Capillaries and arterioles are electrically coupled in hamster cheek pouch

Abstract

In this report we demonstrate electrical communication in the microcirculation between arterioles and capillary networks in situ. Microvessel networks in the hamster cheek pouch, which included capillaries and their feeding arterioles, were labeled with the voltage-sensitive dye di-8-ANEPPS by intraluminal perfusion through a micropipette. Pulses of 140 mM potassium solution were applied by pressure ejection from micropipettes positioned on arterioles several hundred micrometers upstream from capillaries. Potassium caused membrane potential changes of 3-11 mV in capillary segments up to 1,200 micrometers distal to the stimulation site, with time delays of <1 s. Capillary membrane potential changes were biphasic, with initial depolarizations followed by hyperpolarizations. The size of the response decreased exponentially with the distance between the arteriole and capillary, with a 1/e distance of 590 micrometers. The time to peak depolarization of both arteriolar and capillary segments was similar. The time to peak response was significantly faster than that for responses from direct stimulation of capillaries. Capillary responses were also obtained when blood flow was either blocked or directed toward sites of stimulation. Acetylcholine (10(-4) M) and phenylephrine (10(-5) M) applied to the arterioles by iontophoresis produced monophasic hyperpolarizing and depolarizing responses, respectively, in capillaries with <1-s delay between stimulus and onset of the membrane potential change. These results provide evidence in situ of a pathway for electrical communication between arteriolar and capillary levels of the microcirculation.