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Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1

Nature Neuroscience volume 9, pages 569–577 (2006)Cite this article

Abstract

Most functional brain imaging studies use task-induced hemodynamic responses to infer underlying changes in neuronal activity. In addition to increases in cerebral blood flow and blood oxygenation level–dependent (BOLD) signals, sustained negative responses are pervasive in functional imaging. The origin of negative responses and their relationship to neural activity remain poorly understood. Through simultaneous functional magnetic resonance imaging and electrophysiological recording, we demonstrate a negative BOLD response (NBR) beyond the stimulated regions of visual cortex, associated with local decreases in neuronal activity below spontaneous activity, detected 7.15 ± 3.14 mm away from the closest positively responding region in V1. Trial-by-trial amplitude fluctuations revealed tight coupling between the NBR and neuronal activity decreases. The NBR was associated with comparable decreases in local field potentials and multiunit activity. Our findings indicate that a significant component of the NBR originates in neuronal activity decreases.

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Figure 1: BOLD response to stimulation of part of the visual field.
Figure 2: Neuronal and BOLD response to stimulation of part of the visual field.
Figure 3: Dynamics of the NBR and decreases in neuronal activity.
Figure 4: The negative BOLD response is correlated with decreases in neuronal activity.
Figure 5: Prediction of the mean time course of the BOLD response from that of the mean neuronal response and adjacent BOLD response.
Figure 6: Neuronal and BOLD response to stimulation of part of the visual field: LFP and MUA.
Figure 7: Trial-by-trial estimation of the time course of the negative BOLD response based on decreases in LFP, MUA and spiking activity.
Figure 8: Distance between the closest positively responding region and the site where decreases in neuronal activity were detected.

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Acknowledgements

We thank A. Bartels, A. Ghazanfar, K. Hoffman, A. Ishai, C. Kayser, G. Rainer, S. Smirnakis, L. Sugrue and K. Uludag for comments on a previous version of the manuscript; D. Blaurock for English editing; and S. Weber for fine-mechanic work. This study was supported by a long-term fellowship from the European Molecular Biology Organization awarded to A.S., and by the Max Planck Society.

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  1. Max Planck Institute for Biological Cybernetics, Spemannstr. 38, Tuebingen, 72076, Germany

    Amir Shmuel, Mark Augath, Axel Oeltermann & Nikos K Logothetis

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  1. Amir Shmuel
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Correspondence to Amir Shmuel or Nikos K Logothetis.

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Supplementary information

Supplementary Fig. 1

Neuronal response to stimulation of part of the visual field. (PDF 44 kb)

Supplementary Fig. 2

BOLD and neuronal response to stimulation of part of the visual field from 2 experiments with low-amplitude NBR and low-amplitude increases in neuronal activity. (PDF 126 kb)

Supplementary Fig. 3

The negative BOLD response is correlated with decreases in neuronal activity. (PDF 139 kb)

Supplementary Fig. 4

Region of interest adjacent to the NBR in V1. (PDF 22 kb)

Supplementary Fig. 5

Ratio of BOLD response to neuronal response. (PDF 45 kb)

Supplementary Discussion (PDF 74 kb)

Supplementary Methods (PDF 104 kb)

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Shmuel, A., Augath, M., Oeltermann, A. et al. Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 9, 569–577 (2006). https://doi.org/10.1038/nn1675

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