Three-dimensional topography of corticopontine projections from rat barrel cortex: correlations with corticostriatal organization.

Subcortical re-entrant projection systems connecting cerebral cortical areas with the basal ganglia and cerebellum are topographically specific and therefore considered to be parallel circuits or "closed loops." The precision of projections within these circuits, however, has not been characterized sufficiently to indicate whether cortical signals are integrated within or among presumed compartments. To address this issue, we studied the first link of the rat cortico-ponto-cerebellar pathway with anterograde axonal tracing from physiologically defined, individual whisker "barrels" of the primary somatosensory cortex (SI). The labeled axons in the pontine nuclei formed several, sharply delineated clusters. Dual tracer injections into different SI whisker barrels gave rise to partly overlapping, paired clusters, indicating somatotopic specificity. Three-dimensional reconstructions revealed that the clusters were components of concentrically organized lamellar subspaces. Whisker barrels in the same row projected to different pontine lamellae (side by side), the somatotopic representation of which followed an inside-out sequence. By contrast, whisker barrels from separate rows projected to clusters located within the same lamellar subspace (end to end). In the neostriatum, this lamellar topography was the opposite, with barrels in the same row contacting different parts of the same lamellar subspace (end to end). The degree of overlap among pontine clusters varied as a function of the proximity of the cortical injections. Furthermore, corticopontine overlap was higher among projections from barrels in the same row than among projections from different whisker barrel rows. This anisotropy was the same in the corticostriatal projection. These findings have important implications for understanding convergence and local integration in somatosensory-related subcortical circuits.

Overlapping corticostriatal projections from the rodent vibrissal representations in primary and secondary somatosensory cortex.

To determine whether the neostriatum receives overlapping projections from two somatosensory cortical areas, the anterograde tracers biotinylated dextran amine (BDA) and fluoro-ruby (FR) were injected into the whisker representations of primary (SI) and secondary (SII) somatosensory cortex. Reconstructions of labeled terminals and their beaded varicosities in the neostriatum and thalamus were analyzed quantitatively to compare the extent of overlapping projections to both subcortical structures. Corticostriatal projections from focal sites in both somatosensory areas exhibited substantial amounts of divergence within the dorsolateral neostriatum. Most of the labeled terminals were concentrated in densely packed arborizations that occupied lamellar-shaped regions along the dorsolateral edge of the neostriatum. Tracer injections in both cortical areas also produced dense anterograde and retrograde labeling in the thalamus, especially in the ventrobasal complex (VB) and in the medial part of the posterior (POm) nucleus. Because these thalamic regions are topographically organized and have reciprocal connections with corresponding representations in both SI and SII, the amount of labeled overlap in the thalamus was used to indicate the degree of somatotopic correspondence at the SI and SII injection sites. We found that the proportion of overlapping projections to the neostriatum was moderately correlated with the amount of overlap observed in the thalamus. This result strongly indicates that specific sites in the dorsolateral neostriatum receive convergent projections from corresponding somatotopic representations in SI and SII, but also suggests that some of the corticostriatal divergence may reflect neostriatal integration of somatosensory information from noncorresponding representations in SI and SII.

Overlapping corticostriatal projections from the rodent vibrissal representations in primary and secondary somatosensory cortex.

To determine whether the neostriatum receives overlapping projections from two somatosensory cortical areas, the anterograde tracers biotinylated dextran amine (BDA) and fluoro-ruby (FR) were injected into the whisker representations of primary (SI) and secondary (SII) somatosensory cortex. Reconstructions of labeled terminals and their beaded varicosities in the neostriatum and thalamus were analyzed quantitatively to compare the extent of overlapping projections to both subcortical structures. Corticostriatal projections from focal sites in both somatosensory areas exhibited substantial amounts of divergence within the dorsolateral neostriatum. Most of the labeled terminals were concentrated in densely packed arborizations that occupied lamellar-shaped regions along the dorsolateral edge of the neostriatum. Tracer injections in both cortical areas also produced dense anterograde and retrograde labeling in the thalamus, especially in the ventrobasal complex (VB) and in the medial part of the posterior (POm) nucleus. Because these thalamic regions are topographically organized and have reciprocal connections with corresponding representations in both SI and SII, the amount of labeled overlap in the thalamus was used to indicate the degree of somatotopic correspondence at the SI and SII injection sites. We found that the proportion of overlapping projections to the neostriatum was moderately correlated with the amount of overlap observed in the thalamus. This result strongly indicates that specific sites in the dorsolateral neostriatum receive convergent projections from corresponding somatotopic representations in SI and SII, but also suggests that some of the corticostriatal divergence may reflect neostriatal integration of somatosensory information from noncorresponding representations in SI and SII.

Corticostriatal projections from rat barrel cortex have an anisotropic organization that correlates with vibrissal whisking behavior.

To elucidate the detailed organization of corticostriatal projections from rodent somatosensory cortex, the anterograde tracers biotinylated dextran amine (BDA) and fluoro-ruby (FR) were injected into separate parts of the whisker "barrel" representation. In one group of rats, the two tracers were injected into different barrel columns residing in the same row; in the other group of rats, the tracers were deposited into barrel columns residing in different rows. Reconstructions of labeled axonal varicosities in the neostriatum and ventrobasal thalamus were analyzed quantitatively to compare the extent of overlapping projections to these subcortical structures. For both groups of animals, corticostriatal projections terminated in densely packed clusters that occupied curved lamellar-shaped regions along the dorsolateral edge of the neostriatum. When the tracers were injected into different whisker barrel rows, the distribution of BDA- and FR-labeled terminals in the neostriatum followed a crude somatotopic organization in which the amount of overlap was approximately the same as in the ventrobasal thalamus. When both tracers were injected into the same whisker barrel row, however, the amount of corticostriatal overlap was significantly higher than the amount of overlap observed in the ventrobasal thalamus. These results indicate that corticostriatal projections from whisker barrel cortex have an anisotropic organization that correlates with the pattern of vibrissal movements during whisking behavior.

Divergent corticostriatal projections from a single cortical column in the somatosensory cortex of rats.

We injected biotinylated dextran amine (BDA) into single vibrissal 'barrels' of primary somatosensory (SI) cortex and reconstructed the topography of labelled varicosities in the dorsolateral caudate-putamen. Plots of labelled varicosities revealed densely-packed clusters of corticostriatal arborizations along the dorsolateral edge of the caudate-putamen and sparsely-packed arborizations more medially. The medial and lateral clusters of labelled terminals were separated by regions of unlabelled neuropil and lead us to conclude that a single cortical column sends divergent projections to multiple regions of the caudate-putamen.