Pre‐ and postnatal development of efferent connections of the cochlear nucleus in the rat

Abstract

Although the connections of the auditory brainstem nuclei are well described in adult mammals, almost nothing is known concerning how and when these connections develop. The purpose of the present study was to describe the development of the efferent projections of the cochlear nucleus (CN), the first central relay station in the ascending auditory pathway of mammals. We used two tracers in rats aged between embryonic day 15 (E15) and postnatal day 14 (P14; birth in the rat is at E22 = P0). The carbocyanine dye DiI was applied into the CN in aldehyde-fixed tissue. The second tracer, biocytin, was applied into the ventral acoustic stria in an in vitro slice preparation. The ontogeny of the efferent projections from the CN could be divided into three periods. The first period (E15-E17) is characterized by axonal outgrowth. Axons traverse nuclei in the superior olivary complex and the lateral lemniscus and finally grow up into the inferior colliculus, but axon collaterals do not form during this period. The second period (E18-P5) is marked by pronounced collateral branching of CN fibers in auditory brainstem nuclei. Collateralisation in the contralateral inferior colliculus starts shortly before that in the ipsilateral superior olivary complex. The remaining auditory nuclei become successively innervated, as indicated by collaterals found in them. During the third period (P5-P14) terminal structures mature further, as shown by the morphological changes of the calyces of Held in the medial nucleus of the trapezoid body. In conclusion, our results show that the efferent connections from the cochlear nucleus form over a period of almost two weeks and are laid down without forming aberrant internuclear connections. On a nuclear level, an adult-like projection pattern is already achieved one week prior to the onset of physiological hearing.

Diffusion and imaging properties of three new lipophilic tracers, NeuroVue™ Maroon, NeuroVue™ Red and NeuroVue™ Green and their use for double and triple labeling of neuronal profile

“…Likewise, tract tracing with DiI made it possible for the first time to study the fiber growth in embryos from the cochlear nuclei to the inferior colliculus [20]. While useful, these studies have also highlighted the limits of the single color approach: contact formation with developing target neurons has to be painstakingly reconstructed in independent analyses, with the possibilities for topological errors.…”

Quantitative assessment of developing afferent patterns in the cat inferior colliculus revealed with calbindin immunohistochemistry and tract tracing methods

“…In fact, other developmental studies indicate that brainstem auditory projections to the IC develop remarkably early, well before functional hearing and any role for sensory experience. For instance, Kandler and Friauf (1993) showed that cochlear nucleus projections to the contralateral IC reach their targets prenatally and are well refined even by birth. Also, in ferret kits, an altricial carnivore that does not hear until 1 month postnatally, the relative laterality of the LSO inhibitory projections to the ipsilateral IC and excitatory projections to the contralateral IC are already established at birth (Henkel and BrunsoBechtold, 1993).…”

Multiple Large Inputs to Principal Cells in the Mouse Medial Nucleus of the Trapezoid Body

“…Afferent and efferent connections of the MNTB are also changing during this age (Kandler and Friauf 1993;Kim and Kandler 2003;Kuwabara et al 1991), which is the age used for patch-clamp studies. If indeed some MNTB principal cells do receive multiple calyces, it will be important to determine whether this is a transitory phenomenon during development like that seen in the other instances of strong single inputs or whether it persists in adulthood.…”

“…Axons from the globular bushy cells in the ventral cochlear nucleus (VCN) cross the midline in the trapezoid body and give rise to one or two calyces (Smith et al 1991). Anatomical studies in the young and mature rat (Casey and Feldman 1985;Kandler and Friauf 1993;Sätzler et al 2002;Taschenberger et al 2002), cat (Morest 1968a;Smith et al 1991), and other animals (e.g., Lenn and Reese 1966) have reported that each postsynaptic principal cell receives input from only one calyx. In addition to the calyceal synapse, other, smaller, bouton contacts onto the principal cell and its dendrites have been observed (e.g., Lenn and Reese 1966).…”