Direct projections from cochlear nuclear complex to auditory thalamus in the rat

Abstract

It is known that the dorsal cochlear nucleus and medial geniculate body in the auditory system receive significant inputs from somatosensory and visual-motor sources, but the purpose of such inputs is not totally understood. Moreover, a direct connection of these structures has not been demonstrated, because it is generally accepted that the inferior colliculus is an obligatory relay for all ascending input. In the present study, we have used auditory neurophysiology, double labeling with anterograde tracers, and retrograde tracers to investigate the ascending projections of the cochlear nuclear complex. We demonstrate that the dorsal cochlear nucleus and the small cell cap of the ventral cochlear nucleus have a direct projection to the medial division of the medial geniculate body. These direct projections from the cochlear nucleus complex bypass the inferior colliculus and are widely distributed within the medial division of the medial geniculate, suggesting that the projection is not topographic. As a nonlemniscal auditory pathway that parallels the conventional auditory lemniscal pathway, its functions may be distinct from the perception of sound. Because this pathway links the parts of the auditory system with prominent nonauditory, multimodal inputs, it may form a neural network through which nonauditory sensory and visual-motor systems may modulate auditory information processing.

Fig. 1.

Axons in the medial division of the MGM labeled by anterograde transport of dextran after an injection in the DCN (Table1, R-117). a, Micrograph of the injection (micropipette,white circle) at best frequency (4.5 kHz).b, Low-magnification micrograph of the IC showing laminar axons in the central nucleus (arrow).c, High-magnification micrograph of labeled axons in MGM (see inset, drawing of MGB, dashed circle). Scale bars: a, b, 500 μm; c, 50 μm. D, Dorsal;M, medial; L, lateral.

Fig. 2.

Distribution of axonal labeling after two separate injections in the DCN and PVCN (Table 1, R-034). a, Camera lucida drawing of a TRD injection (red, red pipette) in 6 kHz DCN. b, Injection of fluorescein–dextran and biotinylated dextran (FD + BDA;black, yellow pipette) into the PVCN in the same animal at 1.5 kHz best frequency. c, Plots of serial sections showing the location of TRD axons (red) that form a continuous plexus of terminal boutons confined to the MGM and overlap with BDA axons (black).d, Camera lucida drawing of a Nissl-stained section through the MGB, also shown as a photomicrograph in d′.e, Adjacent section to that shown in d′.e, Photomicrograph of the axons in MGM also shown at higher magnification (red window) in f. Observe the overlap of red and blackaxons (asterisk) as opposed to the two distinct laminas seen in the IC (g, arrows). Scale bars: a–e, g, 500 μm;f, 100 μm. D, Dorsal; M, medial; L, lateral.

Fig. 3.

Labeling in the MGM (c) and IC (b) after two injections in the DCN (a) one octave apart, 27 kHz (black–yellow, pipette) and 13.5 kHz (red, pipette) (Table 1, R-119). Nonoverlapping laminas are labeled in the IC (b, red andblack arrows), whereas contiguous and overlapping axonal termination is seen in the MGM (c,arrows within outline of MGM). Scale bars:a, b, 500 μm; c, 100 μm; inset in a, 250 μm.D, Dorsal; M, medial; L, lateral.

Fig. 4.

Axonal labeling in the MGM (b, c) after two injections (a) at the same best frequency, 11 kHz, one in the DCN (black, pipette) and the other in the AVCN (gray, pipette) (Table 1, R-021).b, Labeled axons in the medial geniculate body are seen only from the injection in the DCN in the lower-power micrograph (b, MGB, dashed lines) and the enlargement (c). Scale bars: a,b, 500 μm; c, 100 μm.D, Dorsal; M, medial; L, lateral.

Fig. 5.

Retrograde labeling of the projection from the cochlear nuclear complex to the medial geniculate body.a, Injection of HRP in the MGM (black, pipette). b, Labeling in the DCN and PVCN (black dots). c, A typical example of labeled giant cell. Scale bars: a, b, 1 mm; c, 50 μm. D, Dorsal; M, medial;L, lateral.