Oscillating neuro-capillary coupling during cortical spreading depression as observed by tracking of FITC-labeled RBCs in single capillaries

Minoru Tomita, Yutaka Tomita, Miyuki Unekawa, Haruki Toriumi, Norihiro Suzuki

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Coupling between capillary red blood cell (RBC) movements and neuronal dysfunction during cortical spreading depression (CSD) was examined in rats by employing a high-speed camera laser-scanning confocal fluorescence microscope system in conjunction with our Matlab domain software (KEIO-IS2). Following microinjection of K+ onto the surface of the brain, changes in electroencephalogram (EEG), DC potential and tissue optical density were all compatible with the occurrence of a transient spreading neuronal depression. RBC flow in single capillaries was not stationary. Unpredictable redistribution of RBCs at branches of capillaries was commonly observed, even though no change in diameter was apparent at the reported site of the capillary sphincter and no change of arteriolar-venule pressure difference was detected. There appeared to be a slow morphological change of astroglial endfeet. When local neurons were stunned transiently by K+ injection, the velocity and oscillation frequency of RBCs flowing in nearby capillaries started to decrease. The flow in such capillaries was rectified, losing oscillatory components. Sluggish floating movements of RBCs in pertinent capillaries were visualized, with occasional full stops. When CSD subsided, RBC movements recovered to the original state. We postulate that neuronal depolarization blocks oscillatory signaling to local capillaries via low-shear plasma viscosity increases in the capillary channels, and a complex interaction between the RBC surface and the buffy coat on the capillary wall surface increases the capillary flow resistance. Then, when CSD subsides and oscillatory neuronal function is recovered, the normal physiological conditions are restored.

Original languageEnglish
Pages (from-to)1001-1010
Number of pages10
JournalNeuroImage
Volume56
Issue number3
DOIs
Publication statusPublished - 2011 Jun 1

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Cortical Spreading Depression
Fluorescein-5-isothiocyanate
Erythrocytes
Cell Movement
Capillary Resistance
Venules
Microinjections
Viscosity
Electroencephalography
Lasers
Software
Fluorescence

Keywords

  • Capillary plasma viscosity
  • Cortical spreading depression
  • Neuro-capillary coupling
  • RBC in single capillary
  • RBC tracking map
  • Stunned neurons

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Neurology

Cite this

Oscillating neuro-capillary coupling during cortical spreading depression as observed by tracking of FITC-labeled RBCs in single capillaries. / Tomita, Minoru; Tomita, Yutaka; Unekawa, Miyuki; Toriumi, Haruki; Suzuki, Norihiro.

In: NeuroImage, Vol. 56, No. 3, 01.06.2011, p. 1001-1010.

Research output: Contribution to journalArticle

Tomita, Minoru ; Tomita, Yutaka ; Unekawa, Miyuki ; Toriumi, Haruki ; Suzuki, Norihiro. / Oscillating neuro-capillary coupling during cortical spreading depression as observed by tracking of FITC-labeled RBCs in single capillaries. In: NeuroImage. 2011 ; Vol. 56, No. 3. pp. 1001-1010.
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