Patterns of reciprocity in auditory thalamocortical and corticothalamic connections: Study with horseradish peroxidase and autoradiographic methods in the rat medial geniculate body

Abstract

The patterns of reciprocity between retrogradely labeled thalamocortical cells of origin and anterogradely projecting corticothalamic axon terminals were studied in the subdivisions of the adult rat medial geniculate body following auditory cortical injections of mixtures of horseradish peroxidase and [³H]leucine. The labeling produced by each method was examined independently, both qualitatively and quantitatively, in adjacent series of tetramethylbenzidine-processed sections and in autoradiographs after 24–96 hour survivals. The distribution and number of labeled cells and axon terminals were assessed separately for each method and compared systematically throughout the rostro-caudal extent of the medial geniculate complex. The principal finding was that zones containing many retrogradely labeled neuronal somata are not completely coextensive with areas of heavy terminal labeling within the medial geniculate body, although there is a gross congruence of thalamocortical-corticothalamic projections. Conversely, we found many zones of autoradiographic silver grains without retrogradely labeled somata in the adjacent sections; in general, the autoradiographic zones of non-reciprocity were more extensive and marked than were retrograde zones of non-reciprocity. The rat medial geniculate complex could be subdivided on the basis of its neuronal organization, cytoarchitecture, fiber architecture, and thalamocortical and corticothalamic connections into three major parts: the ventral, dorsal, and medial divisions. This pattern of organization was comparable, though not identical, to that of the corresponding subdivisions in the cat medial geniculate body (Winer: Adv. Anat. Embryol. Cell Biol. 86:1–98, '85). While the retrograde labeling appeared to mark many of the different types of neurons in each of the three divisions, there were distinct local and quantitative and qualitative differences in the distribution of autoradiographic terminal labeling. The ventral division received the heaviest cortical input, the medial division the least labeling, while the dorsal division was intermediate. Thus, corticogeniculate projections to the ventral division often produced values 20–100 times above background (absolute values: 2,001–10,000 silver grains/14,400 μm²; background: 2); the same projection to the dorsal division usually resulted in grain counts no more than 5–20 times above background (501–2,000/14,400 μm²), while in the medial division the number of silver grains rarely exceeded two to five times the background (201–500/14,400 μm²). These distinctive local patterns in the density of the anterograde transport suggest that the pattern of corticothalamic innervation varies systematically in the subdivisions of the auditory thalamus, perhaps as a result of different populations of corticothalamic cells of origin innervating the subdivisions of the medial geniculate complex. The bulk of the corticothalamic labeling was in the neuropil, with comparatively few silver grains overlying neuronal somata. With regard to the retrograde labeling, each subdivision of the medial geniculate complex probably contains more than one type of thalamocortical projection neuron, based on a comparison of the retrogradely labeled somatodendritic profiles with the form of Golgi-impregnated neurons. Many of the different classes of medial geniculate cells in the various subdivisions appear to have been labeled. We conclude that, despite a large-scale topographical overlap in the spatial territories of thalamocortical cells of origin and corticothalamic axonal terminal fields, there are many local zones of non-reciprocity, and different internuclear patterns of corticothalamic projections. These patterns may have functional significance for spatially segregating the flow of ascending and descending information within the auditory thalamus.