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. 1995 Dec;187(Pt 3):547–562.

Segregation and convergence of specialised pathways in macaque monkey visual cortex.

S Shipp 1, S Zeki 1
PMCID: PMC1167459  PMID: 8586555

Abstract

At the level of cortical area V2, the various visual inputs to the cortex have reorganised to form 3 distinct channels. Anatomically these are embodied in the thick and thin dark stripes, and paler interstripes characteristic of cytochrome oxidase architecture. Do the outputs of these compartments remain segregated at higher levels of processing, or are they in turn combined and repackaged? To examine this question we have injected distinct orthograde tracers into the functionally distinct areas V4 and V5 of one hemisphere in 3 macaque monkeys (Macaca fascicularis). V4 is known to receive input from both thin stripes and interstripes of V2, but some parts of V4 receive only interstripe afferents, others receive a relatively greater contribution from the thin stripes. Thus V4 itself is thought to possess subcompartments of at least two distinct types, acting to extend the blob-thin stripe and interblob-interstripe pathways through V1 and V2. The experiments reported here reveal no further divergence between these channels: both types of V4 subcompartment make rather similar patterns of connection with further visual areas and subcortical structures. In contrast to V4, area V5 receives input from the thick stripes of V2. V4 and V5 are weakly interconnected, at best, and there is limited direct convergence in their two sets of ascending connections. For instance, both areas send output to area LIP; but V4 targets the dorsal half of the area, and V5 the ventral half, with some minor overlap. Projections to the superior temporal sulcus are also mainly separate, although we found instances of direct convergence in areas FST and possibly V4t. Segregation is also the rule for subcortical connections to the pulvinar from these two areas. In summary, the segregated outputs of V2 can remain largely distinct through at least two subsequent stages of cortical processing.

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Selected References

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  1. Amir Y., Harel M., Malach R. Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex. J Comp Neurol. 1993 Aug 1;334(1):19–46. doi: 10.1002/cne.903340103. [DOI] [PubMed] [Google Scholar]
  2. Andersen R. A., Asanuma C., Essick G., Siegel R. M. Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J Comp Neurol. 1990 Jun 1;296(1):65–113. doi: 10.1002/cne.902960106. [DOI] [PubMed] [Google Scholar]
  3. Bender D. B. Retinotopic organization of macaque pulvinar. J Neurophysiol. 1981 Sep;46(3):672–693. doi: 10.1152/jn.1981.46.3.672. [DOI] [PubMed] [Google Scholar]
  4. Benevento L. A., Rezak M. The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Macaca mulatta): an autoradiographic study. Brain Res. 1976 May 21;108(1):1–24. doi: 10.1016/0006-8993(76)90160-8. [DOI] [PubMed] [Google Scholar]
  5. Boussaoud D., Desimone R., Ungerleider L. G. Visual topography of area TEO in the macaque. J Comp Neurol. 1991 Apr 22;306(4):554–575. doi: 10.1002/cne.903060403. [DOI] [PubMed] [Google Scholar]
  6. Colby C. L., Duhamel J. R., Goldberg M. E. Ventral intraparietal area of the macaque: anatomic location and visual response properties. J Neurophysiol. 1993 Mar;69(3):902–914. doi: 10.1152/jn.1993.69.3.902. [DOI] [PubMed] [Google Scholar]
  7. Cowan W. M., Gottlieb D. I., Hendrickson A. E., Price J. L., Woolsey T. A. The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res. 1972 Feb 11;37(1):21–51. doi: 10.1016/0006-8993(72)90344-7. [DOI] [PubMed] [Google Scholar]
  8. DeYoe E. A., Felleman D. J., Van Essen D. C., McClendon E. Multiple processing streams in occipitotemporal visual cortex. Nature. 1994 Sep 8;371(6493):151–154. doi: 10.1038/371151a0. [DOI] [PubMed] [Google Scholar]
  9. DeYoe E. A., Van Essen D. C. Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature. 1985 Sep 5;317(6032):58–61. doi: 10.1038/317058a0. [DOI] [PubMed] [Google Scholar]
  10. Desimone R., Ungerleider L. G. Multiple visual areas in the caudal superior temporal sulcus of the macaque. J Comp Neurol. 1986 Jun 8;248(2):164–189. doi: 10.1002/cne.902480203. [DOI] [PubMed] [Google Scholar]
  11. Distler C., Boussaoud D., Desimone R., Ungerleider L. G. Cortical connections of inferior temporal area TEO in macaque monkeys. J Comp Neurol. 1993 Aug 1;334(1):125–150. doi: 10.1002/cne.903340111. [DOI] [PubMed] [Google Scholar]
  12. Felleman D. J., Van Essen D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex. 1991 Jan-Feb;1(1):1–47. doi: 10.1093/cercor/1.1.1-a. [DOI] [PubMed] [Google Scholar]
  13. Fink R. P., Heimer L. Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Res. 1967 Apr;4(4):369–374. doi: 10.1016/0006-8993(67)90166-7. [DOI] [PubMed] [Google Scholar]
  14. Gattass R., Gross C. G., Sandell J. H. Visual topography of V2 in the macaque. J Comp Neurol. 1981 Oct 1;201(4):519–539. doi: 10.1002/cne.902010405. [DOI] [PubMed] [Google Scholar]
  15. Gattass R., Sousa A. P., Gross C. G. Visuotopic organization and extent of V3 and V4 of the macaque. J Neurosci. 1988 Jun;8(6):1831–1845. doi: 10.1523/JNEUROSCI.08-06-01831.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hendry S. H., Yoshioka T. A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science. 1994 Apr 22;264(5158):575–577. doi: 10.1126/science.8160015. [DOI] [PubMed] [Google Scholar]
  17. Lachica E. A., Beck P. D., Casagrande V. A. Parallel pathways in macaque monkey striate cortex: anatomically defined columns in layer III. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3566–3570. doi: 10.1073/pnas.89.8.3566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Livingstone M. S., Hubel D. H. Anatomy and physiology of a color system in the primate visual cortex. J Neurosci. 1984 Jan;4(1):309–356. doi: 10.1523/JNEUROSCI.04-01-00309.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Livingstone M. S., Hubel D. H. Connections between layer 4B of area 17 and the thick cytochrome oxidase stripes of area 18 in the squirrel monkey. J Neurosci. 1987 Nov;7(11):3371–3377. doi: 10.1523/JNEUROSCI.07-11-03371.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Livingstone M. S., Hubel D. H. Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. J Neurosci. 1987 Nov;7(11):3416–3468. doi: 10.1523/JNEUROSCI.07-11-03416.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lund J. S., Yoshioka T., Levitt J. B. Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cereb Cortex. 1993 Mar-Apr;3(2):148–162. doi: 10.1093/cercor/3.2.148. [DOI] [PubMed] [Google Scholar]
  22. Maguire W. M., Baizer J. S. Visuotopic organization of the prelunate gyrus in rhesus monkey. J Neurosci. 1984 Jul;4(7):1690–1704. doi: 10.1523/JNEUROSCI.04-07-01690.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maunsell J. H., van Essen D. C. The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci. 1983 Dec;3(12):2563–2586. doi: 10.1523/JNEUROSCI.03-12-02563.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nakamura H., Gattass R., Desimone R., Ungerleider L. G. The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques. J Neurosci. 1993 Sep;13(9):3681–3691. doi: 10.1523/JNEUROSCI.13-09-03681.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nealey T. A., Maunsell J. H. Magnocellular and parvocellular contributions to the responses of neurons in macaque striate cortex. J Neurosci. 1994 Apr;14(4):2069–2079. doi: 10.1523/JNEUROSCI.14-04-02069.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Newcombe F., Ratcliff G., Damasio H. Dissociable visual and spatial impairments following right posterior cerebral lesions: clinical, neuropsychological and anatomical evidence. Neuropsychologia. 1987;25(1B):149–161. doi: 10.1016/0028-3932(87)90127-8. [DOI] [PubMed] [Google Scholar]
  27. Ogren M. P., Hendrickson A. E. The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey. Brain Res. 1977 Dec 2;137(2):343–350. doi: 10.1016/0006-8993(77)90344-4. [DOI] [PubMed] [Google Scholar]
  28. Perry V. H., Cowey A. Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience. 1984 Aug;12(4):1125–1137. doi: 10.1016/0306-4522(84)90007-1. [DOI] [PubMed] [Google Scholar]
  29. Perry V. H., Oehler R., Cowey A. Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience. 1984 Aug;12(4):1101–1123. doi: 10.1016/0306-4522(84)90006-x. [DOI] [PubMed] [Google Scholar]
  30. Rezak M., Benevento L. A. A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey. Brain Res. 1979 May 5;167(1):19–40. doi: 10.1016/0006-8993(79)90260-9. [DOI] [PubMed] [Google Scholar]
  31. Rockland K. S., Pandya D. N. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 1979 Dec 21;179(1):3–20. doi: 10.1016/0006-8993(79)90485-2. [DOI] [PubMed] [Google Scholar]
  32. Shipp S., Zeki S. Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature. 1985 May 23;315(6017):322–325. doi: 10.1038/315322a0. [DOI] [PubMed] [Google Scholar]
  33. Shipp S., Zeki S. The Organization of Connections between Areas V5 and V1 in Macaque Monkey Visual Cortex. Eur J Neurosci. 1989;1(4):309–332. doi: 10.1111/j.1460-9568.1989.tb00798.x. [DOI] [PubMed] [Google Scholar]
  34. Shipp S., Zeki S. The Organization of Connections between Areas V5 and V2 in Macaque Monkey Visual Cortex. Eur J Neurosci. 1989;1(4):333–354. doi: 10.1111/j.1460-9568.1989.tb00799.x. [DOI] [PubMed] [Google Scholar]
  35. Standage G. P., Benevento L. A. The organization of connections between the pulvinar and visual area MT in the macaque monkey. Brain Res. 1983 Mar 7;262(2):288–294. doi: 10.1016/0006-8993(83)91020-x. [DOI] [PubMed] [Google Scholar]
  36. Tootell R. B., Switkes E., Silverman M. S., Hamilton S. L. Functional anatomy of macaque striate cortex. II. Retinotopic organization. J Neurosci. 1988 May;8(5):1531–1568. doi: 10.1523/JNEUROSCI.08-05-01531.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ungerleider L. G., Desimone R. Cortical connections of visual area MT in the macaque. J Comp Neurol. 1986 Jun 8;248(2):190–222. doi: 10.1002/cne.902480204. [DOI] [PubMed] [Google Scholar]
  38. Ungerleider L. G., Desimone R., Galkin T. W., Mishkin M. Subcortical projections of area MT in the macaque. J Comp Neurol. 1984 Mar 1;223(3):368–386. doi: 10.1002/cne.902230304. [DOI] [PubMed] [Google Scholar]
  39. Ungerleider L. G., Galkin T. W., Mishkin M. Visuotopic organization of projections from striate cortex to inferior and lateral pulvinar in rhesus monkey. J Comp Neurol. 1983 Jun 20;217(2):137–157. doi: 10.1002/cne.902170203. [DOI] [PubMed] [Google Scholar]
  40. Van Essen D. C., Felleman D. J., DeYoe E. A., Olavarria J., Knierim J. Modular and hierarchical organization of extrastriate visual cortex in the macaque monkey. Cold Spring Harb Symp Quant Biol. 1990;55:679–696. doi: 10.1101/sqb.1990.055.01.064. [DOI] [PubMed] [Google Scholar]
  41. Wong-Riley M. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 1979 Jul 27;171(1):11–28. doi: 10.1016/0006-8993(79)90728-5. [DOI] [PubMed] [Google Scholar]
  42. Yoshioka T., Levitt J. B., Lund J. S. Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: anatomy of interlaminar projections. Vis Neurosci. 1994 May-Jun;11(3):467–489. doi: 10.1017/s0952523800002406. [DOI] [PubMed] [Google Scholar]
  43. Zeki S. M. Cortical projections from two prestriate areas in the monkey. Brain Res. 1971 Nov;34(1):19–35. doi: 10.1016/0006-8993(71)90348-9. [DOI] [PubMed] [Google Scholar]
  44. Zeki S., Shipp S. Modular Connections between Areas V2 and V4 of Macaque Monkey Visual Cortex. Eur J Neurosci. 1989;1(5):494–506. doi: 10.1111/j.1460-9568.1989.tb00356.x. [DOI] [PubMed] [Google Scholar]

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