Parallel streams for the relay of vibrissal information through thalamic barreloids

Abstract

This study investigated the organization of a vibrissal pathway that arises from the interpolar division of the spinal trigeminal complex (SP5i), transits through the ventral posterior medial nucleus (VPM), and innervates the somatosensory cortical areas in the rat. Using Fluoro-Gold and biotinylated dextran amine, respectively, as retrograde and anterograde tracers, the following organization plan was disclosed. The SP5i projection arises from a population of small-sized neurons that selectively innervate the ventral lateral part of VPM. In cytochrome oxidase-stained material, this region does not display any barreloid arrangement, but Fluoro-Gold injections in single barrel columns labeled rods of cells that extend caudally into the ventral lateral division of VPM. Thus, on the basis of retrograde labeling, barreloids were divided into core and tail compartments, which correspond to the rod segments running across the dorsal and ventral lateral parts of VPM, respectively. Double-labeling experiments revealed that SP5i afferents innervate the tail of barreloids. The anterograde labeling of thalamocortical axons show that most "core cells" project to a single barrel column, whereas some "tail cells" give rise to branching axons that innervate the second somatosensory area and the dysgranular zone of the barrel field. Injections that straddled the transition zone between the core and tail regions disclosed cells projecting to a single barrel column and to the surrounding dysgranular zone. These results suggest that the projection of "barreloids cells" to the granular and/or dysgranular zones relates to the class of prethalamic input(s) they receive.

Fig. 1.

Distribution of SP5i terminal fields in the rat VPM. A–C show, in CO-stained sections, the topography of BDA-labeled SP5i terminal fields at different frontal planes (rostral to caudal in A–C). Note the segregation of terminal fields in VPMvl. In tissue processed only for CO histochemistry (D), VPMvl displays lighter staining than the dorsal part of the nucleus.Asterisks outline the frontier between VPM and VPL. Scale bar in A also applies to B andC.

Fig. 2.

Distribution of retrogradely labeled trigeminothalamic cells after FG injections in different parts of the somatosensory thalamus. Injections sites in dorsal VPM, VPMvl, and Po are shown in A–C, with the corresponding maps of retrogradely labeled cells below. Each map represents the counts of five consecutive sections. sp5, Spinal trigeminal tract; SP5o, oral division of the spinal trigeminal complex; VC, ventral cochlear nucleus;7n, tract of the facial nerve.

Fig. 3.

Comparative distributions of the cross-sectional areas of cell somata of SP5i neurons that project to VPMvl (black bars) and Po (white bars).InsetsA and B show FG-labeled cells projecting to VPMvl and Po, respectively. Injection sites in Po and VPMvl are shown in Figure 2.

Fig. 4.

Retrograde labeling in the rat VPM after FG injections in barrel column C2. Tangential sections in Aand D show the cortical injection sites.B and C show, respectively, the core and tail of barreloid C2 in coronally cut sections. The core and tail of the same barreloid, as they appear in horizontal sections, are shown inE and F, respectively. A, Anterior; L, lateral; P, posterior.

Fig. 5.

Three-dimensional structure of thalamic barreloids as revealed by the retrograde transport of FG injected in barrel columns D3 (A) and B2 (B). Horizontal, frontal, and sagittal views are shown from left to right. Theblack and gray dots represent, respectively, neurons within the core and tail of barreloids. The transition between the core and tail was assumed to occur at the dorsal VPM/VPMvl border. A, Anterior; D, dorsal;M, medial; P, posterior.

Fig. 6.

Selective innervation of the tail of barreloids by SP5i afferents. The injection sites of BDA in SP5i and of FG in barrel columns C2/C3 are shown in A andB, respectively. Dark blue SP5i fibers inC are seen beneath the rod ofbrown-labeled somata forming the core of barreloids. In the tail region (D), dark bluefibers and terminals are seen among the cluster of FG-labeled cells.

Fig. 7.

Thalamocortical projections arising from the dorsal part of VPM and from VPMvl. Biotinylated dextran injections in dorsal VPM (A) label fibers that terminate in the barrels (B), whereas injections in VPMvl (C) produce terminal labeling in interbarrel regions (D). Scale bars:C, 500 μm; D, 250 μm.

Fig. 8.

Camera lucida reconstructions of thalamocortical fibers arising from the dorsal part of VPM and from VPMvl. The “standard” type of barrel-specific fiber, which was labeled after BDA injections in dorsal VPM, is shown in A.B shows the areal distribution of thalamocortical axons labeled after BDA injection in VPMvl. Four consecutive sections were used for the reconstruction. Branching axons that project to the dysgranular zone of S1 and to S2 are shown in C. A fiber that innervates both a barrel and the surrounding dysgranular zone is shown in D (see Results). Shaded patchesrepresent cortical barrels. CPu, Caudate putamen;GP, globus pallidus; Rf, rhinal fissure.