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

Abstract

The precise arrangement of patterned inputs into discrete functional domains is a common organizational feature of primary sensory structures. While the specific organization of patterned connections has been well documented in the visual and somatosensory systems, comparatively little is known about the arrangement of neighboring afferent patterns in the emerging auditory system. Here we report early projection specificity for multiple converging inputs to the rat central nucleus of the inferior colliculus (ICC). Afferents arising from the dorsal cochlear nucleus (DCN), the dorsal nucleus of the lateral lemniscus (DNLL), and the lateral superior olive (LSO) establish discernible axonal layers a week prior to experience. By hearing onset, contralateral DCN and contralateral LSO layers are clearly defined and segregated from contralateral DNLL terminal zones. Layering of the ipsilateral LSO projection, on the other hand, exhibits considerable spatial overlap with the contralateral DNLL pattern. This fine laminar structure of interdigitating and overlapping inputs likely underlies the complex signal processing performed in the auditory midbrain and may serve as a model system for examining competitive interactions between neighboring excitatory and inhibitory projections early in development.

Auditory System

“…The development of some afferents to the CIC has been studied in great detail in rats (Kandler and Friauf, 1993;Niblock et al, 1995;Gabriele et al, 2000aGabriele et al, , 2000bFathke and Gabriele, 2009). The development of the CNC and DNL projections to the IC can be divided into several periods (Kandler and Friauf, 1993;Gabriele et al, 2000aGabriele et al, , 2000b.…”

“…Such findings suggest that evoked activity may not be required for the initial organization of patterned projections in the ascending auditory pathway. More recently Fathke and Gabriele (2009) have demonstrated in an elegant study that afferents arising from the DC, the DNLL, and the LSO establish distinct axonal layers a week prior to experience. By hearing onset, contralateral DCN and contralateral LSO layers are clearly defined and segregated from contralateral DNLL terminal zones while layering of the ipsilateral LSO projection demonstrate considerable spatial overlap with the contralateral DNLL pattern.…”

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

“…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). Much like their layered counterparts in the CNIC, modular (Wallace et al, 2013) and extramodular (Torii et al, 2013) LCIC arrangements emerge during early postnatal development.…”

Ephrin‐B2 reverse signaling is required for topography but not pattern formation of lateral superior olivary inputs to the inferior colliculus

“…It has been proposed that, within patterned tonotopic arrangements, secondary ‘‘nucleotopic’’ maps exist in mosaic form in which discrete neuronal compartments or modules receive varying input arrays (Oliver and Heurta, 1992). Accurate alignment of inputs defines functional zones necessary for processing additional stimulus features (Schreiner and Langner, 1997; Fathke and Gabriele, 2009). Given the significance of topographic maps and the spatial precision necessary in defining functional auditory circuits, surprisingly little is known about the mechanisms that guide such connections early in development.…”

“…The present study examines protein interactions thought to play a role in the establishment of orderly connections in the auditory midbrain or inferior colliculus (IC). The IC receives numerous converging inputs terminating within a single topographical framework (Fathke and Gabriele, 2009), making it an excellent model for studying targeting questions.…”