Cooperative Function of Two Active Ears via Interaural Coupling

The left and right ears of some non-mammals can act as a “pressure-gradient receiver” to improve directional sensitivity by virtue of acoustic coupling of the tympanic membranes via the interaural canal (IAC). A seminal study by Roongthumskul et al. (2019) extended this to show that the two active inner ears of a gecko can also effectively synchronize (i.e., each adjusts their self-oscillation frequencies due to coupling). This result is significant because it suggests that the two ears can expend energy to influence one another, with myriad implications for auditory function (e.g., low sound level localization). A subsequent study examining Anolis lizards showed that spontaneous and evoked otoacoustic emissions (OAE) are readily measurable in the IAC using an orally placed probe (Bergevin et al., 2020). Further, acoustic modeling of the IAC using known morphology showed that the motion of one eardrum, presumably driven by the ipsilateral inner ear, was sufficient to drive the contralateral eardrum and thereby couple the two (inner) ears. We expand upon those studies by reporting simultaneous SOAE measurements made externally at the left and right meatuses from six anoles. Several general features were considered, including overlap of SOAE spectral magnitudes across ears and vector strength determined from the phase. Half the experiments showed clear magnitude overlap from both ears above 1.5 − 2 kHz but less of a match below. The other lizards exhibited SOAE activity that was not as well-matched between ears. Similar to that reported for geckos, vector strength was often observed to be elevated in regions of overlapping SOAE activity, including about the “valleys” between peaks. Further, vector strengths could show larger maximum values for anole compared to gecko. Individual SOAE peaks were also filtered to extract amplitude (AM) and frequency modulations (FM), from which we performed fluctuation correlation analyses. We found that ipsilateral pairs (i.e., peaks at different frequencies measured from one ear) could show weak AM correlations (usually for nearest neighbors), but no FM correlations were present. However, relatively much stronger AM and FM correlations could be observed for peaks at similar frequencies measured simultaneously across ears – even at the valleys between peaks. Further, correlation delays between ears were not constant (i.e., it did not appear that one ear was uniformly driving the other). Additionally, we examined the effect of external sound stimulation to determine a “trans-IAC” transfer function (i.e., from one probe sealed at the external meatus relative to the other). These exhibited attenuation across the spectrum and phase-gradient delays slightly longer than expected, given the probe separation. These measurements suggest additional delay contributions beyond airborne acoustic propagation (e.g., tympanic motions) and that an emission measured ipsilaterally may contain contributions from both ears. In summary, this study bolsters evidence that the two ears of a lizard may act cooperatively by actively synchronizing via the IAC.

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