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

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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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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.

Author information

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.

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) doi:10.1038/nn.2173

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