Page 70 - Summer2020

ADAPTED EARS OF TERRESTRIAL MAMMALS
clouded leopards and unpublished findings from our laboratory suggesting that other members of Panthera may exhibit the same trait, the unusual timing relation- ship considered here may have been passed to tigers and other large cats but may have washed out of the taxonomic flow in the other felid lineages in which the trait has not been observed.
Regardless, efforts to begin considering potential mecha- nisms that might underlie this unusual physiology require us to briefly review a few key elements in inner ear bio- mechanics for those who may be less familiar with the process. The prevailing textbook explanation of the stan- dard mammalian latency-frequency relationship borrows from classical filter theory and derives from a notably large and consistent inner ear biomechanics literature. Sensory scientists have known from the time of von Békésy (1960) that vibrations on the BM propagate as traveling waves in a base to apex direction, consuming time as they travel toward inner ear mechanical filters that match stimula- tion frequencies and toward their so-called characteristic place along the BM. Therefore, travel time is a clear and relevant term in the latency/frequency equation, but it is not the only relevant timing factor. In addition to passive cochlear delays, timing is influenced by active cochlear filter-response times that are dependent on outer hair cell electromotility (Brownell, 2017), the mechanism that amplifies responses near the characteristic place and sharpens filter responses. The ultimate outcome of all of this from a response-timing perspective is that high-fre- quency propagation times are normally shorter than times associated with lower frequency responses (cf. Figure 4, B and C). Clearly, some members of the Panthera lineage, including the tiger and clouded leopard, settled on a dif- ferent auditory timing strategy than other mammals.
The natural questions emerging from this finding are, first, where in the inner ear does this presumed adaptation origi- nate, and second, what specific inner ear structure, if any, underwent adaptation? To attempt to answer this question, we turn our attention to morphological features in the organ of Corti in search for evidence of adaptation, and particular attention will be paid to the base of the cochlea, the region responsive to high- and mid-range frequencies. The deci- sion to concentrate on basal regions was driven primarily by preliminary findings from a masking study conducted in our laboratory on a Bengal tiger (Panthera tigris tigris).
Although preliminary in large measure because of the limited access to these very large and endangered animals, findings from that effort suggest that a substantial signal from the basal half of the tiger cochlea contributes consid- erably to the fast response times to low frequencies in this big cat (Figure 5A). A hypothetical scenario based on a few key relevant findings is offered in A Hypothetical Answer to the Response-Timing Conundrum.
A Hypothetical Answer to the Response- Timing Conundrum
That a relatively narrow band of low-frequency, moderate-
level sounds drive up discharge rates of individual auditory nerve fibers tuned to high frequencies is a well-known phe- nomenon in auditory neuroscience circles. This so-called
Figure 5. A: results of a study showing that the basal half of the tiger’s cochlea contributes substantially to the latency of a response to a relatively low-frequency tone (2 kHz). Insets: extremes of the stimulus spectra shown schematically (pink, signal or “probe tone”; green, high-pass noise masker). Starting with a relatively broadband noise that masks responses from all cochlear regions basal to the probe tone (A, bottom left), the noise cutoff frequency was increased, decreasing the area of the cochlea being masked (A, bottom right), and resulting in faster response times. Red circles, latencies of the control (C) and recovery (R) responses to the probe tone recorded before and after the masker was presented, respectively. B: example of a tuning curve recorded from an auditory nerve fiber of a domestic cat, indicating the
“tip” and “tail” resonances. Red arrow, direction of threshold shift of a hypersensitive tail. Inset: photograph of the authors preparing to record brain potentials from a tiger.
70 Acoustics Today • Summer 2020