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Voluntary orienting is dissociated from target detection in human posterior parietal cortex

Nature Neurosciencevolume 3pages292297 (2000) | Download Citation

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  • An Erratum to this article was published on 01 May 2000

Abstract

Human ability to attend to visual stimuli based on their spatial locations requires the parietal cortex. One hypothesis maintains that parietal cortex controls the voluntary orienting of attention toward a location of interest. Another hypothesis emphasizes its role in reorienting attention toward visual targets appearing at unattended locations. Here, using event-related functional magnetic resonance (ER-fMRI), we show that distinct parietal regions mediated these different attentional processes. Cortical activation occurred primarily in the intraparietal sulcus when a location was attended before visual-target presentation, but in the right temporoparietal junction when the target was detected, particularly at an unattended location.

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Notes

  1. 1.

    Editorial Correction:

    The printed version of this article contained an error. Because of a technical problem, some of the numbers in Table 1 were printed in the wrong columns. The full-text web version of this table is now correct. We regret the error.

References

  1. 1

    Mesulam, M. M. A cortical network for directed attention and unilateral neglect. Ann. Neurol. 10, 309–315 (1981).

  2. 2

    Heilman, K. M., Watson, R. T. & Valenstein, E. in Clinical Neuropsychology (eds. Heilman, K. M. & Valenstein, E.) 243–293 (Oxford, New York, 1985).

  3. 3

    Halligan, P. W. & Marshall, J. C. Toward a principled explanation of unilateral neglect. Special Issue: The cognitive neuropsychology of attention. Cognit. Neuropsychol. 11, 167–206 (1994).

  4. 4

    Posner, M. I., Walker, J. A., Friedrich, F. J. & Rafal, R. D. Effects of parietal injury on covert orienting of attention. J. Neurosci. 4, 1863–1874 ( 1984).

  5. 5

    Morrow, L. A. & Ratcliff, G. The disengagement of covert attention and the neglect syndrome. Psychobiology 16, 261–269 (1988).

  6. 6

    Di Pellegrino, G. Clock-drawing in a case of left visuospatial neglect: a deficit of disengagement? Neuropsychologia 33, 353– 358 (1995).

  7. 7

    Friedrich, F. J., Egly, R., Rafal, R. D. & Beck, D. Spatial attention deficits in humans: a comparison of superior parietal and temporo-parietal junction lesions. Neuropsychology 12, 193 –207 (1998).

  8. 8

    Bushnell, M. C., Goldberg, M. E. & Robinson, D. L. Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective attention. J. Neurophysiol. 46, 755– 772 (1981).

  9. 9

    Colby, C. L., Duhamel, J. R. & Goldberg, M. E. Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J. Neurophysiol. 76, 2841–2852 ( 1996).

  10. 10

    Snyder, L. H., Batista, A. P. & Andersen, R. A. Coding of intention in the posterior parietal cortex . Nature 386, 167–170 (1997).

  11. 11

    Gottlieb, J. P., Kusunoki, M. & Goldberg, M. E. The representation of visual salience in monkey parietal cortex. Nature 391, 481– 484 (1998).

  12. 12

    Corbetta, M., Miezin, F. M., Shulman, G. L. & Petersen, S. E. A PET study of visuospatial attention. J. Neurosci. 13, 1202–1226 (1993).

  13. 13

    Nobre, A. C. et al. Functional localization of the system for visuospatial attention using positron emission tomography. Brain 120, 515–533 (1997).

  14. 14

    Vandenberghe, R. et al. The influence of stimulus location on the brain activation pattern in detection and orientation discrimination-a PET study of visual attention. Brain 119, 1263– 1276 (1996).

  15. 15

    Gitelman, D. R. et al. Functional imaging of human right hemispheric activation for exploratory movements. Ann. Neurol. 39, 174–179 (1996).

  16. 16

    Corbetta, M. et al. A common network of functional areas for attention and eye movements. Neuron 21, 761– 773 (1998).

  17. 17

    Shulman, G. L. et al. Areas involved in encoding and applying directional expectations to moving objects. J. Neurosci. 19, 9480 –9496 (1999).

  18. 18

    Zarahn, E., Aguirre, G. & D'Esposito, M. A trial-based experimental design for fMRI. Neuroimage 6, 122–138 ( 1997).

  19. 19

    Friston, K. J., Josephs, O., Rees, G. & Turner, R. Nonlinear event-related responses in fMRI. Magn. Reson. Med. 39, 41–52 (1998).

  20. 20

    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).

  21. 21

    Chawla, D., Reese, G. & Friston, K. J. The physiological basis of attentional modulations in visual areas. Nat. Neurosci. 2, 671– 676 (1999).

  22. 22

    Dupont, P. et al. The kinetic occipital region in human visual cortex. Cereb. Cortex 7, 283–292 (1997).

  23. 23

    Mendola, J. D., Dale, A. M., Fischl, B., Liu, A. K. & Tootell, R. B. The representation of illusory and real contours in human cortical visual areas revealed by functional magnetic resonance imaging . J. Neurosci. 19, 8560– 8572 (1999).

  24. 24

    Watson, J. D. et al. Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb. Cortex 3, 79–94 ( 1993).

  25. 25

    Tootell, R. B. H. et al. Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J. Neurosci. 15, 3215–3230 (1995).

  26. 26

    Tootell, R. B. H. et al. The retinotopy of visual spatial attention. Neuron 21, 1409–1422 ( 1998).

  27. 27

    Posner, M. I. Orienting of attention. Q. J. Exp. Psychol. 32, 3–25 (1980).

  28. 28

    Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193– 222 (1995).

  29. 29

    Le, T. H., Pardo, J. V. & Hu, X. 4T-fMRI study of nonspatial shifting of selective attention: cerebellar and parietal contributions. J. Neurophysiol. 79, 1535–1548 (1998).

  30. 30

    Lumer, E. D., Friston, K. J. & Rees, G. Neural correlates of perceptual rivalry in the human brain. Science 280, 1930– 1934 (1998).

  31. 31

    Colby, C. L., Gattass, R., Olson, C. R. & Gross, C. G. Topographic organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. J. Comp. Neurol. 238, 1257–1299 (1988).

  32. 32

    Gnadt, J. W. & Andersen, R. A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Brain Res. 70, 216–220 ( 1988).

  33. 33

    Culham, J. C. et al. Cortical fMRI activation produced by attentive tracking of moving targets. J. Neurophysiol. 80, 2657 –2670 (1998).

  34. 34

    Courtney, S. M., Ungerleider, L. G., Keil, K. & Haxby, J. V. Transient and sustained activity in a distributed neural system for human working memory. Nature 386, 608– 611 (1997).

  35. 35

    Cohen, J. D. et al. Temporal dynamics of brain activation during a working memory task. Nature 386, 604–607 (1997).

  36. 36

    Mesulam, M.-M Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann. Neurol. 28, 597 –613 (1990).

  37. 37

    Knight, R. T. & Scabini, D. Anatomic bases of event-related potentials and their relationship to novelty detection in humans. J. Clin. Neurophysiol. 15, 3–13 (1998).

  38. 38

    Pardo, J. V., Fox, P. T. & Raichle, M. E. Localization of a human system for sustained attention by positron emission tomography. Nature 349, 61–64 (1991).

  39. 39

    Foote, S. L. & Morrison, J. H. Extrathalamic modulation of cortical function. Annu. Rev. of Neurosci. 10, 67–96 (1987).

  40. 40

    Robertson, I. H., Mattingley, J. B., Rorden, C. & Driver, J. Phasic alerting of neglect patients overcomes their spatial deficit in visual awareness. Nature 395, 169– 172 (1998).

  41. 41

    Parasuraman, R., Warm, J. S. & See, J. E. in The Attentive Brain (ed. Parasuraman, R.) 221–256 (MIT Press, Cambridge, Massachusetts, 1998).

  42. 42

    Weinberg, J. et al. Visual scanning training effects on reading-related tasks in acquired brain-damage. Arch. Phys. Med. Rehabil. 58, 479–486 (1977).

  43. 43

    Antonucci, G. et al. Effectiveness of neglect rehabilitation in a randomized group study. J. Clin. Exp. Neuropsychol. 17, 383 –389 (1995).

  44. 44

    Raczkowski, D., Kalat, J. W. & Nebes, R. Reliability and validity of some handedness questionnaire items. Neuropsychologia 12, 43– 47 (1974).

  45. 45

    Braver, T. S. et al. A parametric study of prefrontal cortex involvement in human working memory. Neuroimage 5, 49– 62 (1997).

  46. 46

    Worsley, K. J. et al. A unified statistical approach for detemining significant signals in images of cerebral activation. Hum. Brain Mapp. 4, 58–73 (1995).

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Acknowledgements

This research was supported by NIH EY00379 and EY12148 (M.C.). We thank Thomas Conturo, Avi Snyder and Erbil Akbudak for technical support.

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Affiliations

  1. Department of Neurology and Neurological Surgery, Washington University School of Medicine, 4525 Scott Avenue, St. Louis, 63110, Missouri, USA

    • Maurizio Corbetta
    • , J. Michelle Kincade
    •  & Gordon L. Shulman
  2. Mallinckrodt Institute of Radiology, Washington University School of Medicine, 4525 Scott Avenue, St. Louis , 63110, Missouri, USA

    • Maurizio Corbetta
    • , John M. Ollinger
    •  & Marc P. McAvoy
  3. Department of Anatomy and Neurobiology, Washington University School of Medicine, 4525 Scott Avenue, St. Louis, 63110, Missouri, USA

    • Maurizio Corbetta
  4. Department of Psychology, Washington University School of Medicine, 4525 Scott Avenue, St. Louis, 63110, Missouri, USA

    • J. Michelle Kincade

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Correspondence to Maurizio Corbetta.

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https://doi.org/10.1038/73009

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