Cerebellar Terminations in the Red Nucleus of Macaca fascicularis : An Electron-Microscopic Study Utilizing the Anterograde Transport of WGA:HRP

Abstract

The red nucleus (RN) of the macaque monkey is divided into a rostral two-thirds, the parvicellularis (RNp), which projects to the cerebellum by way of the inferior olivary nucleus, and a caudal third, the magnocellularis (RNm), which projects to the spinal cord via the rubrospinal tract. The RNp and RNm receive afferents from two principal sources: the cerebral motor cortices and the deep cerebellar nuclei. The terminations of these two afferent projections tend to be spatially segregated on rubral neurons, in that most corticorubral afferents terminate on more distal dendrites, and those from the deep cerebellar nuclei terminate more proximally. The present electron-microscopic analysis of the cerebellar terminations in the macaque RN provides anatomical evidence for the presence of labeled afferents in both divisions of this motor nucleus, following injection of wheatgerm agglutinin conjugated to horseradish peroxidase (WGA:HRP) into the deep cerebellar nuclei and the anterograde transport of the tracer to the RN. The cerebellar terminal afferents are large; contain numerous mitochondria and primarily rounded synaptic vesicles; and form asymmetric synaptic contacts with rubral neurons. Unlike other terminals in the nucleus, they possess an electron-lucent cytoplasmic matrix and less densely packed synaptic vesicles. They are termed “large, round, pale” (LRP) terminals because of the morphological characteristics that distinguish them from other afferent terminal types found in RN. Labeled cerebellar afferents in RNp and RNm contact primarily neuronal somata, proximal dendrites emerging from the cell body, large-diameter dendrites, and the spines of rubral neurons that arise from somata and proximal dendrites. In general, afferents of the deep cerebellar nuclei in the RN do not contact vesicle-containing dendritic appendages of the γ-aminobutyric acid (GABA)-immunoreactive interneuronal population; nor do they tend to form complex synaptic arrangements, such as triads or glomeruli. They are not observed to be presynaptic to any axonal type of terminal. Previous physiological evidence suggests that the deep cerebellar nuclei exert a powerful influence over rubral neurons. In agreement with the physiological findings, the present study provides morphological evidence for the presence of cerebellar afferents synapsing upon somata and proximal dendrites. This, coupled with the presumed lack of GAB A modulation of cerebellar signals, allows the cerebellum to have significant influence over the firing properties of rubral neurons.

Key Words:

• cerebellorubral
• cerebellum
• red nucleus
• monkey
• WGA:HRP
• anterograde transport
• electron microscopy