Laterally projecting cerebrospinal fluid‐contacting cells in the lamprey spinal cord are of two distinct types

Abstract

Cerebrospinal fluid-contacting (CSF-c) cells are found in all vertebrates, but their function remains elusive. In the lamprey spinal cord, they surround the central canal and some have processes passing the gray matter to the lateral edge of the flattened spinal cord. Stimulation of CSF-c cells at the central canal elicits GABAergic inhibitory postsynaptic potentials (IPSPs) in intraspinal stretch receptor neurons (edge cells). Here, we characterize laterally projecting CSF-c cells according to their morphology, phenotype, and neuronal properties by using immunohistochemistry, retrograde tracing, calcium imaging, and whole-cell recordings. We identify two types of CSF-c cells. Type 1 cells have a bulb-like ending that protrudes into the central canal and a lateral process that ramifies ventrolaterally and laterally with a dense plexus surrounding the mechanosensitive dendrites of the edge cells. Most type 1 cells fire spontaneous action potentials that are abolished by tetrodotoxin, and all display spontaneous excitatory postsynaptic potentials and IPSPs that remain in the presence of tetrodotoxin. GABA and somatostatin are colocalized in type 1 cells, and they express both GABA and glutamate receptors. Type 2 cells, on the other hand, have a flat ending protruding into the central canal and a laterally projecting process that ramifies only at the lateral edge. These cells show immunoreactivity to taurine, but they do not express GABA or somatostatin, nor do they have any active neuronal properties. Type 2 cells might be a form of glia. Type 1 CSF-c cells are neurons and may play a modulatory role by influencing edge cells and thus the locomotor-related sensory feedback.

Investigation of spinal cerebrospinal fluid-contacting neurons expressing PKD2L1: evidence for a conserved system from fish to primates

“…Peptides such as the vasoactive intestinal polypeptide (VIP), somatostatin or urotensin II-related peptide (URP2) have been found in CSF-cNs (Buchanan et al, 1987; Yulis and Lederis, 1988a,b; Christenson et al, 1991a; Lamotte and Shapiro, 1991; Lopez et al, 2007; Wyart et al, 2009; Parmentier et al, 2011; Jalalvand et al, 2014). Ventral CSF-cNs were found dopaminergic in tetrapods such as birds (Acerbo et al, 2003) and amphibians (Gonzalez and Smeets, 1991, 1993; Gonzalez et al, 1993), as well as in some teleosts such as the eel and the trout (Roberts et al, 1995), in dogfish (Sueiro et al, 2004) and lampreys (Schotland et al, 1996; Rodicio et al, 2008).…”

Comparative Distribution and In Vitro Activities of the Urotensin II-Related Peptides URP1 and URP2 in Zebrafish: Evidence for Their Colocalization in Spinal Cerebrospinal Fluid-Contacting Neurons

“…It is likely that the presence of URP1 and/or URP2 in CSF-cNs is an ancestral feature of gnathostomes since the occurrence of CSF-cNs containing UII-like immunoreactivity has also been reported in a chondrichthyan species, Hydolagus collieri [ 54 ]. Beside URP1 and URP2, several other neuropeptides have been detected in CSF-cNs, such as vasoactive intestinal peptide (VIP) and SS [ 53 , 55 – 57 ]. In this respect, it is noteworthy that in coho salmon Oncorhynchus kisutch , SS- and UII-immunoreactive material do not localize in the same CSF-cNs [ 58 ] suggesting the occurrence of distinct CSF-cN types.…”

Neural stem/progenitor cells are activated during tail regeneration in the leopard gecko (Eublepharis macularius)

“…Evidence from lamprey has revealed two distinct classes of CSF-c cells, which differ on the basis of electrophysiological properties (type 1 evoke action potentials, type 2 do not), cell morphology (type 1 protrude into the lumen of the central canal, type 2 do not), and protein expression (Jalalvand, Robertson, Wall en, Hill, & Grillner, 2014). Our data points toward gecko CSF-c cells as most closely resembling the type 1 phenotype based on neuronal marker expression (HuC/D1 and TUJ11) and morphology (with bulb-like endings that project into the central canal and ventro-laterally oriented processes) (Jalalvand et al, 2014;Russo et al, 2004). Additionally, there is evidence that CSF-c cells in lizards are GABA-ergic neurons (Alibardi et al, 1993).…”