Conducted depolarization in arteriole networks of the guinea‐pig small intestine: effect of branching of signal dissipation.

Abstract

with an Appendix by Timothy 0. Neild 1. Blood flow control requires co-ordinated activity among many branches of arteriole networks, which may be achieved by conduction of membrane potential changes between arteriolar smooth muscle cells and endothelial cells. 2. We investigated the effect of branching upon the passive conduction of electrical signals through the syncytium of electrically coupled cells in arteriole networks (n = 12) prepared from the guinea-pig submucosa. To describe the effect of branching on cable properties, the expansion parameter B was calculated (B = 1 for an unbranched cable; B > 1 with branching) for a point in each arteriole network based on anatomy. 3. An estimate of B(B') was also obtained by measuring the spread of depolarization caused by a high-K+ stimulus applied to one region. Membrane potential (-74 + 4 mV (± S.D.) at rest) was recorded from smooth muscle cells (verified with intracellular dye labelling). A micropipette containing 120 mm KCl was positioned at 150 ,sm increments along an arteriole (width, 50-75 #sm) up to -1 2 mm from a stationary recording site, producing stable depolarization which decreased as separation distance increased. The dissipation of depolarization with separation was greater when recording near branch origins rather than continuous segments. 4. B ranged in value from 0 99 to 2-28. In any one experiment, values of B and B' were correlated (correlation coefficient, r = 0 71; P < 0 05), but B' was consistently greater than B, and we discuss methodological factors which could lead to erroneously high values for B'.5. For pooled electrophysiological data, depolarization decayed to 37 % (1/e) of initial values in -700 ,sm, consistent with B > 1. In contrast, the conduction of vasoconstriction and vasodilatation exceeds 2 mm in arteriole networks in previous studies. To explain this discrepancy, we suggest that active electrical events in cells of the arteriole wall augment passive electrical conduction during blood flow control.

Endothelial Cell Pathway for Conduction of Hyperpolarization and Vasodilation Along Hamster Feed Artery

“…This effective distance for conduction along feed arteries is considerably greater than reported for arterioles of the hamster cheek pouch 2,6 and skeletal muscle 11,25 or for guinea pig submucosa, 16 where conducted responses decayed by Ͼ50% within 1 to 2 mm. Given that the wall morphology of the feed arteries in the present study (Figures 2 and 6) appears similar to that of proximal arterioles, 6,8 the greater effective distance for conduction along feed arteries may be explained instead by their lack of branching (and signal dissipation) when compared with arteriolar networks.…”

“…With 2 minutes of rest in between, this stimulus was repeated at each distance in random order. 15,16 The impaled cell was identified by characteristic dye labeling (Figure 2). 6,9…”

“…Given that the wall morphology of the feed arteries in the present study (Figures 2 and 6) appears similar to that of proximal arterioles, 6,8 the greater effective distance for conduction along feed arteries may be explained instead by their lack of branching (and signal dissipation) when compared with arteriolar networks. 11,16 Either Lucifer yellow 6,9 or a 3-kDa FCD 15 was used in the microelectrode to identify the cell impaled during intracellular recording (Figure 2). Whereas Lucifer yellow has been our dye of choice because of its strong fluorescence, 26 it has been suggested that the dual sulfate groups on this molecule can selectively block myoendothelial gap junctions whereas fluorescein does not.…”

The Vascular Conducted Response in Cerebral Blood Flow Regulation

“…18 The electrical intercellular communication underlying the conduction of vasomotor responses along the vascular wall has been measured using sharp microelectrodes inserted in either VSMC or EC at various locations along the arteriole. 27,[30][31][32][33] Usually investigators impale only one cell at the time and stimulate at various locations along the vessel successively, ending up with a number of V m measurements along the conduction pathway obtained at different time points. A few studies have also obtained V m recordings in arterioles at dual sites, making it possible to record conducted responses in VSMCs and ECs simultaneously, or to inject current at the local site and record V m deflections at the conducted site.…”

Bioelectric impact of pathological angiogenesis on vascular function

“…Because almost nothing is known about the electrogenic profile of neovascular complexes and how these complexes functionally interact with their parent vessels, we focused on the bioelectric features of neovascularization. These gaps in knowledge are surprising, considering that it is well established that the transmembrane voltage of vascular cells (1), as well as electrotonic cell-cell interactions within a vascular network (2)(3)(4), play vital roles in regulating blood flow.…”