Influence of Surgical Plugging on Horizontal Semicircular Canal Mechanics and Afferent Response Dynamics

Abstract

Mechanical occlusion of one or more of the semicircular canals is a surgical procedure performed clinically to treat certain vestibular disorders and used experimentally to assess individual contributions of separate canals and/or otoliths to vestibular neural pathways. The present experiments were designed to determine if semicircular canal afferent nerve modulation to angular head acceleration is blocked by occlusion of the endolymphatic duct, and if not, what mechanism(s) might account for a persistent afferent response. The perilymphatic space was opened to gain acute access to the horizontal canal (HC) in the oyster toadfish, Opsanus tau. Firing rate responses of HC afferents to sinusoidal whole-body rotation were recorded in the unoccluded control condition, during the process of duct occlusion, and in the plugged condition. The results show that complete occlusion of the duct did not block horizontal canal sensitivity; individual afferents often exhibited a robust firing rate modulation in response to whole-body rotation in the plugged condition. At high stimulus frequencies (about >8 Hz) the average sensitivity (afferent gain; spikes/s per °/s of head velocity) in the plugged condition was nearly equal to that observed for unoccluded controls in the same animals. At low stimulus frequencies (about <0.1 Hz), the average sensitivity in the plugged condition was attenuated by more than two orders of magnitude relative to unoccluded controls. The peak afferent firing rate for sinusoidal stimuli was phase advanced ∼90° in plugged canals relative to their control counterparts for stimulus frequencies ∼0.1–2 Hz. Data indicate that afferents normally sensitive to angular velocity in the control condition became sensitive to angular acceleration in the plugged condition, whereas afferents sensitive to angular acceleration in the control condition became sensitive to the derivative of acceleration or angular jerk in the plugged condition. At higher frequencies (>8 Hz), the phase of afferents in the plugged condition became nearly equal, on average, to that observed in controls. A three-dimensional biomechanical model of the HC was developed to interpret the residual response in the plugged condition. Labyrinthine fluids were modeled as incompressible and Newtonian; the membranous duct, osseous canal and temporal bone were modeled as visco-elastic materials. The predicted attenuation and phase shift in cupular responses were in close agreement with the observed changes in afferent response dynamics after canal plugging. The model attributes the response of plugged canals to labyrinthine fluid pressure gradients that lead to membranous duct deformation, a spatial redistribution of labyrinthine fluids and cupular displacement. Validity of the model was established through its ability to predict: the relationship between plugged canal responses and unoccluded controls (present study), the relationship between afferent responses recorded during mechanical indentation of the membranous duct and physiological head rotation, the magnitude and phase of endolymphatic pressure generated during HC duct indentation, and previous model results for cupular gain and phase in the rigid-duct case. The same model was adjusted to conform to the morphology of the squirrel monkey and of the human to investigate the possible influence of canal plugging in primates. Membranous duct stiffness and perilymphatic cavity stiffness were identified as the most salient model parameters. Simulations indicate that canal plugging may be the most effective in relatively small species having small labyrinths, stiff round windows, and stiff bony perilymphatic enclosures.