Projection and innervation patterns of individual thalamic reticular axons in the thalamus of the adult rat: a three-dimensional, graphic, and morphometric analysis

Abstract

The gamma-aminobutyric acid-ergic thalamic reticular nucleus (Rt), which carries matching topographical maps of both the thalamus and cortex and in which constituent cells can synaptically communicate between each other, is the major extrinsic source of thalamic inhibitions and disinhibitions. Whether all the Rt axonal projections into the thalamus are similarly organized and have common projection and innervation patterns are questions of great interest to further our knowledge of the functioning of the Rt. The present study provides architectural and morphometric data of individual, anterogradely labeled axonal arbors that arose from distinct parts of the Rt. One hundred twenty-seven Rt neurons from all regions of Rt were marked juxtacellularly with biocytin or Neurobiotin in urethane-anesthetized adult rats. Eighteen two-dimensional and 14 three-dimensional reconstructions of single tracer-filled Rt neurons were made from serial, frontal, horizontal, or sagittal sections. Both the somatodendritic and axonal fields of tracer-filled Rt cells were mapped in three dimensions and illustrated to provide a complementary stereotaxic reference for future studies. Most marked units projected to a single nucleus of the anterior, dorsal, intralaminar, posterior, or ventral thalamus. Axons emerging from cells in distinct sectors of the Rt projected to distinct nuclei. Within a sector, neurons with separate dendritic fields innervated separate regions either in a single nucleus or into different but functionally related thalamic nuclei. Neurons with an overlap of their dendritic fields gave rise either to overlapping axonal arborizations or, more rarely, to distinct axonal arbors within two different thalamic nuclei implicated in the same function. In rare instances, an Rt axon could project within these two nuclei. Thalamic reticular axons commonly displayed a single well-circumscribed arbor containing a total of about 4,000 +/- 1,000 boutons. Every arbor was composed of a dense central core, which encompassed a thalamic volume of 5-63 x 10(6) microm3 and was made up of patches of maximal innervation density (10 +/- 4 boutons/tissue cube of 25 microm each side), surrounded by a sparse component. The metric relationships between the Rt axonal arbors and the dendrites of their target thalamocortical neurons were determined. Both the size and maximal innervation density of the axonal patches were found to fit in with the somatodendritic architecture of the target cells. The Rt axonal projections of adult rats are thus characterized by their (1) well-focused terminal field with a patchy distribution of boutons and (2) parallel organization with a certain degree of divergence. The role of the Rt-mediated thalamic inhibition and disinhibition may be to contrast significant with nonrelevant ongoing thalamocortical information.