Development of the time coding pathways in the auditory brainstem of the barn owl

Abstract

The barn owl's head grows after hatching, causing interaural distances to more than double in the first 3 weeks posthatch. These changes expose the bird to a constantly increasing range of interaural time cues. We have used Golgi and ultrastructural techniques to analyze the development of the connections and cell types of the nucleus magnocellularis (NM) and the nucleus laminaris (NL) with reference to the growth of the head. The time coding circuit is formed but immature at the time of hatching. In the month posthatch, the auditory nerve projection to the NM matures, and appears adult-like by posthatch day (P)21. NM neurons show a late growth of permanent dendrites starting at P6. Over the first month, these dendrites change in length and number, depending upon rostrocaudal position, to establish the adult pattern in which high best frequency neurons have few or no dendrites. These changes are not complete by P21, when NM neurons still have more dendrites than in the adult owl. The neurons of NL have many short dendrites before hatching. Their number is greatly reduced by P6, and then does not change during later development. Like NM neurons, NL neurons and dendrites grow in the first month posthatch, and at P21, NL dendrites are longer than those in the adult owl. Thus, the auditory brainstem circuits grow in the first month after hatching, but are not yet mature at the time the head reaches its adult size.

Primary innervation of the avian and mammalian cochlear nucleus

“…It does, however, represent a potentially interesting site for making lesions that would selectively denervate NM for behavioral studies. As the fiber courses caudal-to-rostral above the NM, it gives off several branches (three to six in the barn owl, [31]). Each collateral branch descends ventrally to form a single endbulb on a NM cell body and the distribution of the endings corresponds to the tonotopic organization of the nucleus [165,201].…”

“…Each collateral branch descends ventrally to form a single endbulb on a NM cell body and the distribution of the endings corresponds to the tonotopic organization of the nucleus [165,201]. Endbulbs are a large calyx-like axosomatic ending formed by auditory nerve fibers in a wide variety of terrestrial vertebrates, including turtles [24], lizards [199], birds [31,78,140], mice [22,102], guinea pigs [208], cats [103,170,175], and humans [1]. The endbulb arises from the main axon as several gnarled branches that arborize repeatedly to enclose the postsynaptic cell in a nest of en passant swellings and terminal boutons (Fig.…”

“…The evolutionary advantages conferred by accurate timing information are embedded in sound localization acuity and auditory discrimination skills. Chick endbulbs are from Jhaveri and Morest [77,78], Plenum Press; owl endbulbs are from Carr and Boudreau [31], Wiley-Liss publishers; mouse endbulbs are from Limb and Ryugo [102], Springer publishers; cat endbulbs are from Ryugo et al [174], Wiley-Liss publishers, and Sento and Ryugo [185], Liss publishers; monkey endbulb is from Ryugo, unpublished data; human endbulb is from Adams [1], American Medical Association.…”

“…The avian NM contains a population of neurons called bushy cells [30,31,78,187]. These cells exhibit large round-to-oval cell bodies with many short somatic spines; in hatchling chickens, 40% of NM neurons have a single rudimentary dendrite [40].…”

Early life exposure to noise alters the representation of auditory localization cues in the auditory space map of the barn owl

“…Furthermore, the connections from the nucleus magnocellularis to the nucleus laminaris (the major input source to the ITD processing pathway) matures at about posthatch day 30 (Cheng and Carr 2007;Carr and Boudreau 1996), and the maturation of the acoustical properties of the head is achieved at ϳ2 mo (Haresign and Moiseff 1998). Thus extensive developmental processes must take place during the first 2 mo of life to form a functionally mature map.…”