Three-Dimensional Topography of Corticopontine Projections from Rat Barrel Cortex: Correlations with Corticostriatal Organization

Abstract

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...

Organization of Cerebral Projections to Identified Cerebellar Zones in the Posterior Cerebellum of the Rat

“…The ipsilateral contribution of cerebrocerebellar connections correlated nicely with the laterality of the CTb labeling in the pontine nuclei suggesting that this ipsilateral connection predominantly stems from the bilateral projection of the pontine nuclei to the cerebellar cortex (Serapide et al, 2002) rather than from a bilateral corticopontine projection (Legg et al, 1989;Leergaard et al, 2000b). Although the ipsilateral distribution of cortical RV labeling was similar to that observed contralaterally, local differences in density were observed; e.g., the density of the rostral M1/M2 patch was usually increased with respect to the ipsilateral main patch of labeling (Fig.…”

“…To some extent this is due to the complex transformations that take place in the cerebro-ponto-cerebellar pathway (Leergaard et al, 2006). Approaches to understand its functional organization are hampered by its multisynaptic nature and complex organization (Leergaard et al, 2000b(Leergaard et al, , 2006; e.g., only scant information is available on the relation between the functional cerebral regions and the so-called fractured cerebellar maps (Welker, 1987;Bower, 2011) or with the olivocerebellar modules. These modules are based on the matching organizations of projections from the olivocerebellar climbing fibers to longitudinal strips or zones of the Purkinje cells, the projections from these Purkinje cells to the cerebellar nuclei and their subsequent and selective projection patterns Teune et al, 2000;Sugihara and Shinoda, 2004;Voogd and Ruigrok, 2004;Pijpers et al, 2005;Apps and Hawkes, 2009;Ruigrok, 2011).…”

Motor Skill Learning Depends on Protein Synthesis in Motor Cortex after Training

“…Posteriorparietal injections were designed as a control intervention and demonstrate that the effects of PSI on motor learning are specific to motor cortex. The cerebellum has a lateralized organization, although the degree of lateralization may be less than in motor cortex (Luft et al, 1998;Leergaard et al, 2000;Matsushita and Xiong, 2001). However, even with unilateral PSI, some dampening of the learning curve would be expected if protein synthesis in cerebellar cortex is required for skill learning.…”

Functional circuits mediating sensorimotor integration: Quantitative comparisons of projections from rodent barrel cortex to primary motor cortex, neostriatum, superior colliculus, and the pons

“…To mediate somesthesia-guided behaviors, specific parts of the neural substrate must convey somatosensory information to the motor system. In rodents, for example, tracing studies have shown that primary somatosensory (SI) cortex projects to many brain regions involved in motor control including the primary motor (MI) cortex, neostriatum, superior colliculus, and the pontine nuclei (Wise and Jones, 1977a;Wiesendanger and Wiesendanger, 1982;Donoghue and Parham, 1983;Mihailoff et al, 1985;McGeorge and Faull, 1989;Miyashita et al, 1994;Izraeli and Porter, 1995;Schwarz and Thier, 1995;Brown et al, 1998;Wright et al, 1999;Leergaard et al, 2000aLeergaard et al, , 2003. Because MI cortex and superior colliculus project directly to motor nuclei in the brainstem and spinal cord (Liang et al, 1991;Imai and Aoki, 1993;Miyashita and Mori, 1995), SI projections to these regions provide a relatively direct route by which somatosensory information may modulate behavior.…”