller, R.E. & Kaas, J.H. (1983). Retinotopic patterns of connections of area 17 with visual areas V-II and MT in macaque monkeys. Journal of Comparative Neurology 220, 253–279.CrossRefGoogle ScholarPubMed
Weller, R.E. & Kaas, J.H. (1985). Cortical projections of the dorsolateral visual area in owl monkeys: the prestriate relay to inferior temporal cortex. Journal of Comparative Neurology 234, 35–39.CrossRefGoogle ScholarPubMed
Weller, R.E. & Kaas, J.H. (1987). Subdivisions and connections of inferior temporal cortex in owl monkeys. Journal of Comparative Neurology 256, 137–172.CrossRefGoogle ScholarPubMed
Weller, R.E., Wall, J.T. & Kaas, J.H. (1984). Cortical connections of the middle temporal visual area (MT) and the superior temporal cortex in owl monkeys. Journal of Comparative Neurology 228, 81–104.CrossRefGoogle ScholarPubMed
Weller, R.E., Steele, G. & Cusick, C.G. (1987). Cortical connections of a dorsal visual area in squirrel monkeys. Society for Neuroscience Abstracts 13, 626.Google Scholar
Wong-Riley, M.T.T. (1978). Reciprocal connections between striate and prestriate cortex in squirrel monkey as demonstrated by combined peroxidase histochemistry and autoradiography. Brain Research 147, 159–164.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1979 a). Columnar cortico-cortical interconnections within the visual system of the squirrel and macaque monkeys. Brain Research 162, 201–217.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1979 b). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. & Carroll, E.W. (1984). Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in VII prestriate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 18–37.CrossRefGoogle Scholar
Zeki, S.M. (1969). Representation of central visual field in prestriate cortex of monkey. Brain Research 14, 271–291.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1971). Cortical projections from two prestriate areas in the monkey. Brain Research 34, 19–35.CrossRefGoogle ScholarPubMed