Cytoarchitecture and ultrastructure of neural stem cell niches and neurogenic complexes maintaining adult neurogenesis in the olfactory midbrain of spiny lobsters, Panulirus argus

Abstract

New interneurons are continuously generated in small proliferation zones within neuronal somata clusters in the olfactory deutocerebrum of adult decapod crustaceans. Each proliferation zone is connected to a clump of cells containing one neural stem cell (i.e., adult neuroblast), thus forming a “neurogenic complex.” Here we provide a detailed analysis of the cytoarchitecture of neurogenic complexes in adult spiny lobsters, Panulirus argus, based on transmission electron microscopy and labeling with cell-type-selective markers. The clump of cells is composed of unique bipolar clump-forming cells that collectively completely envelop the adult neuroblast and are themselves ensheathed by a layer of processes of multipolar cell body glia. An arteriole is attached to the clump of cells, but dye perfusion experiments show that hemolymph has no access to the interior of the clump of cells. Thus, the clump of cells fulfills morphological criteria of a protective stem cell niche, with clump-forming cells constituting the adult neuroblast’s microenvironment together with the cell body glia processes separating it from other tissue components. Bromodeoxyuridine pulse-chase experiments with short survival times suggest that adult neuroblasts are not quiescent but rather cycle actively during daytime. We propose a cell lineage model in which an asymmetrically dividing adult neuroblast repopulates the pool of neuronal progenitor cells in the associated proliferation zone. In conclusion, as in mammalian brains, adult neurogenesis in crustacean brains is fueled by neural stem cells that are maintained by stem cell niches that preserve elements of the embryonic microenvironment and contain glial and vascular elements.

Neurogenesis is required for behavioral recovery after injury in the visual system of Xenopus laevis

“…The manufacturer tested the specificity of this antibody by western blot and found that it recognized a single band of 17KDa in colchemid-arrested HeLa cells as predicted. This antibody has been reported to detect mitotic cells in several species, including the optic tectum of chick, fish, and xenopus where staining is concentrated in mitotically active nuclei that line the ventricular layer of the tectum, similar to the expression we report (Schmidt and Derby, 2011; Tibber et al, 2006; Wirsching et al, 2012). We found that the antibody labels select nuclei in the Xenopus tadpole tectal proliferative zone that display morphological features of nuclei in various phases of mitosis.…”

“…This antibody was raised against 5-iodo-2′-deoxyuridine conjugated to ovalbumin and binds to 5-bromo-2′-deoxyuridine as well as 5-iodo-2′-deoxyuridine, according to the manufacturer's information. Several studies have shown that this antibody specifically labels nuclei that have incorporated BrdU or IdU into their newly synthesized DNA during the S-phase of the cell cycle (Schmidt and Derby, 2011). We have previously shown that this antibody labels cells in the proliferative layer of the Xenopus optic tectum in animals that have been exposed to BrdU or IdU, and that no labeling is present in the brains of animals that have not been exposed to BrdU or IdU (Sharma and Cline, 2010).…”

First‐generation neuronal precursors in the crayfish brain are not self‐renewing

“…We proposed, therefore, that (1) primary neuronal precursor cells in the crayfish niche are not self‐renewing, and (2) a source extrinsic to the niche provides cells that replenish the niche precursor pool (Beltz et al, 2011; Benton et al, 2011). This proposal is in contrast to the view that large mitotic cells in the crayfish niche (putative neuroblasts) persist beyond embryonic life, providing a self‐renewing source of neurons (Song et al, 2009; Schmidt and Derby, 2011). To resolve this issue, we directly tested the self‐renewal capacity of niche precursor cells.…”

Enriched Environment Increases PCNA and PARP1 Levels in Octopus vulgaris Central Nervous System: First Evidence of Adult Neurogenesis in Lophotrochozoa

“…Comparably, in insects, cell proliferation takes place in mushroom bodies, as a center of multimodal integration, where newborn cells migrate into the depth of the cortex placing among the older interneurons (Cayre et al., , ). In crustaceans, adult neurogenesis is detectable in the central olfactory pathway where an overall increase in olfactory sensory neurons is evident (Schmidt and Harzsch, ; Schmidt and Derby, ). Among mammals, the cell proliferation affects the olfactory bulb, first processing stage of olfactory information, in which immature neuroblasts differentiate into two types of interneurons that integrate themselves in existent circuits (Petreanu and Alvarez‐Buylla, ; Nissant et al., ; Breton‐Provencher and Saghatelyan, ).…”

“…This fascinating process, in adult organisms, recapitulates the whole neural development from neural progenitor to fate determination passing through differentiation, migration, axonal, and dendritic development of newborn neurons, as well as synapses formation and functional integration into the existing neural circuitries (Duan et al., ; Sun et al., ). All these processes occur in animals with a complex nervous system that exhibit a range of sophisticated behaviors such as mammals (Kempermann et al., ; Gage et al., ; Gould et al., ; Amrein et al., ; Lepousez et al., ), humans included (Eriksson et al., ; Bergmann et al., ), nonmammals vertebrates (Alvarez‐Buylla et al., ; Marchioro et al., ; Zupanc et al., ; Kaslin et al., ; Simmons et al., ), and insects and crustaceans (Cayre et al., ; Dufour and Gadenne, ; Schmidt and Derby, ; Fernández‐Hernández et al., ; Benton et al., ; Kim et al., ). Mammals and invertebrates show that their adult neurogenesis is not widespread throughout the brain, but it is restricted to specific neural areas, that is, the multimodal associative centers considered the anatomical and functional substrate of the higher cognitive capabilities (Kempermann, ).…”