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Attention modulates responses in the human lateral geniculate nucleus

Abstract

Attentional mechanisms are important for selecting relevant information and filtering out irrelevant information from cluttered visual scenes. Selective attention has previously been shown to affect neural activity in both extrastriate and striate visual cortex. Here, evidence from functional brain imaging shows that attentional response modulation is not confined to cortical processing, but can occur as early as the thalamic level. We found that attention modulated neural activity in the human lateral geniculate nucleus (LGN) in several ways: it enhanced neural responses to attended stimuli, attenuated responses to ignored stimuli and increased baseline activity in the absence of visual stimulation. The LGN, traditionally viewed as the gateway to visual cortex, may also serve as a 'gatekeeper' in controlling attentional response gain.

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Figure 1: Visual stimuli and experimental design.
Figure 2: Time series of fMRI signals in the LGN (ac) and visual cortex (df).
Figure 3: Attentional response modulation in the LGN and in visual cortical areas V1, V2, V3/VP, V4, TEO, V3A and MT/MST.
Figure 4: Spatial selectivity of attention effects in the LGN (a) and in visual cortex (b).
Figure 5: Frequency histograms of eye position for experiments 1 (top), 3 (middle) and 4 (bottom).

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References

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

    Article  CAS  PubMed  Google Scholar 

  2. Kastner, S. & Ungerleider, L.G. Mechanisms of visual attention in the human cortex. Annu. Rev. Neurosci. 23, 315–341 (2000).

    Article  CAS  PubMed  Google Scholar 

  3. Kanwisher, N. & Wojciulik, E. Visual attention: insights from brain imaging. Nat. Rev. Neurosci. 1, 91–100 (2000).

    Article  CAS  PubMed  Google Scholar 

  4. Maunsell, J.H.R. The brain's visual world: representation of visual targets in cerebral cortex. Science 270, 764–769 (1995).

    Article  CAS  PubMed  Google Scholar 

  5. Moran, J. & Desimone, R. Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784 (1985).

    Article  CAS  PubMed  Google Scholar 

  6. Motter, B.C. Focal attention produces spatially selective processing in visual cortical areas V1, V2 and V4 in the presence of competing stimuli. J. Neurophysiol. 70, 909–919 (1993).

    Article  CAS  PubMed  Google Scholar 

  7. Watanabe, T. et al. Task-dependent influences of attention on the activation of human primary visual cortex. Proc. Natl. Acad. Sci. USA 95, 1489–1492 (1998).

    Google Scholar 

  8. Gandhi, S.P., Heeger, D.J. & Boynton, G.M. Spatial attention affects brain activity in human primary visual cortex. Proc. Natl. Acad. Sci. USA 96, 3314–3319 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Somers, D.C., Dale, A.M., Seiffert, A.E. & Tootell, R.B.H. Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. Proc. Natl. Acad. Sci. USA 96, 1663–1668 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  11. Ito, M. & Gilbert, C.D. Attention modulates contextual influences in the primary visual cortex of alert monkeys. Neuron 22, 593–604 (1999).

    Article  CAS  PubMed  Google Scholar 

  12. Jones, E.G. The Thalamus (Plenum Press, New York, 1985).

    Book  Google Scholar 

  13. Sherman, S.M. & Guillery, R.W. Exploring the Thalamus (Academic Press, San Diego, 2001).

    Google Scholar 

  14. Guillery, R.W. & Sherman, S.M. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33, 163–175 (2002).

    Article  CAS  PubMed  Google Scholar 

  15. Corbetta, M., Miezin, F.M., Dobmeyer, S., Shulman, G.L. & Petersen S.E. Attentional modulation of neural processing of shape, color and velocity in humans. Science 248, 1556–1559 (1991).

    Article  Google Scholar 

  16. Rees, G., Frith, C.D. & Lavie, N. Modulating irrelevant motion perception by varying attentional load in an unrelated task. Science 278, 1616–1619 (1997).

    Article  CAS  PubMed  Google Scholar 

  17. 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).

    Article  CAS  PubMed  Google Scholar 

  18. 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  PubMed  Google Scholar 

  19. 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  PubMed  Google Scholar 

  20. Ress, D., Backus, B.T. & Heeger, D.J. Activity in primary visual cortex predicts performance in a visual detection task. Nat. Neurosci. 9, 940–945 (2000).

    Article  Google Scholar 

  21. Chen, W. et al. Mapping of lateral geniculate nucleus activation during visual stimulation in human brain using fMRI. Magn. Reson. Med. 39, 89–96 (1998).

    Article  CAS  PubMed  Google Scholar 

  22. Chen, W., Zhu, X.H., Thulborn, K.R. & Ugurbil, K. Retinotopic mapping of lateral geniculate nucleus in humans using functional magnetic resonance imaging. Proc. Natl. Acad. Sci. USA 96, 2430–2434 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Posner, M.I. & Gilbert, C.D. Attention and primary visual cortex. Proc. Natl. Acad. Sci. USA 96, 2585–2587 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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  PubMed  Google Scholar 

  25. Kastner, S. et al. Modulation of sensory suppression: implications for receptive field sizes in the human visual cortex. J. Neurophysiol. 86, 1398–1411 (2001).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  27. Lavie, N. & Tsal, Y. Perceptual load as a major determinant of the locus of selection in visual attention. Percept. Psychophys. 56, 183–197 (1994).

    Article  CAS  PubMed  Google Scholar 

  28. Mehta, A.D., Ulbert, I. & Schroeder, C.E. Intermodal selective attention in monkeys. I: Distribution and timing of effects across visual areas. Cereb. Cortex 10, 343–358 (2000).

    Article  CAS  PubMed  Google Scholar 

  29. Mehta, A.D., Ulbert, I. & Schroeder, C.E. Intermodal selective attention in monkeys. II: Physiological mechanisms of modulation. Cereb. Cortex 10, 359–370 (2000).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Bender, D.B. & Youakim, M. Effect of attentive fixation in macaque thalamus and cortex. J. Neurophysiol. 85, 219–234 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Vanduffel, W., Tootell, R.B.H. & Orban, G.A. Attention-dependent suppression of metabolic activity in the early stages of the macaque visual system. Cereb. Cortex 10, 109–126 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Logothetis, N.K., Pauls, J., Augath, M., Trinath, T. & Oeltermann, A. Neurophysiological investigation of the basis of the fMRI signal. Nature 412, 150–157 (2001).

    Article  CAS  PubMed  Google Scholar 

  34. Koch, C. & Ullman, S. Shifts in selective visual attention: towards the underlying neural circuitry. Hum. Neurobiol. 4, 219–227 (1985).

    CAS  PubMed  Google Scholar 

  35. Sherman, S.M. Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 24, 122–126 (2001).

    Article  CAS  PubMed  Google Scholar 

  36. Guillery, R.W., Feig, S.L. & Lozsadi, D.A. Paying attention to the thalamic reticular nucleus. Trends Neurosci. 21, 28–32 (1998).

    Article  CAS  PubMed  Google Scholar 

  37. Reppas, J.B., Usrey, W.M. & Reid, R.C. Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 35, 961–974 (2002).

    Article  CAS  PubMed  Google Scholar 

  38. Woods, R.P., Mazziotta, J.C. & Cherry, S.R. MRI-PET registration with automated algorithm. J. Comput. Assist. Tomogr. 17, 536–546 (1993).

    Article  CAS  PubMed  Google Scholar 

  39. Friston, K.J. et al. Analysis of fMRI time-series revisited. Neuroimage 2, 45–53 (1995).

    Article  CAS  PubMed  Google Scholar 

  40. Talairach, J. & Tournoux, P. Co-Planar Stereotactic Atlas of the Human Brain (Thieme, New York, 1988).

    Google Scholar 

  41. Hadjikhani, N.K., Liu, A.K., Dale, A.M., Cavanagh, P. & Tootell, R.B.H. Retinotopy and color sensitivity in human visual cortical area V8. Nat. Neurosci. 1, 235–241 (1998).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank J. D. Cohen, G. M. Doniger, M. S. A. Graziano, C. G. Gross, J. V. Haxby, F. Tong and A. Treisman for valuable discussions, and M. Gilzenrat for help with eye movement measurements. Supported by National Science Foundation Graduate Research Fellowships to D.H.O. and M.A.P. and by grants from the National Institute of Mental Health and the Whitehall Foundation to S.K.

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Correspondence to Sabine Kastner.

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O'Connor, D., Fukui, M., Pinsk, M. et al. Attention modulates responses in the human lateral geniculate nucleus. Nat Neurosci 5, 1203–1209 (2002). https://doi.org/10.1038/nn957

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