Review
The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates

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Abstract

Until recently, it was believed that adult brains were unable to generate any new neurons. However, it is now commonly known that stem cells remain in the adult central nervous system and that adult vertebrates as well as adult invertebrates are currently adding new neurons in some specialized structures of their central nervous system. In vertebrates, the subventricular zone and the dentate gyrus of the hippocampus are the sites of neuronal precursor proliferation. In some insects, persistent neurogenesis occurs in the mushroom bodies, which are brain structures involved in learning and memory and considered as functional analogues of the hippocampus. In both vertebrates and invertebrates, secondary neurogenesis (including neuroblast proliferation and neuron differentiation) appears to be regulated by hormones, transmitters, growth factors and environmental cues. The functional implications of adult neurogenesis have not yet been clearly demonstrated and comparative study of the various model systems could contribute to better understand this phenomenon. Here, we review and discuss the common characteristics of adult neurogenesis in the various animal models studied so far.

Introduction

The formation of the nervous system has been widely studied during development in species and models from different evolutionary origins as invertebrates, amphibians, birds and mammals. However, although the study of brain maturation in adult animals has long been ignored, it is now clear that central nervous system plasticity does not stop at the end of development. The ability of an animal to adapt its behavior to an infinity of environmental situations reflects a degree of functional, but also probably structural brain plasticity. Furthermore, the quality of environment, i.e. the variety of sensory stimuli has been shown to influence the ratio synapses/neurons and to modulate neuronal survival (Turner and Greenough, 1985). Axogenesis and synaptogenesis have been observed in adults and, even in the absence of any pathological process, synaptic remodelling occurs in response to physiological cues (hormonal titers, stress, neuronal activity...) (Theodosis and Poulain, 1993, Frankfurt, 1994). Thus, the dogma of the neural fixity in the brain of adult animals is no more a question of the day, especially since production of new neurons, or secondary neurogenesis, has been demonstrated in the brain of various adult invertebrate and vertebrate species (including humans).

Indeed, although Altman evoked the possibility of a persistent neurogenesis in the brain of adult rodents as early as 1962, this observation remained unnoticed until 1977 when Kaplan and Hinds, using electron microscopy, confirmed the neuronal fate of the newly generated cells in the dentate gyrus and in the olfactory bulb (Kaplan and Hinds, 1977). Concomitantly, several studies on non-mammalian vertebrates (amphibians, fish, reptiles, birds) showed that new neurons were produced during the whole life, especially in structures involved in vision (John and Easter, 1977, Raymond and Easter, 1983, Chetverukhin and Polenov, 1993). Finally, our group showed for the first time that, even in insects, the nervous system of which had often been considered as particularly inflexible, neurogenesis still persists in adults (Cayre et al., 1994, Cayre et al., 1996a).

Recently, the discovery of cell proliferation and neuronal production in human hippocampus (Eriksson et al., 1998) aroused interest of the neurobiologists.

Section snippets

In invertebrates

In some insect species, new interneurons continue to be added throughout adulthood in the main associative centre of the insect brain, the mushroom bodies. These structures are involved in the integration of multisensorial inputs from the antennae, the complex eyes and the palpae (Kenyon, 1896, Erber, 1978, Mobbs, 1982, Li and Strausfeld, 1997). It is a paired structure consisting in densely packed intrinsic neurons: the Kenyon cells, and differentiated neuropils.

The neuropil is typically

Stem cells and progenitor cells

The occurrence of secondary neurogenesis implies that neural stem cells are not only present in the developing nervous system but also in the adult nervous system. The term ‘neural stem cell’ is used for a cell that presents two main properties: it should be able to divide symmetrically to generate high numbers of identical cells (multiplication, expansion), and to divide asymmetrically to produce progenitor cells which in turn will give rise to different cell types such as neurons and glial

In vivo regulation of secondary neurogenesis

Neuroblast proliferation and survival of newly formed neurons appear to be regulated by both internal (hormones, neurotransmitters, growth factors...) and environmental (seasons, sensorial stimuli...) cues.

Functional implications of adult neurogenesis

The reasons why progenitor cells persist in the adult central nervous system and give rise to new neurons in some particular brain structures remain unclear, and this question is of great interest. When the first evidences of proliferative neuroblasts in adult rodent brain were published (Kaplan and Hinds, 1977), it was then thought that this persistent neurogenesis was only a vestige of development without necessarily functional importance. Since, many other studies have demonstrated the

Concluding remarks

From the above data, it appears that similar processes are underlying neurogenesis in the adult brain of invertebrates and vertebrates.

Stem- or progenitor-cells are still present in the central nervous system of adults. However, it must be underlined that progenitor cell repartition differs in vertebrates and insects. Whereas progenitor cells are scattered along the border of the SVZ or the granular layer of hippocampus in mammals, the persistent neuroblasts of crickets are arranged in a

Acknowledgements

We thank Drs Hanne Duve and Alan Thorpe for helpful comments and careful editing of the manuscript.

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    This paper was submitted as part of the proceedings of the 20th Conference of European Comparative Endocrinologists, organized under the auspices of the European Society of Comparative Endocrinology, held in Faro, Portugal, 5–9 September 2000.

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