Auditory brainstem projections to the ferret superior colliculus: Anatomical contribution to the neural coding of sound azimuth

Abstract

The mammalian superior colliculus (SC) contains a neural map of auditory space. It is not known whether this topographic representation emerges at the level of the SC or is relayed there from other auditory areas. We have used retrograde labelling techniques in ferrets to examine the sources and pattern of innervation from auditory brainstem nuclei. After multiple injections of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) into the SC, the heaviest concentrations of labelled cells were found in the nucleus of the brachium (BIN) and external nucleus of the inferior colliculus, with much weaker labelling in the nucleus sagulum, dorsal, intermediate and ventral nuclei of the lateral lemniscus, paralemniscal regions, and periolivary nuclei. The projections were predominantly ipsilateral, although labelled cells were found on both sides of the brainstem. Single injections of WGA-HRP or discrete injections of red and green latex microspheres revealed that the caudal and lateral regions of the SC receive the heaviest projections, although the majority of the retrogradely labelled neurons in the contralateral BIN project to rostral SC. On the ipsilateral side, neurons in rostral and caudal regions of the BIN were labelled primarily by the tracer injected into rostral and caudal regions of the SC, respectively. However, no clear segregation was apparent in the BIN after injections into the medial and lateral regions or in any of the other nuclei after either injection paradigm. These data suggest that converging inputs from several auditory brainstem nuclei contribute to the construction of the auditory space map in the SC, although information about sound azimuth may be conveyed to this nucleus via a spatially ordered projection from the ipsilateral BIN.

Functional Topography of Converging Visual and Auditory Inputs to Neurons in the Rat Superior Colliculus

“…Anatomical studies in several species have shown that the nBIC provides a large projection to the dSC (Edwards et al 1979;King et al 1998a) and recordings in both ferrets (Schnupp and King 1997) and cats (Aitkin and Jones 1992) have confirmed that nBIC neurons are acoustically responsive and have spatially tuned receptive fields. The tracing data presented here show that nBIC neurons extend axons that terminate in the dSC, suggesting that this pathway is also likely to provide a major route in by which auditory information reaches the SC in rats.…”

“…Previous studies in several species (reviewed in King et al 1998a) have indicated that the dSC receives a substantial auditory projection from the inferior colliculus (IC), the largest component of which comes from the nBIC. An IC-to-dSC projection has also been described in the rat (Cadusseau and Roger 1985;Druga and Syka 1984), but the regions of the IC that supply the SC afferents have not been identified.…”

“…First, the external cortex of the inferior colliculus (ICx) and the nucleus of the brachium of the inferior colliculus (nBIC), the main sources of ascending auditory inputs (Edwards et al 1979;King et al 1998a), contain only coarse or partial spatial maps (Binns et al 1992;Schnupp and King 1997), whereas the dSC is apparently the only midbrain area to contain a complete topographic representation of both sound azimuth and elevation (King and Hutchings 1987;Middlebrooks and Knudsen 1984;Palmer and King 1982). Second, partial aspiration of the sSC in neonatal ferrets impairs the emergence of auditory topography in the region of the dSC underlying the aspirated sSC (King et al 1998b).…”

Lateralization of Interimplant Timing and Level Differences in Children Who Use Bilateral Cochlear Implants

“…Further areas of consideration include higher centres implicated in the coding of auditory space, such as the superior colliculus (King et al 1998;King et al 2000;Middlebrooks and Knudsen 1984) and the primary auditory cortex (King et al 2000). In order to promote binaural processing in children with bilateral cochlear implants, an understanding of the effect of deafness on the development of these important auditory centres is necessary.…”

Tectotectal Neurons and Projections: A Proposal to Establish a Consistent Nomenclature

“…As expected from this location, the NBIC receives dense projections from the ipsilateral IC (Kudo and Niimi, 1980). 8) The NBIC innervates densely the ipsilateral and contralateral SC and these projections seem essential for the emergence of a map of auditory space in the intermediate and deep layers of the SC (King et al, 1998b;Nodal et al, 2005). 9) The connections between the NBIC and the SC are reciprocal, as the NBIC receives significant, topographically organized input back from the ipsilateral SC (Doubell et al, 2000).…”