Capillary K+-sensing initiates retrograde hyperpolarization to increase local cerebral blood flow

Longden et al . demonstrate that brain capillaries function as a vast sensory web, monitoring neuronal activity by sensing K + and translating this into a K IR -channel-mediated regenerative retrograde hyperpolarizing signal that propagates to upstream arterioles to drive vasodilation and an increas...

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Bibliographic Details
Published in:Nature neuroscience Vol. 20; no. 5; pp. 717 - 726
Main Authors: Longden, Thomas A, Dabertrand, Fabrice, Koide, Masayo, Gonzales, Albert L, Tykocki, Nathan R, Brayden, Joseph E, Hill-Eubanks, David, Nelson, Mark T
Format: Journal Article
Language:English
Published: New York Nature Publishing Group US 01.05.2017
Nature Publishing Group
Subjects:
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Animal Genetics and Genomics
Animals
Behavioral Sciences
Biological Techniques
Biomedicine
Blood vessels
Brain
Brain - blood supply
Capillaries - physiology
Endothelial Cells - physiology
Male
Membrane Potentials - physiology
Mice
Mice, Knockout
Mice, Transgenic
Neurobiology
Neurons
Neurosciences
Potassium - physiology
Potassium Channels, Inwardly Rectifying - genetics
Potassium Channels, Inwardly Rectifying - physiology
Sensors
Vasodilation - physiology
Veins & arteries
ISSN:1097-6256, 1546-1726, 1546-1726
Online Access:Get full text
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Summary:Longden et al . demonstrate that brain capillaries function as a vast sensory web, monitoring neuronal activity by sensing K + and translating this into a K IR -channel-mediated regenerative retrograde hyperpolarizing signal that propagates to upstream arterioles to drive vasodilation and an increase in blood flow into the capillary bed. Blood flow into the brain is dynamically regulated to satisfy the changing metabolic requirements of neurons, but how this is accomplished has remained unclear. Here we demonstrate a central role for capillary endothelial cells in sensing neural activity and communicating it to upstream arterioles in the form of an electrical vasodilatory signal. We further demonstrate that this signal is initiated by extracellular K + —a byproduct of neural activity—which activates capillary endothelial cell inward-rectifier K + (K IR 2.1) channels to produce a rapidly propagating retrograde hyperpolarization that causes upstream arteriolar dilation, increasing blood flow into the capillary bed. Our results establish brain capillaries as an active sensory web that converts changes in external K + into rapid, 'inside-out' electrical signaling to direct blood flow to active brain regions.
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ISSN:1097-6256
1546-1726
1546-1726
DOI:10.1038/nn.4533