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Two hierarchically organized neural systems for object information in human visual cortex

Abstract

The primate visual system is broadly organized into two segregated processing pathways, a ventral stream for object vision and a dorsal stream for space vision. Here, evidence from functional brain imaging in humans demonstrates that object representations are not confined to the ventral pathway, but can also be found in several areas along the dorsal pathway. In both streams, areas at intermediate processing stages in extrastriate cortex (V4, V3A, MT and V7) showed object-selective but viewpoint- and size-specific responses. In contrast, higher-order areas in lateral occipital and posterior parietal cortex (LOC, IPS1 and IPS2) responded selectively to objects independent of image transformations. Contrary to the two-pathways hypothesis, our findings indicate that basic object information related to shape, size and viewpoint may be represented similarly in two parallel and hierarchically organized neural systems in the ventral and dorsal visual pathways.

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Figure 1: Experimental design.
Figure 2: Time courses of fMRI signals in V1, LOC and IPS1–4 from the 2D-object experiment.
Figure 3: Mean signal changes in V1, LOC and IPS1–4.
Figure 4: Adaptation index.
Figure 5: Mean signal changes in V1, LOC and IPS1–4.

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References

  1. Ungerleider, L.G. & Mishkin, M. Two cortical visual systems. In Analysis of Visual Behavior (eds. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W.) 549–586 (MIT Press, Cambridge, Massachusetts, USA, 1982).

    Google Scholar 

  2. Goodale, M.A. & Milner, A.D. Separate visual pathways for perception and action. Trends Neurosci. 15, 20–25 (1992).

    Article  CAS  Google Scholar 

  3. Malach, R. et al. Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc. Natl. Acad. Sci. USA 92, 8135–8139 (1995).

    Article  CAS  Google Scholar 

  4. Grill-Spector, K. et al. Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24, 187–203 (1999).

    Article  CAS  Google Scholar 

  5. Kourtzi, Z. & Kanwisher, N. Representation of perceived object shape by the human lateral occipital complex. Science 293, 1506–1509 (2001).

    Article  CAS  Google Scholar 

  6. Grill-Spector, K., Kushnir, T., Edelman, S., Itzchak, Y. & Malach, R. Cue-invariant activation in object-related areas of the human occipital lobe. Neuron 21, 191–202 (1998).

    Article  CAS  Google Scholar 

  7. Kourtzi, Z. & Kanwisher, N. Cortical regions involved in perceiving object shape. J. Neurosci. 20, 3310–3318 (2000).

    Article  CAS  Google Scholar 

  8. Vuilleumier, P., Henson, R.N., Driver, J. & Dolan, R.J. Multiple levels of visual object constancy revealed by event-related fMRI of repetition priming. Nat. Neurosci. 5, 491–499 (2002).

    Article  CAS  Google Scholar 

  9. James, T.W., Humphrey, G.K., Gati, J.S., Menon, R.S. & Goodale, M.A. Differential effects of viewpoint on object-driven activation in dorsal and ventral streams. Neuron 35, 793–801 (2002).

    Article  CAS  Google Scholar 

  10. Sawamura, H., Georgieva, S., Vogels, R., Vanduffel, W. & Orban, G.A. Using functional magnetic resonance imaging to assess adaptation and size invariance of shape processing by humans and monkeys. J. Neurosci. 25, 4294–4306 (2005).

    Article  CAS  Google Scholar 

  11. Gross, C.G., Rocha-Miranda, C.E. & Bender, D.B. Visual properties of neurons in inferotemporal cortex of the macaque. J. Neurophysiol. 35, 96–111 (1972).

    Article  CAS  Google Scholar 

  12. Desimone, R., Albright, T.D., Gross, C.G. & Bruce, C. Stimulus-selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051–2062 (1984).

    Article  CAS  Google Scholar 

  13. Logothetis, N.K. & Sheinberg, D.L. Visual object recognition. Annu. Rev. Neurosci. 19, 577–621 (1996).

    Article  CAS  Google Scholar 

  14. Booth, M.C. & Rolls, E.T. View-invariant representations of familiar objects by neurons in the inferior temporal visual cortex. Cereb. Cortex 8, 510–523 (1998).

    Article  CAS  Google Scholar 

  15. Murata, A., Gallese, V., Luppino, G., Kaseda, M. & Sakata, H. Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. J. Neurophysiol. 83, 2580–2601 (2000).

    Article  CAS  Google Scholar 

  16. Sakata, H. The role of the parietal cortex in grasping. Adv. Neurol. 93, 121–139 (2003).

    PubMed  Google Scholar 

  17. Sereno, A.B. & Maunsell, J.H. Shape selectivity in primate lateral intraparietal cortex. Nature 395, 500–503 (1998).

    Article  CAS  Google Scholar 

  18. Sereno, M.E., Trinath, T., Augath, M. & Logothetis, N.K. Three-dimensional shape representation in monkey cortex. Neuron 33, 635–652 (2002).

    Article  CAS  Google Scholar 

  19. Lehky, S.R. & Sereno, A.B. Comparison of shape encoding in primate dorsal and ventral visual pathways. J. Neurophysiol. 97, 307–319 (2007).

    Article  Google Scholar 

  20. Kourtzi, Z., Bulthoff, H.H., Erb, M. & Grodd, W. Object-selective responses in the human motion area MT/MST. Nat. Neurosci. 5, 17–18 (2002).

    Article  CAS  Google Scholar 

  21. Grill-Spector, K. & Malach, R. The human visual cortex. Annu. Rev. Neurosci. 27, 649–677 (2004).

    Article  CAS  Google Scholar 

  22. Sereno, M.I. et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889–893 (1995).

    Article  CAS  Google Scholar 

  23. Engel, S.A., Glover, G.H. & Wandell, B.A. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex 7, 181–192 (1997).

    Article  CAS  Google Scholar 

  24. Swisher, J.D., Halko, M.A., Merabet, L.B., McMains, S.A. & Somers, D.C. Visual topography of human intraparietal sulcus. J. Neurosci. 27, 5326–5337 (2007).

    Article  CAS  Google Scholar 

  25. Huk, A.C., Dougherty, R.F. & Heeger, D.J. Retinotopy and functional subdivision of human areas MT and MST. J. Neurosci. 22, 7195–7205 (2002).

    Article  CAS  Google Scholar 

  26. Sereno, M.I., Pitzalis, S. & Martinez, A. Mapping of contralateral space in retinotopic coordinates by a parietal cortical area in humans. Science 294, 1350–1354 (2001).

    Article  CAS  Google Scholar 

  27. Schluppeck, D., Glimcher, P.W. & Heeger, D.J. Topographic organization for delayed saccades in human posterior parietal cortex. J. Neurophysiol. 94, 1372–1384 (2005).

    Article  Google Scholar 

  28. Kastner, S. et al. Topographic maps in human frontal cortex revealed in memory-guided saccade and spatial working-memory tasks. J. Neurophysiol. 97, 3494–3507 (2007).

    Article  Google Scholar 

  29. Silver, M.A., Ress, D. & Heeger, D.J. Topographic maps of visual spatial attention in human parietal cortex. J. Neurophysiol. 94, 1358–1371 (2005).

    Article  Google Scholar 

  30. Culham, J.C., Cavina-Pratesi, C. & Singhal, A. The role of parietal cortex in visuomotor control: what have we learned from neuroimaging? Neuropsychologia 44, 2668–2684 (2006).

    Article  Google Scholar 

  31. Chao, L.L. & Martin, A. Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12, 478–484 (2000).

    Article  CAS  Google Scholar 

  32. Sakata, H. et al. Neural coding of 3D features of objects for hand action in the parietal cortex of the monkey. Phil. Trans. R. Soc. Lond. B 353, 1363–1373 (1998).

    Article  CAS  Google Scholar 

  33. Kanwisher, N., Chun, M.M., McDermott, J. & Ledden, P.J. Functional imaging of human visual recognition. Brain Res. Cogn. Brain Res. 5, 55–67 (1996).

    Article  CAS  Google Scholar 

  34. Kourtzi, Z., Erb, M., Grodd, W. & Bulthoff, H.H. Representation of the perceived 3-D object shape in the human lateral occipital complex. Cereb. Cortex 13, 911–920 (2003).

    Article  Google Scholar 

  35. Grill-Spector, K. The neural basis of object perception. Curr. Opin. Neurobiol. 13, 159–166 (2003).

    Article  CAS  Google Scholar 

  36. Corbetta, M. Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? Proc. Natl. Acad. Sci. USA 95, 831–838 (1998).

    Article  CAS  Google Scholar 

  37. Kastner, S., Pinsk, M.A., De Weerd, P., Desimone, R. & Ungerleider, L.G. Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22, 751–761 (1999).

    Article  CAS  Google Scholar 

  38. Colby, C.L. & Goldberg, M.E. Space and attention in parietal cortex. Annu. Rev. Neurosci. 22, 319–349 (1999).

    Article  CAS  Google Scholar 

  39. O'Connor, D.H., Fukui, M.M., Pinsk, M.A. & Kastner, S. Attention modulates responses in the human lateral geniculate nucleus. Nat. Neurosci. 5, 1203–1209 (2002).

    Article  CAS  Google Scholar 

  40. Riesenhuber, M. & Poggio, T. Neural mechanisms of object recognition. Curr. Opin. Neurobiol. 12, 162–168 (2002).

    Article  CAS  Google Scholar 

  41. Desimone, R., Schein, S.J., Moran, J. & Ungerleider, L.G. Contour, color and shape analysis beyond the striate cortex. Vision Res. 25, 441–452 (1985).

    Article  CAS  Google Scholar 

  42. Gallant, J.L., Connor, C.E., Rakshit, S., Lewis, J.W. & Van Essen, D.C. Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey. J. Neurophysiol. 76, 2718–2739 (1996).

    Article  CAS  Google Scholar 

  43. Pasupathy, A. & Connor, C.E. Population coding of shape in area V4. Nat. Neurosci. 5, 1332–1338 (2002).

    Article  CAS  Google Scholar 

  44. Andersen, R.A. Multimodal integration for the representation of space in the posterior parietal cortex. Phil. Trans. R. Soc. Lond. B 352, 1421–1428 (1997).

    Article  CAS  Google Scholar 

  45. Nakamura, H. et al. From three-dimensional space vision to prehensile hand movements: the lateral intraparietal area links the area V3A and the anterior intraparietal area in macaques. J. Neurosci. 21, 8174–8187 (2001).

    Article  CAS  Google Scholar 

  46. Craighero, L., Fadiga, L., Umilta, C.A. & Rizzolatti, G. Evidence for visuomotor priming effect. Neuroreport 8, 347–349 (1996).

    Article  CAS  Google Scholar 

  47. Rao, S.C., Rainer, G. & Miller, E.K. Integration of what and where in the primate prefrontal cortex. Science 276, 821–824 (1997).

    Article  CAS  Google Scholar 

  48. Brainard, D.H. The Psychophysics Toolbox. Spat Vis 10, 433–436 (1997).

    Article  CAS  Google Scholar 

  49. Pelli, D.G. The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10, 437–442 (1997).

    Article  CAS  Google Scholar 

  50. Friston, K.J., Frith, C.D., Turner, R. & Frackowiak, R.S. Characterizing evoked hemodynamics with fMRI. Neuroimage 2, 157–165 (1995).

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by grants from the US National Institutes of Health (RO1 MH64043, RO1 EY017699, P50 MH-62196) to S.K. and a grant from the German Academic Exchange Service to C.S.K. We thank M. Graziano and A. Treisman for comments on an earlier draft and members of the Kastner lab for discussions and help in scanning experiments.

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Authors

Contributions

C.S.K. and S.K. designed the experiments; C.S.K. acquired and analyzed the data; C.S.K. and S.K. wrote the manuscript.

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Correspondence to Christina S Konen.

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Supplementary Figures 1–6, Supplementary Table 1, Supplementary Methods (PDF 832 kb)

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Konen, C., Kastner, S. Two hierarchically organized neural systems for object information in human visual cortex. Nat Neurosci 11, 224–231 (2008). https://doi.org/10.1038/nn2036

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