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 Ϯ 4 to 139 Ϯ 5 mg) in S and 22% (192 Ϯ 3 to 150 Ϯ 3 mg) in EDL between 12 and 35 mo of age, without decline in body mass. Capillary density increased 65% (1,387 Ϯ 54 to 2,291 Ϯ 238 mm Ϫ2 ) in S and 130% (964 Ϯ 95 to 2,216 Ϯ 311 mm Ϫ2 ) 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 Ϯ 78 to 2,750 Ϯ 271 mm Ϫ2 ) and 113% (1,194 Ϯ 112 to 2,540 Ϯ 343 mm Ϫ2 ) 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, capillaryto-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. capillary anisotropy; morphometry; ultrastructure; sarcopenia THE REDUCTION IN MUSCLE MAXIMAL capacity for aerobic work with aging is well known, and previous studies have shown alterations in both convective and diffusive components of O 2 transport in muscles. For example, reduced leg blood flow and increased leg O 2 extraction were found in older (63 Ϯ 2 yr old) compared with younger (27 Ϯ 1 yr old) endurance-trained men during submaximal exercise (42), and blood flow redistribution from highly oxidative to highly glycolytic muscles was recently demonstrated in the hindlimb of old (27-29 mo old) compared with young (6 -8 mo old) F344BN rats during submaximal exercise (37). Using an in situ pump-perfused hindlimb preparation to match convective O 2 delivery and eliminate age-related decline in blood flow, Hepple et al. (15) found a 22% decrease in the mass-specific O 2 uptake of the distal hindlimb in late middle aged (28 -39 mo) compared with young adult (8 mo) F344BN rats. In contrast, structural data on muscle capacity for O 2 transfer from capillary to fiber mitochondria have been contradictory. Human and/or animal studies have shown decreased (5, 12, 14, 38), unchanged (3, 4, 36), or even increased (8, 19, 36) capillary-to-fiber number ratios in skeletal muscles with aging. Part of the discrepancies have been attributed to the fact that differences in activit...