Differential Effects of Cold Exposure on Muscle Fibre Composition and Capillary Supply in Hibernator and Non‐Hibernator Rodents

Abstract

Changes in the composition of fibre types and the capillary supply of skeletal muscle (tibialis anterior) were quantified in rats and hamsters subjected to 8‐10 weeks of cold exposure and reduced photoperiod (10 °C, 1 h light‐23 h dark). Muscle mass decreased in both species (by 12% and 17%, respectively). Following acclimation to cold there were no specific changes in fibre cross‐sectional area (FCSA) in rats, whereas in hamsters there was a substantial atrophy of Type II, but not Type I fibres. In rat muscle there was little difference between the two groups in average capillary to fibre ratio (C:F) (1.76 ± 0.15, normothermia, N; 1.69 ± 0.05, hypothermia, H) and average capillary density (CD) (188 ± 14 mm−2, N; 201 ± 12 mm‐2, H). Similarly, the average C:F was unaltered in hamsters (2.75 ± 0.11, N; 2.72 ± 0.15, H), although the 30% smaller fibre size observed with hypothermia resulted in a corresponding increase in average CD, to 1539 ± 80 mm−2 (P < 0.01). However, there was a coordinated regional adaptation to cold exposure in hamsters resulting in capillary rarefaction in the glycolytic cortex and angiogenesis in the oxidative core. Following acclimation of rats to cold there was a reduction in the supply area of individual vessels (capillary domain), particularly in the cortex (9310, N; 8938 μm2, H; P < 0.05). In contrast, hypothermic hamsters showed only a small decrease in mean domain area in the cortex (948 μm2, N; 846 μm2, H; n.s.) but a marked reduction in the core (871 μm2, N; 604 μm2, H; P < 0.01). Rats showed little or no change in local capillary supply (LCFR) to fast fibres on acclimation to cold, while in hamsters the LCFR of Type IIb fibres showed a decrease in the cortex (2.7, N; 2.3, H) and an increase in the core (3.0, N; 3.3, H) during acclimation to cold. These data suggest that during a simulated onset of winter rats maintain FCSA and capillary supply as part of an avoidance strategy, whereas hamsters increase muscle capillarity in part as a consequence of disuse atrophy.

Modelling capillary oxygen supply capacity in mixed muscles: Capillary domains revisited

“…These observations are also robust to variations in the adjustable parameters of the transport model (Al-Shammari et al, 2012). Therefore, in the absence of extremes that are only associated with pathologies, our modelling predicts that VP provide a computationally simple and accurate approximation of functional capillary supply for muscle tissue cross sections of heterogeneous fibre types, which in turn theoretically validates the conclusions of modelling studies taking Voronoi polygons as a basis for morphometric analyses of maximal capillary supply in skeletal muscle tissues (Degens et al, 1992(Degens et al, , 2002(Degens et al, , 2006(Degens et al, , 2008Egginton et al, 2001;Wüst et al, 2009a;Ahmed et al, 1997).…”

“…1A is a light microscopy image of rat hindlimb skeletal muscle, m. extensor digitorum longus, prepared via flash freezing in liquid nitrogen-cooled isopentane and cryostat sectioned at -20 • C with the capillary location identified using alkaline phosphatase staining (Egginton et al, 2001).…”

“…1B) generate a space-filling alternative (Egginton & Ross, 1989 thereby allowing the exploration of the local influences associated with microvascular remodelling, as well as any mismatch between angiogenesis and local O 2 demand (Degens et al, 1992(Degens et al, , 2002(Degens et al, , 2006(Degens et al, , 2008Egginton et al, 2001;Wüst et al, 2009a). This gives Voronoi polygons an advantage in assessing the efficacy of applications to pathological scenarios, such as ischaemia, where potential therapeutic interventions include strength training (Deveci & Egginton, 2002;Suzuki et al, 2000), endurance exercise (Ahmed et al, 1997;Scott et al, 2009), electrical stimulation (Ebina et al, 2002), and alterations in muscle temperature (Egginton et al, 2001;Egginton, 2002). In addition to their ability to reproduce robust versions of the aforementioned global measures, Voronoi polygons have the capacity to provide indices of capillary supply to individual fibres, with both direct contact and indirect influence, and to fibres of different metabolic activities.…”

A Low Temperature Environment Delays the Changes in Muscle Fiber Type Composition Induced by Unloading

“…Other studies have shown that there was no significant change in the fiber cross-sectional area in loaded rats exposed to LT [5], whereas the study in hamsters showed atrophy of type-II fibers, but not type-I fibers [12]. These findings may demonstrate a difference in the muscle responses to LT between hibernating and non-hibernating animals.…”

“…Most hibernating animals exhibit physiological changes in response to seasonal cold temperatures and become hypothermic during hibernation [5]. The notable exception among hibernating animals is the black bear which can retain muscle size and maintain near-normal body temperatures of 31-35C during hibernation [15,26].…”