A temporal study on musculoskeletal morphology and metabolism in hibernating Daurian ground squirrels (Spermophilus dauricus)

Hibernators provide a natural model to study the mechanisms underlying the prevention of disuse-induced musculoskeletal deterioration. Currently, however, these mechanisms remain poorly understood. Here, we investigated changes in morphology and metabolic indices in the hindlimb skeletal muscle and bone of Daurian ground squirrels (Spermophilus dauricus) during different periods of hibernation, and further explored the possible mechanisms involved in the musculoskeletal maintenance of hibernators after prolonged inactivity. Results showed that, compared with levels in the summer active group (SA), almost all morphological indices of skeletal muscle and bone, including muscle mass, muscle fiber cross-sectional area, bone mass, bone length, and bone mechanical properties, were unchanged in the different periods of hibernation. Only a few microstructural parameters of bone showed deterioration in the post-hibernation group (POST), including increased specific bone surface (+71%), decreased trabecular thickness (−43%), and decreased average cortical thickness (−51%) in the tibia, and increased trabecular separation (+60%) in the femur. Furthermore, most examined metabolic indices involved in muscle protein turnover and bone remodeling were unchanged, except for several indices in the inter-bout arousal group (IBA), i.e., increase in the phosphorylation of eukaryotic initiation factor 4E binding protein 1 (4E-BP1) (IBA vs. SA, +80%) in the vastus medialis muscle, increase in chymotrypsin-like activity (IBA vs. SA, +62%) in the tibialis anterior muscle, increase in osteoblast number (IBA vs. SA, +110%; IBA vs. torpor (TOR), +68%) and osteoclast number (IBA vs. TOR, +105%) per bone surface in the tibia, and increase in osteoclast surface per bone surface (IBA vs. TOR, +128%) in the femur. The above evidence demonstrates that the musculoskeletal morphology of squirrels was largely preserved, and musculoskeletal metabolism was generally maintained after prolonged hibernation inactivity. These findings suggest that the well-maintained musculoskeletal metabolism may be a vital mechanism underlying the preservation of the musculoskeletal system during hibernation. The coincident up-regulation of several metabolic indicators during IBA indicates that musculoskeletal metabolism may be relatively active during this period; however, its role in musculoskeletal maintenance during hibernation needs further clarification.