Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections.

Abstract

To ascertain whether the auditory neocortex also innervates the central nucleus of the inferior colliculus (CNIC) and not only its dorsal (DCIC) and external (ECIC) cortices, the anterograde tracers Phaseolus vulgaris-leucoagglutinin (PHA-L) and biotinylated dextran (BD) were injected into the primary auditory neocortex of albino rats (Te1), and labeled corticocollicular fibers were studied via light and electron microscopy. Axons from discrete regions of Te1 form two rostrocaudally oriented laminar plexuses of terminal fibers in the ipsilateral inferior colliculus (IC) and one in the contralateral IC. The first ipsilateral plexus, located in the medial half of the IC, has a dorsomedial to ventrolateral orientation, parallel to the isofrequency planes of the IC; is continuous through the CNIC and DCIC; and extends into the rostral ECIC. The second plexus is located in the deep layers of the lateral ECIC. These two plexuses meet caudally and ventrally, at the border between the CNIC and the lateral ECIC. The plexus in the contralateral IC is less dense and shorter than the two ipsilateral plexuses and is symmetric to the medial plexus. The thickness of the three plexuses is correlated with the size of the injection site, and their mediolateral and dorsoventral positions change as the injection site in Te1 is displaced rostrocaudally, with more caudal injections resulting in more dorsolateral medial plexuses and more dorsomedial lateral plexuses. Furthermore, the ventromedial border of the IC receives nontopographic, convergent projections from wide regions of rostral portions of Te1. The distribution of these corticocollicular plexuses mimics the topography of previously described intracollicular fibers. Electron microscopy shows that, in all three subdivisions of the ipsilateral IC, corticocollicular fibers form small boutons with features generally associated with excitatory transmission; i.e., they contain round synaptic vesicles and form asymmetric synapses with thin dendritic shafts and spines. These results demonstrate that the auditory corticocollicular projections innervate more extensive regions of the IC than were previously observed. Although peripheral regions receive the densest projection, the entire IC appears to be the target of corticofugal input.