Projections from the ventral nucleus of the trapezoid body to the dorsal cochlear nucleus in the rat: Morphology, distribution, and cellular origin

Abstract

Animals integrate auditory and somatosensory stimuli because the perception of sounds depends not only on their position relative to the sound source, but also on the posture of the head and ears. In the mammalian brain, audiotactile integration already occurs in the dorsal cochlear nucleus (DCN), a very early station of the central auditory pathway. In the DCN, auditory inputs preferentially target the deep layer, whereas somatosensory inputs innervate granule cells, whose axons target the superficial, molecular layer. However, there is an often overlooked major pathway that presumably conveys direct auditory information to the molecular layer of the DCN: the projection from the contralateral ventral nucleus of the trapezoid body (VNTB), first characterized by Warr and Beck (1996, Hear. Res., 93:83–101).

To investigate in detail the morphology and distribution of the VNTB-to-DCN projection, we injected the bidirectional tracer biotinylated dextran amine (BDA) into the VNTB of adult rats and analyzed the axons that innervate the DCN. Moreover, to identify the neurons that innervate the DCN, we injected BDA into the DCN and analyzed the retrogradely labeled VNTB neurons.

Our results show that the VNTB-to-DCN projection is very predominantly contralateral. The axons reach the cochlear nuclei via the rostral part of the trapezoid body. Within the DCN, VNTB axons form a very dense plexus that covers the entire molecular layer and, to a lesser extent, the underlying fusiform cell layer. These axons bear a high number of en passant and terminal synaptic boutons. In the plexus, parasagittal bands of higher density perpendicular to the pial surface alternate with bands of lower density. The VNTB-to-DCN projection is tonotopic. The DCN is innervated by medium-sized multipolar neurons that occupy the ventral two-thirds of the VNTB and are distributed throughout the rostrocaudal extent of the nucleus. Moreover, the deep layer of the DCN is innervated by the ipsilateral lateral nucleus of the trapezoid body.

Although the biological role of the VNTB-to-DCN projection remains unknown, the available evidence from the literature suggests that it is GABAergic. Given its density, the projection may be very relevant to the functions of the DCN. Therefore, this projection should be considered in future investigations of DCN physiology and pathology, and should be incorporated into future morphofunctional schemes and models of the DCN.