Local potassium signaling couples neuronal activity to vasodilation in the brain.
- Authors
- Filosa, Jessica A; Bonev, Adrian D; Straub, Stephen V; Meredith, Andrea L; Wilkerson, M Keith; Aldrich, Richard W; Nelson, Mark T
- Year
- 2006
- Journal
- Nature neuroscience
- PMID
- 17013381
- DOI
- 10.1038/nn1779
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 Ca2+ signal is decoded by astrocytic BK channels, which locally release K+ into the perivascular space to activate SMC Kir channels and cause vasodilation.
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| Interpreting BOLD: towards a dialogue between cognitive and cellular neuroscience. | Hall CN et al. | β | 2016 | β |
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| The Gatekeepers in the Mouse Ophthalmic Artery: Endothelium-Dependent Mechanisms of Cholinergic Vasodilation. | Manicam C et al. | β | 2016 | β |
| The K+ channel KIR2.1 functions in tandem with proton influx to mediate sour taste transduction. | Ye W et al. | β | 2016 | β |
| The roadmap for estimation of cell-type-specific neuronal activity from non-invasive measurements. | Uhlirova H et al. | β | 2016 | β |
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| Astrocyte and microvascular imaging in awake animals using two-photon microscopy. | Tran CH et al. | β | 2015 | β |
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| Diversity of astrocyte functions and phenotypes in neural circuits. | Khakh BS et al. | β | 2015 | β |
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| Enhanced parenchymal arteriole tone and astrocyte signaling protect neurovascular coupling mediated parenchymal arteriole vasodilation in the spontaneously hypertensive rat. | Iddings JA et al. | β | 2015 | β |
| Generation of Kcnma1fl-tdTomato, a conditional deletion of the BK channel Ξ± subunit in mouse. | Zemen BG et al. | β | 2015 | β |
| Genetic ablation of CaV3.2 channels enhances the arterial myogenic response by modulating the RyR-BKCa axis. | Harraz OF et al. | β | 2015 | β |
| Mechanical restriction of intracortical vessel dilation by brain tissue sculpts the hemodynamic response. | Gao YR et al. | β | 2015 | β |
| Microbiology: Electrical signalling goes bacterial. | Beagle SD et al. | β | 2015 | β |
| Neuronal-derived nitric oxide and somatodendritically released vasopressin regulate neurovascular coupling in the rat hypothalamic supraoptic nucleus. | Du W et al. | β | 2015 | β |
| Neurovascular coupling and the influence of luminal agonists via the endothelium. | Dormanns K et al. | β | 2015 | β |
| Neurovascular coupling: a parallel implementation. | Dormanns K et al. | β | 2015 | β |
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| Astrocytic Gq-GPCR-linked IP3R-dependent Ca2+ signaling does not mediate neurovascular coupling in mouse visual cortex in vivo. | Bonder DE et al. | β | 2014 | β |
| BK channels regulate sinoatrial node firing rate and cardiac pacing in vivo. | Lai MH et al. | β | 2014 | β |
| Ca(V)3.2 channels and the induction of negative feedback in cerebral arteries. | Harraz OF et al. | β | 2014 | β |
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| Organic salt NEDC (N-naphthylethylenediamine dihydrochloride) assisted laser desorption ionization mass spectrometry for identification of metal ions in real samples. | Hou J et al. | β | 2014 | β |
| Rhythmic expression of cytochrome P450 epoxygenases CYP4x1 and CYP2c11 in the rat brain and vasculature. | Carver KA et al. | β | 2014 | β |
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| The role of glia in stress: polyamines and brain disorders. | Skatchkov SN et al. | β | 2014 | β |
| The role of K+ and Cl- channels in the regulation of retinal arteriolar tone and blood flow. | Needham M et al. | β | 2014 | β |
| TRPM4 channels couple purinergic receptor mechanoactivation and myogenic tone development in cerebral parenchymal arterioles. | Li Y et al. | β | 2014 | β |
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| Cerebral blood flow modulation by Basal forebrain or whisker stimulation can occur independently of large cytosolic Ca2+ signaling in astrocytes. | Takata N et al. | β | 2013 | β |
| Dendritic peptide release mediates interpopulation crosstalk between neurosecretory and preautonomic networks. | Son SJ et al. | β | 2013 | β |
| Elevated potassium provides an ionic mechanism for deep brain stimulation in the hemiparkinsonian rat. | Sutton AC et al. | β | 2013 | β |
| Endfeet serve as diffusion-limited subcellular compartments in astrocytes. | Nuriya M et al. | β | 2013 | β |
| Functional hyperemia and mechanisms of neurovascular coupling in the retinal vasculature. | Newman EA | β | 2013 | β |
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| Is potassium a ubiquitous mediator of vasodilation in the central nervous system? | Bekar LK et al. | β | 2013 | β |
| Lanthanum chloride promotes mitochondrial apoptotic pathway in primary cultured rat astrocytes. | Yang J et al. | β | 2013 | β |
| Locus coeruleus stimulation recruits a broad cortical neuronal network and increases cortical perfusion. | Toussay X et al. | β | 2013 | β |
| Modeling secondary messenger pathways in neurovascular coupling. | Hadfield J et al. | β | 2013 | β |
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| Neurovascular coupling: in vivo optical techniques for functional brain imaging. | Liao LD et al. | β | 2013 | β |
| Neurovascular interactions in the retina: physiological and pathological roles. | Nakahara T et al. | β | 2013 | β |
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| Prostaglandin E2, a postulated astrocyte-derived neurovascular coupling agent, constricts rather than dilates parenchymal arterioles. | Dabertrand F et al. | β | 2013 | β |
| Protein kinase A regulation of T-type Ca2+ channels in rat cerebral arterial smooth muscle. | Harraz OF et al. | β | 2013 | β |
| Regional registration of [6-(14)C]glucose metabolism during brain activation of Ξ±-syntrophin knockout mice. | Cruz NF et al. | β | 2013 | β |
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| TRPV4 channels stimulate Ca2+-induced Ca2+ release in astrocytic endfeet and amplify neurovascular coupling responses. | Dunn KM et al. | β | 2013 | β |
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| Acidosis dilates brain parenchymal arterioles by conversion of calcium waves to sparks to activate BK channels. | Dabertrand F et al. | β | 2012 | β |
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| Impairment of neurovascular coupling in type 1 diabetes mellitus in rats is linked to PKC modulation of BK(Ca) and Kir channels. | Vetri F et al. | β | 2012 | β |
| Intercellular Ca(2+) waves: mechanisms and function. | Leybaert L et al. | β | 2012 | β |
| Inversion of neurovascular coupling by subarachnoid blood depends on large-conductance Ca2+-activated K+ (BK) channels. | Koide M et al. | β | 2012 | β |
| It matters how you slice it. | Bryan RM | β | 2012 | β |
| K(+) channels: function-structural overview. | GonzΓ‘lez C et al. | β | 2012 | β |
| Learning on Jupiter, learning on the Moon: the dark side of the G-force. Effects of gravity changes on neurovascular unit and modulation of learning and memory. | Porte Y et al. | β | 2012 | β |
| Peripheral circulation. | Laughlin MH et al. | β | 2012 | β |
| Relative contribution of cyclooxygenases, epoxyeicosatrienoic acids, and pH to the cerebral blood flow response to vibrissal stimulation. | Liu X et al. | β | 2012 | β |
| S100 calcium binding proteins and ion channels. | Hermann A et al. | β | 2012 | β |
| The BK channel: a vital link between cellular calcium and electrical signaling. | Rothberg BS | β | 2012 | β |
| The early contribution of cerebrovascular factors to the pathogenesis of Alzheimer's disease. | Pimentel-Coelho PM et al. | β | 2012 | β |
| A guide to delineate the logic of neurovascular signaling in the brain. | Kleinfeld D et al. | β | 2011 | β |
| Bidirectional control of arteriole diameter by astrocytes. | Gordon GR et al. | β | 2011 | β |
| Contribution of K(ir)2 potassium channels to ATP-induced cell death in brain capillary endothelial cells and reconstructed HEK293 cell model. | Yamazaki D et al. | β | 2011 | β |
| Do TRPC-like currents and G protein-coupled receptors interact to facilitate myogenic tone development? | Anfinogenova Y et al. | β | 2011 | β |
| Epoxyeicosatrienoic acid-dependent cerebral vasodilation evoked by metabotropic glutamate receptor activation in vivo. | Liu X et al. | β | 2011 | β |
| Exercise training increases inwardly rectifying K(+) current and augments K(+)-mediated vasodilatation in deep femoral artery of rats. | Jin CZ et al. | β | 2011 | β |
| Expression of the voltage- and Ca2+-dependent BK potassium channel subunits BKΞ²1 and BKΞ²4 in rodent astrocytes. | Seidel KN et al. | β | 2011 | β |
| Fundamental increase in pressure-dependent constriction of brain parenchymal arterioles from subarachnoid hemorrhage model rats due to membrane depolarization. | Nystoriak MA et al. | β | 2011 | β |
| Glutamate-induced calcium signals stimulate CO production in piglet astrocytes. | Xi Q et al. | β | 2011 | β |
| Human immunodeficiency virus infection of human astrocytes disrupts blood-brain barrier integrity by a gap junction-dependent mechanism. | Eugenin EA et al. | β | 2011 | β |
| Ictal but not interictal epileptic discharges activate astrocyte endfeet and elicit cerebral arteriole responses. | GΓ³mez-Gonzalo M et al. | β | 2011 | β |
| Intermediate-conductance calcium-activated potassium channels participate in neurovascular coupling. | Longden TA et al. | β | 2011 | β |
| In vivo 3D morphology of astrocyte-vasculature interactions in the somatosensory cortex: implications for neurovascular coupling. | McCaslin AF et al. | β | 2011 | β |
| Models of neurovascular coupling via potassium and EET signalling. | Farr H et al. | β | 2011 | β |
| Molecular and electrophysiological evidence for the expression of BK channels in oligodendroglial precursor cells. | Buttigieg J et al. | β | 2011 | β |
| Neurovascular coupling in the human visual cortex is modulated by cyclooxygenase-1 (COX-1) gene variant. | Hahn T et al. | β | 2011 | β |
| Neurovascular function in Alzheimer's disease patients and experimental models. | Nicolakakis N et al. | β | 2011 | β |
| Optical detection of brain function: simultaneous imaging of cerebral vascular response, tissue metabolism, and cellular activity in vivo. | Du C et al. | β | 2011 | β |
| Potassium-selective microelectrode revealed difference in threshold potassium concentration for cortical spreading depression in female and male rat brain. | AdΓ‘mek S et al. | β | 2011 | β |
| Preictal and ictal neurovascular and metabolic coupling surrounding a seizure focus. | Zhao M et al. | β | 2011 | β |
| Role of astrocytes in neurovascular coupling. | Petzold GC et al. | β | 2011 | β |
| Slice cultures as a model to study neurovascular coupling and blood brain barrier in vitro. | KovΓ‘cs R et al. | β | 2011 | β |
| Subverting the hegemony of the synapse: complicity of neurons, astrocytes, and vasculature in spreading depression and pathology of the cerebral cortex. | Grafstein B | β | 2011 | β |
| The effect of single cerebroside compounds on activation of BKCa channels. | Xu H et al. | β | 2011 | β |
| The physiology of developmental changes in BOLD functional imaging signals. | Harris JJ et al. | β | 2011 | β |
| Vascular pathology and blood-brain barrier disruption in cognitive and psychiatric complications of type 2 diabetes mellitus. | Serlin Y et al. | β | 2011 | β |
| Vasomotor response induced by change of extracellular potassium and magnesium in cerebral penetrating arterioles. | Murata T et al. | β | 2011 | β |
| A novel key-lock mechanism for inactivating amino acid neurotransmitters during transit across extracellular space. | Baslow MH | β | 2010 | β |
| A role for BK channels in heart rate regulation in rodents. | Imlach WL et al. | β | 2010 | β |
| Astrocytic endfoot Ca2+ and BK channels determine both arteriolar dilation and constriction. | Girouard H et al. | β | 2010 | β |
| ATP, glia and central respiratory control. | Erlichman JS et al. | β | 2010 | β |
| Brain oscillations: ideal scenery to understand the neurovascular coupling. | Riera JJ et al. | β | 2010 | β |
| Cardiomyocyte sulfonylurea receptor 2-KATP channel mediates cardioprotection and ST segment elevation. | Stoller DA et al. | β | 2010 | β |
| Cerebral blood flow response to functional activation. | Paulson OB et al. | β | 2010 | β |
| Current profiles of astrocytes from the corpus callosum of newborn and 28-day-old rats. | Montiel-Herrera M et al. | β | 2010 | β |
| Do astrocytes really exocytose neurotransmitters? | Hamilton NB et al. | β | 2010 | β |
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| Inwardly rectifying potassium channels: their structure, function, and physiological roles. | Hibino H et al. | β | 2010 | β |
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| Pharmacological uncoupling of activation induced increases in CBF and CMRO2. | Leithner C et al. | β | 2010 | β |
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| Revisiting the role of neurons in neurovascular coupling. | Cauli B et al. | β | 2010 | β |
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| Ca2+- and thromboxane-dependent distribution of MaxiK channels in cultured astrocytes: from microtubules to the plasma membrane. | Ou JW et al. | β | 2009 | β |
| Cholesterol and Kir channels. | Levitan I | β | 2009 | β |
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| A review of the role of glial cells in understanding retinal disease. | Fletcher EL et al. | β | 2008 | β |
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