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Prefrontal modulation of visual processing in humans

Abstract

Single neuron, evoked potential and metabolic techniques show that attention influences visual processing in extrastriate cortex. We provide anatomical, electrophysiological and behavioral evidence that prefrontal cortex regulates neuronal activity in extrastriate cortex during visual discrimination. Event-related potentials (ERPs) were recorded during a visual detection task in patients with damage in dorsolateral prefrontal cortex. Prefrontal damage reduced neuronal activity in extrastriate cortex of the lesioned hemisphere. These electrophysiological abnormalities, beginning 125 ms after stimulation and lasting for another 500 ms, were accompanied by behavioral deficits in detection ability in the contralesional hemifield. The results provide evidence for intrahemispheric prefrontal modulation of visual processing.

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Figure 1: Visual attention deficits and prefrontal lesions.
Figure 2: Early and late ERPs and voltage maps.
Figure 3: Scalp topography of early and late extrastriate responses.

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References

  1. Hillyard, S. A., Mangun, G. R., Woldorff, M. G. & Luck, S. J. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) 665–681 (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  2. Hillyard, S. A. & Anllo-Vento, L. Event-related brain potentials in the study of visual selective attention. Proc. Natl. Acad. Sci. USA 95, 781–787 (1998).

    Article  CAS  Google Scholar 

  3. Luck, S. J. Multiple mechanisms of visual-spatial attention: recent evidence from human electrophysiology. Behav. Brain Res. 71, 113–123 (1995).

    Article  CAS  Google Scholar 

  4. Müller, M. M., Teder-Salejarvi, W. & Hillyard, S. A. The time course of cortical facilitation during cued shifts of spatial attention. Nat. Neurosci. 1, 631–634 (1998).

    Article  Google Scholar 

  5. Wijers, A. A., Lange, J. J., Mulder, G. & Mulder, L. J. M. An ERP study of visual spatial attention and letter target detection for isoluminant and nonisoluminant stimuli. Psychophysiology 34, 553–565 (1997).

    Article  CAS  Google Scholar 

  6. Mangun, G. R. Neural mechanisms of visual selective attention. Psychophysiology 32, 4–18 (1995).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Posner, M. I. & Dehaene, S. Attentional networks. Trends Neurosci. 17, 75–79 (1994).

    Article  CAS  Google Scholar 

  9. Webster, M. J. & Ungerleider, L. G. in The Attentive Brain (ed. Parasuraman, R.) 19–34 (MIT Press, Cambridge, Massachusetts 1999).

    Google Scholar 

  10. Webster, M. J., Bachevalier, J. & Ungerleider, L. G. Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb. Cortex 5, 470–483 (1994).

    Article  Google Scholar 

  11. Tomita, H., Ohbayashi, M., Nakahara, K., Hasegawa, I. & Miyashita, Y. Top-down signal from prefrontal cortex in executive control of memory retrieval. Nature 401, 699–703 (1999).

    Article  CAS  Google Scholar 

  12. Wilson, F. A. W., Scalaidhe, P. O. & Goldman-Rakic, P. S. Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260, 1955–1958 (1993).

    Article  CAS  Google Scholar 

  13. Rainer, G., Asaad, W. F. & Miller, E. K. Selective representation of relevant information by neurons in the primate prefrontal cortex. Nature 393, 577–579 (1998).

    Article  CAS  Google Scholar 

  14. 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 

  15. Knight, R. T. A distributed cortical network for visual attention. J. Cogn. Neurosci. 9, 75–91 (1997).

    Article  CAS  Google Scholar 

  16. Nielsen-Bohlman, L. C. & Knight, R. T. Prefrontal cortex involvement in visual working memory. Cogn. Brain Res. 8, 299–310, 1999.

    Article  CAS  Google Scholar 

  17. Büchel, C. & Friston, K. J. Modulation of connectivity in visual pathways by attention: Cortical interactions evaluated with structural equation modeling and fMRI. Cereb. Cortex 7, 768–778 (1997).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. Rees, G., Frackowiak, R. & Frith, C. Two modulatory effects of attention that mediate object categorization in human cortex. Science 275, 835–838 (1997).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  21. McIntosh, A. R. et al. Network analysis of cortical visual pathways mapped with PET. J. Neurosci. 14, 655–666 (1994).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. 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 

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

    Article  CAS  Google Scholar 

  25. Heinze, H. J. et al. Combined spatial and temporal imaging of brain activity during visual selective attention in humans. Nature 372, 543–546 (1994).

    Article  CAS  Google Scholar 

  26. Martinez, A. et al. Involvement of striate and extrastriate visual cortices areas in spatial attention. Nat. Neurosci. 2, 364–369 (1999).

    Article  CAS  Google Scholar 

  27. Clark, V. P., Fan, S. & Hillyard, S. A. Identification of early visual evoked potential generators by retinotopic and topographic analyses. Hum. Brain Mapp. 2, 170–187 (1995).

    Article  Google Scholar 

  28. Woldorff, M. G. et al. Retinotopic organization of early visual spatial attention: effects as revealed by PET and ERP data. Hum. Brain Mapp. 5 280–286 (1997).

    Article  CAS  Google Scholar 

  29. Luck, S. J., Chelazzi, L., Hillyard, S. A. & Desimone, R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77, 24–42 (1997).

    Article  CAS  Google Scholar 

  30. Smid, H. G. O. M., Jakob, A. & Heinze, H.-J. An event-related brain potential study of visual selective attention to conjunctions of color and shape. Psychophysiology 36, 264–279 (1999).

    Article  CAS  Google Scholar 

  31. Hansen, J. C. & Hillyard, S. A. Endogenous brain potentials associated with selective auditory attention. Electroencephalogr. Clin. Neurophysiol. 49, 277–290 (1980).

    Article  CAS  Google Scholar 

  32. Karayanidis, F. & Michie, P. T. Evidence of visual processing negativity with attention to orientation and color in central space. Electroencephalogr. Clin. Neurophysiol. 103, 282–297 (1997).

    Article  CAS  Google Scholar 

  33. McCarthy, G. & Wood, C. C. Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. Electroencephalogr. Clin. Neurophysiol. 62, 203–208 (1985).

    Article  CAS  Google Scholar 

  34. Valdes-Sosa, M., Bobes, M. A., Rodríguez, V. & Pinilla, T. Switching attention without shifting the spotlight: object-based attentional modulation of brain potentials. J. Cogn. Neurosci. 10, 137–151 (1998).

    Article  CAS  Google Scholar 

  35. Miller, E. K. The prefrontal cortex: Complex neural properties for complex behavior. Neuron 22, 15–17 (1999).

    Article  CAS  Google Scholar 

  36. Chao, L. L. & Knight, R. T. Contribution of human prefrontal cortex to delay performance. J. Cogn. Neurosci. 10, 167–177 (1998).

    Article  CAS  Google Scholar 

  37. Rosahl, S. K. & Knight, R. T. Role of prefrontal cortex in generation of the contingent negative variation. Cereb. Cortex 2, 123–134 (1995).

    Article  Google Scholar 

  38. Rajkowska, G. & Goldman-Rakic, P. S. Cytoarchitechtonic definition of prefrontal areas in the normal human cortex: I. Remapping of areas 9 and 46 using quantitative criteria. Cereb. Cortex 5, 307–322 (1995).

    Article  CAS  Google Scholar 

  39. Rajkowska, G. & Goldman-Rakic, P. S. Cytoarchitechtonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach coordinate system. Cereb. Cortex 5, 323–337 (1995).

    Article  CAS  Google Scholar 

  40. 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).

    Article  CAS  Google Scholar 

  41. Knight, R. T. Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr. Clin. Neurophysiol. 59, 9–20 (1984).

    Article  CAS  Google Scholar 

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Acknowledgements

Supported by Fundación Complutense del Amo, Comunidad de Madrid grant 08.5/0012/98 and NINDS grant NS21135. We thank Clay C. Clayworth for technical support. An earlier version of this work was presented at the 39th Meeting of the Society for Psychophysiological Research (Granada 1999).

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Correspondence to Robert T. Knight.

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Barceló, F., Suwazono, S. & Knight, R. Prefrontal modulation of visual processing in humans. Nat Neurosci 3, 399–403 (2000). https://doi.org/10.1038/73975

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