Bilateral projections to the thalamus from individual neurons in the inferior colliculus

Abstract

The medial geniculate body (MG) receives a large input from the ipsilateral inferior colliculus (IC) and a smaller but substantial input from the contralateral IC. Both crossed and uncrossed inputs comprise a large percentage of glutamatergic cells and a smaller percentage of GABAergic cells. We used double labeling with fluorescent retrograde tracers to identify individual IC cells that project bilaterally to the MGs in adult guinea pigs. We also used immunohistochemistry for glutamic acid decarboxylase to distinguish GABAergic from glutamatergic cells that project bilaterally to the MG. We found cells in the IC that contained both retrograde tracers, indicating that they project bilaterally. Across cases, the bilaterally projecting cells constituted up to 37% of the cells that project to the ipsilateral MG and up to 73% of the cells that project to the contralateral MG. GABAergic cells averaged 20% of the bilaterally-projecting population. We conclude that a population of IC cells sends branching axonal projections to innervate the MG bilaterally. Most of the neurons in this population are glutamatergic, with a minority that are GABAergic. A mixed projection, with glutamatergic cells outnumbering GABAergic cells, originates from each of the major IC subdivisions (central nucleus, dorsal cortex, and lateral cortex). The bilaterally projecting cells are likely to serve functions different from the larger unilateral projections, perhaps synchronizing activity on the two sides of the auditory brain.

Keywords: GABA; collateral; inferior colliculus; medial geniculate body; synchronization, RRID:AB_2278725, RRID:AB_260754.

Figure 1.

Injection sites of retrograde tracers typically involved all major subdivisions of the MG. Photomicrographs show a representative case with large deposits of red beads in the left medial geniculate body (MG) (a) and FluoroGold in the right MG (b) in a single animal (GP636). Each row shows a series of transverse sections arranged from caudal to rostral. D − dorsal; L − lateral; LG − lateral geniculate nucleus; LP − lateral posterior nucleus; M − medial; MGd − dorsal division of the MG; MGm − medial division of the MG; s − shell of the MG; MGsg − suprageniculate division of the MG; MGv − ventral division of the MG; PP/PIN − peripeduncular nucleus and posterior intralaminar nucleus.

Figure 2.

Bilaterally projecting IC cells could be GAD⁻ (white arrowheads) or GAD⁺ (green arrowheads). Each row shows a single region of the IC with cells labeled by a tracer injected into one MG (left column: FluoroGold or Fast Blue) and/or a second tracer injected into the other MG (center column: red beads) and immunostained with anti-GAD (right column, green). Arrowheads identify cells labeled by both retrograde tracers, whereas arrows identify cells labeled by a single retrograde tracer. For both symbols, white indicates GAD⁻ cells and green indicates GAD⁺ cells. Scale bar = 20 μm. Cells are from GP 636 left IC (a) or right IC (b-d) and GP 640 right IC (e).

Figure 3.

Bilaterally-projecting tectothalamic cells represent a small proportion of the IC cells that project to the ipsilateral MG and a larger proportion of IC cells that project to the contralateral MG. The largest population projects to the ipsilateral MG and does not project to the contralateral MG (red circles). A much smaller population projects to the contralateral MG and includes a substantial number of cells that project bilaterally (purple circle). There may be a third, small population that projects to the contralateral MG and not to the ipsilateral MG (blue circle). Numbers show the maximum values of bilaterally projecting cells as a percentage of cells that project to one or the other MG. Each pathway - ipsilateral, contralateral and bilateral - arises from both GABAergic and non-GABAergic (i.e., glutamatergic) neurons (not shown).