Jim Hudspeth – Rockefeller University
Wednesday, March 19th , 10:45AM EST
The physiology and physics of hearing: How the ear's works work
As the gateway to human communication, the sense of hearing is of enormous importance in our lives. Hearing commences with the capture of sound energy by hair cells, the ear's sensory receptors, which convert that energy into electrical signals that the brain can then interpret. However, uniquely among our sensory receptors, hair cells are not passive recipients of stimuli, but instead use an active process to enhance their inputs. This active process amplifies mechanical stimuli by as much as a thousandfold, thus greatly increasing our sensitivity to weak sounds. When this process fails, we become hard of hearing. Amplification is accompanied by frequency tuning, which restricts each hair cell's response to a narrow frequency band. If the active process deteriorates, we grow less sensitive to subtle differences in frequency and therefore suffer a diminished ability to discriminate speech and localize sound sources. The active process produces a compressive nonlinearity that renders the ear sensitive to sounds over a millionfold range of amplitude or an astonishing trillionfold range in power. By enhancing weak stimuli and suppressing strong ones, this feature allows us to enjoy an instrumental soloist as comfortably as a full orchestra hundreds of times as loud. Finally, the active process can be so exuberant as to become unstable; as a result, in a very quiet environment most normal ears spontaneously emit sound!
Numerous experiments on the ears of amphibians have revealed that these features emerge from the operation of hair cells in a critical regime at the brink of Hopf bifurcation. In mammals, however, the delicate nature of the cochlea has restricted the evidence for an active process to studies in vivo, where it is generally attributed to the collective effort of the outer hair cells that energize the traveling wave along the cochlear spiral. As a result, the cellular mechanisms that underlie the properties of mammalian hearing remain contested, with uncertainty about whether criticality plays a role in the cochlea's active process and even whether an active process exists. Using an excised preparation of the gerbil's cochlea, we have confirmed that a cochlear segment displays amplification, frequency tuning, and compressive nonlinearity and can generate distortion products. By freeing the active process from the constraints of traveling waves, we show that mammalian hair cells, like those of other tetrapods, achieve active amplification through a nonlinear dynamical system operating at criticality.