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Evidence that the negative BOLD response is neuronal in origin: a simultaneous EEG–BOLD–CBF study in humans

Mullinger, Karen J.; Mayhew, Stephen D.; Bagshaw, Andrew P.; Bowtell, Richard W.; Francis, Susan T.

Authors

Stephen D. Mayhew

Andrew P. Bagshaw

Susan T. Francis



Abstract

Unambiguous interpretation of changes in the BOLD signal is challenging because of the complex neurovascular coupling that translates changes in neuronal activity into the subsequent haemodynamic response. In particular, the neurophysiological origin of the negative BOLD response (NBR) remains incompletely understood. Here, we simultaneously recorded BOLD, EEG and cerebral blood flow (CBF) responses to 10 s blocks of unilateral median nerve stimulation (MNS) in order to interrogate the NBR. Both negative BOLD and negative CBF responses to MNS were observed in the same region of the ipsilateral primary sensorimotor cortex (S1/M1) and calculations showed that MNS induced a decrease in the cerebral metabolic rate of oxygen consumption (CMRO2) in this NBR region. The ∆CMRO2/∆CBF coupling ratio (n) was found to be significantly larger in this ipsilateral S1/M1 region (n = 0.91 ± 0.04, M = 10.45%) than in the contralateral S1/M1 (n = 0.65 ± 0.03, M = 10.45%) region that exhibited a positive BOLD response (PBR) and positive CBF response, and a consequent increase in CMRO2 during MNS. The fMRI response amplitude in ipsilateral S1/M1 was negatively correlated with both the power of the 8–13 Hz EEG mu oscillation and somatosensory evoked potential amplitude. Blocks in which the largest magnitude of negative BOLD and CBF responses occurred therefore showed greatest mu power, an electrophysiological index of cortical inhibition, and largest somatosensory evoked potentials. Taken together, our results suggest that a neuronal mechanism underlies the NBR, but that the NBR may originate from a different neurovascular coupling mechanism to the PBR, suggesting that caution should be taken in assuming the NBR simply represents the neurophysiological inverse of the PBR.

Citation

Mullinger, K. J., Mayhew, S. D., Bagshaw, A. P., Bowtell, R. W., & Francis, S. T. (2014). Evidence that the negative BOLD response is neuronal in origin: a simultaneous EEG–BOLD–CBF study in humans. NeuroImage, 94, https://doi.org/10.1016/j.neuroimage.2014.02.029

Journal Article Type Article
Acceptance Date Feb 13, 2014
Online Publication Date Mar 12, 2014
Publication Date Jul 1, 2014
Deposit Date Jul 18, 2016
Publicly Available Date Jul 18, 2016
Journal NeuroImage
Print ISSN 1053-8119
Electronic ISSN 1095-9572
Publisher Elsevier
Peer Reviewed Peer Reviewed
Volume 94
DOI https://doi.org/10.1016/j.neuroimage.2014.02.029
Public URL http://eprints.nottingham.ac.uk/id/eprint/35148
Publisher URL http://www.sciencedirect.com/science/article/pii/S1053811914001426
Copyright Statement Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0

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Copyright Statement
Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0





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