How and when the fMRI BOLD signal relates to underlying neural activity: The danger in dissociation

doi:10.1016/j.brainresrev.2009.12.004

Brain Research Reviews

Volume 62, Issue 2, March 2010, Pages 233-244

https://doi.org/10.1016/j.brainresrev.2009.12.004 Get rights and content

Abstract

Functional magnetic resonance imaging (fMRI) has become the dominant means of measuring behavior-related neural activity in the human brain. Yet the relation between the blood oxygen-level dependent (BOLD) signal and underlying neural activity remains an open and actively researched question. A widely accepted model, established for sensory neo-cortex, suggests that the BOLD signal reflects peri-synaptic activity in the form of the local field potential rather than the spiking rate of individual neurons. Several recent experimental results, however, suggest situations in which BOLD, spiking, and the local field potential dissociate. Two different models are discussed, based on the literature reviewed to account for this dissociation, a circuitry-based and vascular-based explanation. Both models are found to account for existing data under some testing situations and in certain brain regions. Because both the vascular and local circuitry-based explanations challenge the BOLD-LFP coupling model, these models provide guidance in predicting when BOLD can be expected to reflect neural processing and when the underlying relation with BOLD may be more complex than a direct correspondence.

Section snippets

Introduction: fMRI and cognitive neuroscience

Functional magnetic resonance imaging (fMRI) has become a mainstay of research in both clinical and cognitive neuroscience and is currently the dominant paradigm for assessing behavior-related brain physiological changes in humans. Yet there still remains much for us to understand about this relatively new methodology. Perhaps most importantly, we are still learning what aspect of neural processing the blood oxygen level-dependent (BOLD) response, the signal that forms the basis of fMRI,

Acknowledgments

Thanks to Eve Isham, Charan Ranganath, Andy Yonelinas, Yevgeniy Sirotin, Michael Kahana, and Andrew Watrous for constructive comments on the manuscript.

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ReviewHow and when the fMRI BOLD signal relates to underlying neural activity: The danger in dissociation

Abstract

Section snippets

Introduction: fMRI and cognitive neuroscience

Acknowledgments

Neuroimage

Trends Neurosci.

Prog. Neurobiol.

Neuron

Magn. Reson. Imaging

Curr. Biol.

Brain Res.

Magn. Reson. Imaging

Neuroimage

Neuroimage

J. Neurosci. Methods

Neuroimage

Neuroimage

Neuron

Neuroimage

Neuroimage

Neuroimage

Neuroimage

Neuroimage

Curr. Biol.

Neuroimage

Neuropsychologia

Brain Cogn.

Neuroimage

Brain Res. Bull.

Neuroimage

Behav. Brain Res.

Increased glucose metabolism during long-duration recurrent inhibition of hippocampal pyramidal cells

J. Neurosci.

Hippocampal neuroanatomy

The BOLD response in the rat hippocampus depends rather on local processing of signals than on the input or output activity. A combined functional MRI and electrophysiological study

J. Neurosci.

An energy budget for signaling in the grey matter of the brain

J. Cereb. Blood Flow. Metab.

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J. Neurosci.

Working memory-related hippocampal deactivation interferes with long-term memory formation

J. Neurosci.

Evolution of hippocampal CA-1 diffusion lesions in transient global amnesia

Ann. Neurol.

Pre-surgical language mapping with functional magnetic resonance imaging

Neuropsychol. Rev.

Metabolic anatomy of brain: a comparison of regional capillary density, glucose metabolism, and enzyme activities

J. Comp. Neurol.

Simultaneous recording of evoked potentials and T2⁎-weighted MR images during somatosensory stimulation of rat

Magn. Reson. Med.

Modeling the hemodynamic response to brain activation

Neuroimage

Dissociation of spikes, synaptic activity, and activity-dependent increments in rat cerebellar blood flow by tonic synaptic inhibition

Proc. Natl. Acad. Sci. U. S. A.

Calibrated functional MRI: mapping the dynamics of oxidative metabolism

Proc. Natl. Acad. Sci. U. S. A.

Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring

J. Neurosci.

Ischemic lesions of the hippocampus and their relation to Ammon's horn sclerosis. A neuropathological study of two cases and a comparison to the vascular anatomy

J. Neurol.

Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal

J. Neurosci.

The Human Hippocampus: Functional Anatomy, Vascularization, and Serial Sections with MRI

Contrasting roles of neural firing rate and local field potentials in human memory

Hippocampus

Correlation between BOLD fMRI and theta-band local field potentials in the human hippocampal area

J. Neurophysiol.

Remote effects of focal hippocampal seizures on the rat neocortex

J. Neurosci.

Cortical deactivation induced by subcortical network dysfunction in limbic seizures

J. Neurosci.

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Glia

Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans

Brain

Review
How and when the fMRI BOLD signal relates to underlying neural activity: The danger in dissociation