Abstract
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.
Highlights
Sound pressure waves are used by many animal species to gain sensory input from their environment that is vital for their survival and communication
The fluid jet produces a uniform deflection of the hair bundle (Corns et al, 2014) and for inner hair cells (IHCs), which are stimulated in vivo by fluid motion within the cochlear partition (Fettiplace and Kim, 2014), it provides a near-physiological stimulation without affecting their resting position
To mimic in vivo conditions as closely as possible, recordings were obtained from IHCs maintained at body temperature and their hair bundles were perfused with an extracellular solution containing an endolymphatic low-Ca2+ concentration (40 mM: see Materials and methods)
Summary
Sound pressure waves are used by many animal species to gain sensory input from their environment that is vital for their survival and communication. Auditory hair cells in lower vertebrates such as the turtle and bullfrog (Fettiplace and Fuchs, 1999), where the hearing sensitivity spans a generally low-frequency range (from around 100 Hz to 1 kHz), show intrinsic membrane tuning such that the membrane potential oscillates at the cells’ characteristic frequency (CF). In these animals, the interplay between the Ca2+ and Ca2+-activated K+ channels, which are differentially expressed along the auditory organ, are thought to be the main mechanism determining hair cell frequency selectivity (Hudspeth and Lewis 1988; Wu et al, 1995). In order to do this, mammals have developed an elaborate auditory organ where much of the frequency tuning is carried out by the mechanics of the basilar membrane (Robles and Ruggero, 2001) and electromotility of the outer hair cells (OHCs)
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