What is the nature of bone in vivo electricity?

The nature of bone electricity is a recurrent question in bone biomechanics. Even if the electro-chemical couplings are supposed to play an important role in the mechanotransduction of bone remodelling (Lemaire et al. 2008), the origin itself of bone in vivo electricity is still an open question (Ahn and Grodzinsky 2009). In the 1960s, collagen piezoelectricity was invoked as a potential mechanism by which the mechanosensitive cells of bone could detect areas of greater stress. Thus, applied stress would generate local potential gradients along the collagen fibres providing a local stimulus for bone-remodelling cells (Bassett et al. 1964). Afterwards, this idea faded away when other mechanisms, such as streaming potential (Salzstein and Pollack 1987) and fluid-generated shear stress (Weinbaum et al. 1994), were described. Recent advances in the understanding of bone physiology raise again a possible relevance of piezoelectricity effects in bone (Ahn and Grodzinsky 2009). Are the in vivo measured potentials due to the piezoelectric property of collagen or to the strain-induced electro-osmotic flow? This study aims at determining the nature of the in vivo electricity that can be experimentally observed. Our approach combines electrokinetics involved in interstitial bone fluid flow with the piezoelectric behaviour of the collagen apatite matrix (Lemaire et al. 2010a, 2011a, 2011b). To capture the origin of in vivo bone electricity, the microscopic electro-chemical phenomena are propagated at the organ scale by homogenisation. An illustrative recovery of the in vivo electric potentials measured on a walking dog is also proposed.