Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T05:31:38.735Z Has data issue: false hasContentIssue false
  • English
  • Français

Bistratified distribution of terminal arbors of individual axons projecting from area V1 to middle temporal area (MT) in the macaque monkey

Published online by Cambridge University Press:  02 June 2009

Kathleen S. Rockland
Kathleen S. Rockland
Affiliation:
Eye Research Institute and Department of Anatomy, Boston University School of Medicine, Boston
Get access Rights & Permissions [Opens in a new window]

Abstract

In the present study, the anterograde tracer Phaseolus vulgaris-leucoagglutinin was injected into area V1 in order to demonstrate the detailed morphology of individual axons terminating in prestriate area MT. On the basis of 24 axon reconstructions, several representative (but not necessarily comprehensive) characteristics have been identified: (1) Most axons arborize in a patchy manner over a widespread territory, frequently greater than 1.0 mm and often up to 1.5 × 1.8 mm (dimensions uncorrected for shrinkage). (2) Terminal arbors are distributed to layers 3, 4, and 6. Those in layer 6 need not be in register with those in the upper layers. (3) Number and size of terminal arbors are variable. One axon may have 1–4 arbors in the middle layers; typically at least one of these will have a diameter of 200–250 µm, while the others may be less developed. There are from 1–3 arbors in layer 6, usually 50 µm (but sometimes up to 100 µm) in diameter. (4) Terminal boutons are of mixed morphology, but usually beaded and large (up to 3.0 µm). (5) In the white matter, many axons travel in the external sagittal stratum but some are part of the U-fiber system. Axons commonly branch, sometimes at depths up to 0.75–1.0 mm, below the gray matter of MT. In summary, these axons are not stereotyped, but rather vary in the number and size of their terminal arbors, as well as in their branching and overall geometry.

Connections from area V1 to MT have been associated with the magnocellular-dominated “processing channel.” As widespread arborizations and bistratified terminations are common to both striate axons in MT and to geniculocortical axons in layer 4Cα of primary visual cortex, these features might be correlated with magnocellular-specific processing requirements.

Keywords

Axon terminal distributionCortico-cortical afferentsModular organizationPHA-LVisual cortex
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 2 , August 1989 , pp. 155 - 170
Copyright
Copyright © Cambridge University Press 1989

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.D. (1984). Direction and orientation selectivity of neurons in visual area MT of the macaque. Journal of Neurophysiology 52, 1106–1130.CrossRefGoogle ScholarPubMed
Albright, T.D., Desimone, R. & Gross, C.G. (1984). Columnar organization of directionality selective cells in visual area MT of the macaque. Journal of Neurophysiology 51, 16–31.CrossRefGoogle ScholarPubMed
Albright, T.D. & Desimone, R. (1987). Precision of visuotopic organization in area MT of the macaque. Experimental Brain Research 65, 582–592.CrossRefGoogle ScholarPubMed
Blasdel, G.G. & Frrzpatrick, 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
DeFelipe, J., Conley, M. & Jones, E.G. (1986). Long-range focal col-lateralization of axons arising from corticocortical cells in monkey sensory-motor cortex. Journal of Neuroscience 6, 3749–3766.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
DeYoe, E.A. & Essen, D.C.Van (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219–226.CrossRefGoogle ScholarPubMed
Dubner, R. & Zeki, S.M. (1971). Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus of the monkey. Brain Research 35, 528–532.CrossRefGoogle Scholar
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
Gerfen, C.R. & Sawchenko, P.E. (1984). An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris-leucoagglutinin (PHA–L). Brain Research 290, 219–238.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Wiesel, T.N. (1983). Clustered intrinsic connections in cat visual cortex. Journal of Neuroscience 3, 1116–1133.CrossRefGoogle ScholarPubMed
Kaas, J.H. (1986). The structural basis for information processing in the primate visual system. In Visual Neuroscience, ed. Pettigrew, J.P., Sanderson, K.J. & Levick, W.R., pp. 315–340. Cambridge: Cambridge University Press.Google Scholar
Kennedy, H. & Bullier, J. (1985). A double-labelling investigation of the afferent connectivity to cortical areas V1 and V2 in the macaque monkey. Journal of Neuroscience 5, 2815–2830.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1987). 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. & Boothe, R.G. (1975). Interlaminar connections and pyramidal neuron organization in the visual cortex, area 17, of the macaque monkey. Journal of Comparative Neurology 164, 287–304.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
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 5B and 6. Journal of Comparative Neurology 276, 1–29.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. (1987). Physiological evidence for two visual systems. In Matters of Intelligence, ed. Vaina, L., pp. 59–88, Boston: D. Reidel Publishing Company.CrossRefGoogle Scholar
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. & Essen, D.C.Van (1983 a). Functional properties of neurons in middle temporal visual area of the macaque monkey, I: Selectivity for stimulus direction speed, and orientation. Journal of Neurophysiology 49, 1127–1147.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Essen, D.C.Van (1983 b). 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
Maunsell, J.H.R. & Essen, D.C.Van (1987). Topographic organization of the middle temporal visual area in the macaque monkey: representational biases and the relationship to callosal connections and myeloarchitectonic boundaries. Journal of Comparative Neurology 266, 535–555.CrossRefGoogle ScholarPubMed
McGuire, B.A., Hornung, J.-P., Gilbert, C.D. & Wiesel, T.N. (1984). Patterns of synaptic input to layer 4 of cat striate cortex. Journal of Neuroscience 4, 3021–3033.CrossRefGoogle ScholarPubMed
MiKami, A., Newsome, W.T. & Wurtz, R.H. (1986). Motion selectivity in macaque visual cortex, I: Mechanisms of direction and speed selectivity in extrastriate area MT. Journal of Neurophysiology 55, 1308–1327.CrossRefGoogle ScholarPubMed
Montero, V.M. (1980). Patterns of connections from the striate cortex to cortical visual areas in superior temporal sulcus of macaque and middle temporal gyrus of owl monkey. Journal of Comparative Neurology 189, 45–55.CrossRefGoogle ScholarPubMed
Newsome, W.T. & Pare, E.B. (1988). A selective impairment of motion perception following lesions of the middle temporal visual area (MT). Journal of Neuroscience 8, 2201–2211.CrossRefGoogle ScholarPubMed
Newsome, W.T., Wurtz, R.H., Dursteler, M.R. & Mlkami, A. (1985). Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. Journal of Neuroscience 5, 825–840.CrossRefGoogle ScholarPubMed
Petersen, S.E., Miezin, F.M. & Allman, J.M. (1988). Transient and sustained responses in four extrastriate visual areas of the owl monkey. Experimental Brain Research 70, 55–60.CrossRefGoogle ScholarPubMed
Polyak, S.L. (1957). The Vertebrate Visual System. Chicago: University of Chicago Press.Google Scholar
Rockland, K.S. & Pandya, D.N. (1981). Cortical connections of the occipital lobe in the rhesus monkey: interconnections between areas 17, 18, 19, and the superior temporal sulcus. Brain Research 212, 249–270.CrossRefGoogle Scholar
Rockland, K.S. & Virga, A. (1989 a). Organization of individual cortical axons projecting from area V1 (area 17) to V2 (area 18) in the macaque monkey. Visual Neuroscience (submitted).CrossRefGoogle Scholar
Rockland, K.S. & Virga, A. (1989 b). Terminal arbors of individual “feedback” axons projecting from area V2 to V1 in the macaque monkey: a study using immunohistochemistry of anterogradely transported Phaseolus vulgaris-leucoagglutinin. Journal of Comparative Neurology (in press).CrossRefGoogle ScholarPubMed
Seltzer, B. & Pandya, D.N. (1978). Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Research 149, 1–24.CrossRefGoogle ScholarPubMed
Tanaka, K., Hikosaka, K., Sarro, H.A., Yukie, M., Fukada, Y. & Iwai, E. (1986). Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey. Journal of Neuroscience 6, 134–144.CrossRefGoogle ScholarPubMed
Tusa, R.J. & Ungerleider, L.G. (1985). The inferior longitudinal fasciculus: a reexamination in humans and monkeys. Annals of Neurology 18, 583–591.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1979). The striate projection zone in the superior temporal sulcus of Macaca mulatto: location and topographic organization. Journal of Comparative Neurology 188, 347–366.CrossRefGoogle Scholar
Ungerleider, L.G. & Mishktn, M. (1982) Two cortical visual systems. In Analysis of Visual Behavior, ed. Ingle, D.L., Goodale, M.A. & Mansfield, R.J.W., pp. 549–580, Cambridge, MA: MIT Press.Google Scholar
Ungerleider, L.G. & Desimone, R. (1986 a). Projections to the superior temporal sulcus from the central and peripheral field representations of V1 and V2. Journal of Comparative Neurology 248, 147–163.CrossRefGoogle Scholar
Ungerleider, L.G. & Desimone, R. (1986 b). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190–222.CrossRefGoogle ScholarPubMed
Valverde, F. (1978). The organization of area 18 in the monkey. A Golgi study. Anatomy and Embryology 154, 305–334.CrossRefGoogle ScholarPubMed
Essen, D.C.Van (1985). Functional organization of primate visual cortex. In Cerebral Cortex, Vol. 3., ed. Peters, A. & Jones, E.G., pp. 259–329. New York: Plenum Press.Google Scholar
Essen, D.C.Van, Maunsell, J.H.R. & Bixby, J.L. (1981). The middle temporal visual area in the macaque: myeloarchitecture, connections, functional properties, and topographic organization. Journal of Comparative Neurology 199, 293–326.CrossRefGoogle ScholarPubMed
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
Zeki, S.M. (1969). Representation of central visual fields in prestriate cortex of monkey. Brain Research 14, 271–291.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1974). Functional organization of a visual area in the posterior bank of the superior temporal sulcus in the rhesus monkey. Journal of Physiology (London) 236, 549–573.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1976). The projections to the superior temporal sulcus from areas 17 and 18 in the rhesus monkey. Proceedings of the Royal Society B (London) 193, 199–207.Google Scholar
Zeki, S. & Shipp, S. (1988). The functional logic of cortical connections. Nature 335, 311–317.CrossRefGoogle ScholarPubMed