Adult neurogenesis: A common strategy across diverse species

Abstract

Adult neurogenesis, the generation of new neurons from adult precursor cells, occurs in the brains of a phylogenetically diverse array of animals. In the higher (amniotic) vertebrates, these precursor cells are glial cells that reside within specialized regions, known as neurogenic niches, the elements of which both support and regulate neurogenesis. The in vivo identity and location of the precursor cells responsible for adult neurogenesis in nonvertebrate taxa, however, remain largely unknown. Among the invertebrates, adult neurogenesis has been particularly well characterized in freshwater crayfish (Arthropoda, Crustacea), although the identity of the precursor cells sustaining continuous neuronal proliferation in these animals has yet to be established. Here we provide evidence suggesting that, as in the higher vertebrates, the precursor cells maintaining adult neurogenesis in the crayfish Procambarus clarkii are glial cells. These precursor cells reside within a specialized region, or niche, on the ventral surface of the brain, and their progeny migrate from this niche along glial fibers and then proliferate to form new neurons in the central olfactory pathway. The niche in which these precursor cells reside has many features in common with the neurogenic niches of higher vertebrates. These commonalities include: glial cells functioning as both precursor and support cells, directed migration, close association with the brain vasculature, and specialized basal laminae. The cellular machinery maintaining adult neurogenesis appears, therefore, to be shared by widely disparate taxa. These extensive structural and functional parallels suggest a common strategy for the generation of new neurons in adult brains. Indexing termsglia; migration; neurogenic niche; olfaction; vasculature New neurons continue to be added to specific regions in the brains of many animals throughout adulthood (Kempermann, 2000). In vertebrates, adult-born neurons are the progeny of precursor cells residing within specialized brain regions, termed neurogenic niches (GarciaVerdugo et al., 2002;Doetsch, 2003a;Ma et al., 2005). The cellular and extracellular elements that make up these niches not only support the precursor cells structurally but also functionally regulate their activity and the development of their progeny (Song et al., 2002;Doetsch, 2003a,b;Shen et al., 2004;Ma et al., 2005). Glial cells are key components of the neurogenic niches of adult vertebrates, acting both as the precursor cells and in the support and regulation of neurogenesis (Garcia-Verdugo et al., 2002;Song et al., 2002;Doetsch, 2003a,b;Garcia et al., 2004;Seri et al., 2004;Ma et al., 2005). These cells also guide and regulate the migration of newborn cells to the regions of the brain in which they differentiate into neurons (Lois et al., 1996;Bolteus and Bordey, 2004 Garcia-Verdugo et al., 2002;Mercier et al., 2002;Palmer, 2002;Doetsch, 2003a;Ma et al., 2005).While adult neurogenesis is known to occur in a phylogenetically diverse array of animals, neur...

Adult neurogenesis and cell cycle regulation in the crustacean olfactory pathway: from glial precursors to differentiated neurons

“…The length of time required to label cells within the cluster with BrdU suggests that they are relatively quiescent, as are neuronal precursor cells in adult vertebrates, which may rest in the G 1 phase of the cell cycle for several days between cell divisions (Morshead et al 1994;Maslov et al 2004). Indeed, a G 1 phasespecific marker (MCM2-7; Cvetic and Walter 2006) reliably labels cells in each subpopulation of the glial soma cluster (Sullivan et al 2005(Sullivan et al , 2007. Together, these results demonstrate that the GSC contains a small number of mitotically active cells and that these cells exhibit in vivo properties of precursor cells.…”

“…3A, B) (Sullivan et al 2005(Sullivan et al , 2007. These cells differ from other brain glia in the close proximity of their somata and the fasciculation of their processes into tracts (Linser et al 1997;Sullivan and Beltz 2005c;Allodi et al 2006) and occur in both juvenile and adult crayfish (Sullivan et al 2005(Sullivan et al , 2007. Lateral and medial subpopulations within the glial soma cluster (GSC) are grouped around a central, circular region that does not label with glial markers (Fig.…”

“…The problem of maintaining neurogenesis in adult brains over several decades appears, therefore, to require the establishment of a different proliferative system, distinct from the neuroblasts that are responsible for the generation of the CNS during embryogenesis. The first evidence providing insights into the nature of this system arose from recent experiments examining olfactory neurogenesis in juvenile and sexually mature crayfish, Procambarus clarkii (Sullivan et al 2007). …”

“…Examination of the GSC using several cell cycle markers indicates that this region represents an additional proliferative site in the adult crayfish brain (Sullivan et al 2007). Long periods of exposure to BrdU (10-14 days) reliably label 1-2 cells in both the lateral and medial subpopulations of the cluster.…”

“…The axons of the OL projection neurons join with those of the AL projection neurons upon leaving the lobes to form a large tract, known as the olfactory globular tract (OGT), which bifurcates in the centre of the brain before projecting bilaterally to higher-order regions of the brain, known collectively as the lateral protocerebrum (Hanström 1925;Sullivan and Beltz 2004). Most cluster 10 projection neurons express the neuropeptide crustaceanSIFamide (Yasuda et al 2004;Sullivan and Beltz 2005b,c;Yasuda-Kamatani and Yasuda 2006;Sullivan et al 2007). …”