Remote arteriolar dilations in response to muscle contraction under capillaries.

In hamster cremaster muscle, it has been shown previously that contraction of skeletal muscle fibers underlying small groups of capillaries (modules) induces dilations that are proportional to metabolic rate in the two arteriolar generations upstream of the stimulated capillaries (Berg BR, Cohen KD, and Sarelius IH. Am J Physiol Heart Circ Physiol 272: H2693-H2700, 1997). These remote dilations were hypothesized to be transmitted via gap junctions and not perivascular nerves. In the present study, halothane (0.07%) blocked dilation in the module inflow arteriole, and dilation in the second arteriolar generation upstream, the branch arteriole, was blocked by both 600 mosM sucrose and halothane but not tetrodotoxin (2 microM). Dilations in both arterioles were not blocked by the gap junction uncoupler 18-beta-glycyrrhetinic acid (40 microM), and 80 mM KCl did not block dilation of the module inflow arteriole. These data implicate a gap junctional-mediated pathway insensitive to 18-beta-glycyrrhetinic acid in dilating the two arterioles upstream of the capillary module during "remote" muscle contraction. Dilation in the branch arteriole, but not the module inflow arteriole, was attenuated by 100 microM N(omega)-nitro-L-arginine. Thus selective contraction of muscle fibers underneath capillaries results in dilations in the upstream arterioles that have characteristics consistent with a signal that is transmitted along the vessel wall through gap junctions, i.e., a conducted vasodilation. The observed insensitivities to 18-beta-glycyrrhetinic acid, to KCl, and to N(omega)-nitro-L-arginine suggest, however, that there are multiple signaling pathways by which remote dilations can be initiated in these microvessels.

Direct coupling between blood flow and metabolism at the capillary level in striated muscle.

In hamster cremaster muscle, capillary networks consist of anatomically invariant subunits termed modules [Berg, B. R., and I. H. Sarelius, Am. J. Physiol. 268 (Heart Circ. Physiol. 37): H1215-H1222, 1995]. To explore local coupling between blood flow and metabolism, we used micropipettes to stimulate five to six muscle fibers running underneath specified capillary modules. Capillary erythrocyte flow increased significantly at all stimulation frequencies because of increased erythrocyte content at 2 Hz and increased erythrocyte velocity at 4 and 8 Hz. Erythrocyte flow did not increase when the fibers underlying the module were mechanically tugged but did not actively contract at these frequencies. Increased capillary flow was accommodated by dilation of three upstream arteriolar generations: the module inflow arteriole dilated significantly at all frequencies, and further upstream, dilations were significant at higher frequencies. Other module inflow arterioles in the same capillary network as the stimulated module did not dilate. Dilations in the module inflow arteriole were abolished by 600 mosM sucrose but were unaffected by 10(-6) M tetrodotoxin. These data suggest that local coupling between capillary flow and muscle contraction includes a conducted vasodilation that is responsible for the remote upstream dilations.

Erythrocyte flux in capillary networks during maturation: implications for oxygen delivery.

Erythrocyte (RBC) flow variables were measured with videomicroscopy in hamster cremaster muscle capillary networks. Capillary networks consist of subgroups, termed modules, with architectural characteristics that are invariant with maturation [B. R. Berg and I. H. Sarelius. Am. J. Physiol, 268 (Heart Circ. Physiol. 37): H1215-H1222, 1995]. RBC flux in modules decreased from 82.0 +/- 4.3 (SE) cells/s at 51 days of age to 59.5 +/- 7.5 and 27.5 +/- 2.8 cells/s at 65 and 79 days of age, respectively. Mean cell velocity at 51 days (385 +/- 10 microns/s) was higher than at 65 or 79 days (285 +/- 15 and 241 +/- 12 microns/s, respectively). Cell content (number of cells per unit length) decreased later, between 65 and 79 days (from 0.21 +/- 0.01 and 0.23 +/- 0.02 cells/micron at 51 and 65 days, respectively, to 0.12 +/- 0.01 cells/micron at 79 days). These temporal differences in the decrease in cell velocity and cell content suggest different regulatory mechanisms. The capacity of capillary networks to deliver oxygen was modeled by using the calculated mean PO2 at the capillary wall to indicate the capacity to delivery oxygen. During maturation, the mean capillary wall PO2 remained unchanged (15.5 +/- 1.2 and 11.4 +/- 2.7 Torr in maximal dilation and 24.5 +/- 1.4 and 22.8 +/- 2.4 Torr at rest at 51 and 79 days, respectively). Thus, despite changes in RBC flow variables with maturation, the capacity for networks to deliver oxygen remains constant.

Functional capillary organization in striated muscle.

In striated muscle, capillaries occur as independent network groups. Network architecture was quantitated in cremaster muscle of pentobarbital sodium-anesthetized hamsters in three age groups [51 +/- 1 (SE), 65 +/- 1, and 79 +/- 1 days old]. We observed that networks consist of independent subgroups of capillaries, called modules. Module architecture did not vary significantly with age during maximal dilation (Max, 10(-4) M adenosine): tissue area (A) = 1.87 +/- 0.16, 1.19 +/- 0.13, and 1.81 +/- 0.3 x 10(5) microns 2; total segment length (sigma L) = 3.07 +/- 0.23, 2.15 +/- 0.21, and 3.02 +/- 0.45 x 10(3) microns; and segment number (N) = 14.5 +/- 1.1, 9.9 +/- 1.1, and 12.6 +/- 1.6, at ages 51, 65, and 79 days, respectively. Max module architecture was not different at 65 days of age at a second site of known higher O2 inflow: A = 2.03 +/- 0.32 x 10(5) microns 2; sigma L = 3.07 +/- 0.47 x 10(3) microns; and N = 13.1 +/- 2.1. During control conditions (Rest) there was also no significant difference with age: A = 1.68 +/- 0.18, 1.15 +/- 0.19, and 1.64 +/- 0.24 x 10(5) microns 2; sigma L = 2.31 +/- 0.23, 1.91 +/- 0.33, and 2.82 +/- 0.37 x 10(3) microns; N = 10.2 +/- 1.0, 7.8 +/- 1.3, and 11.0 +/- 1.4, at ages 51, 65, and 79 days, respectively.(ABSTRACT TRUNCATED AT 250 WORDS)