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Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey

Nature Neuroscience volume 11, pages 1193–1200 (2008)Cite this article

Abstract

The role of primary visual cortex (V1) in determining the contents of perception is controversial. Human functional magnetic resonance imaging (fMRI) studies of perceptual suppression have revealed a robust drop in V1 activity when a stimulus is subjectively invisible. In contrast, monkey single-unit recordings have failed to demonstrate such perception-locked changes in V1. To investigate the basis of this discrepancy, we measured both the blood oxygen level–dependent (BOLD) response and several electrophysiological signals in two behaving monkeys. We found that all signals were in good agreement during conventional stimulus presentation, showing strong visual modulation to presentation and removal of a stimulus. During perceptual suppression, however, only the BOLD response and the low-frequency local field potential (LFP) power showed decreases, whereas the spiking and high-frequency LFP power were unaffected. These results demonstrate that the coupling between the BOLD and electrophysiological signals in V1 is context dependent, with a marked dissociation occurring during perceptual suppression.

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Figure 1: Generalized flash suppression protocol for the block design experiment.
Figure 2: Modulation of BOLD responses during perceptual suppression in two monkeys.
Figure 3: Divergence of V1 single-unit activity and fMRI BOLD response during perceptual suppression.
Figure 4: Spectral analysis of LFP signals obtained during suppression and control trials.
Figure 5: Population average of band-limited power (BLP) and spiking time courses for different experimental conditions.
Figure 6: Summary of perceptual modulation in the BOLD response and in each of the electrophysiological signals (as computed from the raw data of both monkeys shown in Figs. 3b and 5).
Figure 7: Schematic illustration of main results.

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References

  1. Blake, R. & Logothetis, N.K. Visual competition. Nat. Rev. Neurosci. 3, 13–21 (2002).

    Article  CAS  Google Scholar 

  2. Crick, F. & Koch, C. Are we aware of neural activity in primary visual cortex? Nature 375, 121–123 (1995).

    Article  CAS  Google Scholar 

  3. Polonsky, A., Blake, R., Braun, J. & Heeger, D.J. Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry. Nat. Neurosci. 3, 1153–1159 (2000).

    Article  CAS  Google Scholar 

  4. Tong, F. & Engel, S.A. Interocular rivalry revealed in the human cortical blind-spot representation. Nature 411, 195–199 (2001).

    Article  CAS  Google Scholar 

  5. Haynes, J.D. & Rees, G. Predicting the stream of consciousness from activity in human visual cortex. Curr. Biol. 15, 1301–1307 (2005).

    Article  CAS  Google Scholar 

  6. Haynes, J.D., Deichmann, R. & Rees, G. Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus. Nature 438, 496–499 (2005).

    Article  CAS  Google Scholar 

  7. Wunderlich, K., Schneider, K.A. & Kastner, S. Neural correlates of binocular rivalry in the human lateral geniculate nucleus. Nat. Neurosci. 8, 1595–1602 (2005).

    Article  CAS  Google Scholar 

  8. Lee, S.H., Blake, R. & Heeger, D.J. Traveling waves of activity in primary visual cortex during binocular rivalry. Nat. Neurosci. 8, 22–23 (2005).

    Article  CAS  Google Scholar 

  9. Lee, S.H. & Blake, R. V1 activity is reduced during binocular rivalry. J. Vis. 2, 618–626 (2002).

    Article  Google Scholar 

  10. Leopold, D.A. & Logothetis, N.K. Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry. Nature 379, 549–553 (1996).

    Article  CAS  Google Scholar 

  11. Leopold, D.A., Maier, A., Wilke, M. & Logothetis, N.K. Binocular rivalry and the illusion of monocular vision. in Binocular Rivalry and Perceptual Ambiguity (eds. Alais, D. & Blake, R.) (MIT Press, Cambridge, Massachusetts, 2004).

    Google Scholar 

  12. Gail, A., Brinksmeyer, H.J. & Eckhorn, R. Perception-related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry. Cereb. Cortex 14, 300–313 (2004).

    Article  Google Scholar 

  13. Wilke, M., Logothetis, N.K. & Leopold, D.A. Local field potential reflects perceptual suppression in monkey visual cortex. Proc. Natl. Acad. Sci. USA 103, 17507–17512 (2006).

    Article  CAS  Google Scholar 

  14. Tong, F. Primary visual cortex and visual awareness. Nat. Rev. Neurosci. 4, 219–229 (2003).

    Article  CAS  Google Scholar 

  15. Tong, F., Meng, M. & Blake, R. Neural bases of binocular rivalry. Trends Cogn. Sci. 10, 502–511 (2006).

    Article  Google Scholar 

  16. Wilke, M., Logothetis, N.K. & Leopold, D.A. Generalized flash suppression of salient visual targets. Neuron 39, 1043–1052 (2003).

    Article  CAS  Google Scholar 

  17. Bonneh, Y.S., Cooperman, A. & Sagi, D. Motion-induced blindness in normal observers. Nature 411, 798–801 (2001).

    Article  CAS  Google Scholar 

  18. Wolfe, J.M. Reversing ocular dominance and suppression in a single flash. Vision Res. 24, 471–478 (1984).

    Article  CAS  Google Scholar 

  19. Maier, A., Logothetis, N.K. & Leopold, D.A. Context-dependent perceptual modulation of single neurons in primate visual cortex. Proc. Natl. Acad. Sci. USA 104, 5620–5625 (2007).

    Article  CAS  Google Scholar 

  20. Logothetis, N.K. & Schall, J.D. Neuronal correlates of subjective visual perception. Science 245, 761–763 (1989).

    Article  CAS  Google Scholar 

  21. Gauthier, C. & Hoge, R.D. BOLD-perfusion coupling during monocular and binocular stimulation. Int. J. Biomed. Imaging published online, 10.1155/2008/628718 (2 March 2008).

  22. Logothetis, N.K. The neural basis of the blood-oxygen-level–dependent functional magnetic resonance imaging signal. Phil. Trans. R. Soc. Lond. B 357, 1003–1037 (2002).

    Article  Google Scholar 

  23. Mitchell, J.F., Sundberg, K.A. & Reynolds, J.H. Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55, 131–141 (2007).

    Article  CAS  Google Scholar 

  24. Iadecola, C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 5, 347–360 (2004).

    Article  CAS  Google Scholar 

  25. Logothetis, N.K. The underpinnings of the BOLD functional magnetic resonance imaging signal. J. Neurosci. 23, 3963–3971 (2003).

    Article  CAS  Google Scholar 

  26. Niessing, J. et al. Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309, 948–951 (2005).

    Article  CAS  Google Scholar 

  27. Viswanathan, A. & Freeman, R.D. Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat. Neurosci. 10, 1308–1312 (2007).

    Article  CAS  Google Scholar 

  28. Super, H., Spekreijse, H. & Lamme, V.A. Two distinct modes of sensory processing observed in monkey primary visual cortex (V1). Nat. Neurosci. 4, 304–310 (2001).

    Article  CAS  Google Scholar 

  29. Lamme, V.A., Super, H., Landman, R., Roelfsema, P.R. & Spekreijse, H. The role of primary visual cortex (V1) in visual awareness. Vision Res. 40, 1507–1521 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  31. Maier, A., Aura, C. & Leopold, D.A. Laminar differences in perceptual modulation of V1 local field potentials. Soc. Neurosci. Abstr. 451.12 (2007).

  32. Shmuel, A. & Leopold, D.A. Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest. Hum. Brain Mapp. 29, 751–761 (2008).

    Article  Google Scholar 

  33. Mukamel, R. et al. Coupling between neuronal firing, field potentials and FMRI in human auditory cortex. Science 309, 951–954 (2005).

    Article  CAS  Google Scholar 

  34. Nir, Y. et al. Coupling between neuronal firing rate, gamma LFP and BOLD fMRI is related to interneuronal correlations. Curr. Biol. 17, 1275–1285 (2007).

    Article  CAS  Google Scholar 

  35. Judge, S.J., Richmond, B.J. & Chu, F.C. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res. 20, 535–538 (1980).

    Article  CAS  Google Scholar 

  36. Mitz, A.R. A liquid-delivery device that provides precise reward control for neurophysiological and behavioral experiments. J. Neurosci. Methods 148, 19–25 (2005).

    Article  Google Scholar 

  37. Gruetter, R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn. Reson. Med. 29, 804–811 (1993).

    Article  CAS  Google Scholar 

  38. Mansfield, P. Multi-planar image formation using NMR spin echoes. J. Phys. C Solid State Phys. 10, L55–L58 (1977).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  40. Leopold, D.A., Murayama, Y. & Logothetis, N.K. Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb. Cortex 13, 422–433 (2003).

    Article  Google Scholar 

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Acknowledgements

We would like to thank G. Dold, D. Ide, N. Nichols and T. Talbot, as well as K. Smith, N. Phipps and J. Yu for technical assistance. We also thank H. Merkle for extensive guidance on the design and fabrication of radio frequency coils, R. Cox for assistance with magnetic resonance image alignment, D. Sheinberg for help with the stimulus software, K. King and C. Brewer for auditory testing and ear plug manufacture, W. Vinje for help with the multi-contact electrodes, K. Tanji, A.H. Bell and Z. Saad for help with the fMRI analysis, and S. Guderian, M. Schmid and K.-M. Mueller for discussions. This work was supported by the Intramural Research Programs of the National Institute of Mental Health, the National Institute of Neurological Disorders and Stroke and the National Eye Institute.

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Authors and Affiliations

  1. Department of Health and Human Services, Unit on Cognitive Neurophysiology and Imaging, Laboratory of Neuropsychology, National Institute of Mental Health, US National Institutes of Health, 49 Convent Dr., B2J-45, MSC 4400, Bethesda, 20892, Maryland, USA

    Alexander Maier, Melanie Wilke, Christopher Aura & David A Leopold

  2. Department of Health and Human Services, Neurophysiology Imaging Facility, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Eye Institute, US National Institutes of Health, 49 Convent Dr., B2J-45, MSC 4400, Bethesda, 20892, Maryland, USA

    Charles Zhu, Frank Q Ye & David A Leopold

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  1. Alexander Maier
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Contributions

A.M., M.W. and D.A.L. designed the experiments. A.M., M.W., C.A., C.Z., F.Q.Y. and D.A.L. contributed to the fMRI experiments. A.M., M.W. and C.A. carried out the electrophysiological testing, and M.W. collected the psychophysical data. A.M. analyzed the fMRI and electrophysiological data. A.M. and D.A.L. wrote the paper.

Corresponding author

Correspondence to Alexander Maier.

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Maier, A., Wilke, M., Aura, C. et al. Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey. Nat Neurosci 11, 1193–1200 (2008). https://doi.org/10.1038/nn.2173

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