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...
A survey of the morphology of the brains (cerebral ganglia) of 13 species of decapods shows that all have common areas of neuropil that are developed to differing degrees in the different groups. The neuropils of the paired accessory lobes, however, appear to have evolved de novo in the Reptantia. Phylogenetic relationships within the Reptantia suggest that the accessory lobes were initially large but became reduced in size during the evolution of the brachyurans and anomalans. The cerebral ganglia of many arthropods are subdivided into recognisable areas of neuropil linked to one another by axon tracts. Some of these neuropil areas are geometrically structured, with serially arranged fascicles of axons or synaptic areas, such as in the first three ganglia lying behind the retina. Other areas are "glomerular" and contain either columns or spheres of fine-fibered synaptic fields, such as the olfactory lobes. Still other areas have no recognisable substructure, but like the structured neuropils, are always found in the same place with the same axon tracts linking them to their neighbours or via nerve roots to specific receptor organs or muscles.Such a fixed and orderly organisation of the substructures in vertebrate brains has been long recognised and accepted, but that the same rigid organisation of neuropil areas in the arthropod brains can also be found has not received the same attention, nor has it been fully exploited in any comparative study of arthropod brains.In the arthropods, the primary function of many of the brain neuropils can be deduced from the sensory organ which projects to them and the motor neurons that extend from them. In crustaceans, for example, the olfactory lobe receives its total input from the chemoreceptors on the first antenna. The mechanoreceptors of the second antenna and the motor neurons that control the movements of the second antenna are confined to the antenna neuropil. This is not true for all neuropils, however, for there are several that apparently do not receive the endings of primary afferent fibers, nor do they contain the dendrites of motor neurons. There is little or no physiological information about many of these higher order neuropils that could provide a clue to their inputs, outputs, or function. Virtually the only information about them is that they do not occur in all species and that, ifthey are present, they may vary considerably in their relative sizes in different species.Neuropils that can be identified with particular receptor organs often reflect the numbers of primary afferent inputs, and therefore the importance to the animal, of the sense organ that projects to it. By the same token the relative sizes of the higher order neuropils may be reflected in some unique aspect of the behavioural habits of the different animals, thus providing a clue to their function. The problem with this approach is that species belonging to a monophyletic group may exhibit a great uniformity in the relative size of a given higher order neuropil. Their behavioural hab...
BackgroundAdult neurogenesis, the production and integration of new neurons into circuits in the brains of adult animals, is a common feature of a variety of organisms, ranging from insects and crustaceans to birds and mammals. In the mammalian brain the 1st-generation neuronal precursors, the astrocytic stem cells, reside in neurogenic niches and are reported to undergo self-renewing divisions, thereby providing a source of new neurons throughout an animal's life. In contrast, our work shows that the 1st-generation neuronal precursors in the crayfish (Procambarus clarkii) brain, which also have glial properties and lie in a neurogenic niche resembling that of vertebrates, undergo geometrically symmetrical divisions and both daughters appear to migrate away from the niche. However, in spite of this continuous efflux of cells, the number of neuronal precursors in the crayfish niche continues to expand as the animals grow and age. Based on these observations we have hypothesized that (1) the neuronal stem cells in the crayfish brain are not self-renewing, and (2) a source external to the neurogenic niche must provide cells that replenish the stem cell pool.ResultsIn the present study, we tested the first hypothesis using sequential double nucleoside labeling to track the fate of 1st- and 2nd-generation neuronal precursors, as well as testing the size of the labeled stem cell pool following increasing incubation times in 5-bromo-2'-deoxyuridine (BrdU). Our results indicate that the 1st-generation precursor cells in the crayfish brain, which are functionally analogous to neural stem cells in vertebrates, are not a self-renewing population. In addition, these studies establish the cycle time of these cells. In vitro studies examining the second hypothesis show that Cell Tracker™ Green-labeled cells extracted from the hemolymph, but not other tissues, are attracted to and incorporated into the neurogenic niche, a phenomenon that appears to involve serotonergic mechanisms.ConclusionsThese results challenge our current understanding of self-renewal capacity as a defining characteristic of all adult neuronal stem cells. In addition, we suggest that in crayfish, the hematopoietic system may be a source of cells that replenish the niche stem cell pool.
The birth of new neurons and their incorporation into functional circuits in the adult brain is a characteristic of many vertebrate and invertebrate organisms, including decapod crustaceans. Precursor cells maintaining life-long proliferation in the brains of crayfish (Procambarus clarkii, Cherax destructor) and clawed lobsters (Homarus americanus) reside within a specialized niche on the ventral surface of the brain; their daughters migrate to two proliferation zones along a stream formed by processes of the niche precursors. Here they divide again, finally producing interneurons in the olfactory pathway. The present studies in P. clarkii explore (1) differential proliferative activity among the niche precursor cells with growth and aging, (2) morphological characteristics of cells in the niche and migratory streams, and (3) aspects of the cell cycle in this lineage. Morphologically symmetrical divisions of neuronal precursor cells were observed in the niche near where the migratory streams emerge, as well as in the streams and proliferation zones. The nuclei of migrating cells elongate and undergo shape changes consistent with nucleokinetic movement. LIS1, a highly conserved dynein-binding protein, is expressed in cells in the migratory stream and neurogenic niche, implicating this protein in the translocation of crustacean brain neuronal precursor cells. Symmetrical divisions of the niche precursors and migration of both daughters raised the question of how the niche precursor pool is replenished. We present here preliminary evidence for an association between vascular cells and the niche precursors, which may relate to the life-long growth and maintenance of the crustacean neurogenic niche.
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