Geometry of blood-tissue exchange in bat flight muscle compared with bat hindlimb and rat soleus muscle

1992 ◽  
Vol 262 (6) ◽  
pp. R955-R965 ◽  
Author(s):  
O. Mathieu-Costello ◽  
J. M. Szewczak ◽  
R. B. Logemann ◽  
P. J. Agey
Keyword(s):  
Soleus Muscle ◽  
Sarcomere Length ◽  
Flight Muscle ◽  
Fiber Surface ◽  
Capillary Length ◽  
Fiber Volume ◽  
Cross Sectional ◽  
Fiber Size ◽  
Rat Soleus Muscle ◽  
Mitochondrial Volume

We investigated the relationship between capillary-to-fiber geometry and muscle aerobic capacity by comparing the bat flight muscle (pectoralis muscle), i.e., an ultimate case of extreme O2 demand in a mammalian skeletal muscle, with bat hindlimb and rat soleus muscles. At a given sarcomere length (2.1 microns), fiber cross-sectional area was considerably smaller in bat muscles (pectoralis 318 +/- 10 microns 2, hindlimb 447 +/- 35 microns 2) than in rat soleus muscle (2,027 +/- 125 microns 2). Capillary number per fiber cross-sectional area was much greater in bat pectoralis (6,394 +/- 380/mm2) than in bat hindlimb and rat soleus muscle (2,865 +/- 238 and 1,301 +/- 129/mm2, respectively; all values normalized to 2.1-microns sarcomere length). At the same sarcomere length (2.1 microns), the degree of tortuosity and branching of capillaries were significantly greater in bat pectoralis than in bat hindlimb and rat soleus muscle. In bat flight muscle, capillary length per fiber volume was very high (9,025 +/- 342/mm2). It was 2.2- and 5.4-fold larger than in bat hindlimb and rat soleus, respectively. Mitochondria occupied 35.3 +/- 1.2, 16.5 +/- 1.3, and 6.1 +/- 0.9% of the muscle fiber volume in bat pectoralis, hindlimb, and rat soleus muscles, respectively. There was a strong correlation between capillary length (as well as capillary surface) per fiber volume and mitochondrial volume density in all muscles. Considering capillary supply and mitochondrial volume on an individual fiber basis, we found that 1) the number of capillaries around a fiber was linearly related to mitochondrial volume per micron length of fiber in the muscles but that 2) capillary surface per fiber surface, at given mitochondrial volume per micron length of fiber, was about twice as large in bat pectoralis as in rat soleus muscle, whereas in bat hindlimb it was intermediate between that in bat pectoralis and that in rat soleus muscle. This was due to the differences in fiber size (rat soleus greater than bat muscles) and capillary-to-fiber ratio (bat pectoralis greater than hindlimb) between the muscles. It is notable that in the bat, the substantially greater O2 transfer capacity of the flight muscle compared with hindlimb was achieved by increasing the size of the capillary-to-fiber interface, i.e., capillary-to-fiber surface, via an increase in capillary number rather than by substantially reducing fiber size.

Capillary–fiber geometrical relationships in tuna red muscle

1992 ◽  
Vol 70 (6) ◽  
pp. 1218-1229 ◽  
Author(s):  
Odile Mathieu-Costello ◽  
Peter J. Agey ◽  
Richard B. Logemann ◽  
Richard W. Brill ◽  
Peter W. Hochachka
Keyword(s):  
Fiber Surface ◽  
Fish Muscle ◽  
Volume Density ◽  
Capillary Length ◽  
Fiber Volume ◽  
Cross Sectional ◽  
Red Muscle ◽  
Rat Soleus Muscle ◽  
Mitochondrial Volume ◽  
Mitochondrial Volume Density

The aim of this study was to examine the size and geometry of the capillary network in tuna red muscle, one of the most aerobic muscles in fish. Deep red muscle of 1.5- to 2-kg skipjack tuna, Katsuwonus pelamis, was perfusion fixed in situ, processed for electron microscopy, and analyzed by morphometry. Fiber cross-sectional area was 560 ± 30 (SE) μm2 in the samples. Capillary length per fiber volume was 4143 ± 242 (SE) mm−2 and mitochondrial volume density 28.5 ± 1.0 (SE) %. Indexes of capillarity such as average number of capillaries around a fiber, capillary length and surface per fiber volume, and capillary surface per fiber surface were high for a fish muscle. In fact, the size of the capillary–fiber interface (i.e., capillary to fiber surface) at a given mitochondrial volume per fiber was not significantly different in tuna red muscle compared with rat soleus muscle. However, calculation of mitochondrial respiratory rates in tuna red muscle yielded a substantially lower value (approximately 1/20th) compared with muscles of mammals. Besides the possible effect of differences in operating temperatures and (or) mitochondrial function(s) in fish compared with mammals, this suggests that the large capillary–fiber interface in tuna may be related to functions other than oxygen delivery per se, such as substrate and (or) heat transfer between capillaries and muscle fiber.

Increased capillarity in leg muscle of finches living at altitude

1998 ◽  
Vol 85 (5) ◽  
pp. 1871-1876 ◽  
Author(s):  
Russell T. Hepple ◽  
Peter J. Agey ◽  
Larnelle Hazelwood ◽  
Joseph M. Szewczak ◽  
Richard E. MacMillen ◽  
...  
Keyword(s):  
Sarcomere Length ◽  
Fiber Surface ◽  
Carpodacus Mexicanus ◽  
Fiber Structure ◽  
Capillary Length ◽  
Cross Sectional ◽  
Fiber Number ◽  
Mitochondrial Volume ◽  
Leg Muscle

An increased ratio of muscle capillary to fiber number (capillary/fiber number) at altitude has been found in only a few investigations. The highly aerobic pectoralis muscle of finches living at 4,000-m altitude ( Leucosticte arctoa; A) was recently shown to have a larger capillary/fiber number and greater contribution of tortuosity and branching to total capillary length than sea-level finches ( Carpodacus mexicanus; SL) of the same subfamily (O. Mathieu-Costello, P. J. Agey, L. Wu, J. M. Szewczak, and R. E. MacMillen. Respir. Physiol. 111: 189–199, 1998). To evaluate the role of muscle aerobic capacity on this trait, we examined the less-aerobic leg muscle (deep portion of anterior thigh) in the same birds. We found that, similar to pectoralis, the leg muscle in A finches had a greater capillary/fiber number (1.42 ± 0.06) than that in SL finches (0.77 ± 0.05; P < 0.01), but capillary tortuosity and branching were not different. As also found in pectoralis, the resulting larger capillary/fiber surface in A finches was proportional to a greater mitochondrial volume per micrometer of fiber length compared with that in SL finches. These observations, in conjunction with a trend to a greater (rather than smaller) fiber cross-sectional area in A than in SL finches (A: 484 ± 42, SL: 390 ± 26 μm2, both values at 2.5-μm sarcomere length; P = 0.093), support the notion that chronic hypoxia is also a condition in which capillary-to-fiber structure is organized to match the size of the muscle capillary-to-fiber interface to fiber mitochondrial volume rather than to minimize intercapillary O2diffusion distances.

Capillary and fiber geometry in rat diaphragm perfusion fixed in situ at different sarcomere lengths

1992 ◽  
Vol 73 (1) ◽  
pp. 151-159 ◽  
Author(s):  
D. C. Poole ◽  
O. Mathieu-Costello
Keyword(s):  
Airway Pressure ◽  
Sarcomere Length ◽  
Total Lung Capacity ◽  
Potential Range ◽  
Residual Volume ◽  
Capillary Length ◽  
Fiber Volume ◽  
Cross Sectional ◽  
Lung Capacity

To determine the potential range of diaphragm sarcomere lengths in situ and the effect of changes in sarcomere length on capillary and fiber geometry, rat diaphragms were perfusion fixed in situ with glutaraldehyde at different airway pressures and during electrical stimulation. The lengths of thick (1.517 +/- 0.007 microns) and thin (1.194 +/- 0.048 microns) filaments were not different from those established for rat limb muscle. Morphometric techniques were used to determine fiber cross-sectional area, sarcomere length, capillary orientation, and capillary length and surface area per fiber volume. All measurements were referenced to sarcomere length, which averaged 2.88 +/- 0.08 microns at -20 to -25 cmH2O airway pressure (residual volume) and 2.32 +/- 0.05 microns at +20 to +26 cmH2O airway pressure (total lung capacity). The contribution of capillary tortuosity and branching to total capillary length was dependent on sarcomere length and varied from 5 to 22%, consistent with that shown previously for mammalian limb muscles over this range of sarcomere lengths. Capillary length per fiber volume [Jv(c,f)] was significantly greater at residual volume (3,761 +/- 193 mm-2) than at total lung capacity (3,142 +/- 118 mm-2) and correlated with sarcomere length [l; r = 0.628, Jv(c,f) = 876l + 1,156, P less than 0.01; n = 18]. We conclude that the diaphragm is unusual in that the apparent in situ minimal sarcomere length is greater than 2.0 microns.(ABSTRACT TRUNCATED AT 250 WORDS)

Fiber capillarization relative to mitochondrial volume in diaphragm of shrew

2002 ◽  
Vol 93 (1) ◽  
pp. 346-353 ◽  
Author(s):  
O. Mathieu-Costello ◽  
S. Morales ◽  
J. Savolainen ◽  
M. Vornanen
Keyword(s):  
Body Mass ◽  
Fiber Surface ◽  
Volume Density ◽  
Capillary Length ◽  
Fiber Volume ◽  
Hindlimb Muscle ◽  
Mitochondrial Volume ◽  
Flight Muscles ◽  
Mitochondrial Volume Density ◽  
Sorex Minutus

The objective was to examine fiber capillarization in relation to fiber mitochondrial volume in the highly aerobic diaphragm of the shrew, the smallest mammal. The diaphragms of four common shrews [ Sorex araneus; body mass, 8.2 ± 1.3 (SE) g] and four lesser shrews ( Sorex minutus, 2.6 ± 0.1 g) were perfusion fixed in situ, processed for electron microscopy, and analyzed by morphometry. Capillary length per fiber volume was extremely high, at values of 8,008 ± 1,054 and 12,332 ± 625 mm−2 in S. araneus and S. minutus, respectively ( P= 0.012), with no difference in capillary geometry between the two species. Fiber mitochondrial volume density was 28.5 ± 2.3% ( S. araneus) and 36.5 ± 1.4% ( S. minutus; P = 0.025), yielding capillary length per milliliter mitochondria values ( S. araneus, 27.8 ± 1.5 km; S. minutus, 33.9 ± 2.2 km; P = 0.06) as high as in the flight muscle of the hummingbird and small bats. The size of the capillary-fiber interface (i.e., capillary surface per fiber surface ratio) per fiber mitochondrial volume in shrew diaphragm was also as high as in bird and bat flight muscles, and it was about two times greater than in rat hindlimb muscle. Thus, whereas fiber capillary and mitochondrial volume densities decreased with increased body mass in S. araneus compared with S. minutusSoricinae shrews, fiber capillarization per milliliter mitochondria in both species was much higher than previously reported for shrew diaphragm, and it matched that of the intensely aerobic flight muscles of birds and mammals.

Whole body and muscle respiratory capacity with dobutamine and hindlimb suspension

1991 ◽  
Vol 71 (6) ◽  
pp. 2419-2424 ◽  
Author(s):  
D. Desplanches ◽  
R. Favier ◽  
B. Sempore ◽  
H. Hoppeler
Keyword(s):  
Soleus Muscle ◽  
Metabolic Response ◽  
Volume Density ◽  
Hindlimb Suspension ◽  
Whole Body ◽  
Capillary Length ◽  
Muscle Weight ◽  
Cross Sectional ◽  
Beneficial Effects ◽  
Mitochondrial Volume

The effects of repeated injections of dobutamine, a synthetic catecholamine, were studied in control and tail-suspended rats to determine whether this drug could improve the metabolic response to unweighting. Dobutamine prevented the decrease in maximal oxygen uptake (VO2max) induced by hindlimb suspension. Furthermore, VO2max was 12% greater in dobutamine-treated animals than in saline-treated control animals. Soleus muscle weight and mean fiber cross-sectional area were decreased by 60 and 75%, respectively, in saline- and dobutamine-treated suspended rats. Total capillary length was unaffected by unweighting and increased 21% in all animals receiving dobutamine. The drug prevented the increase in total mitochondrial volume density (+30%) induced by unweighting but did not change total mitochondrial volume. Our results suggest that 1) dobutamine is useful to prevent the decrease of total aerobic capacity during hindlimb suspension, 2) dobutamine increases VO2max in control rats, and 3) total capillary length in soleus muscle is increased by the drug in all groups, although no beneficial effects on mitochondria can be detected.

Rat soleus muscle ultrastructure after hindlimb suspension

1990 ◽  
Vol 69 (2) ◽  
pp. 504-508 ◽  
Author(s):  
D. Desplanches ◽  
S. R. Kayar ◽  
B. Sempore ◽  
R. Flandrois ◽  
H. Hoppeler
Keyword(s):  
Soleus Muscle ◽  
Capillary Density ◽  
Volume Density ◽  
Hindlimb Suspension ◽  
Tail Suspension ◽  
Cross Sectional ◽  
Muscle Ultrastructure ◽  
Rat Soleus Muscle ◽  
Mitochondrial Volume ◽  
Mitochondrial Volume Density

The aim of the present investigation was to determine, by quantitative electron microscopy, the effects of a 5-wk tail-suspension period on rat soleus muscle ultrastructure. A marked decline (-60%) in muscle mass occurred. The mean fiber cross-sectional area decreased to a greater extent (-75%) than the capillary-to-fiber ratio (-37%), leading to a higher capillary density (+148%) after hypokinesia. The total mitochondrial volume density remained unchanged, whereas the volume density of myofibrils was slightly but significantly reduced (-6%). A shift from subsarcolemmal to interfibrillar mitochondria occurred. Interfibrillar mitochondrial volume density was highest near the fiber border and decreased toward the fiber center. An increase in volume density of satellite cells suggested muscle regenerative events. Soleus atrophy with tail suspension greatly decreases the muscular volume but leaves the ultrastructural composition of muscle fibers relatively unaffected.

Greater capillary-fiber interface per fiber mitochondrial volume in skeletal muscles of old rats

2005 ◽  
Vol 99 (1) ◽  
pp. 281-289 ◽  
Author(s):  
O. Mathieu-Costello ◽  
Y. Ju ◽  
M. Trejo-Morales ◽  
L. Cui
Keyword(s):  
Fiber Type ◽  
Fiber Surface ◽  
Volume Ratio ◽  
Capillary Density ◽  
Volume Density ◽  
Capillary Length ◽  
Fiber Volume ◽  
Fiber Number ◽  
Mitochondrial Volume ◽  
Fiber Atrophy

The objective was to examine whether muscle structural capacity for O2 flux (i.e., capillary-to-fiber surface ratio) relative to fiber mitochondrial volume deteriorates with the muscle atrophy of aging in predominantly slow- (soleus, S) and fast-twitch (extensor digitorum longus, EDL) muscles of old (24 mo) and very old (35 mo) F344BN rats compared with adult (12 mo old). Wet muscle mass decreased 29% (196 ± 4 to 139 ± 5 mg) in S and 22% (192 ± 3 to 150 ± 3 mg) in EDL between 12 and 35 mo of age, without decline in body mass. Capillary density increased 65% (1,387 ± 54 to 2,291 ± 238 mm−2) in S and 130% (964 ± 95 to 2,216 ± 311 mm−2) in EDL, because of the muscle fiber atrophy, whereas capillary per fiber number remained unchanged. Altered capillary geometry, i.e., lesser contribution of tortuosity and branching to capillary length, was found in S at 35 compared with 12 and 24 mo, and not in EDL. Accounting for capillary geometry revealed 55% (1,776 ± 78 to 2,750 ± 271 mm−2) and 113% (1,194 ± 112 to 2,540 ± 343 mm−2) increases in capillary length-to-fiber volume ratio between 12 and 35 mo of age in S and EDL, respectively. Fiber mitochondrial volume density was unchanged over the same period, causing mitochondrial volume per micrometer fiber length to decrease in proportion to the fiber atrophy in both muscles. As a result of the smaller fiber mitochondrial volume in the face of the unchanged capillary-to-fiber number ratio, capillary-to-fiber surface ratio relative to fiber mitochondrial volume not only did not deteriorate, but in fact increased twofold in both muscles between 12 and 35 mo of age, independent of their different fiber type.

Mechanical load-dependent regulation of satellite cell and fiber size in rat soleus muscle

2006 ◽  
Vol 290 (4) ◽  
pp. C981-C989 ◽  
Author(s):  
X. D. Wang ◽  
F. Kawano ◽  
Y. Matsuoka ◽  
K. Fukunaga ◽  
M. Terada ◽  
...  
Keyword(s):  
Satellite Cell ◽  
Muscle Fiber ◽  
Satellite Cells ◽  
Central Region ◽  
Sarcomere Length ◽  
Sectional Area ◽  
Cross Sectional ◽  
Fiber Properties ◽  
Rat Soleus Muscle ◽  
The Mean

The effects of mechanical unloading and reloading on the properties of rat soleus muscle fibers were investigated in male Wistar Hannover rats. Satellite cells in the fibers of control rats were distributed evenly throughout the fiber length. After 16 days of hindlimb unloading, the number of satellite cells in the central, but not the proximal or distal, region of the fiber was decreased. The number of satellite cells in the central region gradually increased during the 16-day period of reloading. The mean sarcomere length in the central region of the fibers was passively shortened during unloading due to the plantarflexed position at the ankle joint: sarcomere length was maintained at <2.1 μm, which is a critical length for tension development. Myonuclear number and domain size, fiber cross-sectional area, and the total number of mitotically active and quiescent satellite cells of whole muscle fibers were lower than control fibers after 16 days of unloading. These values then returned to control values after 16 days of reloading. These results suggest that satellite cells play an important role in the regulation of muscle fiber properties. The data also indicate that the satellite cell-related regulation of muscle fiber properties is dependent on the level of mechanical loading, which, in turn, is influenced by the mean sarcomere length. However, it is still unclear why the region-specific responses, which were obvious in satellite cells, were not induced in myonuclear number and fiber cross-sectional area.

Muscle capillary-to-fiber perimeter ratio: morphometry

1991 ◽  
Vol 261 (5) ◽  
pp. H1617-H1625 ◽  
Author(s):  
O. Mathieu-Costello ◽  
C. G. Ellis ◽  
R. F. Potter ◽  
I. C. MacDonald ◽  
A. C. Groom
Keyword(s):  
Surface Area ◽  
Muscle Fiber ◽  
Sarcomere Length ◽  
Fiber Surface ◽  
Capillary Surface ◽  
Capillary Length ◽  
Hindlimb Muscles ◽  
Using Data ◽  
Degree Of Extension

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)

Capillary and Fiber Size Interrelationships in Regenerating Rat Soleus Muscle after Ischemia: A Quantitative Study

1991 ◽  
Vol 142 (1) ◽  
pp. 70-76 ◽  
Author(s):  
E. Artacho-P&eacute;rula ◽  
R. Rold&aacute;n-Villalobos ◽  
R. Vaamonde-Lemos
Keyword(s):  
Quantitative Study ◽  
Soleus Muscle ◽  
Fiber Size ◽  
Rat Soleus Muscle
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