The electrotonic architecture of the retinal microvasculature: modulation by angiotensin II

Non‐technical summary  In the quest to understand how the circulatory system adjusts microvascular function to meet local metabolic demand, we focused on the retina whose circulatory system consists exclusively of microvessels. Since voltages induced by extracellular signals play a key role in gener...

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Bibliographic Details
Published in:The Journal of physiology 2011-05, Vol.589 (9), p.2383-2399
Main Authors: Zhang, Ting, Wu, David M., Xu, Ge‐zhi, Puro, Donald G.
Format: Article
Language:English
Subjects:
Angiotensin II - metabolism
Animals
Arterioles - metabolism
Capillaries - metabolism
Cardiovascular
Cell Communication
Electric Conductivity
Female
Male
Membrane Potentials
Microcirculation
Patch-Clamp Techniques
Rats
Rats, Long-Evans
Receptor, Angiotensin, Type 1 - metabolism
Regional Blood Flow
Retinal Vessels - metabolism
Time Factors
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Summary:Non‐technical summary  In the quest to understand how the circulatory system adjusts microvascular function to meet local metabolic demand, we focused on the retina whose circulatory system consists exclusively of microvessels. Since voltages induced by extracellular signals play a key role in generating vasomotor responses, we characterized the movement of voltage within the retinal microvasculature. To do this, we quantified voltage transmission between pairs of recording pipettes located at well‐defined sites in capillary/arteriole plexuses freshly isolated from the rat retina. We found that the retinal microvasculature is not simply a homogeneous syncytium, but has a complex electrotonic architecture with differing efficacies of voltage transmission. Furthermore, we discovered that the electrotonic architecture is not static, but is modulated by angiotensin. This newly appreciated action reveals that vasoactive signals can alter the functional organization of the microvasculature and, thereby, regulate the spatial extent of the circulatory system's response to voltage‐changing inputs.   The capillary/arteriole complex is the key operational unit regulating local perfusion to meet metabolic demand. However, much remains to be learned about how this multicellular unit is functionally organized. To help address this challenge, we characterized the electrotonic architecture of the retinal microvasculature, which is particularly well adapted for the decentralized control of blood flow. In this study, we quantified the transmission of voltage between pairs of perforated‐patch pipettes sealed onto abluminal cells located on microvascular complexes freshly isolated from the adult rat retina. These complexes consisted of capillaries, as well as tertiary and secondary arterioles. Dual recording experiments revealed that voltage spreading axially through a capillary, tertiary arteriole or secondary arteriole is transmitted very efficiently with a decay rate of only ∼5% per 100 μm. However, the retinal microvasculature is not simply a well‐coupled syncytium since we detected significant voltage dissipation with radial abluminal cell‐to‐endothelium transmission and also at branch points between a capillary and its tertiary arteriole and between tertiary and secondary arterioles. Consistent with capillaries being particularly well‐suited for the task of transmitting voltages induced by vasoactive signals, radial transmission is most efficient in this portion of the
ISSN:0022-3751
1469-7793
DOI:10.1113/jphysiol.2010.202937