Organisms rely on mechanosensing mechanisms to adapt to changes in their mechanical environment. Fluid-filled network structures not only ensure efficient transport but can also be employed for mechanosensation. The lacunocanalicular network (LCN) is a fluid-filled network structure, which pervades our bones and accommodates a cell network of osteocytes. For the mechanism of mechanosensation, it was hypothesized that load-induced fluid flow results in forces that can be sensed by the cells. We use a controlled in vivo loading experiment on murine tibiae to test this hypothesis, whereby the mechanoresponse was quantified experimentally by in vivo micro-computed tomography (µCT) in terms of formed and resorbed bone volume. By imaging the LCN using confocal microscopy in bone volumes covering the entire cross-section of mouse tibiae and by calculating the fluid flow in the three-dimensional (3D) network, we could perform a direct comparison between predictions based on fluid flow velocity and the experimentally measured mechanoresponse. While local strain distributions estimated by finite-element analysis incorrectly predicts preferred bone formation on the periosteal surface, we demonstrate that additional consideration of the LCN architecture not only corrects this erroneous bias in the prediction but also explains observed differences in the mechanosensitivity between the three investigated mice. We also identified the presence of vascular channels as an important mechanism to locally reduce fluid flow. Flow velocities increased for a convergent network structure where all of the flow is channeled into fewer canaliculi. We conclude that, besides mechanical loading, LCN architecture should be considered as a key determinant of bone adaptation.

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IntroductionTo prepare laying hens for life in cage-free aviaries, they must be reared in aviaries that accustom them to the challenges of navigating a complex three-dimensional structure. Rearing aviaries vary in design and contain a brooding compartment in which chicks are confined during the first six weeks of age. These compartments vary greatly in their size and complexity. The present study aimed to examine the impact of environmental complexity during early life and birds’ genetic strain on their space use and forms/types of exercise.MethodsFour consecutive flocks of brown and white chicks were raised in three styles of rearing aviary with low, intermediate, or high complexity. Behavioral observations were performed at three ages during the brooding phase (weeks 1, 3, and 5) and the open phase when the brooding compartments were opened (weeks 7, 11, and 17). Behaviors observed were categorized as aerial locomotion, perching, dynamic load-bearing behavior (DLB), and wing-involved load-bearing behavior (WLB).ResultsDuring the brooding phase, chicks in aviaries of high complexity exercised most frequently (e.g., DLB events/minute: 1.75 in High vs 1.11 in Mid and 0.10 in Low, p<0.0001), and the effect remained for whites, but not the browns, during the open phase. White pullets exercised more than brown pullets both in brooding (e.g., 1.47 vs 1.28 DLB events/minute, p<0.0001) and open phases in High and Mid (e.g., 1.17 vs 0.93 DLB events/minute, housing x stain interaction p=0.009). Throughout rearing, whites had higher odds of perching than browns (brooding: 0.52 vs 0.45, p=0.04, open: 0.27 vs 0.17, p=0.0007).DiscussionWe concluded that rearing aviary design can affect behavior during the brooding phase; however, once the brooding compartments were opened, housing differences almost exclusively affected white pullets. The data suggest that genetic strain of birds must be considered in the design of pullet housing with the goal of maximizing space use and musculoskeletal development of laying hen pullets.