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. INDEXING TERMSproliferation; decapod crustacean; arthropod; brain; glia Neurogenesis persists throughout adulthood and leads to continuous production of new neurons in certain brain regions. Adult neurogenesis is well documented in brains of mammals and other vertebrates, including fish, amphibians, reptiles, and birds, but it is also a constitutive process in brains of many arthropods (Lindsey and Tropepe, 2006). In mammalian brains, adult neurogenesis predominantly produces new local interneurons of the olfactory bulb (periglomerular cells and granule cells) and the hippocampal dentate gyrus (granule cells; Kriegstein and Alvarez-Buylla, 2009). In brains of some insect species, adult neurogenesis generates new local interneurons (Kenyon cells) of the mushroom bodies (Cayre et al., 1994(Cayre et al., , 1996Gu et al., 1999;Dufour and Gadenne, 2006;Mashaly et al., 2008;Zhao et al., 2008;Ghosal et al., 2009 NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript neuropils that in most insects receive projections neurons (PNs) from the antennal lobes and thus represent the second stage of the central olfactory pathway; moreover, they are centers for multisensory integration (Strausfeld et al., 2009). Throughout decapod crustaceans, adult neurogenesis leads to the formation of new local intern...

Adult neurogenesis in crayfish: Origin, expansion, and migration of neural progenitor lineages in a pseudostratified neuroepithelium

“…In contrast to the findings of Song et al () and to results in spiny lobsters and non‐reptant decapod crustaceans (Schmidt, ; Schmidt & Derby, ; Wittfoth & Harzsch, ), we did not detect an enlarged NP in every crayfish DPS studied. In fact, a substantial portion of our 3d‐analyzed samples lacked this morphologically conspicuous cell type (Table ).…”

“…An alternative to the hemocyte identity we have suggested here is their potential glial nature. Pointing in this direction, similar cytoplasmic labeling of a PH3 antibody was reported in the brains of spiny lobsters (Schmidt & Derby, ), where the cells were interpreted as glia due to their multipolar processes.…”

“…In the latter, the deutocerebral proliferative system (DPS; sensu Wittfoth & Harzsch, ) generates adult‐born neurons that integrate into the central olfactory pathway (e.g., Schmidt, ; Sullivan & Beltz, ). DPS anatomy is best understood in the spiny lobster Panulirus argus (e.g., Schmidt, ; Schmidt & Derby, ) and in crayfish (e.g., Sullivan, Benton, Sandeman, & Beltz, ; Chaves da Silva, Benton, Beltz, & Allodi, ), which have proved suitable for mechanistic studies.…”

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

“…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, ).…”

Adult neural stem cells: Long‐term self‐renewal, replenishment by the immune system, or both?

“…These studies also ruled out persistent neuroblasts (i.e. traditional ectodermal precursors of neurons) as a source of adult‐born neurons in crayfish , as was previously proposed .…”