Mechanical indentation of the vestibular labyrinth and its relationship to head rotation in the toadfish, Opsanus tau

Abstract

1. In the present study we examine the response of the semicircular canal of the toadfish (Opsanus tau) to head rotation and to mechanical indentation of the membranous labyrinth. The relationship between the two stimuli is described by a new elastohydrodynamic model that delineates the three-dimensional (3-D) spatiotemporal distribution of endolymph pressure and flow. In vivo electrophysiological recordings of primary afferents supplying the horizontal canal (HC) were employed to validate the model predictions. Data were collected from 213 afferents in 18 fish during independent head rotation. HC indentation, utricle (U) indentation, and paired stimuli. To quantify the afferent response and the relationship between the applied sinusoidal stimuli, the magnitude (gain) and temporal relationship (phase) of the first harmonic of modulation were calculated and compared with theoretical predictions. 2. A mathematical based extensively on the 3-D morphology of a toadfish labyrinth and the physical properties of endolymph is presented to describe the relationship between head rotation and mechanical indentation. All model parameters specifying labyrinthine morphology and physical properties of endolymph are known; the model contains no free parameters. New results are independent of the structural properties of the cupula. The analysis employs an asymptotic solution of the Navier-Stokes equations in the three toroidal ducts that includes the 3-D fluid-structure interaction taking place within the enlarged ampulla. The solution addresses the differential pressure (delta P) acting across the cupula and the dilatational pressure acting on both sides of the cupula. The analysis quantifies the hydrodynamics of the HC for mechanical indentations of the long and slender portion of the canal duct (HC indentation) and the U (U indentation). Results specifically relate the indentation stimuli to head rotation. Linear commutations of HC indentation, U indentation, and rotation stimuli are analyzed by matching delta P acting across the cupula for the three stimulus modalities. 3. HC afferents show a linear correspondence between HC indentation, U indentation, and rotation stimuli. Specific experimental results for sinusoidal stimuli at frequencies < 2 Hz show 1) +/- 1 micron-HC indentation commutates with +/- 4 degrees/s rotation, 2) + 1-micron HC indentation commutates with -/+ 15-microns U indentation, and 3) -/+ 15-microns U indentation commutates with +/- 4 degrees/s rotation. These results were obtained by adjusting the relative amplitude and phase of two stimuli presented simultaneously to achieve destructive interaction that minimizes the afferent modulation (balanced). Equivalent results were obtained using afferent responses to the stimuli applied independently.(ABSTRACT TRUNCATED AT 400 WORDS)

Discharge regularity in the turtle posterior crista: comparisons between experiment and theory

“…As has been established in a variety of species (review: Lysakowski and Goldberg 2004), including turtles (Brichta and Goldberg 2000a), the rotational responses of irregular units have larger gains and larger phase leads than do the responses of regular units. Reflecting the similar biomechanics governing canal-duct indentation and head rotations (Dickman and Correia 1989a;Rabbitt et al 1995), such trends are also observed when indentations replace rotations. Regressions with CV* in the present study give a 30-fold increase in spike gain (Fig.…”

“…Direct measures of mean AHPs and synaptic noise allowed us to compare the influences of d V /dt and V on CV*. Responses to canal-duct indentation (Dickman and Correia 1989a;Rabbitt et al 1995) were studied to identify the presynaptic and postsynaptic contributions to gains and phases. An improved version of an integrate-and-fire model (Smith and Goldberg 1986) was used to interpret empirical data.…”

Mechanical amplification by hair cells in the semicircular canals

“…5A plots the amplitude (first plus second harmonics) as a function of angular velocity of the head. Results for three animals were converted to equivalent angular head velocity using a 1-μm indentation as equivalent to a 4°/s angular velocity (31). The response was nearly linear for cupula motions >500 nm and mechanical stimuli >7°/s but deviated from linearity at lower levels.…”

Responses of Irregularly Discharging Chinchilla Semicircular Canal Vestibular-Nerve Afferents During High-Frequency Head Rotations

“…4 and 5. The physiologic basis for this lead effect is hypothesized to be a combination of mechanical and transduction effects in the neuroepithelium (Rabbitt et al 1995). Goldberg and Fernandez (1971) ( HF1 s ϩ 1).…”