The frog inner ear: picture perfect?

This is the accepted manuscript of a paper published in the Journal of the Association for Research in Otolaryngology (2015) DOI: 10.1007/s10162-015-0506-zMany recent accounts of the frog peripheral auditory system have reproduced Wever's (1973) schematic cross-section of the ear of a leopard frog. We sought to investigate to what extent this diagram is an accurate and representative depiction of the anuran inner ear, using three-dimensional reconstructions made from serial sections of Rana pipiens, Eleutherodactylus limbatus and Xenopus laevis. In Rana, three discrete contact membranes were found to separate the posterior otic (=endolymphatic) labyrinth from the periotic (=perilymphatic) system: those of the amphibian and basilar recesses and the contact membrane of the saccule. The amphibian 'tegmentum vasculosum' was distinguishable as a thickened epithelial lining within a posterior recess of the superior saccular chamber. These features were also identified in Eleutherodactylus, but in this tiny frog the relative proportions of the semicircular canals and saccule resemble those of ranid tadpoles. There appeared to be a complete fluid pathway between the right and left periotic labyrinths in this species, crossing the cranial cavity. Xenopus lacks a tegmentum vasculosum and a contact membrane of the saccule; the Xenopus ear is further distinguished by a lateral passage separating stapes from periotic cistern and a more direct connection between periotic cistern and basilar recess. The basilar and lagenar recesses are conjoined in this species. Wever's diagram of the inner ear of Rana retains its value for diagrammatic purposes, but it is not anatomically accurate or representative of all frogs. Although Wever identified the contact membrane of the saccule, most recent studies of frog inner ear anatomy have overlooked both this and the amphibian tegmentum vasculosum. These structures deserve further attention.The authors wish to thank Emanuel Mora for his help and support with this project. Dave Simpson kindly provided the Xenopus specimens. The CT scan of Xenopus was made by Alan Heaver of the University of Cambridge Department of Engineering, with thanks going also to Norman Fleck for the use of his equipment. The authors are very grateful to Dolores Bozovic, Alan D. Grinnell, Tammy Hoang, Victoria Sandoval and Felix E. Schweizer for facilitating the Rana CT scan, which was made by Ting-Ling Chang at the UCLA School of Dentistry, Division of Advanced Prosthodontics. Stephan Kamrad helped with translations. The research of JMS and PvD was supported by the Heinsius Houbolt Foundation and is part of the research programme Healthy Ageing and Communication of the Department of Otorhinolaryngology at the University Medical Center Groningen. Finally, the authors wish to thank the reviewers and editors of the manuscript for their very helpful comments

Mechanics of the exceptional anuran ear

The anuran ear is frequently used for studying fundamental properties of vertebrate auditory systems. This is due to its unique anatomical features, most prominently the lack of a basilar membrane and the presence of two dedicated acoustic end organs, the basilar papilla and the amphibian papilla. Our current anatomical and functional knowledge implies that three distinct regions can be identified within these two organs. The basilar papilla functions as a single auditory filter. The low-frequency portion of the amphibian papilla is an electrically tuned, tonotopically organized auditory end organ. The high-frequency portion of the amphibian papilla is mechanically tuned and tonotopically organized, and it emits spontaneous otoacoustic emissions. This high-frequency portion of the amphibian papilla shows a remarkable, functional resemblance to the mammalian cochlea

Input-output characteristics of the tectorial membrane in the frog basilar papilla

The basilar papilla (BP) in the frog inner ear is a relatively simple auditory receptor. Its hair cells are embedded in a stiff support structure, with the stereovilli connecting to a flexible tectorial membrane (TM). Acoustic energy passing the papilla presumably causes displacement of the TM, which in turn deflects the stereovilli and stimulates the hair cells. In this paper we present optical measurements of the mechanical response of the TM to various stimulus levels. Results were obtained from 3 specimens (4 ears). The phase of the displaced area of the TM was constant across stimulus levels. Phase differences between the orthogonal spatial motion components were either close to 0 degrees or 180 degrees. These findings were consistent with a TM motion along the epithelium surface. The TM response was linear for stimulus levels up to -30 dB (re. 1 mu m) at the operculum. This amplitude was estimated to exceed that at which neural responses saturate. Apparently, saturation of the neural response in the frog inner ear is not based on saturation of the mechanical response of the tectorial membrane. (C) 2010 Elsevier B.V. All rights reserved

Wiener kernel analysis of inner ear function in the American bullfrog

The response of 17 primary auditory nerve fibers in the American bullfrog (Rana catesbeiana) to acoustic noise stimulation of the tympanic membrane was recorded. For each fiber, the first- and second-order Wiener kernels, k(1)(tau(1)) and k(2)(tau(1),tau(2)), were computed by cross correlation of the stimulus and the response. The kernels revealed amplitude and phase characteristics of auditory filters of both phase-locking and non-phase-locking fibers. Wiener kernels of high- and midfrequency fibers (best frequency, BF>500 Hz), implied a simple sandwich model, consisting of a cascade of a linear bandpass filter, a static nonlinearity, a linear low-pass filter, and a spike generator. The bandpass filter was at least of order 7, and had a linear phase response, for both the high- and the midfrequency fibers. Averaged across fibers, filter order 2, and cutoff frequency 451 Hz for the second filter in the model was observed. The responses of low-frequency fibers (BF<500 Hz) could not be fit with the sandwich model, because the Fourier transform K-2(f(1),f(2)) of the second-order Wiener kernel showed significant components at off-diagonal frequencies f(1) not equal+/-f(2). The presence of these off-diagonal components shows that, in addition to the phase and gain characteristics of auditory filters, the Wiener kernel analysis reveals nonlinear two-tone interactions