Skip to main content
Human Brain Mapping logoLink to Human Brain Mapping
. 1998 Dec 7;6(4):316–328. doi: 10.1002/(SICI)1097-0193(1998)6:4<316::AID-HBM9>3.0.CO;2-6

A sequence of object‐processing stages revealed by fMRI in the human occipital lobe

Kalanit Grill‐Spector 1, Tammar Kushnir 2, Talma Hendler 2, Shimon Edelman 3, Yacov Itzchak 2, Rafael Malach 1,
PMCID: PMC6873387  PMID: 9704268

Abstract

Functional magnetic resonance imaging was used in combined functional selectivity and retinotopic mapping tests to reveal object‐related visual areas in the human occpital lobe. Subjects were tested with right, left, up, or down hemivisual field stimuli which were composed of images of natural objects (faces, animals, man‐made objects) or highly scrambled (1,024 elements) versions of the same images. In a similar fashion, the horizontal and vertical meridians were mapped to define the borders of these areas. Concurrently, the same cortical sites were tested for their sensitivity to image‐scrambling by varying the number of scrambled picture fragments (from 16–1,024) while controlling for the Fourier power spectrum of the pictures and their order of presentation. Our results reveal a stagewise decrease in retinotopy and an increase in sensitivity to image‐scrambling. Three main distinct foci were found in the human visual object recognition pathway (Ungerleider and Haxby [1994]: Curr Opin Neurobiol 4:157–165): 1) Retinotopic primary areas V1–3 did not exhibit significant reduction in activation to scrambled images. 2) Areas V4v (Sereno et al., [1995]: Science 268:889–893) and V3A (DeYoe et al., [1996]: Proc Natl Acad Sci USA 93:2382–2386; Tootell et al., [1997]: J Neurosci 71:7060–7078) manifested both retinotopy and decreased activation to highly scrambled images. 3) The essentially nonretinotopic lateral occipital complex (LO) (Malach et al., [1995]: Proc Natl Acad Sci USA 92:8135–8139; Tootell et al., [1996]: Trends Neurosci 19:481–489) exhibited the highest sensitivity to image scrambling, and appears to be homologous to macaque the infero‐temporal (IT) cortex (Tanaka [1996]: Curr Opin Neurobiol 523–529). Breaking the images into 64, 256, or 1,024 randomly scrambled blocks reduced activation in LO voxels. However, many LO voxels remained significantly activated by mildly scrambled images (16 blocks). These results suggest the existence of object‐fragment representation in LO. Hum. Brain Mapping 6:316–328, 1998. © 1998 Wiley‐Liss, Inc.

Keywords: object recognition, visual cortex, visual areas, brain mapping, form perception

Full Text

The Full Text of this article is available as a PDF (1,008.2 KB).

References

  1. Allison T, Ginter H, McCarthy G, Nobre AC, Puce A, Luby M, Spencer DD (1994): Face recognition in human extrastriate cortex. J Neurophysiol 71: 821–825. [DOI] [PubMed] [Google Scholar]
  2. Baker JR, Hoppel BE, Stern CE (1993): Dynamic functional imaging of the complete human cortex using gradient‐echo and asymmetric spin‐echo echo planar magnetic resonance imaging. Soc Magn Reson Med Abstr 1400.
  3. Biederman I (1987): Recognition‐by‐components: A theory of human image understanding. Psychol Rev 94: 115–147. [DOI] [PubMed] [Google Scholar]
  4. Boynton GM, Engel SA, Glover GH, Heeger DJ (1996): Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci 16: 4207–4221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cave CB, Kosslyn SM (1993): The role of parts and spatial relations in object identification. Perception 22: 229–248. [DOI] [PubMed] [Google Scholar]
  6. DeYoe EA, Carman GJ, Bandettini P, Glickman S, Wieser J, Cox R, Miller D, Neitz J (1996): Mapping striate and extrastriate visual areas in human cerebral cortex. Proc Natl Acad Sci USA 93: 2382–2386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edelman S (1995): Representation, similarity, and the chorus of prototypes. Minds Machines 5: 45–68. [Google Scholar]
  8. Edelman S (1998): Representation is a representation of similarity. Behav Brain Sci (in press). [DOI] [PubMed]
  9. Engel SA, Rumelhart DE, Wandell BA, Lee AT, Glover GH, Chichilnisky EJ, Shadlen MN (1994): fMRI of human visual cortex. Nature 369: 525. [DOI] [PubMed] [Google Scholar]
  10. Fox PT, Miezin FM, Allman JM, Van Essen DC, Raichle ME (1987): Retinotopic organization of human visual cortex mapped with positron‐emission tomography. J Neurosci 7: 913–922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Friston KJ, Homes A, Worsley K, Frith C, Frackwowiak R (1995): Statistical parametric maps in functional imaging, a general linear approach. Hum Brain Mapp 2: 189–210. [Google Scholar]
  12. Fukushima K (1988): Neocognitron: A hierarchical neural network capable of visual pattern recognition. Neural Networks 1: 119–130. [Google Scholar]
  13. Grill‐Spector K, Kushnir T, Edelman S, Itzchak Y, Malach R (1998): Convergence of visual cues in object related areas of the human occipital lobe. Neuron (in press). [DOI] [PubMed]
  14. Haxby JV, Horwitz B, Ungerleider LG, Maisog JM, Pietrini P, Grady CL (1994): The functional organization of human extrastriate cortex: A PET‐rCBF study of selective attention to faces and locations. J Neurosci 14: 6336–6353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Haxby JV, Ungerleider LG, Horwitz B, Maisog JM, Rapoport SI, Grady CL (1996): Face encoding and recognition in the human brain. Proc Natl Acad Sci USA 93: 922–927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ishai A, Ungerleider LG, Martin A, Maisog JM, Haxby JV (1997): fMRI reveals differential activation in the ventral object recognition pathway during the perception of faces, houses and chairs. Neuroimage 5: 149. [Google Scholar]
  17. Kanwisher N, Chun MM, Ledden P (1996): Functional imaging of human visual recognition. Cogn Brain Res 5: 55–67. [DOI] [PubMed] [Google Scholar]
  18. Kanwisher N, McDermott J, Chun MM (1997a): The fusiform face area: A module in human extra‐striate cortex specialized for face perception. J Neurosci 17: 1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kanwisher N, Woods RP, Iacoboni M, Mazziotta JC (1997b): A locus in human extrastriate cortex for visual shape analysis. J Cogn Neurosci 9: 133–142. [DOI] [PubMed] [Google Scholar]
  20. Kobatake E, Tanaka K (1994): Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. J Neurophysiol 71: 856–867. [DOI] [PubMed] [Google Scholar]
  21. Malach R, Reppas JB, Benson R, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RBH (1995): Objectrelated activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA 92: 8135–8139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Martin A, Wiggs CL, Ungerleider LG, Haxby JV (1996): Neural correlates of category‐specific knowledge. Nature 379: 649–652. [DOI] [PubMed] [Google Scholar]
  23. Puce A, Allison T, Gore JC, McCarthy G (1995): Face‐sensitive regions in human extrastriate cortex studied by functional MRI. J Neurophysiol 74: 1192–1199. [DOI] [PubMed] [Google Scholar]
  24. Reyment R, Joreskog K (1993): Applied Factor Analysis in the Natural Sciences, Cambridge, MA: Cambridge University Press. [Google Scholar]
  25. Schneider W, Noll DC, Cohen JD (1993): Functional topographic mapping of the cortical ribbon in human vision with conventional MRI scanners. Nature 365: 150–153. [DOI] [PubMed] [Google Scholar]
  26. Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995): Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268: 889–893. [DOI] [PubMed] [Google Scholar]
  27. Sergent J, Ohta S, Macdonald B (1992): Functional neuroanatomy of face and object processing. A positron emission tomography study. Brain 115: 15–36. [DOI] [PubMed] [Google Scholar]
  28. Talairach J, Tournoux P (1988): Co‐Planar Stereotaxic Atlas of the Human Brain, New York: Thieme Medical Publishers. [Google Scholar]
  29. Tanaka K (1996): Inferotemporal cortex and object recognition. Annu Rev Neurosci 19: 109–139. [DOI] [PubMed] [Google Scholar]
  30. Tanaka K (1997): Mechanisms of visual object recognition: Monkey and human studies. Curr Opin Neurobiol 523–529. [DOI] [PubMed]
  31. Tootell RBH, Dale AM, Sereno MI, Malach R (1996): New images from human visual cortex. Trends Neurosci 19: 481–489. [DOI] [PubMed] [Google Scholar]
  32. Tootell RBH, Mendola J, Hadjikhani N, Ledden P, Liu A, Reppas J, Sereno M, Kwong K, Dale AM (1997): Functional analysis of V3a and related visual areas in human visual cortex. J Neurosci 71: 7060–7078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ungerleider LG, Haxby JV (1994): What and “where” in the human brain. Curr Opin Neurobiol 4: 157–165. [DOI] [PubMed] [Google Scholar]
  34. Van Essen DC, Drury H (1997): Structural and functional analyses of human cerebral cortex using a surface based atlas. J Neurosci 17: 7079–7102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wachsmuth E, Oram MW, Perrett DI (1994): Recognition of objects and their component parts: Responses of single units in the temporal cortex of the macaque. Cereb Cortex 4: 509–522. [DOI] [PubMed] [Google Scholar]

Articles from Human Brain Mapping are provided here courtesy of Wiley

RESOURCES