Motivated by recent developments suggesting that interaural coupling in non-mammals allows for the two active ears to effectively synchronize, this report describes otoacoustic measurements made in the oral cavity of lizards. As expected from that model, spontaneous otoacoustic emissions (SOAEs) were readily measurable in the mouth, which is contiguous with the interaural airspace. Additionally, finite element model calculations were made to simulate the interaural acoustics based upon SOAE-related tympanic membrane vibrational data. Taken together, these data support the notion of two active ears synchronizing by virtue of acoustic coupling and have potential implications for sound localization at low-levels.

A mesoscopic approach to modeling the auditory periphery for non-mammals is emerging that considers two facets: the inner ear as a collection of coupled nonlinear active elements [e.g., Vilfan and Duke (2008)] and that two ears are acoustically coupled together via the middle ear [e.g., Roongthumskul et al. (2019)]. Such an approach motivates a biophysical principle underlying the auditory periphery—synchrony amongst the disparate constituent parts of the ear. That is, synchrony refers to the dynamics associated with weakly-coupled self-sustained (i.e., active) oscillators (Pikovsky et al., 2003). Given the fairly nonlinear nature of the inner ear, synchrony elucidates how coupling plays a crucial role in giving rise to the ear's remarkable functionality. The present goal of this paper is to examine a key testable prediction that emerges from such a framework.

In many classes of terrestrial non-mammalian vertebrates, two ears are acoustically coupled by means of a pathway called the interaural canal (IAC), which spans across the head (i.e., the middle ear space in contiguous between left and right ears). Numerous studies have indicated this interaural coupling has important implications for passive sound localization (Fletcher and Thwaites, 1979; Rosowski and Saunders, 1980). As a “pressure difference receiver,” the basic physical mechanism is that acoustic “crosstalk” differentially affects ipsi- and contralateral tympanic membrane (TyM) motions [e.g., see Fig. 1 from Christensen-Dalsgaard and Manley (2008)]. Thereby each TyM is effectively driven from both sides, not just via sound fields external to the head, leading to a “directional ear” (Fletcher and Thwaites, 1979). This notion is chiefly passive in nature, as it ignores the active properties of the inner ear.

However, ample evidence exists to indicate the inner ear is active (i.e., contains energy-producing mechanisms) (Manley et al., 2001), raising important implications for such models of azimuthal localization. A mesoscopic approach toward studying such is to treat an active ear as a collection of coupled nonlinear active limit-cycle oscillators [e.g., Bergevin (2016); Bergevin and Shera (2016); Vilfan and Duke (2008)] and with two inner ears that are coupled acoustically via the IAC [e.g., Livens et al. (2019); Roongthumskul et al. (2019)]. Indeed, recent evidence indicates that the two active ears of geckos do synchronize (Roongthumskul et al., 2019). That important result has significant implications, such as measurements being interpreted as arising from “one ear” may in fact represent a collective response.

The present study is focused on testing a key prediction of this mesoscopic model in lizards. Specifically, the results of Roongthumskul et al. (2019) suggest that spontaneous otoacoustic emissions (SOAEs) should be present in the oral cavity, which is contiguous with the interaural space [see Figs. 3(A) and 3(B)]. Further, the model would suggest that the spontaneous TyM motion of SOAE activity [e.g., Bergevin et al. (2018)] provides a mechanism to internally broadcast energy to the contralateral ear. Thus, it is desirable to quantitatively characterize the net forces generated on the contralateral ear given the pressure inside the IAC due to the SOAE-driven motion of one ear. To achieve these aims, we focus on Anolis lizards, which have a relatively simple inner ear morphology (Miller, 1985; Negandhi et al., 2018; Wever, 1978) and robust SOAE activity that shows numerous sharp peaks well above the noise floor with statistical properties generally consistent with a limit-cycle oscillation (Bergevin et al., 2015, 2010, 2011; Manley, 2006; Manley and Gallo, 1997). The auditory papillae of the green anole (Anolis carolinensis) each have 150 hair cells, the majority of which are not covered by any tectorial structure (i.e., the bundles are “free-standing”). Further, there is ample evidence to suggest that anoles do not have the classic analog of a basilar membrane traveling wave (Manley et al., 1988; Peake and Ling, 1980). We note that an overlying tectorial structure(s), chiefly absent for anoles, is commonly assumed important to couple bundles together and thereby help overcome viscous forces to affect tuning properties [e.g., Bergevin et al. (2010); Manley (2011)] or change the effective mechanical loading (Ó Maoiléidigh et al., 2012). Further, μCT data of the entire head of the green anole are available (Gauthier et al., 2012) and a recent finite element (FE) model was proposed for the middle ear of the brown anole (A. sagrei) (Livens et al., 2019), facilitating exploration of how coupling affects the two ears.

Otoacoustic measurements were made in six green anoles (Anolis carolinensis). Lizards were lightly anesthetized and placed on a regulated heating blanket to stabilize their body temperature. Output from a sensitive microphone (ER-10C, Etymotic, Elk Grove Village, IL) was digitized (sample rate of 44.1 kHz with a 24 bit-depth) using a customized data acquisition system. Two types of spectral measures were obtained. First, recordings were made of a 120 s waveform. Subsequently, the fast Fourier transform was computed and the magnitude extracted of 400 successive artifact-free 8192 point buffers to obtain an averaged spectrum [e.g., Figs. 2(A)–2(C)]. The second method was similar, though it entailed buffers of 32 768 points with 60 spectral averages [e.g., Fig. 2(D)].

For meatal placement [Fig. 1(A)], the probe was gently coupled to the side of the head and sealed with grease. A thermocouple was placed in the mouth to monitor temperature, slightly propping it open. For oral probe placement [Fig. 1(B)], a larger coupling tip was used to make a tight seal between the oral and interaural spaces. The respiratory pathway does not appear blocked, as their nasal passages run in parallel above the roof of the oral cavity (not shown in Fig. 3 but apparent in the μCT data). Thus placement of the probe did not appear to produce hypoxic effects, but still achieved an effectively closed coupling.

Fig. 1.

(Color online) Comparison of otoacoustic probe placement for both the external meatus (A) and the oral cavity (B).

Fig. 1.

(Color online) Comparison of otoacoustic probe placement for both the external meatus (A) and the oral cavity (B).

Close modal

To characterize the interaural space [see Figs. 3(A) and 3(B)], X-ray μCT based image-stacks of an Anolis carolinensis head were downloaded from the DigiMorph repository (License CC-BY=NC; Specimen FMNH 242 298; Scans by Matthew Colbert, University of Texas High resolution X-Ray CT Facility, funded by NSF Grant Nos. IIS-0208675 and EF-0334961). The scans had an X and Y resolution of 0.01445 mm and Z resolution of 0.0317 mm. The air space of the middle ear and the oral cavity was identified in the CT image-stacks and segmentation was carried out using a three-dimensional (3-D) Slicer (v4.6.2, https://www.slicer.org/). The TyMs form the outer limits of the ear canal that is included in this air-space. An STL mesh of the air-space surface was generated. The mesh was smoothed and artifacts removed using MeshLab (v.1.3.4, Visual Computing Lab-ISTI-CNR, http://meshlab.sourceforge.net) and MeshMixer (v3.3.15, Autodesk).

COMSOL Multiphysics (v5.4a) was used to FE model interaural acoustics, simulate the sound field, measure the resulting forces impinging on both tympana, and calculate the resulting displacements. The effects of the ossicles, inner ear coupling, the nasal passages, and the tympanal annulus were not considered. A thermo-viscous acoustic-shell interaction multi-physics module was used, which models the interaction between an acoustics field and a thin plate. This model also accounts for acoustic losses due to the thermal and viscous boundary layers formed in small geometries and their effects on the propagation of acoustic fields. The 3D mesh from the μCT data was imported, and the surface that constituted the TyMs and the tympanal annulus were approximately demarcated using appropriately positioned workplanes [see Fig. 3(B)]. The IAC was designated as being filled with air and having reflective boundaries. The acoustic field developed within this shape could then interact with the tympana, which were modelled as thin plates. The boundary conditions were set such that the outer edge of the annulus was fixed to the ear canal boundary. Both were given a thickness of 28 μm, a density of 1100 kg/m3, a Poisson's ratio of 0.3, and isotropic damping with a loss factor of 0.2. The tympana were designated as having an isotropic Young's modulus of 4 MPa. These values are based on a previous Anolis model (Livens et al., 2019). The uncertainty about the actual value of the lizard Young's modulus appears to mainly influence the prediction of the displacement of the contralateral TyM. The pressure distribution within the acoustic cavity is largely independent of this infinitesimal motion, and therefore so are the predictions of the net force acting upon the membrane.

In the open mouth condition, acoustic loss due to radiation was accounted for by using perfectly matched layers which have been developed as a method to simulate sound radiation without any model-induced reflections. The tetrahedral mesh used to solve the model had ≈28 000 elements with a minimum element size of 0.769 mm and was generated before the model was solved. The highest frequency modeled was 10 kHz, corresponding to a wavelength of 3.4 cm. Thereby, each wavelength is divided into at least five elements, which was considered sufficient spatial resolution. The left TyM was assigned as the driven one and the entire surface was moved periodically with a 60 pm amplitude at a range of frequencies, from 0.1 to 10 kHz with 100 steps per decade. This drive is intended to mimic a situation where one TyM is driven by spontaneous oscillations emanating from the inner ear. The resulting acoustic field then interacts with the contralateral ear, creating a net force on that membrane and causing it to move. Results from a previous study (Bergevin et al., 2018) showed the Anolis TyM exhibits spontaneous motion driven by (inner ear) SOAE activity with an amplitude of approximately 60 pm, a value used to determine the associated pressure distributions and effects upon the contralateral TyM.

In all animals examined, SOAE activity was readily detectable at both the external meatus (as traditionally measured) and in the oral cavity. Results from four representative animals are shown in Fig. 2. To first order, the meatal and oral otoacoustic emission (OAE) activity match up reasonably well, exhibiting similar levels and spectral peak locations. However, there are instances where the two differ substantially, such as a lack of peaks in the oral measurements for frequencies below 1.8 kHz [Figs. 2(A), 2(C), and 2(D)]. Further, while not shown, oral SOAEs were “suppressible” by an external tone [e.g., at 50 dB sound pressure level (SPL)] at a nearby frequency in a similar fashion to those measured at the external meatus. Evoked emissions such as stimulus frequency otoacoustic emissions and distortion product otoacoustic emissions could also be readily measured in the oral cavity.

Fig. 2.

(Color online) Comparison of otoacoustic data measured at three different locations (left and right external meatuses and the oral cavity) for four different lizards [(A)–(D)]. For the lizard shown in (D), only the left and right spectra are shown as individual waveforms were not measured, precluding their summation as done for the others.

Fig. 2.

(Color online) Comparison of otoacoustic data measured at three different locations (left and right external meatuses and the oral cavity) for four different lizards [(A)–(D)]. For the lizard shown in (D), only the left and right spectra are shown as individual waveforms were not measured, precluding their summation as done for the others.

Close modal

The anolis interaural space is a continuous air cavity, connecting both tympana and the oral cavity in a roughly T-like junction [Figs. 3(A) and 3(B)]. The IAC between two tympana is somewhat flattened along the dorsal-ventral axis of the lizard, flaring out before ending at the back of the tympanal surface. In contrast, the perpendicular pathway that ends in the oral cavity, becomes somewhat inflated toward the anterior end. The nasal passages could also introduce an additional acoustic pathway, although a previous study (Christensen-Dalsgaard and Manley, 2008) has argued that their effect is nominal.

Fig. 3.

(Color online) (A) Coronal section of the μCT data. The black areas indicate airspace, with the vertically-oriented portion on the left representing the interaural space and horizontal band the connection to the oral cavity. (B) 3D reconstruction of the airspace used in the FE model. Note the location of the tympana on the sides, the driven one (see Sec. 2) demarcated in blue on the right (ipsilateral) side. (C) Pressure distribution inside the airspace for the ipsilateral TyM driven as a piston at 60 nm. Note that the color bar span is less than 1 dB. (D) FE model pressure distributions similar to those in (C), however with simpler geometries so as to demonstrate the “closed pipe model” (i.e., resonance at 1/4 wavelength) that arises similarly in both configurations. (E) Frequency response at three different locations (see legend) inside the airspace. Conditions for both a closed mouth (and by similar extension, with a sealed mic in place) and open mouth are shown in the top and bottom, respectively. (F) Displacement of the tympana, with both conditions similar to (E). For the contralateral ear, responses were averaged across the membrane. Note that only the ipsilateral tympanum was constrained to move as a piston.

Fig. 3.

(Color online) (A) Coronal section of the μCT data. The black areas indicate airspace, with the vertically-oriented portion on the left representing the interaural space and horizontal band the connection to the oral cavity. (B) 3D reconstruction of the airspace used in the FE model. Note the location of the tympana on the sides, the driven one (see Sec. 2) demarcated in blue on the right (ipsilateral) side. (C) Pressure distribution inside the airspace for the ipsilateral TyM driven as a piston at 60 nm. Note that the color bar span is less than 1 dB. (D) FE model pressure distributions similar to those in (C), however with simpler geometries so as to demonstrate the “closed pipe model” (i.e., resonance at 1/4 wavelength) that arises similarly in both configurations. (E) Frequency response at three different locations (see legend) inside the airspace. Conditions for both a closed mouth (and by similar extension, with a sealed mic in place) and open mouth are shown in the top and bottom, respectively. (F) Displacement of the tympana, with both conditions similar to (E). For the contralateral ear, responses were averaged across the membrane. Note that only the ipsilateral tympanum was constrained to move as a piston.

Close modal

The pressure field in the IAC associated with SOAE-evoked stimulation was explored using an FE approach. Upon assuming the ipsilateral TyM oscillates at 1 kHz like a piston with an imposed displacement amplitude of 60 pm (Bergevin et al., 2018), Fig. 3(C) shows the resulting pressure field behaves like low frequency “closed pipe” mode [i.e., a pressure minimum occurs just behind the driven ear and a maximum behind the contralateral ear and near the oral cavity; see Fig. 3(D)]. Despite this, the pressure is highly uniform throughout at approximate 25 dB SPL. This value likely represents an upper bound for locations close to the contralateral TyM, given the simplifying assumptions made (e.g., rigid walls, piston-like motion of TyM). Note also that the model is linear, such that an increase in driving TyM amplitude would cause a proportional increase in the pressure amplitude.

To examine variations with frequency, Fig. 3(E) shows the response at three different locations inside the IAC. Overall, for the closed mouth condition (i.e., the mouth is not open widely to space), the pressure near the contralateral TyM and in the oral cavity is either similar to or relatively larger compared to that at the driven ear. For the open mouth condition, the pressure near the two TyMs is closely matched but there is a large uniform drop in oral cavity pressure. Such is consistent with the observation that the oral OAE activity could only be reliably detected when there was a relatively tight acoustic seal between the probe coupler and the back of the mouth. The associated displacement of the contralateral TyM is shown in Fig. 3(F). Note for the closed condition, the displacement was larger than the prescribed 60 pm. This was due to coupling in the FE model, such that the actual tympanal motion is a sum of both the simulated driving force to produce a 60 pm displacement and the induced pressure field in the interaural space.

Despite the similar pressures below 4–5 kHz [Fig. 3(E)], a large difference in the resulting TyM motion is typically observed as shown in Fig. 3(F) (i.e., the contralateral TyM only moves about 1/3 as much at 1 kHz). Such may stem from the ipsilateral driven TyM being forced to oscillate like a piston, while the contralateral TyM is less constrained (i.e., modal patterns could form). To facilitate further discussion, we focus on the relevant eigenmodes (i.e., normal modes, where all spatial elements oscillate at the same frequency with a fixed phase relationship). Two sets of eigenmodes come into play: Those of the IAC pressure and those of the TyM motion. The first two eigenmodes of the IAC are at 6.3 and 14 kHz. At 6.3 kHz, the associated standing wave gives rise to a large anti-node (higher pressure) in the oral cavity, a smaller anti-node (medium pressure) at the contralateral ear, and a node (pressure null) behind the driving tympanum. The contralateral TyM has its first (i.e., simple drum-like) eigenmode at 2.5 kHz. A series of higher eigenmodes, with more complex shapes (e.g., multiple anti-nodes) appear between 3 and 5 kHz. Given that these frequencies are below the IAC acoustic mode, the driving forces at these frequencies are likely to be relatively uniform. Thus, changes in the tympanal displacement, and thereby local variations in pressure levels close to the TyM, would be driven by these changing tympanal mode shapes. For the closed mouth condition in Fig. 3(F), the peaks formed between 2 and 4 kHz for the contralateral ear are thus primarily a result of the tympanal eigenmodes as driven by IAC pressure. In the open mouth condition, the first two eigenmodes of the IAC are 6.6 and 17.6 kHz. Since the tympanal eigenmodes would remain the same, this suggests that the 7 kHz peak is driven by the acoustic pressure eigenmode. While there are several bumps at lower frequencies, the IAC pressure below about 6.6 kHz appears insufficient to generate significant TyM motion when the mouth was open.

Taken together, these observations indicate that there can be substantial pressure responses inside the interaural space due to SOAE-driven motion of the TyM, thereby providing an efficient pathway for coupling energy between the two ears. Further, the modeling results help explain why the presence of observable oral otoacoustic activity would be expected.

The data presented here, both empirical and theoretical, present evidence from Anolis lizards supporting the notion that active ears can effectively synchronize via acoustics of the IAC (Roongthumskul et al., 2019). Such a principle, that the auditory periphery can exhibit synchronization of two active systems, could have broad and significant implications, such as for sound localization at low sound levels and the associated evolutionary considerations. As motivated in Sec. 1, the notion of a “mesoscopic” model helps reinforce a duality with regard to synchronization in the auditory periphery: (1) An individual ear as a collection of synchronized coupled active oscillators and (2) the binaural system as a collection of two synchronized active ears. Sections 4.1, 4.2, and 4.3 focus on, respectively, comparisons to previous work, potential implications for sound localization, and future studies to consider pursuing.

To the best of our knowledge, these results are the first reporting OAEs in the oral cavity. That is, OAEs have previously only been measured “outside” the head or in some instances, intracochlearly using pressure sensors [e.g., Dong and Olson (2006)]. As such, these data help confirm central observations of Roongthumskul et al. (2019). However, several differences are worth noting, chiefly in the context of the modeling approach of the IAC acoustics. Based upon μCT data, the present study uses a 3D geometry that includes the oral cavity, compared to a one-dimensional straight tube (Roongthumskul et al., 2019). As a result, that previous study estimated the characteristic frequency (i.e., fundamental or “first harmonic” of a standing wave resonance) at approximately 15 kHz, significantly higher than approximately 2.5–3 kHz, as estimated by the current study (first TyM eigenmode) and in previous studies (Christensen-Dalsgaard and Manley, 2008; Livens et al., 2019). Further, the current study neglected coupling to the inner ear, whereas Roongthumskul et al. (2019) and Livens et al. (2019) did not. For that latter study in particular, while they reported inter-ear differences not as large as those reported empirically (Christensen-Dalsgaard and Manley, 2008), coupling to the inner ear had a pronounced effect in creating a more uniform response across frequency and thereby making the proposed pressure-difference receiver mechanism more broadband. These effects are not expected to fundamentally change the outcome of what the present modeling efforts were intended to do: Address whether the force (and associated energy) from the inner ear is sufficient to drive the contralateral ear, thereby affecting it and also allowing for oral OAE activity to be observed.

Note that within a given animal, the otoacoustic responses at both the external meatus and oral cavity do not precisely match up (Fig. 2). One might assume that the SOAE spectra measured orally would simply reflect a summation of what is measured at each external meatus, and while qualitatively similar in many regards, that is not quite the case. One reason that may help explain these differences is that the effective acoustic impedance changes between measurement conditions. As similarly discussed with regard to differences between meatal acoustics and SOAE-derived TyM motion (Bergevin et al., 2018), the placement of the probe microphone can change the impedance and thereby affect not only the measured response at the microphone probe tube, but also the generators themselves and their inter-ear coupling. The data shown in Fig. 2 suggest such effects may be more significant below 1.5–2 kHz. Another reason may stem from changes in body temperature that occur while handling the lizards during probe repositioning.

A key motivation underlying the current study stems from the notion that inter-ear coupling affects sound localization. Or more specifically: “This acoustical connection between the two middle ears, with almost perfect transmission from the contralateral ear, generates highly directional tympanic responses that are more pronounced in the lizards than in any other tetrapod studied” (Carr et al., 2016). Roongthumskul et al. (2019) made arguments that the coupling of active inner ears could additionally affect localization, but that remains to be determined. Consider that other non-mammalian groups such as birds have direct interaural coupling between ears (Moiseff and Konishi, 1981; Rosowski and Saunders, 1980) and can exhibit evidence of active mechanisms by virtue of SOAEs. The barn owl in particular shows extensive SOAE activity ranging from 4 to 10 kHz (Bergevin et al., 2015; Taschenberger and Manley, 1997), corresponding to a region that has been described as an “auditory fovea” (Köppl et al., 1993). It is tempting to hypothesize that the principle described here (i.e., interaural coupling effectively synchronizing two ears and thereby contributing to localization) may be at work in those other groups. At present, there is evidence in both directions. On one hand, sound localization at higher frequencies in the barn owl does not appear to make use of interaural coupling, as the IAC acoustics were described as “low-pass” with strong relative attenuation between ears above 4 kHz (Moiseff and Konishi, 1981). On the other hand though, reports [e.g., Köppl (2019); Rosowski and Saunders (1980)] have argued interaural coupling in birds does provide a benefit. All told, the implications for sound localization by virtue of two coupled active ears are still unclear. More specifically, an unresolved question is whether one active inner ear can meaningfully affect the contralateral one, upon taking into account the presence of various sources of noise.

To conclude, several possible considerations are highlighted with regard to further development of a mesoscopic model, especially with regard to “active localization.” The underlying implication that OAE measurements made from one ear may in fact not be derived solely from that ear potentially has significant implications, both for data analysis and theoretical modeling assumptions. Anolis is a useful model for future studies along these lines, given their relative morphological simplicity and robust OAE activity. Empirically, simultaneous measurements from two (or more) microphones would allow several temporal and statistical comparisons without concern of modifying body temperature or changes in effective impedances due to the presence/absence of the probes. Vibrational measurements (e.g., laser Doppler) should also help to better characterize the modal nature of the lizard TyM motion [e.g., Manley (1972)]. Such is central as to how the “drive” from the inner ear sets the TyM into motion, thereby “broadcasting” the SOAE signal both outwards from the meatus as well as inwards into the IAC. On the theoretical side, improvements can be made to the FE model (e.g., non-piston driven TyM, inclusion of ossicles) as well as including the inner ear model treated as a system of coupled nonlinear oscillators. Further, the modeling data here indicates that an open mouth versus a closed mouth can strongly affect the coupling and thereby might be relevant for functional aspects tied to sound localization. Relatedly, one might examine whether there is any evidence that lizards open their mouth as a means to “collect” incident sound energy.

C.B. was supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Grant No. RGPIN-430761-2013.

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