The neural basis of functional brain imaging signals
Abstract
The haemodynamic responses to neural activity that underlie the blood-oxygen-level-dependent (BOLD) signal used in functional magnetic resonance imaging (fMRI) of the brain are often assumed to be driven by energy use, particularly in presynaptic terminals or glia. However, recent work has suggested that most brain energy is used to power postsynaptic currents and action potentials rather than presynaptic or glial activity and, furthermore, that haemodynamic responses are driven by neurotransmitter-related signalling and not directly by the local energy needs of the brain. A firm understanding of the BOLD response will require investigation to be focussed on the neural signalling mechanisms controlling blood flow rather than on the locus of energy use.
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In primates, synaptic activity uses much more energy than action potentials.
“In primates, synaptic activity consumes much more energy than action potentials (131);”
From Electrophysiological source imaging: A noninvasive window to brain dynamics (2018) · cites this paper as [131]
The BOLD response is thought to be generated by local excitatory synaptic activity, leading to precisely localised changes in blood flow in response to the release of glutamate.
“The BOLD response is thought to be generated by local excitatory synaptic activity (Logothetis et al., 2001), leading to precisely localised changes in blood flow in response to the release of glutamate (Attwell and Iadecola, 2002).”
From The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies (2011) · cites this paper as Attwell and Iadecola, 2002
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“Although BOLD activity changes over the slower timescale of neuromodulator action, rather than the millisecond timescale of neural coupling, evidence concerning the relationship between neural firing and subsequent hemodynamic changes is accumulating (Attwell and Iadecola, 2002; Logothetis, 2003).”
BackgroundLayer-specific BOLD activation in human V1
Koopmans, P. J., Barth, M., & Norris, D. G. (2010) · Human Brain Mapping · doi:10.1002/hbm.20936 · Cited by 220 · see citing works
Functional connectivity of the prefrontal cortex and the amygdala in posttraumatic stress disorder
Gilboa, A., Shalev, A. Y., Laor, L., Lester, H., Louzoun, Y., Chisin, R., & Bonne, O. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.08.004 · Cited by 213 · see citing works
Hemodynamic correlates of EEG: a heuristic
Kilner, J. M., Mattout, J., Henson, R., & Friston, K. J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.06.008 · Cited by 206 · see citing works
Kann, O., Huchzermeyer, C., Kovács, R., Wirtz, S., & Schuelke, M. (2011) · Brain · doi:10.1093/brain/awq333 · Cited by 189 · see citing works
Electrophysiological correlates of the BOLD signal for EEG-informed fMRI
Murta, T., Leite, M., Carmichael, D. W., Figueiredo, P., & Lemieux, L. (2015) · Human Brain Mapping · doi:10.1002/hbm.22623 · Cited by 165 · see citing works
Mangia, S., Giove, F., Tkáč, I., Logothetis, N. K., Henry, P.-G., Olman, C. A., Maraviglia, B., Di Salle, F., & Uğurbil, K. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.134 · Cited by 161 · see citing works
Rauch, A., Rainer, G., & Logothetis, N. K. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800312105 · Cited by 146 · see citing works
The physiology of developmental changes in BOLD functional imaging signals
Harris, J. J., Reynell, C., & Attwell, D. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.04.001 · Cited by 142 · see citing works
Self-citationGlial Cell Calcium Signaling Mediates Capillary Regulation of Blood Flow in the Retina
Biesecker, K. R., Srienc, A. I., Shimoda, A. M., Agarwal, A., Bergles, D. E., Kofuji, P., & Newman, E. A. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.1782-16.2016 · Cited by 144 · see citing works
Nonconscious formation and reactivation of semantic associations by way of the medial temporal lobe
Henke, K., Mondadori, C. R. A., Treyer, V., Nitsch, R. M., Buck, A., & Hock, C. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(03)00035-6 · Cited by 128 · see citing works
Limitations of collateral flow after occlusion of a single cortical penetrating arteriole
Nishimura, N., Rosidi, N. L., Iadecola, C., & Schaffer, C. B. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2010.157 · Cited by 117 · see citing works
Self-citationPrincipal neuron spiking: neither necessary nor sufficient for cerebral blood flow in rat cerebellum
Thomsen, K., Offenhauser, N., & Lauritzen, M. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.068072 · Cited by 109 · see citing works
Linear and nonlinear relationships between visual stimuli, EEG and BOLD fMRI signals
Liu, Z., Rios, C., Zhang, N., Yang, L., Chen, W., & He, B. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.01.017 · Cited by 88 · see citing works
Lourenço, C. F., & Laranjinha, J. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.729201 · Cited by 85 · see citing works
fMRI spectral signatures of sleep
Song, C., Boly, M., Tagliazucchi, E., Laufs, H., & Tononi, G. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016732119 · Cited by 65 · see citing works
Wingrove, J., Swedrowska, M., Scherließ, R., Parry, M., Ramjeeawon, M., Taylor, D., Gauthier, G., Brown, L., Amiel, S., Zelaya, F., et al. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.03.032 · Cited by 67 · see citing works
Cudmore, R. H., Dougherty, S. E., & Linden, D. J. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16682508 · Cited by 54 · see citing works
Febo, M. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00043 · Cited by 43 · see citing works
Attention strongly increases oxygen metabolic response to stimulus in primary visual cortex
Moradi, F., Buračas, G. T., & Buxton, R. B. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.07.078 · Cited by 42 · see citing works
Dietary supplementation of creatine monohydrate reduces the human fMRI BOLD signal
Hammett, S. T., Wall, M. B., Edwards, T. C., & Smith, A. T. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.05.054 · Cited by 38 · see citing works
- Authors
- Attwell, D., & Iadecola, C.
- Affiliations
- University College London (GB)
- Cornell University (US)
- Venue
- Trends in Neurosciences
- Publisher
- Elsevier BV
- Published
- 2002-12
- Volume
- 25
- Issue
- 12
- Pages
- 621-625
- ISSN
- 0166-2236 (ISSN-L)
- OpenAlex
- W2148992333
- Cited by
- 957
- References
- 68
- Citations by year
- 2026: 28 · 2025: 25 · 2024: 30 · 2023: 21 · 2022: 29 · 2021: 28 · 2020: 57 · 2019: 60 · 2018: 42 · 2017: 42 · 2016: 40 · 2015: 34 · 2014: 38 · 2013: 45 · 2012: 42
- FWCI
- 5.81
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in Neurosciences (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust
- Royal Society
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Optical Imaging and Spectroscopy Techniques
- Keywords
- BOLD signal, hemodynamic response, functional MRI, brain energy metabolism, postsynaptic currents, action potential, neurotransmitter signalling, cerebral autoregulation
- MeSH terms
- Action Potentials, Astrocytes, Brain, Brain Mapping, Cerebrovascular Circulation, Energy Metabolism, Humans, Magnetic Resonance Imaging, Neural Inhibition, Presynaptic Terminals
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