In Rhesus monkeys, CSF-contacting neurons are the only neurons present in the medullo-spinal peri-ependymal zone

Abstract

In spinal cord and medulla, ependymal cells are organized in a monolayer forming the central canal (cc). In rodents, this region, also known as a stem cell niche, was shown to contain cerebrospinal fluid-contacting neurons (CSF-cNs). These neurons are GABAergic and because of their chemo- and mechanosensory properties they would represent a novel sensory system intrinsic to the central nervous system. In primates, little is known about these neurons and more generally about the region around the cc. Here, using immunohistochemical approaches, we investigated the organization of the cc region and CSF-cN properties in Macaca mulatta Rhesus monkey. In contrast to rodent, we observe along the whole medullo-spinal axis a large zone around the cc delimited by long radial ependymal fibers that is enriched with astrocytes and microglia but largely devoid of neuronal elements except for CSF-cNs. These primate CSF-cNs share with rodent CSF-cNs similar morphological and phenotypical features with a largely immature profile. Our data suggest that they extend their axons in the longitudinal axis to form fiber bundles close to the cc and we further show that CSF-cNs receive GABAergic and serotoninergic synaptic contacts on their soma and dendrite. Taken together our results reveal in Rh. monkey a specific organization of the region around the cc potentially forming a buffer zone between CSF and parenchyma where CSF-cNs would play a crucial role in the detection of CSF signals and their transmission to the central nervous system, a role that would need to be further investigated.