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.
Key words: 3-D reconstruction; basal ganglia; cerebellum; cerebrocerebellar; double anterograde tracing; parallel circuits; pontine nuclei; somatosensory maps; somatotopyNeurons in the cerebral cortex project to a number of subcortical targets. Many of these neurons belong to two major corticosubcortical re-entrant circuits, one including the basal ganglia (for review, see Heimer et al., 1995;Parent and Hazrati, 1995) and another including the pontine nuclei and cerebellum (for review, see Bjaalie, 1992, 1997;Schmahmann and Pandya, 1997). Structural and functional specification have been studied extensively in the first links of these circuits, i.e., in the projections from the cerebral cortex to the pontine nuclei (Brodal, 1968(Brodal, , 1978Mihailoff et al., 1978Mihailoff et al., , 1985Wiesendanger and Wiesendanger, 1982;Bjaalie and Brodal, 1989;Leergaard et al., 2000) and the neostriatum (Webster, 1961;Malach and Graybiel, 1986;Gerfen, 1989;Alloway et al., 1999). During development, the global topography of corticopontine projections appears to be determined by simple temporal and spatial gradients operative within source (cerebral cortex) an...