Spatial distribution and cellular composition of adult brain proliferative zones in the teleost, Gymnotus omarorum

Abstract

Proliferation of stem/progenitor cells during development provides for the generation of mature cell types in the CNS. While adult brain proliferation is highly restricted in the mammals, it is widespread in teleosts. The extent of adult neural proliferation in the weakly electric fish, Gymnotus omarorum has not yet been described. To address this, we used double thymidine analog pulse-chase labeling of proliferating cells to identify brain proliferation zones, characterize their cellular composition, and analyze the fate of newborn cells in adult G. omarorum. Short thymidine analog chase periods revealed the ubiquitous distribution of adult brain proliferation, similar to other teleosts, particularly Apteronotus leptorhynchus. Proliferating cells were abundant at the ventricular-subventricular lining of the ventricular-cisternal system, adjacent to the telencephalic subpallium, the diencephalic preoptic region and hypothalamus, and the mesencephalic tectum opticum and torus semicircularis. Extraventricular proliferation zones, located distant from the ventricular-cisternal system surface, were found in all divisions of the rombencephalic cerebellum. We also report a new adult proliferation zone at the caudal-lateral border of the electrosensory lateral line lobe. All proliferation zones showed a heterogeneous cellular composition. The use of short (24 h) and long (30 day) chase periods revealed abundant fast cycling cells (potentially intermediate amplifiers), sparse slow cycling (potentially stem) cells, cells that appear to have entered a quiescent state, and cells that might correspond to migrating newborn neural cells. Their abundance and migration distance differed among proliferation zones: greater numbers and longer range and/or pace of migrating cells were associated with subpallial and cerebellar proliferation zones.

Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum

“…Other outstanding proliferation and migration processes occurred in the Cb of adult G. omarorum as newborn cells migrated along relatively large distances in all cerebellar divisions (CCb, VCb, and EG) as they relocate from one cerebellar layer to another. There, the migration process involved an almost complete shift of newborn cells between cerebellar layers in a period of 30 days after CldU administration, as previously shown in the Cb of this (Olivera-Pasilio, 2014 ) and other teleost species ( A. leptorhynchus : Zupanc et al, 1996 ; D rerio : Zupanc et al, 2005 ; Kaslin et al, 2009 ; C. auratus : Delgado and Schmachtenberg, 2011 ; O. mossambicus : Teles et al, 2012 ; and M. rume : Radmilovich et al, 2016 ). According to the distribution of DCX cellular process in the CCb of G. omarorum , the migration process of new born cells may involve displacements in the medial-lateral direction along the CCb-mol (as shown by Kaslin et al, 2009 ), as well as in the rostral-caudal direction in the ganglionic layer, not described previously.…”

Adult Neurogenesis in Fish

“…4) (Alunni et al 2010;Ito et al 2010). In teleosts, proliferating cells are present at the dorsal, ventral, and caudal margins of the optic tectum Zupanc and Horschke 1995; Marcus et al 1999;Nguyen et al 1999;Ekstrom et al 2001;Candal et al 2005;Grandel et al 2006;Alunni et al 2010;Ito et al 2010;Kuroyanagi et al 2010;Maruska et al 2012;Teles et al 2012;Olivera-Pasilio et al 2014). In zebrafish and medaka, the majority of proliferating cells are located in the caudal part of the PGZ, in which LRCs are concentrated in the dorsomedial part of the optic tectum.…”

“…T eleost fish display the most prominent and widespread adult neurogenesis throughout the central nervous system compared with any other vertebrate studied so far (Zupanc and Horschke 1995;Zikopoulos et al 2000;Lema et al 2005;Zupanc et al 2005;Adolf et al 2006;Grandel et al 2006;Lindsey and Tropepe 2006;Pellegrini et al 2007;Kaslin et al 2008Kaslin et al , 2009Alunni et al 2010;Kuroyanagi et al 2010;Strobl-Mazzulla et al 2010;Fernandez et al 2011;Maruska et al 2012;Teles et al 2012;Tozzini et al 2012;Olivera-Pasilio et al 2014). Usually, the term adult refers to specimens that have reached their sexual maturity.…”

Adult Hippocampal Neurogenesis in Different Taxonomic Groups: Possible Functional Similarities and Striking Controversies

“…Fish have the highest number of neurogenic zones compared to other vertebrates [31], with up to 16 proliferative zones in some species [15,16,32]. In addition, more new cells are continuously generated in the fish central nervous system (CNS) than in other species, such as rodents [21,32,33,34].…”