Mechanical states encoded by stretch-sensitive neurons in feline joint capsule

P. S. Khalsa, A. H. Hoffman and P. Grigg Department of Physiology, University of Massachusetts Medical School, Worcester 01655, USA. 1. The sensitivity of group II joint afferents innervating cat knee joint capsule to in-plane stretch was studied in vitro. Single afferents were recorded from teased filaments of the posterior articular nerve. The capsule was stretched by applying forces through tabs along the edges of the capsule (3 tabs/edge) with the use of an apparatus that allowed for independent control of each load. The relationships between the neural responses of these afferents and the local continuum mechanical state of the joint capsule have been investigated. By appropriately loading the tissue margins, it was possible to establish states of uniaxial and biaxial tension, including shear. 2. Plane stress was calculated from the loads along the tissue margins. Stress at the location of the mechanoreceptor ending was estimated by interpolation. Strain was calculated from deformations of the capsule measured by tracking markers on its surface. Full characterization of tissue stress and strain made it possible to determine strain energy density and the magnitudes of other coordinate invariant mechanical quantities. 3. Individual afferents (n = 15) exhibited pronounced selectivity to the direction of applied stress and strain. There was no overall preferred orientation across neurons, and simple correlation of individual stress or strain components with the neuronal response revealed no consistent relationship between neuronal response and any single tensor component. However, linear multiple regression of the combined stress and strain components with the neuronal response revealed high correlation (mean R = 0.91), indicating that the measured mechanical states strongly determine the neuronal response. There was a much stronger relationship between neuronal response and stress variables than with strain variables. Simple correlation of the first invariant of the stress tensor with neuronal response had the highest mean correlation of the tensor quantities (R = 0.51). On average, strain energy density was only modestly correlated with the neural response (R = 0.28). 4. These findings indicate that capsule mechanoreceptors are encoding the local continuum mechanical state in the joint capsule. The neural response of these mechanoreceptors is more strongly correlated to local stress than to local strain.