Topography of purkinje cell compartments and mossy fiber terminal fields in lobules ii and iii of the rat cerebellar cortex: Spinocerebellar and cuneocerebellar projections

Abstract

The cerebellar cortex is histologically uniform by conventional staining techniques, but contains an elaborate topography. In particular, on the efferent side the cerebellar cortex can be subdivided into multiple parasagittal compartments based upon the selective expression by Purkinje cell subsets of various molecules, for example the polypeptide antigens zebrin I and II, and on the afferent side many mossy fibers terminate as parasagittal bands of terminals. The relationships between mossy fiber terminal fields and Purkinje cell compartments are important for a full understanding of cerebellar structure and function. In this study the locations of spino- and cuneocerebellar mossy fiber terminal fields in lobules II and III of the rat cerebellum are compared to the compartmentation of the Purkinje cells as revealed by using zebrin II immunocytochemistry. Wheat germ agglutinin-horseradish peroxidase was injected at three different levels in the spinal cord and in the external cuneate nucleus, and the terminal field distributions in lobules II and III of the cerebellar cortex were compared with the Purkinje cell compartmentation. In the anterior lobe, zebrin II immunocytochemistry reveals three prominent, narrow immunoreactive bands of Purkinje cells, P1 + at the midline and P2 + laterally at each side. These are separated and flanked by wide zebrin compartments (P1 − and P2 −). There are also less strongly stained P3 + and P4 + bands more laterally. The spinocerebellar terminals in the granular layer are distributed as parasagittally oriented bands. Projections from the lumbar region of the spinal cord terminate in five bands, one at the midline (L1), a second with its medial border midway across P1 − and its lateral border at the P2 +/P2 − interface (L2), and a third extending laterally from midway across P2 −. The lateral edge of L3 may align with the P3 +/P3 − border. The terminal fields labeled by a tracer injection into the thoracic region give a very similar distribution (T1, T2 and T3). The only systematic difference is in T2, which statistical analysis suggests may be broader than L2. In contrast, anterograde tracer injections into the cervical region label synaptic glomeruli scattered throughout the lobule with much weaker or no evidence of banding. The terminal fields of the cuneocerebellar projection have a complementary distribution to those of thoracic and lumbar spinocerebellar terminals. There are two lateral bands, Cu2 and Cu3. Cu2 lies within the Purkinje cell P1-compartment, abutting L1/T1 medially and L2/T2 laterally. Cu3 lies between L2 and L3 within the P2 − Purkinje cell compartment. The medial edge of Cu3 is tightly aligned with the P2 +/P2 − border. In addition, there may be a weak, narrow Cul band at the midline that either overlaps with L1 and T1 or splits them into two. This highly ordered topography is the anatomical substrate of the elaborate receptive field map of the cerebellum.