Development of banded afferent compartments in the inferior colliculus before onset of hearing in ferrets

Abstract

Axonal projections from the lateral superior olivary nuclei (LSO), as well as from the dorsal cochlear nucleus (DCN) and dorsal nucleus of the lateral lemniscus (DNLL), converge in frequency-ordered layers in the central nucleus of the inferior colliculus (IC) where they distribute among different synaptic compartments. A carbocyanine dye, DiI, was used as a tracer to study the postnatal development of axonal projections in the ferret IC. The results indicated that projections from all three nuclei are present at birth, but are not segregated into bands. During the postnatal week between approximately postnatal days 4 and 12 (P4-P12), axons from LSO proliferate in IC, become more branched, and segregate into a series of bands composed of densely packed fibers and endings. LSO projections in these afferent bands course parallel to IC layers and are separated by intervening regions with few endings. A modest fit of a sine curve (R 2 >0.15) to the pattern of spacing of LSO projections in IC indicated that regularly spaced bands are forming by P7. Similarly, banded patterns of DCN and DNLL projections to IC have developed by the end of the first postnatal week. Thus, well before hearing onset in ferret (P28-30), three different afferent projections have segregated into banded compartments along layers in the central nucleus of the ferret IC. Possible mechanisms in circuit development are discussed.

Axon guidance in the auditory system: Multiple functions of Eph receptors

“…In short, pioneer fibers invade appropriate subdivisions of the embryonic IC and exhibit initially diffuse projection distributions. Shortly after birth, characteristic CNIC layers become apparent as axonal arbors refine themselves, coupling selective pruning with continued elaboration within appropriate postsynaptic sublayers (Kandler and Friauf, 1993, Gabriele et al, 2000b, a, Gabriele et al, 2007, Henkel et al, 2007, Fathke and Gabriele, 2009). Bilateral LSO patterns and those arising from the contralateral DCN and dorsal nucleus of the lateral lemniscus (DNLL) all exhibit remarkable projection specificity prior to experience, targeting defined synaptic domains of frequency-band laminae (Fathke and Gabriele, 2009).…”

Tuning up the developing auditory CNS

“…When animals were reared with two tones presented simultaneously, a significant volume of the IC became responsive to both rearing frequencies [78 *]. The mechanistic basis for this plasticity is somewhat mysterious because the broad frequency responses observed at hearing onset originate primarily in the cochlea, and brain stem afferent projections are topographically organized at this age, although they do undergo a period of anatomical refinement [79-82]. One possibility is that local axonal projections establish and strengthen contacts across the IC tonotopic laminae during development [83].…”

Patterning of multiple layered projections to the auditory midbrain prior to experience

“…Shaping of converging ICC afferent patterns occurs prior to experience and likely defines finer-scale organizational features (Kandler and Friauf, 1993;Gabriele et al, 2000aGabriele et al, ,b, 2007Henkel et al, 2005Henkel et al, , 2007Franklin et al, 2006). The contralateral DNLL input exhibits a diffuse distribution, before segregating into clearly distinguishable ICC layers (Gabriele et al, 2000a,b).…”