Differing mechanisms of cold-induced changes in capillary supply in m. tibialis anterior of rats and hamsters

Abstract

The physiological, metabolic and anatomical adaptations of skeletal muscle to chronic cold exposure were investigated in Wistar rats (Rattus norvegicus), a species that defends core temperature, and Syrian hamsters (Mesocricetus auratus), which may adopt a lower set point under unfavourable conditions. Animals were exposed to a simulated onset of winter in an environmental chamber, progressively shortening photoperiod and reducing temperature from 12 h:12 h L:D and 22degreesC to 1 h:23 h L:D and 5degreesC over 4 weeks. The animals were left at 4degreesC for a further 4 weeks to complete the process of cold acclimation. M. tibialis anterior from control (euthermic) and cold-acclimated animals of similar mass showed a significant hyperactivity-induced hypertrophy in the rat, but a small disuse atrophy in the hamster. Little evidence was found for interconversion among fibre types in skeletal muscle on cold-acclimation, and only modest differences were seen in activity of oxidative or glycolytic enzymes in either species. However, adjustments in Type II fibre size paralleled the muscle hypertrophy in rat and atrophy in hamster. Cold-induced angiogenesis was present in the rat, averaging a 28 % increase in capillary-to-fibre ratio (C:F) but, as this was balanced by fibre hypertrophy across the whole muscle, there was no change in capillary density (CD). In contrast, the C:F was similar in both groups of hamsters, whereas CD rose by 33 % in line with fibre atrophy. Within distinct regions of the m. tibialis anterior, there was a correlation between angiogenesis and fibre size in rats, in which oxygen diffusion distance increased, but not in hamsters, in which there was a reduced oxygen diffusion distance. Consequently, the change in C:F was greatest (39 %) in the glycolytic cortex region of the m. tibialis anterior in rats. We conclude that non-hibernator and hibernator rodents improve peripheral oxygen transport following cold-acclimation by different mechanisms. In rats, an increase in fibre girth was accompanied by a true angiogenesis, while the improved apparent capillary supply in hamsters was due to smaller fibre diameters. These responses are consistent with the strategies of resisting and accommodating, respectively, an annual fall in environmental temperature.