Abstract
Selective visual attention involves dynamic interplay between attentional control systems and sensory brain structures. We used event-related functional magnetic resonance imaging (fMRI) during a cued spatial-attention task to dissociate brain activity related to attentional control from that related to selective processing of target stimuli. Distinct networks were engaged by attention-directing cues versus subsequent targets. Superior frontal, inferior parietal and superior temporal cortex were selectively activated by cues, indicating that these structures are part of a network for voluntary attentional control. This control biased activity in multiple visual cortical areas, resulting in selective sensory processing of relevant visual targets.
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References
Pashler, H. The Psychology of Attention (MIT Press, Cambridge, Massachusetts, 1999).
Posner, M. I. & Petersen, S. E. The attention system of the human brain. Annu. Rev. Neurosci. 13, 25 –42 (1990).
Moran, J. & Desimone, R. Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784 (1985).
Mangun, G. R. & Hillyard, S. A. Modulation of sensory-evoked brain potentials provide evidence for changes in perceptual processing during visual-spatial priming. J. Exp. Psychol. Hum. Percept. Perform. 17, 1057–1074 ( 1991).
Mesulam, M.-M A cortical network for directed attention and unilateral neglect. Ann. Neurol. 10, 309–325 (1981).
Posner, M. I., Walker, J. A., Friedrich, F. A. & Rafal, R. D. Effects of parietal injury on covert orienting of attention. J. Neurosci. 4, 1863–1874 ( 1984).
Corbetta, M., Miezin, F., Shulman, G. & Petersen, S. A PET study of visuospatial attention. J. Neurosci. 13, 1202–1226 (1993).
Gitelman, D. R. et al. A large-scale distributed network for covert spatial attention . Brain 122, 1093–1106 (1999).
Heinze, H. J. et al. Combined spatial and temporal imaging of spatial selective attention in humans. Nature 392, 543– 546 (1994).
Martinez, A. et al. Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat. Neurosci. 2, 364–369 (1999).
Nobre, A. C. et al. Functional localization of the system for visuospatial attention using positron emission tomography. Brain 120, 515–533 (1997).
Harter, M. R., Miller, S. L., Price, N. J., LaLonde, M. E. & Keyes, A. L. Neural processes involved in directing attention. J. Cogn. Neurosci. 1, 223– 237 (1989).
Buckner, R. et al. Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging. Proc. Natl. Acad. Sci. USA 93, 14302– 14303 (1996).
McCarthy, G., Luby, M., Gore, J. & Goldman-Rakic, P. Infrequent events transiently activate human prefrontal and parietal cortex as measured by functional MRI. J. Neurophysiol. 77, 1630–1634 (1997).
Ogawa, S. et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc. Natl. Acad. Sci. USA 89, 5951–5955 ( 1992).
Mangun, G. R., Hopfinger, J., Kussmaul, C., Fletcher, E. & Heinze, H. J. Covariations in ERP and PET measures of spatial selective attention in human extrastriate cortex. Hum. Brain Mapp. 5, 273–279 ( 1997).
Mangun, G. R., Buonocore, M., Girelli, M. & Jha, A. ERP and fMRI measures of visual spatial selective attention. Hum. Brain Mapp. 6, 383–389 ( 1998).
Tootell, R. B. et al. The retinotopy of visual spatial attention. Neuron 21, 1409–1422 ( 1998).
Brefczynski, J. A. & DeYoe, E. A. A physiological correlate of the spotlight of visual attention. Nat. Neurosci. 2, 370–374 ( 1999).
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).
Sereno, M. I. et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889–893 (1995).
Woldorff, M. et al. Retinotopic organization of early visual spatial attention effects as revealed by PET and ERPs. Hum. Brain Mapp. 5, 280–286 (1997).
Treue, S. & Maunsell, J. H. R. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382, 539–541 (1996).
Corbetta, M. et al. A common network of functional areas for attention and eye movements. Neuron, 21, 761– 773 (1998).
Coull, J. T. & Nobre, A. C. Where and when to pay attention: The neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI. J. Neurosci. 18, 7426–7435 (1998).
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 visual attention. J. Neurophysiol. 46, 755 –772 (1981).
LaBar, K. S., Gitelman, D. R., Parrish, T. B. & Mesulam, M. -M. Neuroanatomic overlap of working memory and spatial attention networks: A functional MRI comparison within subjects. Neuroimage 10, 695–704 (1999).
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).
Friedrich, F. J., Egly, R., Rafal, R. & Beck, D. Spatial attention deficits in humans: a comparison of superior parietal and temporal-parietal junction lesions. Neuropsychology 12, 193 –207 (1998).
Watson, R. T., Valenstein, E., Day, A. & Heilman, K. M. Posterior neocortical systems subserving awareness and neglect. Arch. Neurol. 51, 1014–1021 (1994).
Henik, A., Rafal, R. & Rhodes, D. Endogenously generated and visually guided saccades after lesions of the human frontal eye fields. J. Cogn. Neurosci. 6, 400–411 (1984).
Rosen, A. C. et al. Neural basis of endogenous and exogenous spatial orienting: a functional MRI study. J. Cogn. Neurosci. 11, 135–152 (1999).
Petit, L. et al. PET study of the human foveal fixation system. Hum. Brain. Mapp. 8, 28–43 ( 1999).
Jonides, J. et al. Spatial working memory in humans as revealed by PET. Nature 363, 623–625 ( 1993).
Kojima, S. & Goldman-Rakic, P. S. Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response. Brain Res. 248, 43–50 ( 1982).
D'Esposito, M., Ballard, D., Aguirre, G. K. & Zarahn, E. Human prefrontal cortex is not specific for working memory: a functional MRI study. Neuroimage 8, 274– 282 (1998).
Jonides, J., Smith, E. E., Marshuetz, C., Koeppe, R. A. & Reuter-Lorenz, P. A. Inhibition in verbal working memory revealed by brain activation. Proc. Natl. Acad. Sci. USA 95, 8410–8413 ( 1998).
Smith, E. E. & Jonides, J. Neuroimaging analyses of human working memory. Proc. Natl. Acad. Sci. USA 95, 12061 –12068 (1998).
Corbetta, M. in The Attentive Brain (ed. Parasuraman, R.) 95– 122 (MIT Press, Cambridge, Massachusetts, 1998).
Posner, M. I. & DiGirolamo, G. J. in The Attentive Brain (ed. Parasuraman, R.) 401–423 (MIT Press, Cambridge, Massachusetts, 1998).
Luck, S. J. et al. Effects of spatial cuing on luminance detectability: Psychophysical and electrophysiological evidence for early selection. J. Exp. Psychol. Hum. Percept. Perform. 20, 887– 904 (1994).
Van Voorhis, S. T. & Hillyard, S. A. Visual evoked potentials and selective attention to points in space. Percept. Psychophys. 22, 54–62 ( 1977).
McAdams, C. J. & Maunsell, J. H. R. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J. Neurosci. 19, 431– 441 (1999).
Tootell, R. et al. Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J. Neurosci. 15, 3215–3230 (1995).
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).
Chawla, D., Rees, G. & Friston, K. J. The physiological basis of attentional modulation in extrastriate visual areas. Nat. Neurosci. 7, 671–676 (1999).
Kastner, S., Pinsk, M. A., De Weerd, P., Desimone, R. & Ungerleider, L. G. Increased activity in human cerebral cortex during directed attention in the absence of visual stimulation . Neuron 22, 751–761 (1999).
Buonocore, M. H. & Gao, L. Ghost artifact reduction for echo planar imaging using image phase correction. Magn. Reson. Med. 38, 89–100 ( 1997).
Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, New York, 1988).
Friston, K. J. et al. Event-related fMRI: Characterizing differential responses . Neuroimage 7, 30–40 (1998).
Acknowledgements
This research was supported by grants from the National Institute of Mental Health (MH55714 and MH57138) and Human Frontier Science Program to G.R.M., and a National Science Foundation fellowship to J.B.H. We thank Neva Corrigan for assistance in collecting the MRI data, Jeff Maxwell for assistance in collecting the EOG data, Karl Friston and Christian Buechel for advice regarding the event-related fMRI analyses and Kevin LaBar, Kevin Wilson, Barry Geisbrecht, Marty Woldorff, Daniel Weissman, Steven Hillyard and Tamara Swaab for comments on the manuscript.
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Hopfinger, J., Buonocore, M. & Mangun, G. The neural mechanisms of top-down attentional control. Nat Neurosci 3, 284–291 (2000). https://doi.org/10.1038/72999
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DOI: https://doi.org/10.1038/72999
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