Synaptic Transfer from Outer Hair Cells to Type II Afferent Fibers in the Rat Cochlea

Abstract

Type II cochlear afferents receive glutamatergic synaptic excitation from outer hair cells (OHCs) in the rat cochlea. However, it remains uncertain whether this connection is capable of providing auditory information to the brain. The functional efficacy of this connection depends in part on the number of presynaptic OHCs, their probability of transmitter release, and the effective electrical distance for spatial summation in the Type II fiber. The present work addresses these questions using whole-cell recordings from the spiral process of type II afferents that run below OHCs in the apical turn of young (5–9 days postnatal) rat cochlea. A ‘high potassium puffer’ was used to elicit calcium action potentials from individual OHCs and thereby show that the average probability of transmitter release was 0.26 (range 0.02 to 0.73). Electron microscopy showed relatively few vesicles tethered to ribbons in equivalent OHCs. A ‘receptive field’ map for individual type II fibers was constructed by successively puffing onto OHCs along the cochlear spiral, up to 180 µm from the recording pipette. These revealed a conservative estimate of 7 presynaptic OHCs per type II fiber (range 1–11). EPSCs evoked from presynaptic OHCs separated by more than 100 µm did not differ in amplitude or waveform, implying that the type II fiber’s length constant exceeded the length of the synaptic input zone. Taken together these data suggest that type II fibers could communicate centrally by maximal activation of their entire pool of presynaptic OHCs.

Unmyelinated type II afferent neurons report cochlear damage

“…This observation may help to resolve the decades-long conundrum that type II afferents in vivo are very insensitive to sound (9,10) and yet presumably carry some information to the auditory brainstem. Likewise, measured ex vivo, synaptic excitation is weak and could activate type II afferents only if all of the presynaptic OHCs were maximally stimulated (21). Alternatively, ATP potently activates type II afferents (11) and serves as a major contributor to the damage-induced response.…”

“…ATP application produced action potentials in type I fibers only via release of glutamate from IHCs, whereas direct effects of ATP on type I afferent membrane current or voltage were small and subthreshold. In contrast, although ATP can evoke glutamate release from OHCs, that source of excitation on its own is insufficient to activate the type II afferent (11,21). The current evoked by ATP reversed at 0 mV (red; n = 3 afferents) and reversal of UTP-evoked current extrapolated to near −70 mV (blue; n = 6 afferents).…”

Tyrosine Hydroxylase Expression in Type II Cochlear Afferents in Mice

“…After crossing the tunnel of Corti, a single type II afferent is thought to contact as many as 30-60 OHCs, depending on species and cochlear location ( and was functionally coupled to at least 10 OHCs (Weisz et al 2012). Given the low average probability of release, computational modeling suggested that glutamate release from 24 OHCs would be required to cause type II afferent spiking in rat (Weisz et al 2014).…”

“…In contrast, unmyelinated type II afferents extend hundreds of microns along the cochlear coil to receive input from many outer hair cells (OHCs). Despite this extended dendritic arbor, type II afferents are only weakly activated by hair cell glutamate release (Weisz et al 2009;Weisz et al 2012) and are insensitive to sound Robertson 1984;Robertson et al 1999), although they project centrally in parallel with neighboring type I afferents (Berglund and Brown 1994;Brown et al 1988;Brown and Ledwith 1990;Morgan et al 1994). Emerging evidence suggests that type II afferents instead respond to tissue damage (Flores et al 2015;Liu et al 2015) perhaps to serve as cochlear nociceptors.…”

Amplitude modulation of audible sounds by non-audible sounds: Understanding the effects of wind turbine noise

“…ii) Type II auditory nerve fibers that spiral along the tonotopic axis of the cochlea and synapse on cochlear outer hair cells respond in a manner that is consistent with what would be expected from excitation by intense lowfrequency acoustic stimulation (Weisz et al 2012). Outer hair cells have a low probability of neurotransmitter release and, when one does release, it provides only a fraction of the excitation required for a type II fiber to fire.…”