2006Cerebral CortexOpen access

Intracortically Distributed Neurovascular Coupling Relationships within and between Human Somatosensory Cortices

Owen J. Arthurs, Tim Donovan, David Spiegelhalter, J. D. Pickard, Simon Boniface

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Abstract

The coupling of neuronal cellular activity to its blood supply is of critical importance to the physiology of the human brain and has been under discussion for more than a century. Linearity in this relationship has been demonstrated in some animal studies, but evidence is lacking in humans. In this study, we compared scalp evoked potentials and the functional magnetic resonance imaging (fMRI) blood oxygen level-dependent (BOLD) signal from healthy human volunteers with changes in the intensity of a somatosensory stimulus. By weighting the fMRI images according to the evoked potential amplitude at corresponding intensities, we tested for positive and negative covariation between these 2 data sets and the extent to which these were linear. Hemodynamic changes in primary somatosensory cortex covaried positively with neuronal activity in a predominantly linear manner, with a small quadratic contribution. Simultaneously, other cortical areas corresponding to the nonstimulated limbs were found to covary negatively and linearly in the hemispheres ipsilateral and contralateral to the stimulus. These concurrent and bilateral cortical dynamics, as well as the intraregional features of this neurovascular coupling, are both more complex than had been considered to date, with considerable implications.

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The coupling of neuronal cellular activity to its blood supply is of critical importance to the physiology of the human brain and has been under discussion for more than a century. Linearity in this relationship has been demonstrated in some animal studies, but evidence is lacking in humans. In this study, we compared scalp evoked potentials and the functional magnetic resonance imaging (fMRI) blood oxygen level-dependent (BOLD) signal from healthy human volunteers with changes in the intensity of a somatosensory stimulus. By weighting the fMRI images according to the evoked potential amplitude at corresponding intensities, we tested for positive and negative covariation between these 2 data sets and the extent to which these were linear. Hemodynamic changes in primary somatosensory cortex covaried positively with neuronal activity in a predominantly linear manner, with a small quadratic contribution. Simultaneously, other cortical areas corresponding to the nonstimulated limbs were found to covary negatively and linearly in the hemispheres ipsilateral and contralateral to the stimulus. These concurrent and bilateral cortical dynamics, as well as the intraregional features of this neurovascular coupling, are both more complex than had been considered to date, with considerable implications.

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Available abstract

The coupling of neuronal cellular activity to its blood supply is of critical importance to the physiology of the human brain and has been under discussion for more than a century. Linearity in this relationship has been demonstrated in some animal studies, but evidence is lacking in humans. In this study, we compared scalp evoked potentials and the functional magnetic resonance imaging (fMRI) blood oxygen level-dependent (BOLD) signal from healthy human volunteers with changes in the intensity of a somatosensory stimulus. By weighting the fMRI images according to the evoked potential amplitude at corresponding intensities, we tested for positive and negative covariation between these 2 data sets and the extent to which these were linear. Hemodynamic changes in primary somatosensory cortex covaried positively with neuronal activity in a predominantly linear manner, with a small quadratic contribution. Simultaneously, other cortical areas corresponding to the nonstimulated limbs were found to covary negatively and linearly in the hemispheres ipsilateral and contralateral to the stimulus. These concurrent and bilateral cortical dynamics, as well as the intraregional features of this neurovascular coupling, are both more complex than had been considered to date, with considerable implications.

Key concepts: Somatosensory system, Stimulus (psychology), Neuroscience, Functional magnetic resonance imaging, Human brain, Premovement neuronal activity, Scalp, Somatosensory evoked potential

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