Unusual capillary network geometry in a skeletal muscle, as seen in microcorrosion casts of M. pectoralis of pigeon.
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Biomedical subjects
R F Potter
Publications and source records attributed to R F Potter.
Muscle capillary-to-fiber perimeter ratio: morphometry.
It is known that a substantial amount of capillary tortuosity is found in shortened muscles. However, the increased capillary length and surface area contributed by tortuosity and branching are seldom taken into account when capillarity is estimated and/or blood-tissue exchange is modeled in muscles. In this paper, we sought morphometric estimates of capillarity in transverse sections that incorporated data on capillary geometry. We derived equations to estimate capillary perimeter per fiber perimeter (i.e., capillary-to-fiber perimeter ratio) in transverse sections. We show how capillary-to-fiber perimeter ratio is related to capillary surface per fiber surface, i.e., to the amount of capillary surface available for exchange per muscle fiber surface area, and how it can be obtained by morphometry. Because capillary tortuosity and fiber perimeter are both a function of sarcomere length, the degree of extension or shortening of muscle samples obviously needs to be taken into account when capillary-to-fiber perimeter ratio is compared between muscles and/or samples. Using data currently available on capillary length and diameter with fiber shortening and extension, we show that it is a feature of capillary-to-fiber perimeter ratio to change relatively little with sarcomere length. As sarcomere length decreases from 2.80 to 1.58 microns in perfusion-fixed hindlimb muscles of rats, capillary and fiber perimeters in transverse sections increase substantially, whereas the ratio between the two variables, capillary-to-fiber perimeter ratio, changes only less than or equal to 10-15%.(ABSTRACT TRUNCATED AT 250 WORDS)
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Effect of sarcomere length on total capillary length in skeletal muscle: in vivo evidence for longitudinal stretching of capillaries.
It is generally assumed that when a muscle is shortened or extended the total length of capillaries does not change, implying that capillaries are nondistensible, longitudinally. On the basis of stereological estimates of capillary anisotropy versus sarcomere length, we propose that as long as capillaries are in a tortuous configuration muscle extension will merely decrease the tortuosity, leaving vessel length unaltered. Once capillaries have been pulled into a straight configuration, further extension of the muscle will cause the vessels to stretch. By means of intravital videomicroscopy we have demonstrated that stretching of individual capillaries does indeed occur over a sarcomere length range of 2.1 to 2.9 microns in rat extensor digitorum longus muscle. In vivo measurements of the lengths of six capillaries together with the sarcomere lengths of adjacent fibers were made in muscles positioned at various degrees of extension. Normalized data indicated that four capillaries stretched to the same degree as the muscle, one stretched more and another less. This may reflect differences in distensibility or tortuosity of capillaries in series with one another. The elastic stretching of capillaries during muscle activity may have important consequences in terms of shifts in permeability and increases in capillary surface area.
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Temporal distributions of red cell supply rate to individual capillaries of resting skeletal muscle, in frog and rat.
Microvascular red cell (RBC) supply in resting skeletal muscle fluctuates with time and varies from capillary to capillary. Our aim was to quantitate this heterogeneity in two species (frog, rat) with very different oxygen requirements. Video recordings were made of RBC flow in capillaries associated with superficial fibers of frog sartorius and rat gracilis muscles, for periods of 2-10 min. RBC supply rate (cell/s) to individual capillaries was computed as the product of RBC 'content' (measured as lineal density, cells/mm, by a video-densitometric method) and RBC velocity (mm/s, measured by a spatial correlation technique). The videotapes were analyzed at rates of 6 to 15 samples per second. Regression analysis of the mean data showed little or no correlation between RBC content and RBC velocity (r2: frog 0.095, rat 0.002), both parameters contributing equally to variations in RBC supply rate. Temporal distributions of the three supply parameters demonstrate (1) the wide range of values present within each capillary, and (2) the symmetry of the distributions at high mean values versus a pronounced skewness as mean values approached zero. The wide range of mean values of each parameter, found in both species, suggests considerable 'spatial' heterogeneity of RBC supply among capillaries in resting muscle. Temporal heterogeneity of RBC supply rate to individual capillaries increased markedly as either velocity or content (or both) approached zero (overall mean coefficient of variation: frog, 62%; rat, 100%). Both species show remarkably similar rates of convective transport of RBCs per capillary in resting muscle (e.g. mean supply rates 3.2 and 6.2 RBCs/s in frog and rat, respectively).
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Capillary lengths and anastomoses in rat hindlimb muscles, studied by Aquablak perfusion during rest versus exercise.
This investigation shows that provided an adequate perfusion time of the capillary network is allowed following injection of Aquablak, the presence of arterioles and capillaries having zero or near-zero flow rates can be demonstrated in resting muscle. During hyperemia, "flow recruitment" occurs in these vessels, as indicated by their perfusion with Aquablak. Our observations of Aquablak perfusion in hyperemic muscles show that in medial gastrocnemius, gracilis, and soleus the mean arteriolar-to-venular distances, and also the mean capillary pathlengths, were not dramatically different. What was striking, however, was the fact that capillary pathlengths in soleus were divided into twice the number of segments found in gastrocnemius and gracilis. This suggests the possibility that in oxidative muscles the capillary network may exhibit a much higher degree of branching than in glycolytic muscles. This would increase the area for diffusional exchange between blood and tissue in oxidative compared to glycolytic muscle.
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Capillary configuration and fiber shortening in muscles of the rat hindlimb: correlation between corrosion casts and stereological measurements.
It has been a matter of discussion whether the dramatic increase in capillary tortuosity visualized in shortened muscles by vascular cast represents in vivo situations. In this study, we combined vascular cast and stereological methods in the same samples, in order to obtain (1) measurements of sarcomere length in the same muscles from which corrosion casts were prepared, and (2) scanning electron micrographs of the three-dimensional arrangement of capillaries in the same muscles where capillary anisotrophy was estimated by morphometry. Various rat skeletal muscles (soleus, gastrocnemius, and gracilis) were examined at lengths ranging from full shortening to full extension. We found a very good correlation between capillary geometry in material prepared for vascular casts and in muscles perfusion-fixed in situ. All muscles, cast and noncast, showed the same progressive curvilinear decrease in capillary anisotropy with decreasing sarcomere length. Capillary tortuosity visualized by corrosion casts in shortened muscles is a consequence of fiber shortening, within physiological sarcomere lengths; it does not represent an artifact related to the casting procedure.
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Geometric accommodation between the dimensions of erythrocytes and the calibre of heart and muscle capillaries in the rat.
The finer and more closely arrayed the capillaries are, the more efficiently oxygen will be transported to tissue because the same blood volume has greater contact area with the tissue and the diffusion distance for the oxygen is minimized. If these principles are actually governing microvascular structure, then the finest capillaries will be the narrowest channels which circulating erythrocytes can transit. Ascertaining the existence of this geometric limit requires quantitative data of demonstrated reliability on erythrocyte geometry and on capillary diameters. The study was done on Wistar rats. Constant flow perfusion of skeletal and cardiac muscle by a modified Batson's compound for anatomical casting made available rigid three-dimensional replicas of the microvasculature which shrank less than 1% when the tissue was digested with potassium hydroxide. Measurements of individual capillaries were made on high contrast scanning electron micrographs of the casts. Measurements on individual rat erythrocytes were done on photomicrographs of cells on edge. Reliability of these data was tested in three ways. First, repeatability of the tracing of the cell outline was tested by processing a duplicate set of photomicrographs. Secondly, correlations of the various parameters were found. Thirdly, results from other techniques of measuring erythrocytes were examined for areas of agreement and also for causes of possible error for areas in dispute. Because of known variability in erythrocyte sizes and shapes between species and between individuals within a species, we compared the data on erythrocyte geometry and capillary diameters for samples taken from the same individual rat. The data revealed a very positive indication that the lowest range of capillary diameters were at the limits of deformation of the circulating erythrocytes. Ninety-five per cent of the erythrocytes sampled could pass through a channel 2.9 micron in diameter. A small number of the capillaries measured were narrower than this limit. The data on erythrocytes and capillaries were compared for six rats. The limiting diameter for passage of erythrocytes was remarkably uniform for all six animals.
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Microvascular geometry in relation to modeling oxygen transport in contracted skeletal muscle.
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The Krogh cylinder geometry is not appropriate for modelling O2 transport in contracted skeletal muscle.
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Capillary diameter and geometry in cardiac and skeletal muscle studied by means of corrosion casts.
Studies of microvascular geometry made from microscope observations of tissues in vivo or after perfusion with a silastic elastomer or india ink are restricted to a two-dimensional field of view. Microvascular corrosion casts, however, if of sufficient rigidity and structural integrity, can yield three-dimensional information when examined under the scanning electron microscope. We have used modified Batson's No. 17 anatomical casting compound (having a shrinkage less than 1% on setting) to prepare casts of the microvasculature of the heart and skeletal muscles in anesthetized rats. In casts from the L. ventricle the capillary network appeared to parallel the arrangement of the muscle fibers, but showed many capillary loops and anastomoses. In skeletal muscles (gastrocnemius and gracilis) held at full extension, in situ, the casts showed long straight capillaries with fewer branchings than in the heart. In shortened skeletal muscle the capillaries exhibited an undulatory configuration. Capillary diameters (mean +/- SD) were 5.14 +/- 1.42 micrometers (N = 202), 5.04 +/- 1.45 micrometers (N = 294) and 4.84 +/- 1.97 micrometers (N = 335) in L. ventricle, gastrocnemius, and gracilis muscles (both shortened), respectively. The mean values for capillary diameter in these three tissues did not differ significantly. Combining our data with those of L. Henquell, P. L. LaCelle, and C. R. Honig on erythrocyte deformability in the rat (Microvasc. Res. 12, 259-274 (1976)) suggests that even when the capillary bed is fully distended the smallest capillaries, amounting to 1-2% of the total number, must be channels for plasma flow alone. In cross-sectional views of the casts from contracted skeletal muscle the capillaries appeared to form a tightly meshed network of convoluted vessels around the fibers, such that in some regions a large fraction of the surface of each fiber was in contact with blood. The Krogh cylinder geometry appears not to be appropriate for modeling O2 transport in maximally shortened skeletal muscle; a more appropriate model may be that of a cylindrical muscle fiber supplied, at any point down its length, by a uniform peripheral O2 supply.
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Are enlarged fenestrations in the internal elastic lamina of the rabbit thoracic aorta associated with poststenotic dilatation?
A stenosis amounting to 45-60% of the luminal diameter was made in the thoracic aorta of six New Zealand White rabbits. The progress of the ensuing poststenotic dilatation (PSD) was followed by daily X-ray analysis after which angiograms were taken for the calculation of luminal diameters. Specimens of the aorta proximal and distal (PSD) to the stenosis were digested to expose the internal elastic lamina (IEL) and viewed using a scanning electron microscope. The dilatations, which ranged between 7 and 30% reached their maximum diameter after only 8-10 days. The average diameter of the fenestrations distal (2.30 +/- 0.53 SEM) to the stenosis were significantly larger (p less than 0.01) than proximal (1.33 +/- 0.16 SEM) and covered a significantly larger (p less than 0.005) percent of the surface area of the IEL. It is suggested that the enlarged fenestrations may result in changes to the mechanical properties of the IEL which would play an important role in the genesis of PSDs.
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Responses of neurones of the pontine nuclei to stimulation of the sensorimotor, visual and auditory cortex of rats.
The aim of this study was to investigate the degree of convergence of corticofugal neurones from various cortical areas onto single neurones of the pontine nuclei (PN). Eighty-five% of the PN neurones responded to electrical stimulation of at least one of the following cortical areas: sensorimotor, visual, auditory. Slightly less than half of these neurones displayed a convergent input from two or three of functionally different cortical areas. The sensorimotor cortex, particularly the face areas, provided the most important input to the PN; stimulation of the visual cortex was less effective and stimulation of the auditory cortex rarely excited PN neurones. The electrophysiological results suggest that considerable cross-link exists between the anatomically defined cortico-pontine projection columns.
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Effect of superoxide dismutase and 21-aminosteroids (lazaroids) on microvascular perfusion following ischemia-reperfusion in skeletal muscle.
Intravital video microscopy was used to test superoxide dismutase and a lazaroid analogue, U-74389F, as a pretreatment for ischemia-reperfusion-induced microvascular dysfunction in skeletal muscle. Twenty-two male Wistar rats (350-400 g), anesthetized with sodium pentobarbital (65 mg/kg i.p.), were divided into groups to test the lazaroid analogue U-74389F (3 mg/kg; n = 8), a citric acid/citrate mixture (CS-4; n = 4) used as the vehicle for the lazaroid analogue, superoxide dismutase (SOD, 10 mg/kg; n = 5), and saline (n = 5). Normothermic ischemia of the extensor digitorum longus muscle was induced for 3 h by tightening a tourniquet placed around the limb above the muscle. Measurements of the number of perfused capillaries (CDper; mm-1) and capillary red blood cell velocity (VRBC; mm/s) were made after 30, 60 and 90 min of reperfusion. Thirty minutes following release of the tourniquet, all test groups showed a significant drop in CDper. The extent of this reduction was maximal in SOD treated muscles, while it was minimized in the lazaroid-treated muscles following 90 min reperfusion. Hyperemia occurred only in muscles treated with saline or lazaroid. The hyperemia was of limited duration in saline-treated muscles, but lasted the entire reperfusion period following lazaroid treatment. An index of microvascular flow, estimated from the product of VRBC and CDper, indicated that flow was significantly greater in muscles treated with lazaroids as compared with all other groups following the 90-min reperfusion. We conclude that whereas SOD was detrimental, the lazaroid analogue U-74389F improved microvascular perfusion following 3 h of no-flow ischemia and 90 min reperfusion.
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Capillary network morphology and capillary flow.
This paper examines the authors' research on capillary network morphology and the heterogeneity of capillary red cell (RBC) perfusion in skeletal muscle with the aim of demonstrating that capillary network structure plays a major role in determining flow distribution. Capillary network morphology was examined by quantifying the heterogeneity of capillary diameters, path and segment lengths, as well as the changes in configuration that occur as vessels accommodate themselves to continual changes of fiber length. Because of the network complexity and the two-phase nature of the perfusing blood, both spatial (i.e. among capillaries) and temporal heterogeneity of capillary perfusion were predicted to result. By means of computer analysis of video images of the microcirculation in vivo, we have demonstrated that more than 70% of the total spatial heterogeneity of capillary RBC perfusion arises from the capillary network as opposed to the arterioles, and that RBC flow continuously redistributes among capillaries. The spatial heterogeneity increases substantially as the arteriolar input to the network falls, and the data predict that during low-flow states, the network will fail to distribute blood properly among its constituent vessels. Thus passive rheological mechanisms and capillary network morphology are important determinants of functional capillary density.
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