Influence of ageing and physical activity on vascular morphology in rat skeletal muscle

Abstract

Key structural and functional properties of the skeletal muscle vasculature that underlie diminished vascular conductance with ageing remain obscure. The purpose of this investigation was to test the hypotheses that (1) reduced levels of spontaneous physical activity in old rats are associated with skeletal muscle vascular remodelling (e.g. arterial rarefaction), and (2) consequent to a vascular remodelling, calculated shear stress is maintained in feed arteries of aged muscle at levels commensurate with that in young. Activity during daily light and dark cycles (12-12 h) was measured at 30-s intervals for 2 weeks in young (6 months; n = 9) and old (24 months; n = 9) Fisher 344 rats via telemetry. Subsequently, the gastrocnemius complex and soleus muscles were excised and all feed arteries were counted, isolated, cannulated and maximally dilated for measurement of luminal diameter. Resting blood flow was also measured to estimate vessel wall shear-stress in the feed arteries perforating the soleus and gastrocnemius muscles. Overall, young rats were approximately 1.6 times more active during dark periods and approximately 4 times more active during light periods than old rats. In addition, young rats had approximately one additional feed artery perforating both the soleus (young, 3.3 +/- 0.2; old, 2.6 +/- 0.2 vessels; P < 0.05) and gastrocnemius (young, 8.8 +/- 0.1; old, 7.5 +/- 0.2 vessels, P < 0.05) muscles compared with old rats. However, average vessel wall shear stress at rest was similar between young and old rats (soleus: Y, 65 +/- 5; O, 64 +/- 5 dynes cm(-2); gastrocnemius: Y, 329 +/- 22; O, 327 +/- 27 dynes cm(-2)) resulting from a larger vessel diameter in arteries from old rats. In conclusion, lower activity levels of old rats likely contribute to resistance artery rarefaction and, consequently, this provides a plausible mechanism for the altered blood flow patterns observed during exercise in aged skeletal muscle.

Figure 1. The number of feed vessels perforating the soleus and gastrocnemius muscle, as well as the major constituents of the gastrocnemius muscle

There was ∼0.7 less arteries perforating the soleus and ∼1.3 less arteries in the gastrocnemius (Gastroc.). *P < 0.05 versus young.

Figure 2. Average lumen cross-sectional area (CSA) of individual vessels perforating the soleus and gastrocnemius muscle, and the different sections of the gastrocnemius muscle

Old animals demonstrated a greater average lumen CSA than young in arteries of the soleus and gastrocnemius muscle, as well as larger CSA in the red and white sections of the gastrocnemius (Gastroc.). Only in the mixed portion of the gastrocnemius muscle was the average lumen CSA greater in young than in old. *P < 0.05 versus young.

Figure 3. Average vessel wall to lumen ratio derived from video caliper measurements of feed arteries in the soleus and gastrocnemius muscles of young and old rats

No differences were observed in the wall to lumen ratio between age groups. However, in the old group the wall to lumen ratio in the gastrocnemius was significantly greater than that of the soleus.

Figure 4. Haemodynamic measures in the soleus and gastrocnemius muscles measured in conscious, resting young and old rats.

A, resting haemodynamic measures for the soleus and gastrocnemius (Gastroc.) muscles, as well as the separate sections of the gastrocnemius muscle. There were no age-related differences in blood flow to the soleus or gastrocnemius muscle, or the different sections of the gastrocnemius. B, calculated resting shear stress for the soleus and gastrocnemius muscles, as well as for the red, mixed and white fibre-type sections of the gastrocnemius muscle. There were no age-related differences in shear stress to the soleus or gastrocnemius muscles; however, the old animals demonstrated lower shear stress in feed arteries of the red and white portions of the gastrocnemius muscle than in corresponding arteries from the younger animals. *P < 0.05 versus young.

Figure 5. Mean measures of heart rate, core body temperature, and activity from telemetry in young and old rats during diurnal (light, 12 h) and nocturnal (dark, 12 h) daily cycles

A, young and old rats were both significantly more active during the dark period. In addition, young animals were more active than their older counterparts during both activity cycles. Young rats were ∼4 times more active during the light (inactive) period of the day than old animals. B, heart rate was significantly elevated in old versus young rats during both light and dark periods. Both young and old rats demonstrated an elevated mean heart rate during the dark, active period. C, body temperature increased significantly for both groups during the dark versus light period. There was no difference in mean body temperature values between age groups during either period. †P < 0.05 versus light period; ^*P < 0.05 versus young. AU, arbitary units.