The DOI matches its Crossref record; 32 of the 32 references it cites were found in a registry or an index.
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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In the citing paper
“Thus, V1 exhibited the same BOLD signal despite known differences in visual processing for PF and UF (Viswanathan and Freeman, 2007).”
From Perception is associated with the brain’s metabolic response to sensory stimulation (2022) · cites this paper as Viswanathan and Freeman, 2007
In the citing paper
“High (30 Hz) frequency visual stimulation has been found to selectively suppress multiunit activity (MUA) in cat V1 as compared to low frequency (4 Hz) visual stimulation (Viswanathan and Freeman, 2007).”
From Perception is associated with the brain’s metabolic response to sensory stimulation (2022) · cites this paper as Viswanathan and Freeman, 2007
In the citing paper
“Our results suggest that lactate and glutamate may be dissociated from BOLD changes when cortical input and output are differentially modulated by for example, intracortical (Viswanathan and Freeman, 2007) or thalamocortical (Min et al., 2020) inhibition.”
From Perception is associated with the brain’s metabolic response to sensory stimulation (2022) · cites this paper as Viswanathan and Freeman, 2007
In the citing paper
“This conclusion is supported by the fact that high-frequency flickering (30–60 Hz) abolished MUA, a measure of neuronal spiking (putatively from layer II/III) (Viswanathan and Freeman, 2007), but not single neuron recordings from layer IV (Gur and Snodderly, 1997).”
From Perception is associated with the brain’s metabolic response to sensory stimulation (2022) · cites this paper as Viswanathan and Freeman, 2007
In the citing paper
“oxidative metabolism and CMRO2 are enhanced at both low and high flickering frequencies (Viswanathan and Freeman, 2007)”
From Perception is associated with the brain’s metabolic response to sensory stimulation (2022) · cites this paper as Viswanathan and Freeman, 2007
In the citing paper
“Notably, the MAS does not necessarily correlate with mitochondrial respiration and cerebral blood flow, as evidenced by the findings that (1) oxidative metabolism and CMRO2 are enhanced at both low and high flickering frequencies (Viswanathan and Freeman, 2007), and (2) glutamate and aspartate, but not lactate, correlate with BOLD signals during low frequency (~8 Hz) visual stimulation (Bednařík”
From Perception is associated with the brain’s metabolic response to sensory stimulation (2022) · cites this paper as Viswanathan and Freeman, 2007
In the citing paper
“When recorded simultaneously during sensory stimulation, the BOLD response is more correlated with LFP than MUA (129, 130).”
From Electrophysiological source imaging: A noninvasive window to brain dynamics (2018) · cites this paper as [130]
In the citing paper
“Increasing evidence suggests that the primary source of fMRI is synaptic activity, rather than spiking activity, in the gray matter (129, 130).”
From Electrophysiological source imaging: A noninvasive window to brain dynamics (2018) · cites this paper as [130]
Citations
Cites
Neurophysiological investigation of the basis of the fMRI signal
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Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation.
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The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal
Logothetis, N. K. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-10-03963.2003 · Cited by 1,024
Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex
Mukamel, R., Gelbard, H., Arieli, A., Hasson, U., Fried, I., & Malach, R. (2005) · Science · doi:10.1126/science.1110913 · Cited by 1,023
Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations
Niessing, J., Ebisch, B., Schmidt, K. E., Niessing, M., Singer, W., & Galuske, R. A. W. (2005) · Science · doi:10.1126/science.1110948 · Cited by 806
Top-down processing mediated by interareal synchronization
von Stein, A., Chiang, C., & Peter König, B. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.26.14748 · Cited by 748
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Logothetis, N. K. (2008) · Nature · doi:10.1038/nature06976 · Cited by 3,612
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition
Wang, X.-J. (2010) · Physiological Reviews · doi:10.1152/physrev.00035.2008 · Cited by 1,939
Nichols, D. E. (2016) · Pharmacological Reviews · doi:10.1124/pr.115.011478 · Cited by 1,762
Closed-loop brain training: the science of neurofeedback
Sitaram, R., Ros, T., Stoeckel, L., Haller, S., Scharnowski, F., Lewis-Peacock, J., Weiskopf, N., Blefari, M. L., Rana, M., Oblak, E., et al. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.164 · Cited by 1,306
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Metadata
- Authors
- Viswanathan, A., & Freeman, R. D.
- Affiliations
- University of California, Berkeley (US)
- Corresponding author
- Freeman, Ralph D
- ORCID
- Freeman, Ralph D
- Venue
- Nature Neuroscience
- Published
- 2007-09-09
- Volume
- 10
- Issue
- 10
- Pages
- 1308-1312
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2139354009
- Cited by
- 397
- References
- 32
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 9 · 2023: 12 · 2022: 13 · 2021: 7 · 2020: 14 · 2019: 9 · 2018: 16 · 2017: 15 · 2016: 23 · 2015: 25 · 2014: 22 · 2013: 28 · 2012: 31
- FWCI
- 32.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ey003716-05)
- National Eye Institute (EY 03716, EY 01175, R01EY001175)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Optical Imaging and Spectroscopy Techniques
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Keywords
- neurometabolic coupling, BOLD signal, synaptic activity, spiking activity, local field potentials, cerebral cortex, primary visual cortex, tissue oxygen concentration, deoxyhemoglobin, functional MRI, cats
- MeSH terms
- Action Potentials, Animals, Cats, Dose-Response Relationship, Radiation, Evoked Potentials, Visual, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Oxygen, Photic Stimulation, Synapses, Visual Cortex, Visual Pathways
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