Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1998 Dec 7;265(1412):2327–2332. doi: 10.1098/rspb.1998.0579

The theory of multistage integration in the visual brain.

A Bartels 1, S Zeki 1
PMCID: PMC1689532  PMID: 9881478

Abstract

The theory of multistage integration is based on evidence that the visual brain consists of several parallel multistage processing systems, each specialized for a given attribute such as colour or motion. Each stage of a given system processes information at a distinct level of complexity. Our theory supposes that activity at any stage of a given multistage processing system is perceptually explicit--that is to say, it requires no further processing to generate a conscious experience. This activity can be integrated, or bound, with the perceptually explicit activity at any given stage of another or the same multistage processing system. Such binding is therefore not a process that generates a conscious experience, but rather one that brings different conscious experiences together. Many perceptual advantages result from such a flexible and dynamic integrative system. Conversely, there would be disadvantages to limiting perception and binding to hypothetical 'terminal' stages of such processing systems or to hypothetical 'integrator' areas. Although we formulate our hypothesis in terms of the visual brain, we believe it might form a general principle of brain functioning.

Full Text

The Full Text of this article is available as a PDF (122.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allman J. M., Kaas J. H. The organization of the second visual area (V II) in the owl monkey: a second order transformation of the visual hemifield. Brain Res. 1974 Aug 16;76(2):247–265. doi: 10.1016/0006-8993(74)90458-2. [DOI] [PubMed] [Google Scholar]
  2. Barbur J. L., Watson J. D., Frackowiak R. S., Zeki S. Conscious visual perception without V1. Brain. 1993 Dec;116(Pt 6):1293–1302. doi: 10.1093/brain/116.6.1293. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Botez M. I., Serbănescu T. Course and outcome of visual static agnosia. J Neurol Sci. 1967 Mar-Apr;4(2):289–297. doi: 10.1016/0022-510x(67)90107-4. [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. Cragg B. G. The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. Vision Res. 1969 Jul;9(7):733–747. doi: 10.1016/0042-6989(69)90011-x. [DOI] [PubMed] [Google Scholar]
  7. DANIEL P. M., WHITTERIDGE D. The representation of the visual field on the cerebral cortex in monkeys. J Physiol. 1961 Dec;159:203–221. doi: 10.1113/jphysiol.1961.sp006803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Essen D. C., Zeki S. M. The topographic organization of rhesus monkey prestriate cortex. J Physiol. 1978 Apr;277:193–226. doi: 10.1113/jphysiol.1978.sp012269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Gegenfurtner K. R., Kiper D. C., Fenstemaker S. B. Processing of color, form, and motion in macaque area V2. Vis Neurosci. 1996 Jan-Feb;13(1):161–172. doi: 10.1017/s0952523800007203. [DOI] [PubMed] [Google Scholar]
  12. Girard P., Salin P. A., Bullier J. Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. J Neurophysiol. 1992 Jun;67(6):1437–1446. doi: 10.1152/jn.1992.67.6.1437. [DOI] [PubMed] [Google Scholar]
  13. Hadjikhani N., Liu A. K., Dale A. M., Cavanagh P., Tootell R. B. Retinotopy and color sensitivity in human visual cortical area V8. Nat Neurosci. 1998 Jul;1(3):235–241. doi: 10.1038/681. [DOI] [PubMed] [Google Scholar]
  14. Hess R. H., Baker C. L., Jr, Zihl J. The "motion-blind" patient: low-level spatial and temporal filters. J Neurosci. 1989 May;9(5):1628–1640. doi: 10.1523/JNEUROSCI.09-05-01628.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Humphrey G. K., Goodale M. A., Corbetta M., Aglioti S. The McCollough effect reveals orientation discrimination in a case of cortical blindness. Curr Biol. 1995 May 1;5(5):545–551. doi: 10.1016/s0960-9822(95)00107-2. [DOI] [PubMed] [Google Scholar]
  16. Kennard C., Lawden M., Morland A. B., Ruddock K. H. Colour identification and colour constancy are impaired in a patient with incomplete achromatopsia associated with prestriate cortical lesions. Proc Biol Sci. 1995 May 22;260(1358):169–175. doi: 10.1098/rspb.1995.0076. [DOI] [PubMed] [Google Scholar]
  17. Kertesz A. Visual agnosia: the dual deficit of perception and recognition. Cortex. 1979 Sep;15(3):403–419. doi: 10.1016/s0010-9452(79)80067-2. [DOI] [PubMed] [Google Scholar]
  18. Lennie P., Krauskopf J., Sclar G. Chromatic mechanisms in striate cortex of macaque. J Neurosci. 1990 Feb;10(2):649–669. doi: 10.1523/JNEUROSCI.10-02-00649.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Leventhal A. G., Thompson K. G., Liu D., Zhou Y., Ault S. J. Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex. J Neurosci. 1995 Mar;15(3 Pt 1):1808–1818. doi: 10.1523/JNEUROSCI.15-03-01808.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Levitt J. B., Yoshioka T., Lund J. S. Intrinsic cortical connections in macaque visual area V2: evidence for interaction between different functional streams. J Comp Neurol. 1994 Apr 22;342(4):551–570. doi: 10.1002/cne.903420405. [DOI] [PubMed] [Google Scholar]
  21. Livingstone M. S., Hubel D. H. Specificity of intrinsic connections in primate primary visual cortex. J Neurosci. 1984 Nov;4(11):2830–2835. doi: 10.1523/JNEUROSCI.04-11-02830.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Livingstone M., Hubel D. Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science. 1988 May 6;240(4853):740–749. doi: 10.1126/science.3283936. [DOI] [PubMed] [Google Scholar]
  23. Mountcastle V. B. The parietal system and some higher brain functions. Cereb Cortex. 1995 Sep-Oct;5(5):377–390. doi: 10.1093/cercor/5.5.377. [DOI] [PubMed] [Google Scholar]
  24. Moutoussis K., Zeki S. Functional segregation and temporal hierarchy of the visual perceptive systems. Proc Biol Sci. 1997 Oct 22;264(1387):1407–1414. doi: 10.1098/rspb.1997.0196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Paulson H. L., Galetta S. L., Grossman M., Alavi A. Hemiachromatopsia of unilateral occipitotemporal infarcts. Am J Ophthalmol. 1994 Oct 15;118(4):518–523. doi: 10.1016/s0002-9394(14)75806-4. [DOI] [PubMed] [Google Scholar]
  27. Regan D., Giaschi D., Sharpe J. A., Hong X. H. Visual processing of motion-defined form: selective failure in patients with parietotemporal lesions. J Neurosci. 1992 Jun;12(6):2198–2210. doi: 10.1523/JNEUROSCI.12-06-02198.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rockland K. S. A reticular pattern of intrinsic connections in primate area V2 (area 18). J Comp Neurol. 1985 May 22;235(4):467–478. doi: 10.1002/cne.902350405. [DOI] [PubMed] [Google Scholar]
  29. Rodman H. R., Albright T. D. Single-unit analysis of pattern-motion selective properties in the middle temporal visual area (MT). Exp Brain Res. 1989;75(1):53–64. doi: 10.1007/BF00248530. [DOI] [PubMed] [Google Scholar]
  30. Sakai K., Watanabe E., Onodera Y., Uchida I., Kato H., Yamamoto E., Koizumi H., Miyashita Y. Functional mapping of the human colour centre with echo-planar magnetic resonance imaging. Proc Biol Sci. 1995 Jul 22;261(1360):89–98. doi: 10.1098/rspb.1995.0121. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. 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]
  34. Shipp S., de Jong B. M., Zihl J., Frackowiak R. S., Zeki S. The brain activity related to residual motion vision in a patient with bilateral lesions of V5. Brain. 1994 Oct;117(Pt 5):1023–1038. doi: 10.1093/brain/117.5.1023. [DOI] [PubMed] [Google Scholar]
  35. Tootell R. B., Reppas J. B., Dale A. M., Look R. B., Sereno M. I., Malach R., Brady T. J., Rosen B. R. Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature. 1995 May 11;375(6527):139–141. doi: 10.1038/375139a0. [DOI] [PubMed] [Google Scholar]
  36. Vaina L. M. Functional segregation of color and motion processing in the human visual cortex: clinical evidence. Cereb Cortex. 1994 Sep-Oct;4(5):555–572. doi: 10.1093/cercor/4.5.555. [DOI] [PubMed] [Google Scholar]
  37. Weiskrantz L., Barbur J. L., Sahraie A. Parameters affecting conscious versus unconscious visual discrimination with damage to the visual cortex (V1). Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):6122–6126. doi: 10.1073/pnas.92.13.6122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zeki S. M. Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J Physiol. 1974 Feb;236(3):549–573. doi: 10.1113/jphysiol.1974.sp010452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zeki S. M. Functional specialisation in the visual cortex of the rhesus monkey. Nature. 1978 Aug 3;274(5670):423–428. doi: 10.1038/274423a0. [DOI] [PubMed] [Google Scholar]
  40. Zeki S. M. Representation of central visual fields in prestriate cortex of monkey. Brain Res. 1969 Jul;14(2):271–291. doi: 10.1016/0006-8993(69)90110-3. [DOI] [PubMed] [Google Scholar]
  41. Zeki S. A century of cerebral achromatopsia. Brain. 1990 Dec;113(Pt 6):1721–1777. doi: 10.1093/brain/113.6.1721. [DOI] [PubMed] [Google Scholar]
  42. Zeki S., Bartels A. The asynchrony of consciousness. Proc Biol Sci. 1998 Aug 22;265(1405):1583–1585. doi: 10.1098/rspb.1998.0475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zeki S. Cerebral akinetopsia (visual motion blindness). A review. Brain. 1991 Apr;114(Pt 2):811–824. doi: 10.1093/brain/114.2.811. [DOI] [PubMed] [Google Scholar]
  44. Zeki S. Colour coding in the cerebral cortex: the reaction of cells in monkey visual cortex to wavelengths and colours. Neuroscience. 1983 Aug;9(4):741–765. doi: 10.1016/0306-4522(83)90265-8. [DOI] [PubMed] [Google Scholar]
  45. Zeki S. Colour coding in the cerebral cortex: the responses of wavelength-selective and colour-coded cells in monkey visual cortex to changes in wavelength composition. Neuroscience. 1983 Aug;9(4):767–781. doi: 10.1016/0306-4522(83)90266-x. [DOI] [PubMed] [Google Scholar]
  46. Zeki S., Ffytche D. H. The Riddoch syndrome: insights into the neurobiology of conscious vision. Brain. 1998 Jan;121(Pt 1):25–45. doi: 10.1093/brain/121.1.25. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. Zeki S., Watson J. D., Frackowiak R. S. Going beyond the information given: the relation of illusory visual motion to brain activity. Proc Biol Sci. 1993 Jun 22;252(1335):215–222. doi: 10.1098/rspb.1993.0068. [DOI] [PubMed] [Google Scholar]
  49. ffytche D. H., Guy C. N., Zeki S. The parallel visual motion inputs into areas V1 and V5 of human cerebral cortex. Brain. 1995 Dec;118(Pt 6):1375–1394. doi: 10.1093/brain/118.6.1375. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES