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second neural resonance, often referred to as the “tail” of tuning curves, is easily differentiated from the sharply tuned primary resonance, as seen in an auditory nerve fiber tuning curve (Figure 5B). The mechanism responsible for the appearance of the tail has been linked to a second inner ear traveling wave, this one on the tectorial membrane (TM; Allen and Fahey, 1993), a gelatinous, acellular matrix of stri- ated connective tissue that couples the mechanosensitive hair bundles associated with outer hair cells to motions of the BM and playing an important role in the enhancement of cochlear sensitivity (Figure 1B). The importance of this linkage in the context of this discussion is heightened by noting that many studies have shown significant effects on cochlear sensitivity and tuning as well as the expression of the second resonance in transgenic mice exhibiting altered TM composition or detachment of the structure from its mooring on the spiral limbus (Richardson et al., 2008). Moreover, tail hypersensitivity has been reported in animals under conditions of reduced mechanical coupling between the TM and hair bundles resulting from outer hair cell loss or stereocilia damage. This tight connection between the TM and the expression of the second resonance leads, it can be reasonably argued, to the proposition that specialization of the TM might alter its influence on the expression of the second low-frequency resonance.
We do know that the mammalian TM is a viscoelastic structure with electrokinetic, piezoelectric-like proper- ties (Sellon et al., 2019). That is, deformation of the TM creates an electric response within the solid matrix of the structure. We also know that the biomechanical proper- ties are influenced by the concentration of fixed charges associated with the structure; the greater the fixed charge, the greater the electrokinetic effect. This brings us to ask the provocative question: if evolutionary processes led to the exaggeration of fixed charge in the tiger’s TM, could a powerful electrokinetic force enhance the sensitivity of the low-frequency resonance and trigger basal turn responses to low-level, low-frequency stimuli? Could such a system explain, at least partially, the strange case of response timing in tigers and their close relatives? Efforts to address this question are underway, but those efforts are compli- cated by the relative unavailability of subjects.
Conclusion
Over the course of the past 200 million years or so, mam- malian hearing was shaped and refined by the forces of natural selection. The process culminated in the evolution
of hearing organs with remarkable sensitivity, extraordi- nary dynamic range, and an operational range spanning a 10-octave frequency range in some mammalian species. Layer on top of this accounting of evolution the diverse expression of adaptation rarities witnessed in response to virtually every territory invaded by mammals as their populations radiated from one ecosystem to another and the inventiveness of natural selection clarifies. This article has concentrated on one well-understood and much- studied evolutionary wonder, the Namib golden mole, whose middle ear is a true marvel of nature, of evolution, and of natural selection. We also focused on a mysterious, poorly understood twist on our contemporaneous model of inner ear biomechanics, one trait that, potentially, dif- ferentiates the tiger and the clouded leopard, and possibly other big cats, from the rest of the mammalian class. One is the material of textbooks, the other remains shrouded in mystery, awaiting the careful scrutiny of science.
Acknowledgments
We express sincere appreciation to Lee Simmons, Doug- las Armstrong, and Heather Robertson and the veterinary and animal care staff at Omaha’s Henry Doorly Zoo and Aquarium (NE) and the Nashville Zoo at Grassmere (TN) for their cooperation and support of this research.
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