Journal Article

Membrane properties specialize mammalian inner hair cells for frequency or intensity encoding

Johnson, Stuart L

2015

Overview

The auditory pathway faithfully encodes and relays auditory information to the brain with remarkable speed and precision. The inner hair cells (IHCs) are the primary sensory receptors adapted for rapid auditory signaling, but they are not thought to be intrinsically tuned to encode particular sound frequencies. Here I found that under experimental conditions mimicking those in vivo, mammalian IHCs are intrinsically specialized. Low-frequency gerbil IHCs (~0.3 kHz) have significantly more depolarized resting membrane potentials, faster kinetics, and shorter membrane time constants than high-frequency cells (~30 kHz). The faster kinetics of low-frequency IHCs allow them to follow the phasic component of sound (frequency-following), which is not required for high-frequency cells that are instead optimally configured to encode sustained, graded responses (intensity-following). The intrinsic membrane filtering of IHCs ensures accurate encoding of the phasic or sustained components of the cell’s in vivo receptor potential, crucial for sound localization and ultimately survival. Many animals’ survival depends on them accurately and quickly identifying sounds in their environment. In animals with backbones, cells with hair-like projections (called hair cells) inside the ear convert information collected from sound waves into electrical signals. These signals are then transmitted to the brain, which processes the information further. Animals like bullfrogs are adapted to hearing low frequency sounds, like their own mating calls. These frog’s hair cells are individually tuned so that they can capture sounds in this low frequency range. Mammals, on the other hand, have evolved to hear a much wider range of sounds from loud and low frequency sounds, such as thunder, to soft and high frequency sounds, like the cries of their young. In mammals, the part of inner ear involved in hearing (called the cochlea) has an elaborate spiral-like shape. The structure of the cochlea results in different frequencies of sound being transformed by the hair cells into electrical signals at different points around the spiral. Because of this, most researchers didn’t think that hair cells in mammals were individually tuned like those in bullfrogs. Now, Stuart Johnson demonstrates that hair cells in different parts of the gerbil’s cochlea are specialized for encoding sounds of specific frequencies. In conditions that mimic the environment inside the ear, a very precise jet of fluid was used to stimulate single hair cells in a similar way to a sound wave. The experiments then compared how hair cells from the upper and lower parts of the cochlea’s spiral responded. Johnson found that hair cells from the upper portion of the gerbils’ cochlea are specialized to capture low frequency sounds. They have electrical properties that allow them to quickly transmit information to the brain about low frequency sounds. In the lower portion of the cochlea, hair cells are specialized to capture high frequency sounds. That is, their electrical properties make it easier for these hair cells to transmit detailed information to the brain about the volume of high frequency sounds. Together, these findings help explain how these animals are able to localize sounds, which requires capturing both the timing and intensity of different types of sounds.

• Publisher: eLife Science Publications, Ltd,eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Acoustic Stimulation / Animals / Body temperature / Cell Membrane - physiology / Cell membranes / cochlea / gerbil / Gerbillinae / Hair / hair cell / Hair cells / Hair Cells, Auditory, Inner - physiology / Localization / Mammals / Membrane Potentials / Mimicry / Neuroscience / Physiology / Properties / Variance analysis