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. 2012;7(2):e31008.
doi: 10.1371/journal.pone.0031008. Epub 2012 Feb 13.

Tonotopically arranged traveling waves in the miniature hearing organ of bushcrickets

Arun Palghat Udayashankar  1 , Manfred Kössl, Manuela Nowotny
Affiliations

Tonotopically arranged traveling waves in the miniature hearing organ of bushcrickets

Arun Palghat Udayashankar et al. PLoS One. 2012.

Abstract

Place based frequency discrimination (tonotopy) is a fundamental property of the coiled mammalian cochlea. Sound vibrations mechanically conducted to the hearing organ manifest themselves into slow moving waves that travel along the length of the organ, also referred to as traveling waves. These traveling waves form the basis of the tonotopic frequency representation in the inner ear of mammals. However, so far, due to the secure housing of the inner ear, these waves only could be measured partially over small accessible regions of the inner ear in a living animal. Here, we demonstrate the existence of tonotopically ordered traveling waves covering most of the length of a miniature hearing organ in the leg of bushcrickets in vivo using laser Doppler vibrometery. The organ is only 1 mm long and its geometry allowed us to investigate almost the entire length with a wide range of stimuli (6 to 60 kHz). The tonotopic location of the traveling wave peak was exponentially related to stimulus frequency. The traveling wave propagated along the hearing organ from the distal (high frequency) to the proximal (low frequency) part of the leg, which is opposite to the propagation direction of incoming sound waves. In addition, we observed a non-linear compression of the velocity response to varying sound pressure levels. The waves are based on the delicate micromechanics of cellular structures different to those of mammals. Hence place based frequency discrimination by traveling waves is a physical phenomenon that presumably evolved in mammals and bushcrickets independently.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Measurement setup and preparation of the crista acustica.
(a) The bushcricket is waxed onto a freely movable stage and the leg is passed though a chamber filled with insect Ringer and is fixed with wax to avoid movement during the measurement. (b) Crista acustica stained with methylene blue as viewed with a 10× objective. Notice the gradual decrease in dimensions of the cap cells from proximal to distal region of the leg. (c) Magnified view of a cap cell and scolopidium, as viewed with a 40× objective. The bottom panel shows schematic drawings of the cap cell as viewed from the top and side, not to scale. Abbreviations: TM - tectorial membrane, S.C. - scolopidium (d) A laser Doppler vibrometer coupled to a confocal microscope was used to make the vibration measurements. The laser beam was focussed on the scolopidia through a small window opening above the organ location. Scale bars: (b): 100 µm and (c): 10 µm.
Figure 2
Figure 2. Traveling waves along the crista acustica.
(a) Typical preparation of the crista acustica after removing the overlying cuticle, tissue and hemolymph as seen with a 10× objective. (b) Measurement grid used for the measurements. Nodes on the graph represent the points scanned by the laser-Doppler-vibrometer. The edges of the grid were determined by an automated nearest neighbour algorithm built into the measurement software to interpolate the measured points by triangulation to render the surface data. (c) Side view of the interpolated surface measured for stimulus frequency of 12 kHz at 80 dB SPL. The top most panel indicates the maximum RMS amplitude measured at each point during the entire cycle. The subsequent panels indicate the flow of traveling wave from the distal (dist.) to the proximal (prox.) location with time for one period in 60° steps. Increase of the sound frequency leads to a gradual distal shift of the area responding with the maximum rms velocity. The colour coded scale bar indicates the normalized velocity range. Abbreviations: ant. - anterior; at.- acoustic trachea; ca- crista acustica; dist.- distal; post. – posterior, prox.- proximal; sc- scolopidium; Scale bar: 100 µm.
Figure 3
Figure 3. Tonotopic representation of pure tone stimulated motion of the crista acustica.
(a) Normalized mechanical response profiles of the crista acustica along the dendrite axis measured for various frequencies (9–48 kHz) at 80 dB SPL. (b) Corresponding phase responses to a. The values above and below each curve are the maximum and minimum values of the measured phase response. (c) Spatial spread (the width of the response peak at the magnitude 5 dB below the maximum velocity) for a given frequency calculated from the velocity profiles for various frequencies (9–60 kHz) in one preparation. The spatial spread (horizontal lines) and the corresponding midpoints (dots) are marked in the figure. (d) Distribution of midpoints of spatial spread (maximum velocity) along the length of the organ induced by different frequencies. Data points from nine different animals were fitted with an exponential function.
Figure 4
Figure 4. Comparative traveling wave characteristics.
(a) Mean traveling wave velocity for increasing sound frequencies in M. elongata compared to other species. Notice that the slope for each species (except in locusts) is inversely proportional to it's corresponding topographic spread (in Hz/m, indicated in brackets; see text for explanation). Humans have the smallest topographic spread (indicative of an excellent frequency resolution) (b) The corresponding wavelength values to a. Notice that for the bushcrickets and mammals the wavelength values are in the same range for the shown frequency range. Since velocity data for the human cochlea were determined by indirect means, it was not possible to get the corresponding wavelength data.
Figure 5
Figure 5. Compressive nonlinearity of the velocity response in M. elongata.
(a) The velocity response profiles for various sound pressure levels (30–110 dB SPL) at 21 kHz. An increase in sound pressure level leads to a nonlinear of the velocity response. This effect is particularly apparent above 80 dB SPL. (b) The phase response profiles for the same sound pressure levels as in a. The dotted line represents the centre frequency location.
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