Sebastiaan W. F. Meenderink

Reverse Cochlear Propagation in the Intact Cochlea of the Gerbil: Evidence for Slow Traveling Waves

The inner ear can produce sounds, but how these otoacoustic emissions back-propagate through the cochlea is currently debated. Two opposing views exist: fast pressure waves in the cochlear fluids and slow traveling waves involving the basilar membrane. Resolving this issue requires measuring the travel times of emissions from their cochlear origin to the ear canal. This is problematic because the exact intracochlear location of emission generation is unknown and because the cochlea is vulnerable to invasive measurements. We employed a multi-tone stimulus optimized to measure reverse travel times. By exploiting the dispersive nature of the cochlea and by combining acoustic measurements in the ear canal with recordings of the cochlear-microphonic potential, we were able to determine the group delay between intracochlear emission-generation and their recording in the ear canal. These delays remained significant after compensating for middle-ear delay. The results contradict the hypothesis that the reverse propagation of emissions is exclusively by direct pressure waves.

Mechanics of the frog ear

The frog inner ear contains three regions that are sensitive to airborne sound and which are functionally distinct. (1) The responses of nerve fibres innervating the low-frequency, rostral part of the amphibian papilla (AP) are complex. Electrical tuning of hair cells presumably contributes to the frequency selectivity of these responses. (2) The caudal part of the AP covers the mid-frequency portion of the frogs auditory range. It shares the ability to generate both evoked and spontaneous otoacoustic emissions with the mammalian cochlea and other vertebrate ears. (3) The basilar papilla functions mainly as a single auditory filter. Its simple anatomy and function provide a model system for testing hypotheses concerning emission generation. Group delays of stimulus-frequency otoacoustic emissions (SFOAEs) from the basilar papilla are accounted for by assuming that they result from forward and reverse transmission through the middle ear, a mechanical delay due to tectorial membrane filtering and a rapid forward and reverse propagation through the inner ear fluids, with negligible delay.

Climate change and frog calls: long-term correlations along a tropical altitudinal gradient.

Temperature affects nearly all biological processes, including acoustic signal production and reception. Here, we report on advertisement calls of the Puerto Rican coqui frog (Eleutherodactylus coqui) that were recorded along an altitudinal gradient and compared these with similar recordings along the same altitudinal gradient obtained 23 years earlier. We found that over this period, at any given elevation, calls exhibited both significant increases in pitch and shortening of their duration. All of the observed differences are consistent with a shift to higher elevations for the population, a well-known strategy for adapting to a rise in ambient temperature. Using independent temperature data over the same time period, we confirm a significant increase in temperature, the magnitude of which closely predicts the observed changes in the frogs’ calls. Physiological responses to long-term temperature rises include reduction in individual body size and concomitantly, population biomass. These can have potentially dire consequences, as coqui frogs form an integral component of the food web in the Puerto Rican rainforest.

Anatomy, Physiology, and Function of Auditory End-Organs in the Frog Inner Ear

The vertebrate ear is a highly sensitive frequency analyzer that receives sound through a specialized accessory apparatus (the external and middle ears) prior to its transmission to discrete end-organs containing sensory hair cells (the inner ear). Although there are significant differences in the structures used to receive and analyze sound, amphibian and mammalian ears function very similarly to each other. With few exceptions, the amphibian ear consists of a middle ear and an inner ear, but no external ear. As schematized in Figure 7.1, the amphibian middle ear has an exposed eardrum (tympanic membrane) overlying a funnelshaped tympanic cavity that connects to the inner ear near the base of the skull (see Mason, Chapter 6, for a review of the amphibian middle ear). The amphibian inner ear or otic labyrinth is unique among vertebrate animals in that it has two sensory organs specialized for the reception of airborne sound, the amphibian papilla (AP) and the basilar papilla (BP). These sensory papillae reside within the posterior portion of the otic labyrinth and are contained in ventrally located recesses of the large, fluid-filled saccular chamber shared with two vibration-sensitive macular organs, the sacculus and lagena (Fig. 7.1). Both the AP and BP chambers have a thin contact membrane that separates periotic perilymph from the endolymph fluid of the saccular chamber. Sound energy captured by the eardrum as well as other areas along the body of a frog is converted into fluid displacements and travels along pathways of the otic labyrinth that lead into the endolymphatic spaces of the inner ear (Hetherington et al. 1986; Lewis and Lombard 1988; Purgue and Narins 2000a). The sound path eventually leads into the AP and BP recesses before exiting into the caudal portion of the periotic canal and the round window (Purgue and Narins 2000a). Similar to the mammalian ear, the amphibian ear demonstrates exquisite intensity sensitivity and sharp frequency selectivity that are likely to arise from nonlinear, active amplification processes. How theories of mammalian auditory function apply to amphibian hearing is not known. Mechanisms of tuning and sensitivity have been extensively studied in the mammalian cochlea. It is generally agreed that the initial stage of inner ear

Level dependence of distortion product otoacoustic emissions in the leopard frog, Rana pipiens pipiens

The inner ear of frogs holds two papillae specialized in detecting airborne sound, the amphibian papilla (AP) and the basilar papilla (BP). We measured input-output (I/O) curves of distortion product otoacoustic emissions (DPOAEs) from both papillae, and compared their properties. As in other vertebrates, DPOAE I/O curves showed two distinct segments, separated by a notch or kneepoint. The slope of the low-level segment was conspicuously different between the AP and the BP. For DPOAE I/O curves from the AP, slopes were < or = 1 dB/dB, similar to what is found in mammals, birds and some lizards. For DPOAE I/O curves from the BP these slopes were much steeper (approximately 2 dB/dB). Slopes found at high stimulus levels were similar in the AP and the BP (approximately 2 dB/dB). This quantitative difference between the low-level slopes for DPOAEs from the AP and the BP may signify the involvement of different mechanisms in low-level DPOAE generation for the two papillae, respectively.

Detailed f1, f2 area study of distortion product otoacoustic emissions in the frog.

Distortion product otoacoustic emissions (DPOAEs) are weak sounds emitted from the ear when it is stimulated with two tones. They are a manifestation of the nonlinear mechanics of the inner ear. As such, they provide a noninvasive tool for the study of the inner ear mechanics involved in the transduction of sound into nerve fiber activity. Based on the DPOAE phase behavior as a function of frequency, it is currently believed that mammalian DPOAEs are the combination of two components, each generated by a different mechanism located at a different location in the cochlea. In frogs, instead of a cochlea, two separate hearing papillae are present. Of these, the basilar papilla (BP) is a relatively simple structure that essentially functions as a single auditory filter. A two-mechanism model of DPOAE generation is not expected to apply to the BP. In contrast, the other hearing organ, the amphibian papilla (AP), exhibits a tonotopic organization. In the past it has been suggested that this papilla supports a traveling wave in its tectorial membrane. Therefore, a two-mechanism model of DPOAE generation may be applicable for DPOAEs from the AP. In the present study we report on the amplitude and phase of DPOAEs in the frog ear in a detailed f1, f2 area study. The result is markedly different from that in the mammalian cochlea. It indicates that DPOAEs generated by neither papilla agree with the two-mechanism traveling wave model. This confirms our expectation for the BP and does not support the hypothesized presence of a mechanical traveling wave in the AP.

Frequency matching of vocalizations to inner-ear sensitivity along an altitudinal gradient in the coqui frog

Acoustic communication involves both the generation and the detection of a signal. In the coqui frog (Eleutherodactylus coqui), it is known that the spectral contents of its calls systematically change with altitude above sea level. Here, distortion product otoacoustic emissions are used to assess the frequency range over which the inner ear is sensitive. It is found that both the spectral contents of the calls and the inner-ear sensitivity change in a similar fashion along an altitudinal gradient. As a result, the call frequencies and the auditory tuning are closely matched at all altitudes. We suggest that the animals body size determines the frequency particulars of the call apparatus and the inner ear.

Stimulus frequency otoacoustic emissions in the Northern leopard frog, Rana pipiens pipiens: Implications for inner ear mechanics

Otoacoustic emissions (OAEs) are weak sounds that originate from the inner ear which are traditionally classified/named based on their evoking stimulus. Recently, it has been argued that such a classification, at least for mammals, misrepresents the underlying mechanisms of emission-generation. As an alternative classification, it has been suggested to recognize that OAEs arise either via nonlinear distortion or linear coherent reflection. For non-mammalian vertebrates, data on evoked OAEs that arise via the latter mechanism are largely missing. Here, we present the first measurements of stimulus frequency OAEs (SFOAEs), which are emissions thought to arise via linear coherent reflection, from an amphibian (the Northern leopard frog, Rana pipiens pipiens). Their properties as a function of the evoking stimulus frequencies and levels are described and subsequently compared with the previously reported properties of distortion product OAEs (DPOAEs) from the same frog species.

Comparison between distortion product otoacoustic emissions and nerve fiber responses from the basilar papilla of the frog

The basilar papilla (BP) is one of the three end organs in the frog inner ear that is sensitive to airborne sound. Its anatomy and physiology are unique among all classes of vertebrates. Essentially, the BP functions as a single auditory filter presumably arising from a mechanically-tuned mechanism. As such, both neural and distortion product otoacoustic emission (DPOAE) tuning may reflect a single mechanical filtering mechanism. Using the Duffing oscillator as a simple model for both neural and DPOAE tuning from the BP, two predictions can be made: [1] the characteristic frequency (CF) of neural tuning and the best frequency (BF) of DPOAE tuning will coincide and [2] the neural tuning curve and DPOAE-audiogram have a similar shape when the neural tuning curve is scaled by a factor of 4 along the y-axis. We recorded both neural tuning curves and DPOAE-audiograms from the BP of the leopard frog. These recordings show good agreement with the model predictions when the stimulus tones are related by relatively small stimulus frequency ratios. For larger stimulus frequency ratios, DPOAE recordings clearly deviate from model predictions. These differences are most likely caused by the oversimplified representation of the frog BP by the model.

Characteristics of distortion product otoacoustic emissions in the frog from L1,L2 maps

For a given set of stimulus frequencies (f1 ,f2), the level of distortion product otoacoustic emissions (DPOAEs) varies with the levels of the stimulus tones. By variation of the stimulus levels, L1,L2-maps for DPOAEs can be constructed. Here, we report on L1 ,L2-maps for DPOAEs from the frog ear. In general, these maps were similar to those obtained from the mammalian cochlea. We found a conspicuous difference between the equal-level contour lines for low-level and high-level DPOAEs, which could be modeled by a saturating and an expansive nonlinearity, respectively. The transition from the high-level to the low-level response was accompanied by a DPOAE phase-change, which increased from 0 to pi rad with increasing frequency. These results suggest that in the frog low-level and high-level DPOAEs are generated by separate nonlinear mechanisms. Also, there was a conspicuous difference in the growth of the low-level emissions from the two anuran auditory papillae. In the basilar papilla, this growth was expansive for the lowest stimulus levels and saturated for intermediate levels. This is consistent with the behavior of a Boltzman nonlinearity. In the amphibian papilla this growth was compressive, suggesting the additional effect of a compressive amplification mechanism on the generation of DPOAEs.