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Evolutionary Perspective of Cochlear Amplification and NIHL

Shofner, William P. PhD

doi: 10.1097/01.HJ.0000521763.31237.16
Hearing and Evolution

Dr. Shofner is an associate professor and AuD program coordinator in the Department of Speech and Hearing Sciences at Indiana University-Bloomington. His research and teaching interests are in the areas of comparative auditory physiology and perception.

We live in a noisy world. Modern industrialization and technologies have resulted in an acoustic environment that routinely exposes us to high-intensity sounds in various work or recreational settings. Consequently, noise-induced hearing loss (NIHL) has become a common communication disorder. It has long been known that the proximate explanation for NIHL is that exposure to intense sounds results in damage to and/or loss of hair cell stereocilia, particularly of the outer hair cells (OHCs). But evolution also provides a complementary explanation as to why humans are susceptible to NIHL.

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Evolutionary medicine is a relatively new and growing field in the basic sciences that apply the principles of Darwinian evolution to medicine and public health (Evol Applications. 2008;1[1]:28 It does not attempt to explain how evolution shapes human diseases, but rather how evolution has shaped particular human traits that are then susceptible to failure and disease. Evolutionary medicine is not about trying to improve humans as a species (i.e., not about eugenics), nor is it about attempting to change how modern medicine is practiced. Instead, the perspective is to increase our understanding of why diseases occur based on human evolutionary history (e.g., Evol Applications. 2011;4[2]:249 A more comprehensive understanding of hearing, speech, and language as a consequence of natural selection, as well as the application of evolutionary principles to communication sciences, could provide important insights into our understanding of why certain communication disorders occur.

Figure 1 illustrates the amount of basilar membrane (BM) displacement as a function of sound pressure level (i.e., input-output function) for a cochlea with stereocilia loss to OHCs (solid red line in Fig. 1). The threshold BM displacement required for a listener to detect a tone (e.g., as in pure-tone audiometry) is indicated by θ. Note that this BM input-output function is a linear function (solid red line in Fig. 1). A 20 dB increase in dB SPL results in a 100-fold (i.e., 20 dB) increase in BM displacement. This linear input-output function is indicative of a passive cochlea, in which the energy in the propagating traveling wave along the BM is lost due to the viscosity of the cochlear fluids. For the passive cochlea illustrated in this example, the BM input-output function (i) has a high threshold of approximately 50 dB SPL and (ii) a narrow dynamic range of approximately 50 dB. The red shaded area above 100 dB SPL indicates the sound levels in which noise damage is known to occur, and the blue shaded area indicates the corresponding BM displacements that are likely to increase the probability of OHC stereocilia damage. The green function indicates the possibility to increase the sensitivity of the passive cochlea. Threshold is now low at 0 dB SPL, but because the passive cochlea results in a linear BM input-output function, the dynamic range is still approximately 50 dB. The result is that BM displacements larger than 100 nm and damage to OHC stereocilia are now likely to occur at moderate sound levels.

Figure 1 shows that it is not possible to have high sensitivity (i.e., low thresholds) and a wide dynamic range of hearing in a passive cochlea. Evolution has “solved” this paradox with the cochlear amplifier, an active cochlea in which energy is added to boost the BM vibration. The BM input-output function from an active cochlea is a nonlinear function (blue squares and blue line in Fig. 1). This nonlinear input-output function shows the property of amplitude compression, first described by William Rhode (J Acoust Soc Am. 1971;49[4]:1218 For an active cochlea, the BM input-output function has a low threshold of approximately 0 dB SPL and a wide dynamic range of approximately 100 dB.

Amplitude compression arises from the cochlear amplifier, and the source of the active process underlying amplification is the somatic motility of outer hair cells. First described by William Brownell, PhD, and colleagues, somatic motility or electromotility is the ability of OHCs to lengthen and shorten in response to voltage changes in the cochlea during sound stimulation (Science. 1985;227[4683]:194 These length changes are transmitted to the displacement of the BM, providing the boost in BM vibration. However, this ability is not enough; the OHCs need to “push off” of something to transmit length changes to the BM. Mice with OHCs that show somatic motility but have stereocilia that are not physically attached to the tectorial membrane (TM) exhibit passive cochleae (Neuron. 2000;28[1]:273 Thus, the cochlear amplifier requires OHCs to possess somatic motility and have their stereociliary bundles attached to the TM.

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So how did this cochlear amplifier evolve? First, it is important to note that evolution does not proceed to design specific traits; that is, evolution does not proceed with purpose. Evolution of specific traits occurs as a consequence of genetic variation due to a mutation in an organism's present gene or development of new genes. Because genes encode the information used for protein synthesis, a random mutation of a gene can potentially alter a protein, thereby changing its function and consequently changing a specific trait of an organism. If this new trait has an adaptive value (i.e., it increases survival and reproductive success of the organism), then it will be acquired by the population over generations through natural selection.

The process of natural selection does not function to improve an organism's health; rather, it increases the reproductive success of an organism in its environment. For example, consider a population of bacteria in an environment consisting of an antibiotic. A small subpopulation of the bacteria has a genetic mutation that results in resistance to the antibiotic. The bacteria without the trait of resistance will not be able to reproduce in an environment with the antibiotic, while the bacteria with the trait of resistance can reproduce despite the presence of the antibiotic. Over time, the entire bacteria population will have the gene for antibiotic resistance. In this example, the altered trait (i.e., antibiotic resistance) increases the reproductive success of an individual bacterium and, through natural selection, this trait will be acquired by the population.

The earliest mammal-like vertebrates, mammaliaformes, first appeared some 210 million years ago, and true mammals evolved from these mammaliaformes some 145 million years ago. During this period, dinosaurs and crocodiles were the dominant vertebrates, and the acoustic environment had less intense environmental sounds, most likely similar to that of a forest or grassland. Early mammals were thought to be nocturnal; fur and homeothermy were adaptations that allowed them to conserve body heat, which was particularly beneficial on cold nights. Predator avoidance was paramount among early mammals, and having sensitive hearing would have been helpful in evading predators. Those that could avoid predators were more likely to survive into adulthood and reproduce.

Two genetic mutations are notable in the evolution of the cochlear amplifier—the mutations of the genes for prestin and stereocilin. Prestin, the molecular motor that causes the somatic motility of OHCs, is a protein first isolated by the laboratory of Peter Dallos, PhD, and colleagues (Nature. 2000;405:149 Prestin is a member of the solute carrier family 26A (SLC26A) that binds anions, negatively charged ions such as chloride and bicarbonate ions. Following anion binding to the SLC26A protein, the anions are transported across the epithelia. However, in the evolution of early mammals, a random mutation of the SLC26A gene occurred. Because of this mutation, anions could still bind to the protein, but instead of being transported, they undergo a structural change. For example, the molecular shape of prestin changes when chloride binds to it. This difference in molecular shape when anions are or are not bound results in changes in OHC length (i.e., somatic motility). Subsequent research has demonstrated that prestin is found in a variety of vertebrates, but only in mammalian ears does prestin cause motility of OHCs (J Neurophysiol. 2011;105[1]:36 Cochleae that have OHCs with prestin in the cell membrane are active and show cochlear amplification; cochleae that have OHCs without prestin are passive (Nature. 2002;419[6904]:300

Stereocilin is a protein found in the apical ends of the stereociliary bundles of OHCs, but is absent in the stereocilia of inner hair cells (J. Comp. Neurol. 2011;519[2]:194 This protein is essential for providing a connection between OHCs and the TM. In mice that do not produce stereocilin, their cochleae show passive properties (Nature. 2008;456[7219]:255

The genetic mutations of prestin and stereocilin that resulted in somatic motility of the OHCs and a physical connection between OHCs and the TM respectively produced an increased hearing sensitivity in early mammals. Those with this new trait (e.g., amplification) were better able to avoid predators, survive into adulthood, and reproduce compared with those with lower hearing abilities. Through reproduction, the trait was passed on to their offspring, and over time, such increased hearing sensitivity became more common in the population. Ultimately, all individuals in the population exhibited cochlear amplification.

Although natural selection resulted in the adaptation of a highly sensitive ear, the cost was an ear that is also substantially nonlinear and susceptible to intense noise levels. This vulnerability to noise results from the evolution of the connection between OHCs and the TM, an essential structural trait for cochlear amplification. Consequently, during BM vibration at high-intensity levels, the shear force generated as the TM and the reticular lamina slide past each other is large enough to damage the stereocilia of OHCs. IHC stereocilia are much more resilient to damage at high-intensity levels because they have not developed a physical attachment to the TM.

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Why didn't evolution make the ear more noise-resistant? Again, evolution does not proceed with purpose. Simply stated, the human ear did not evolve under conditions of high sound levels. Any genetic mutation that might have led to a noise-resistant ear was likely not selected because it did not provide any benefit for survival and reproductive success in the pre-historic acoustic environment of early mammals. Natural selection is an exceedingly slow process that occurs over many generations, and the susceptibility of the human ear to noise-induced damage shows how natural selection is unable to keep up with rapid changes in an organism's environment (Evol Applications. 2008 Technology has produced an acoustic environment that has changed much faster than the sluggish pace of human evolution. This evolutionary explanation of why the human ear is so susceptible to damage at highly intense noise levels provides a valuable perspective that audiologists can offer patients to prevent NIHL.

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