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Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity

Abstract

In noninvasive neuroimaging, neural activity is inferred from local fluctuations in deoxyhemoglobin. A fundamental question of functional magnetic resonance imaging (fMRI) is whether the inferred neural activity is driven primarily by synaptic or spiking activity. The answer is critical for the interpretation of the blood oxygen level–dependent (BOLD) signal in fMRI. Here, we have used well-established visual-system circuitry to create a stimulus that elicits synaptic activity without associated spike discharge. In colocalized recordings of neural and metabolic activity in cat primary visual cortex, we observed strong coupling between local field potentials (LFPs) and changes in tissue oxygen concentration in the absence of spikes. These results imply that the BOLD signal is more closely coupled to synaptic activity.

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Figure 1: Temporal frequency tuning of tissue oxygen, MUA and LFP responses.
Figure 2: Example recording site of responses to large (60°) stimulus.
Figure 3: Response to small stimulus at high spatial frequency.
Figure 4: Population data: mean LFP responses across sites.

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Acknowledgements

We thank Unisense A/S for continued collaboration in developing the combined sensor, J. Thompson for helpful comments during the conception of the project, P. Mitra and H. Bokil for assistance with LFP analysis, E. Allen and B. Pasley for helpful discussions, and B. Li for help with surgical preparation. This work was supported by research and CORE grants from the US National Eye Institute (EY01175 and EY03716) and a US National Science Foundation Graduate Research Fellowship (A.V.).

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A.V. conducted the experiments and data analysis. Both A.V. and R.D.F. discussed the results and wrote portions of the manuscript.

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Correspondence to Ralph D Freeman.

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Viswanathan, A., Freeman, R. Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat Neurosci 10, 1308–1312 (2007). https://doi.org/10.1038/nn1977

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