ReviewThe common properties of neurogenesis in the adult brain: from invertebrates to vertebrates☆
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.
References (156)
- et al.
Spatial learning affects immature granule cell survival in adult rat dentate gyrus
Neurosci. Lett.
(2000) - et al.
N-Cadherin and Ng-CAM/8D9 are involved serially in the migration of newly generated neurons into the adult songbird brain
Neuron
(1994) - et al.
Characterization of the subventricular zone of the adult human brain: evidence for the involvement of Bcl-2
Neurosci. Res.
(2000) - et al.
Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain
Neurosci. Lett.
(2000) - et al.
Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats
Neuroscience
(1999) - et al.
Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus
Neuroscience
(1994) - et al.
Fate of neuroblast progeny during postembryonic development of mushroom bodies in the house cricket, Acheta domesticus
J. Insect. Physiol.
(2000) - et al.
Neurogenesis persists in the subependymal layer of the adult mouse brain
Neurosci. Lett.
(1993) - et al.
Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse
Neuroscience
(1994) - et al.
Increased granule cell neurogenesis in the adult dentate gyrus following mossy fiber stimulation sufficient to induce long-term potentiation
Brain Res.
(2000)
Synaptogenesis and changes in synaptic morphology related to acquisition of a new behavior
Brain Res.
Subventricular zone astrocytes are neural stem cells in the adult mammalian brain
Cell
Development and experience lead to increased volume of subcompartments of the honey bee mushroom body
Behav. Neurol. Biol.
Neurogenesis is absent in the brain of ault honeybees and does not explain behavioural neuroplastiticy
Neurosci. Lett.
Spatial learning deficits in old rats: a model for memory decline in the aged
Neurobiol. Aging
Postnatal neurogenesis in the olfactory bulbs of a lizard. A tritiated thymidine autoradiographic study
Neurosci. Lett.
Neuronal birth and death
Curr. Opin. Neurobiol.
Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat
Neuroscience
Stress and hippocampal neurogenesis
Biol. Psych.
Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster
Develop. Biol.
Identification of a neural stem cell in the adult mammalian central nervous system
Cell
Morphologic and electrophysiologic maturation in developing dentate gyrus granule cells
Brain Res.
Delayed postnatal neurogenesis in the cerebral cortex of lizards
Brain Res.
Late generated neurons in the medial cortex of adult lizards send axons that reach the Timm-reactive zones
Brain Res. Dev. Brain Res.
Estradiol enhances learning and memory in a spatial memory task and affects levels of monoaminergic neurotransmitters
Horm. Behav.
Peripheral infusion of IGF-1 selectively induces neurogenesis in the adult rat hippocampus
J. Neurosci.
Are new neurons formed in the brains of adult mammals?
Science
Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods
J. Comp. Neurol.
Mechanism of neurogenesis in adult avian brain
Experientia
Migration of young neurons in adult avian brain
Nature
Birth of projection neurons in the adult avian brain may be related to perceptual or motor learning
Science
High vocal center growth and its relation to neurogenesis, neuronal replacement and song acquisition in juvenile canaries
J. Neurobiol.
Brain growth during the adult stage of a Holometabolous insect
Naturwissenschaften
A synaptic model of memory: long-term potentiation in the hippocampus
Nature
Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats
J. Neurosci.
Serotonin may stimulate granule cell proliferation in the adult hippocampus, as observed in rats grafted with raphe neurons
Eur. J. Neurosci.
Neurogenesis in adult canary telencephalon is independent of gonadal hormone levels
J. Neurosci.
Functions for interneuronal nets in the hippocampus
Can. J. Physiol. Pharmacol.
Distinct populations of cells in the adult dentate gyrus undergo mitosis or apoptosis in response to adrenalectomy
J. Comp. Neurol.
Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus
J. Neurosci.
Restoring production of hippocampal neurons in old age
Nat. Neurosci.
Adrenal steroids and N-methyl-d-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway
Neuroscience
Neurogenesis in an adult insect brain and its hormonal control
Nature
Neurogenesis in adult insect mushroom bodies
J. Comp. Neurol.
Inhibition of polyamine biosynthesis alters oviposition behavior in female crickets
Behav. Neurosci.
Inhibitory role of ecdysone on neurogenesis and polyamine metabolism in the adult cricket brain
Arch. Insect. Biochem. Physiol.
Specific requirement of putrescine for the mitogenic action of juvenile hormone on adult insect neuroblasts
Proc. Natl. Acad. Sci. USA
Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus. I. Ventricular zone cell proliferation
Cell Tissue Res.
In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain
J. Neurosci.
Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies
Science
Cited by (80)
Cellular and molecular profiles of anterior nervous system regeneration in Diopatra claparedii Grube, 1878 (Annelida, Polychaeta)
2021, HeliyonCitation Excerpt :Neurogenesis is a process by which a new neuron is produced from a stem/precursor cell during the developmental process from juvenile to adult. However, in some adult insects, it was found that persistent neurogenesis occurs in the mushroom bodies which are known to function in learning and memory (Cayre et al., 2002). Furthermore, a study conducted on an adult serpulid polychaete has demonstrated the outgrowth of a cerebral ganglion as the first feature established during neurogenesis (Brinkmann and Wanninger, 2009).
Time-dependent role of prefrontal cortex and hippocampus on cognitive improvement by aripiprazole in olfactory bulbectomized mice
2017, European NeuropsychopharmacologyFine structure of synaptic sites and circuits in mushroom bodies of insect brains
2016, Arthropod Structure and DevelopmentCitation Excerpt :In honey bees, cockroaches, and Drosophila, structural alterations occur in microglomerular size and density in response to aging (Groh et al., 2006), memory acquisition due to novel task-related behaviours (Farris et al., 2001), to sensory associations (Heisenberg, 2003), or to learning spatial cues, e.g. place memory (Lent et al., 2007). These species do not develop new neurons in mature individuals, in contrast to beetles and crickets that add new mushroom body neurons even after the final molt (see Cayre et al., 2002; Mashaly et al., 2008). Structural changes are quantified using molecular markers.
Intraspecific variation in invertebrate cognition: a review
2024, Behavioral Ecology and Sociobiology
- ☆
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.