Auditory Nerve Response, Afferent Signals
Sequences of action potentials (spikes) of individual auditory nerve fibers (ANFs), the primary auditory afferents, in response to sounds impinging upon the ears.
Acoustic information relayed from the inner ear to the central nervous system is encoded in the sequences of spikes produced by (type I) ANFs. In mammals, each ANF contacts a single receptor cell (inner hair cell, IHC). ANF spikes are initiated by neurotransmitter release from usually only a single active zone per afferent, the “ribbon,” in the IHC, a unique arrangement (Ashmore 2010; Rutherford et al. 2012). Each IHC is contacted by 5–30 ANFs, depending upon species and cochlear location, which thus share some, but not all, functional response properties.
ANFs produce spikes in the absence of external sound (spontaneous activity). The mean spontaneous rate varies between fibers, in mammals from near zero up to more than 100 spikes per second (Pickles 2012). The timing of the spikes of a given fiber is highly variable. The distribution of inter-spike intervals during spontaneous activity can be described as the result of a homogeneous stochastic process generating excitatory transmitter release events in combination with the fiber’s refractory properties (Mountain and Hubbard 1996; Heil et al. 2007).
Sounds impinging on the ipsilateral ear, when of appropriate spectral composition and amplitude, affect the spiking behavior of ANFs, most often increasing the spike rate. A threshold sound level may be defined at which the driven rate of a given ANF exceeds its spontaneous rate by some criterion. The compound action potential (CAP), a gross stimulus-evoked potential which reflects a weighted sum of ANF responses, can be recorded in or near the cochlea, e.g., at the round window (Pickles 2012).
Each ANF is tuned to sound frequency and is most sensitive, i.e., threshold is lowest, at a particular frequency (the characteristic frequency; CF) which is determined by the position along the cochlear partition of the IHC which it contacts (cochleotopy). Threshold versus frequency curves (tuning curves) are approximately V shaped, but those of high-CF ANFs exhibit low-frequency tails. The sharpness of tuning is often quantified by the Q value, defined as the CF divided by the bandwidth of the tuning curve at some level (e.g., 10 dB) above threshold at CF. Q10 values increase with increasing CF (in cats from about 1–10 for CFs from 0.2 to 10 kHz; Pickles 2012) but can reach exceptionally high values (>200) in behaviorally relevant frequency ranges in species such as echo-locating bats.
With increasing sound level, the mean spike rate of a given ANF increases before saturating at several hundred spikes per second at higher sound levels. The range of sound levels over which the spike rate increases (the dynamic range, DR) varies between ANFs. DR is inversely related to the spontaneous rate of an ANF which in turn covaries with the fiber’s sensitivity. These interdependencies are predicted by a recent model of spike rate versus level functions, according to which the spike rate follows a Hill equation, with a Hill coefficient of 3, and the independent parameter is the sum of the sound amplitude and a baseline (Heil et al. 2011). For a given ANF, DR varies with sound frequency, being largest at CF due to compressive growth of mechanical responses in the inner ear with sound level. DR and maximum spike rate also adapt to stimulus statistics (Wen et al. 2009).
Adaptation is also manifest as a decrease in spike rate over time in response to sounds of constant amplitude. Within a few milliseconds, the spike rate drops rapidly and then more gradually. The decrease is often modeled as the sum of multiple exponential decays with different time constants or as a fractional power law (Zilaney et al. 2009). Upon cessation of the sound, the spike rate temporarily decreases below the spontaneous rate before recovering over tens to hundreds of milliseconds.
In response to low-frequency sounds or broadband sounds containing low frequencies, ANFs exhibit phase-locking, i.e., spikes are nonrandomly distributed across the period of a low-frequency component, and tend to occur at a particular phase (Michelet et al. 2012; Pickles 2012). For a given ANF, this phase varies with frequency and sound level. The degree of phase-locking is often quantified by the measure of vector strength. Vector strength also varies with frequency and sound level. Across ANFs, maximum vector strength decreases with increasing frequency in a low-pass fashion, with cutoffs of a few kilohertz, depending on species. Phase-locking is also seen in the responses of low-CF ANFs to acoustic clicks, elicited by the ringing of the basilar membrane caused by these brief broadband sounds. ANFs also phase-lock to the modulation envelope of sinusoidal amplitude-modulated tones and noise.
Several of these properties can be altered by sensorineural hearing loss. Cochlear implants function by evoking spiking activity in ANFs.