Hyperperfusion Counteracted by Transient Rapid Vasoconstriction Followed by Long-Lasting Oligemia Induced by Cortical Spreading Depression in Anesthetized Mice

Cortical spreading depression (CSD) involves mass depolarization of neurons and glial cells accompanied with changes in regional cerebral blood flow (rCBF) and energy metabolism. To further understand the mechanisms of CBF response, we examined the temporal diametric changes in pial arteries, pial v...

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Published inJournal of cerebral blood flow and metabolism Vol. 35; no. 4; pp. 689 - 698
Main Authors Unekawa, Miyuki, Tomita, Yutaka, Toriumi, Haruki, Osada, Takashi, Masamoto, Kazuto, Kawaguchi, Hiroshi, Itoh, Yoshiaki, Kanno, Iwao, Suzuki, Norihiro
Format Journal Article
LanguageEnglish
Published London, England SAGE Publications 01.04.2015
Sage Publications Ltd
Nature Publishing Group
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Online AccessGet full text
ISSN0271-678X
1559-7016
1559-7016
DOI10.1038/jcbfm.2014.250

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Abstract Cortical spreading depression (CSD) involves mass depolarization of neurons and glial cells accompanied with changes in regional cerebral blood flow (rCBF) and energy metabolism. To further understand the mechanisms of CBF response, we examined the temporal diametric changes in pial arteries, pial veins, and cortical capillaries. In urethane-anesthetized mice, the diameters of these vessels were measured while simultaneously recording rCBF with a laser Doppler flowmeter. We observed a considerable increase in rCBF during depolarization in CSD induced by application of KCl, accompanied by a transient dip of rCBF with marked vasoconstriction of pial arteries, which resembled the response to pin-prick-induced CSD. Arterial constriction diminished or disappeared during the second and third passages of CSD, whereas the rCBF increase was maintained without a transient dip. Long-lasting oligemia with a decrease in the reciprocal of mean transit time of injected dye and mild constriction of pial arteries was observed after several passages of the CSD wave. These results indicate that CSD-induced rCBF changes consist of initial hyperemia with a transient dip and followed by a long-lasting oligemia, partially corresponding to the diametric changes of pial arteries, and further suggest that vessels other than pial arteries, such as intracortical vessels, are involved.
AbstractList Cortical spreading depression (CSD) involves mass depolarization of neurons and glial cells accompanied with changes in regional cerebral blood flow (rCBF) and energy metabolism. To further understand the mechanisms of CBF response, we examined the temporal diametric changes in pial arteries, pial veins, and cortical capillaries. In urethane-anesthetized mice, the diameters of these vessels were measured while simultaneously recording rCBF with a laser Doppler flowmeter. We observed a considerable increase in rCBF during depolarization in CSD induced by application of KCl, accompanied by a transient dip of rCBF with marked vasoconstriction of pial arteries, which resembled the response to pin-prick-induced CSD. Arterial constriction diminished or disappeared during the second and third passages of CSD, whereas the rCBF increase was maintained without a transient dip. Long-lasting oligemia with a decrease in the reciprocal of mean transit time of injected dye and mild constriction of pial arteries was observed after several passages of the CSD wave. These results indicate that CSD-induced rCBF changes consist of initial hyperemia with a transient dip and followed by a long-lasting oligemia, partially corresponding to the diametric changes of pial arteries, and further suggest that vessels other than pial arteries, such as intracortical vessels, are involved.
Cortical spreading depression (CSD) involves mass depolarization of neurons and glial cells accompanied with changes in regional cerebral blood flow (rCBF) and energy metabolism. To further understand the mechanisms of CBF response, we examined the temporal diametric changes in pial arteries, pial veins, and cortical capillaries. In urethane-anesthetized mice, the diameters of these vessels were measured while simultaneously recording rCBF with a laser Doppler flowmeter. We observed a considerable increase in rCBF during depolarization in CSD induced by application of KCl, accompanied by a transient dip of rCBF with marked vasoconstriction of pial arteries, which resembled the response to pin-prick-induced CSD. Arterial constriction diminished or disappeared during the second and third passages of CSD, whereas the rCBF increase was maintained without a transient dip. Long-lasting oligemia with a decrease in the reciprocal of mean transit time of injected dye and mild constriction of pial arteries was observed after several passages of the CSD wave. These results indicate that CSD-induced rCBF changes consist of initial hyperemia with a transient dip and followed by a long-lasting oligemia, partially corresponding to the diametric changes of pial arteries, and further suggest that vessels other than pial arteries, such as intracortical vessels, are involved.Cortical spreading depression (CSD) involves mass depolarization of neurons and glial cells accompanied with changes in regional cerebral blood flow (rCBF) and energy metabolism. To further understand the mechanisms of CBF response, we examined the temporal diametric changes in pial arteries, pial veins, and cortical capillaries. In urethane-anesthetized mice, the diameters of these vessels were measured while simultaneously recording rCBF with a laser Doppler flowmeter. We observed a considerable increase in rCBF during depolarization in CSD induced by application of KCl, accompanied by a transient dip of rCBF with marked vasoconstriction of pial arteries, which resembled the response to pin-prick-induced CSD. Arterial constriction diminished or disappeared during the second and third passages of CSD, whereas the rCBF increase was maintained without a transient dip. Long-lasting oligemia with a decrease in the reciprocal of mean transit time of injected dye and mild constriction of pial arteries was observed after several passages of the CSD wave. These results indicate that CSD-induced rCBF changes consist of initial hyperemia with a transient dip and followed by a long-lasting oligemia, partially corresponding to the diametric changes of pial arteries, and further suggest that vessels other than pial arteries, such as intracortical vessels, are involved.
Author Osada, Takashi
Toriumi, Haruki
Unekawa, Miyuki
Suzuki, Norihiro
Kanno, Iwao
Itoh, Yoshiaki
Kawaguchi, Hiroshi
Tomita, Yutaka
Masamoto, Kazuto
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Keywords neurovascular coupling
pial arteries
cortical spreading depression
laser Doppler flowmetry
confocal microscopy
microcirculation
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Present address: Department of Neurology, Osaka City University Graduate School of Medicine, Osaka, Japan.
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Snippet Cortical spreading depression (CSD) involves mass depolarization of neurons and glial cells accompanied with changes in regional cerebral blood flow (rCBF) and...
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SubjectTerms Animals
Capillaries - anatomy & histology
Capillaries - physiology
Cerebral Arteries - anatomy & histology
Cerebral Arteries - physiology
Cerebral Veins - anatomy & histology
Cerebral Veins - physiology
Cerebrovascular Circulation
Cerebrum - blood supply
Cortical Spreading Depression
Hemodynamics
Laser-Doppler Flowmetry
Mice
Microcirculation
Original
Vasoconstriction
Title Hyperperfusion Counteracted by Transient Rapid Vasoconstriction Followed by Long-Lasting Oligemia Induced by Cortical Spreading Depression in Anesthetized Mice
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https://www.ncbi.nlm.nih.gov/pubmed/25586145
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https://pubmed.ncbi.nlm.nih.gov/PMC4420891
Volume 35
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