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Involvement of striate and extrastriate visual cortical areas in spatial attention

Abstract

We investigated the cortical mechanisms of visual-spatial attention while subjects discriminated patterned targets within distractor arrays. Functional magnetic resonance imaging (fMRI) was used to map the boundaries of retinotopic visual areas and to localize attention-related changes in neural activity within several of those areas, including primary visual (striate) cortex. Event-related potentials (ERPs) and modeling of their neural sources, however, indicated that the initial sensory input to striate cortex at 50–55 milliseconds after the stimulus was not modulated by attention. The earliest facilitation of attended signals was observed in extrastriate visual areas, at 70–75 milliseconds. We hypothesize that the striate cortex modulation found with fMRI may represent a delayed, re-entrant feedback from higher visual areas or a sustained biasing of striate cortical neurons during attention. ERP recordings provide critical temporal information for analyzing the functional neuroanatomy of visual attention.

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Figure 1: Experimental design and attention–related activations.
Figure 2: Retinotopically mapped visual areas and co-localized attentional activations.
Figure 3: Grand-averaged ERP waveforms and scalp topographies.
Figure 4: Dipole modeling of cortical sources of ERPs.

References

  1. LaBerge, D. Attention Processing: The Brain's Art of Mindfulness (Harvard Univ. Press, Cambridge, Massachusetts, 1995).

    Book  Google Scholar 

  2. Luck, S. J., Hillyard, S. A., Mouloua, M. & Hawkins, H. L. Mechanisms of visual-spatial attention: Resource allocation or uncertainty reduction. J. Exp. Psychol. Hum. Percept. Perform. 22, 725–737 (1996).

    CAS  Article  Google Scholar 

  3. Posner, M. I., Snyder, C. R. & Davidson, B. J. Attention and the detection of signals. J. Exp. Psychol. Gen. 109, 160–174 (1980).

    CAS  Article  Google Scholar 

  4. Eriksen, C. W. & St. James, J. D. Visual attention within and around the field of focal attention: A zoom lens model. Percept. Psychophysics 40, 225–240 (1986).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  6. 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).

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  8. 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).

    CAS  Article  Google Scholar 

  9. Colby, C. L. The neuroanatomy and neurophysiology of attention. J. Child Neurol. 6, 90–118 (1991).

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  11. 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).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  13. Mangun, G. R. et al. Covariations in ERP and PET measures of spatial selective attention in human extrastriate visual cortex. Hum. Brain Mapp. 5, 273–279 (1997).

    CAS  Article  Google Scholar 

  14. Woldorff, M. G. et al. Retinotopic organization of the early visual-spatial attention effects as revealed by PET and ERPs. Hum. Brain Mapp. 5, 280–286 (1997).

    CAS  Article  Google Scholar 

  15. Kastner, S., De Weerd, P., Desimone, R. & Ungerleider, L. Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. Science 282, 108– 111 (1998).

    CAS  Article  Google Scholar 

  16. Mangun, G. R., Buonocore, M. H., Girelli, M. & Jha, A. ERP and fMRI measures of visual spatial selective attention. Hum. Brain Mapp. 6, 383–389 (1998).

    CAS  Article  Google Scholar 

  17. Gratton, G. Attention and probability effects in the human occipital cortex: An optical imaging study. Neuroreport 8, 1749– 1753 (1997).

    CAS  Article  Google Scholar 

  18. Motter, B. C. in The Attentive Brain (ed. Parasuraman, R.) 51– 69 (MIT Press, Cambridge, Massachusetts, 1998).

    Google Scholar 

  19. Roelfsema, P. R., Lamme, V. A. & Spekreijse, H. Object-based attention in the primary visual cortex of the macaque monkey. Nature 395, 376– 381 (1997).

    Article  Google Scholar 

  20. Vidyasagar, T. R. Gating of neuronal responses in macaque primary visual cortex by an attentional spotlight. Neuroreport 9, 1947– 1952 (1998).

    CAS  Article  Google Scholar 

  21. Shulman, G. L. et al. Top-down modulation of early sensory cortex. Cereb. Cortex 7, 193–206 (1997).

    CAS  Article  Google Scholar 

  22. Dupont, P. et al. Different perceptual tasks performed with the same visual stimulus attribute activate different regions of the human brain: A positron emission tomography study. Proc. Natl. Acad. Sci. USA 90, 10927–10931 (1993).

    CAS  Article  Google Scholar 

  23. Watanabe, T. et al. Attention-regulated activity in human primary visual cortex. J. Neurophysiol. 79, 2218– 2221 (1998).

    CAS  Article  Google Scholar 

  24. Watanabe, T. et al. Task-dependent influences of attention on the activation of human primary visual cortex. Proc. Natl. Acad. Sci. USA 95, 11489–11492 (1998).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  26. Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional proportional system: An approach to cerebral imaging. (Thieme, New York, 1988).

    Google Scholar 

  27. Bandettini, P. A., Jesmanowicz, A., Wong, E. C. & Hyde, J. S. Processing strategies for time-course data sets in functional MRI of the human brain. Magn. Reson. Med. 30, 161– 173 (1993).

    CAS  Article  Google Scholar 

  28. Buxton, R. & Frank, L. A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation. J. Cereb. Blood Flow Metab. 17, 64–72 (1997).

    CAS  Article  Google Scholar 

  29. Clark, V. P. & Hillyard, S. A. Spatial selective attention affects early extrastriate but not striate components of the visual evoked potential. J. Cogn. Neurosci. 8, 387– 402 (1996).

    CAS  Article  Google Scholar 

  30. Scherg, M. in Auditory Evoked Magnetic Fields and Electric Potentials (eds. Grandori, F., Hoke, M. & Roman, G. L.) 40–69 (Karger, Basel, 1990).

    Google Scholar 

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

    Article  Google Scholar 

  32. Crick, F. Function of the thalamic reticular complex: The searchlight hypothesis. Proc. Natl. Acad. Sci. USA 81, 4586– 4590 (1984).

    CAS  Article  Google Scholar 

  33. Skinner, J. E. & Yingling, C. D. in Attention, Voluntary Contraction and Event-Related Cerebral Potentials. (ed. Desmedt, J. E.) 30–69 (Karger, Basel, 1977).

    Google Scholar 

  34. Aine, C. J., Supek, S. & George, J. S. Temporal dynamics of visual-evoked neuromagnetic sources: Effects of stimulus parameters and selective attention. Int. J. Neurosci. 80, 79–104 (1995).

    CAS  Article  Google Scholar 

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

  36. Heinze, H. J., Luck, S. J., Mangun, G. R. & Hillyard, S. A. Visual event-related potentials index focused attention within bilateral stimulus arrays. I. Evidence for early selection. Electroencephalogr. Clin. Neurophysiol. 75, 511–527 (1990).

    CAS  Article  Google Scholar 

  37. Cox, R. W. AFNI—Software for analysis and visualization of functional magnetic resonance neuroimages. Computers Biomed. Res. 29, 162–173 (1996).

    CAS  Article  Google Scholar 

  38. Anllo-Vento, L., Luck, S. J. & Hillyard, S. A. Spatio-temporal dynamics of attention to color: Evidence from human electrophysiology. Hum. Brain Mapp. 6, 216–238 (1998).

    CAS  Article  Google Scholar 

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Acknowledgements

We thank Matt Marlow, Cecelia Kemper and Carlos Nava for technical assistance. Supported by grants from NIMH (MH25594), ONR (N00014-93-0942), NIH (NS36722), HMRI, and from the Deutsch Forschungsgemeinschaft (HE 1531/3).

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Correspondence to S. A. Hillyard.

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Martínez, A., Anllo-Vento, L., Sereno, M. et al. Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat Neurosci 2, 364–369 (1999). https://doi.org/10.1038/7274

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