Emergence of Hearing in the Chicken Embryo

It is commonly held that hearing generally begins on incubation day 12 (E12) in the chicken embryo ( Gallus domesticus). However, little is known about the response properties of cochlear ganglion neurons for ages younger than E18. We studied ganglion neurons innervating the basilar papilla of embryos (E12–E18) and hatchlings (P13–P15). We asked first, when do primary afferent neurons begin to encode sounds? Second, when do afferents evidence frequency selectivity? Third, what range of characteristic frequencies (CFs) is represented in the late embryo? Finally, how does sound transfer from air to the cochlea affect responses in the embryo and hatchling? Responses to airborne sound were compared with responses to direct columella footplate stimulation of the cochlea. Cochlear ganglion neurons exhibited a profound insensitivity to sound from E12 to E16 (stages 39–42). Responses to sound and frequency selectivity emerged at about E15. Frequency selectivity matured rapidly from E16 to E18 (stages 42 and 44) to reflect a mature range of CFs (170–4,478 Hz) and response sensitivity to footplate stimulation. Limited high-frequency sound transfer from air to the cochlea restricted the response to airborne sound in the late embryo. Two periods of ontogeny are proposed. First is a prehearing period (roughly E12–E16) of endogenous cochlear signaling that provides neurotrophic support and guides normal developmental refinements in central binaural processing pathways followed by a period (roughly E16–E19) wherein the cochlea begins to detect and encode sound.