Biophysicists have long been amazed by the ear's extraordinary ability to pick up extremely soft sounds. Although it is known that the thousands of hair cells in the inner ear convert mechanical vibrations produced by incoming sound waves into electric signals that the brain can then process, exactly how the ear achieves its exquisite detection sensitivity remains a mystery. Now, experiments done by physicists in the US suggest that spontaneous vibrations that are known to occur in these hair cells could synchronize with weak incoming sound signals, thereby allowing their detection. The researchers also suggest that the vibrations respond to incoming sound via changes in their phase, and this too could contribute to the sensitivity.

Low-threshold dynamics

The inner ear of humans and other vertebrates contain thousands of "hair cells", each of which contains bundles of 30 to 50 stereocilia. These stereocilia are hair-like projections that jut from the top surface of the cells and are immersed in a fluid substance. However, the precise nature of how this system works is not really understood, according to Yuttana Roongthumskul of the University of California, Los Angeles (UCLA). Roongthumskul and colleagues are trying to figure out how the bundles respond to a signal with a very low threshold.

To do this, the researchers are studying samples of the hair bundles from a bullfrog in vitro. Roongthumskul explains that frog bundles are used because they are much more robust than samples from mammals. "To test this in a mammal is quite hard as the sample is quite hard to dissect...the hair cells are such that the hair bundles and the cell body need to be stored in different solutions in a two-compartment chamber, which is a difficult set-up to maintain," he explains. Unlike mammals, frogs do not possess a cochlea – the bundles themselves perform the cochlear function – but the hearing systems are comparable and equally sensitive.

Spontaneously oscillating

When the team looked at the bundles in vitro, they confirmed previous observations that the bundles oscillate spontaneously – something that is also expected to occur in the ears of live frogs. "These spontaneous oscillations have never been observed in vivo, but we know there is something active in the inner ear that generates a sound," says Roongthumskul, who is a graduate student in the Bozovic Lab at UCLA. He explains that the spontaneously oscillating bundles might synchronize with a weak incoming signal to create a kind of active amplification that allows the sound to be picked up.

The team also studied the varying phase dynamics of the bundle's response to the sound. This involved stimulating a bundle while recording the phase of its spontaneous oscillations. The researchers used a high-speed camera to measure the degree of synchronization between the oscillations and an input sound signal. "We saw that when the stimulation was very strong, the oscillations and our signal showed a constant phase difference: they were always 'phase-locked'. But for a weaker signal, we saw 'phase slips': intermittently there is synchronization, then it is lost for a while, and then it is synchronized again," explains Roongthumskul.

These observations suggest that the phase dynamics follow predictions based on a different set of equations than previously thought. The new equations predict that once a stimulus is applied, the response is very quick and sensitive. This advantage could point to the mechanism that allows for the detection of extremely soft sounds.

Although Roongthumskul cautions that the spontaneous oscillations have not been seen in living ears – it is very hard to image the bundles while they are within the ear – he says that the new results should give a better understanding of the dynamics of hearing. He also admits that much more work is needed. "What we don't understand is how we can hear 0 dB sounds, especially as some of these sounds cause vibrations that are less than the thermal fluctuations or the background noise in the ear itself," he says.

The results are published in Physical Review Letters.