Local potassium signaling couples neuronal activity to vasodilation in the brain

Jessica Andrea Filosa, Adrian D. Bonev, Stephen V. Straub, Andrea L. Meredith, M. Keith Wilkerson, Richard W. Aldrich, Mark T. Nelson

Research output: Contribution to journalArticle

336 Citations (Scopus)

Abstract

The mechanisms by which active neurons, via astrocytes, rapidly signal intracerebral arterioles to dilate remain obscure. Here we show that modest elevation of extracellular potassium (K+) activated inward rectifier K+ (Kir) channels and caused membrane potential hyperpolarization in smooth muscle cells (SMCs) of intracerebral arterioles and, in cortical brain slices, induced Kir-dependent vasodilation and suppression of SMC intracellular calcium (Ca2+) oscillations. Neuronal activation induced a rapid (<2 s latency) vasodilation that was greatly reduced by Kir channel blockade and completely abrogated by concurrent cyclooxygenase inhibition. Astrocytic endfeet exhibited large-conductance, Ca2+-sensitive K+ (BK) channel currents that could be activated by neuronal stimulation. Blocking BK channels or ablating the gene encoding these channels prevented neuronally induced vasodilation and suppression of arteriolar SMC Ca2+, without affecting the astrocytic Ca2+ elevation. These results support the concept of intercellular K+ channel-to-K+ channel signaling, through which neuronal activity in the form of an astrocytic Ca 2+ signal is decoded by astrocytic BK channels, which locally release K+ into the perivascular space to activate SMC Kir channels and cause vasodilation.

Original languageEnglish (US)
Pages (from-to)1397-1403
Number of pages7
JournalNature Neuroscience
Volume9
Issue number11
DOIs
StatePublished - Nov 1 2006
Externally publishedYes

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Large-Conductance Calcium-Activated Potassium Channels
Vasodilation
Smooth Muscle Myocytes
Potassium
Brain
Arterioles
Inwardly Rectifying Potassium Channel
Calcium Signaling
Prostaglandin-Endoperoxide Synthases
Astrocytes
Membrane Potentials
Neurons
Genes

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Filosa, J. A., Bonev, A. D., Straub, S. V., Meredith, A. L., Wilkerson, M. K., Aldrich, R. W., & Nelson, M. T. (2006). Local potassium signaling couples neuronal activity to vasodilation in the brain. Nature Neuroscience, 9(11), 1397-1403. https://doi.org/10.1038/nn1779

Local potassium signaling couples neuronal activity to vasodilation in the brain. / Filosa, Jessica Andrea; Bonev, Adrian D.; Straub, Stephen V.; Meredith, Andrea L.; Wilkerson, M. Keith; Aldrich, Richard W.; Nelson, Mark T.

In: Nature Neuroscience, Vol. 9, No. 11, 01.11.2006, p. 1397-1403.

Research output: Contribution to journalArticle

Filosa, JA, Bonev, AD, Straub, SV, Meredith, AL, Wilkerson, MK, Aldrich, RW & Nelson, MT 2006, 'Local potassium signaling couples neuronal activity to vasodilation in the brain', Nature Neuroscience, vol. 9, no. 11, pp. 1397-1403. https://doi.org/10.1038/nn1779
Filosa JA, Bonev AD, Straub SV, Meredith AL, Wilkerson MK, Aldrich RW et al. Local potassium signaling couples neuronal activity to vasodilation in the brain. Nature Neuroscience. 2006 Nov 1;9(11):1397-1403. https://doi.org/10.1038/nn1779
Filosa, Jessica Andrea ; Bonev, Adrian D. ; Straub, Stephen V. ; Meredith, Andrea L. ; Wilkerson, M. Keith ; Aldrich, Richard W. ; Nelson, Mark T. / Local potassium signaling couples neuronal activity to vasodilation in the brain. In: Nature Neuroscience. 2006 ; Vol. 9, No. 11. pp. 1397-1403.
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