Adult Neurogenesis in Mammals: History
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Please note this is an old version of this entry, which may differ significantly from the current revision.
Contributor:
Katarzyna Bartkowska
,
Beata Tepper
,
Krzysztof Turlejski
,
Ruzanna Djavadian

In eutherians, the generation of new neurons in the central nervous system (CNS) and the formation of almost all brain structures occur during embryonic development, known as developmental neurogenesis. It is now well established that new neurons are continuously produced in adult mammalian brains, and this process is known as adult neurogenesis. 

  • marsupials
  • adult neurogenesis
  • dentate gyrus

1. Introduction

A number of brain areas are considered to be proliferative zones in adults of mammalian species. Two areas, the subventricular zone (SVZ) and the dentate gyrus, are well-known neurogenic zones where the proliferation of cells occurs throughout life. According to available data on adult neurogenesis in mammals, new neurons are generated in the adult brain of opossums [1] and the fat-tailed dunnarts [2], rodents, including laboratory mice and rats [3][4][5][6], carnivores [7][8], sheep [9][10], shrews [11][12], giant otter shrews [13], tree shrews [14][15], the rock hyrax and sengi [16], hedgehogs and European moles [17], bats [18][19], and primates, including humans [20][21][22]. More and more evidence is currently accumulating about adult brain structures, such as the piriform cortex, cerebral cortex, corpus callosum, striatum, amygdala, and hypothalamus, where cells express different markers for cell proliferation (for review, see [23][24]). This indicates that cells can be added to these structures in adult brains. More data on adult neurogenesis in various mammalian species are presented in Table 1.
Table 1. Mammals that appear to have adult neurogenesis. AC: anterior commissure; AD: adult; AMG: amygdala; BLA: basolateral amygdala; BrST: brainstem; CER: cerebellum; CN: caudate nucleus; CP: caudate putamen; CTX: cerebral cortex; DG: dentate gyrus; EC: entorhinal cortex; EPN: endopiriform nucleus; HTH: hypothalamus; mth: month; OB: olfactory bulb; OT: olfactory tubercle; P: postnatal; PIR: piriform cortex; SN: substantia nigra; STR: striatum; SVZ: subventricular zone; TT: tenia tecta; wk: week; yrs: years.
Order/Family Species Gestation Eyes Opening Lifespan Postnatal Developmental Neurogenesis Adult Neurogenesis
OB DG CER OB/SVZ DG CER PIR Other
Didelphimorphia/Didelphidae Gray short-tailed opossum 14–15 days P35–P37 2.5 yrs up to P28 [25][26]   P1-P155 [27] 5 mth-2 yrs [1] 6.5–21.5 mth [1]   up to P270  
Dasyuromorphia/Dasyuridae Fat-tailed dunnart 13–16 days P45 1–2 yrs         4–24 mth [2]      
Diprotodontia/Phalangeridae Brush-tailed possum 18 days P110 13 yrs   P5–P82 [28] up to 3 mth [29]          
Diprotodontia/Macropodidae Tammar wallaby 25–28 days P140 11–14 yrs up to P25 [30]              
Quokka wallaby 28 days P110 8–15 yrs   P20-P85 [31]            
Euliptyphla/Erinaceidae White-breasted hedgehog 35 days P21 3–5 yrs       AD [17] AD [17]   AD [17]  
Eulipotyhla/Talpidae European mole 30 days P22 2–3 yrs       AD [17] AD [17]   AD [17]  
Eulipotphla/Soricidae Hottentot golden mole             AD [16] AD [16]   AD [16] CTX [16]
Giant other shrew 22 days P20–P24 5 yrs       AD [13] AD [13]   AD [13] OT, EPN [13]
Pygmy shrew,
Common shrew		 22–24 days P20–P24 1 yr       1 yr [11] 5 mth [11]      
Greater white-toothed shrew, Eurasian water shrew, African giant shrew, Asian house shrew 20–31 days P20–P24 1.5–3 yrs       AD [12] AD [12]      
Rodentia/Muridae Rats (Long Evans, Sprague-Dawley, Wistar, Fischer 344, Brown Norway wild rats) 21–23 days P13–P15 2 yrs P0-P10 [32] P6-P15 [3][33]
up to P14 [34]		 up to P21 [35] AD [36] 6–21 mth [4][37]
8–9 wk [33]		   AD [38] HTH 2 mth [39][40]
CTX, STR 9–10 wk [41]
BrSt AD [42]
Mice (C57BL/6, CD1, BALB/c, ICR, A/J, FVB, C3H/HeJ, 129/SvJ, DBA/1, DBA/2) 19–21 days P10–P13 1–1.5 yrs P0-P20 [43][44] up to P20 [45][46][47] up to P15 [48] 3–4 mth [49]
2 mth [50]		 3–4 mth [49][51]   AD [52] SN 2–20 mth [53]
BLA 2–4 mth [54]
CTX, STR 2–4 mth [49][55]
HTH 3–4 mth [56]
Rodentia/Cricetidae Syrian hamster 16 days P12–P14 2–3 yrs       2.5 mth [57] P28-P49 [58]     BLA, HTH P28-P49 [58]
Meadow vole, Prairie vole 21 days P14 3–16 mth       3–5 mth
[59][60][61]		 3–5 mth [59][60][61]     CTX, CP, BLA,
THT 3–5 mth [59][60]
Rodentia/Caviidae Guinea pig 65–68 days Born with open eyes 4–5 yrs   up to P30 [5]   6, 12 mth [62] 1 yr [5][63]   12–14 mth [64]  
Rodentia/Bathyergidae Highveld mole-rat, Cape mole-rat, Naked mole-rat, Damaraland mole-rat 70 days P14 6–15 yrs         1 yr [65]
2–9 yrs [66]
AD [67][68]		   2–9 yrs [66] BLA, 2–9 yrs [66]
Rodentia/Leporidae New Zeland white rabbit 31 days P7 9 yrs     P10 [3]     1–3 yrs [3]   CN, AD [69]
Hyracoidea/Procaviidae Rock hyrax 200 days Born with open eyes 8–12 yrs       AD [16] AD [16]   AD [16] CTX, AD [16]
Macrosce-lidea/Macroscelididae Eastern rock sengi, Four-toed sengi 40–60 days Born with open eyes 4–6 yrs       AD [16] AD [16]   AD [16] CTX, AD [16]
Artiodactyla/Bovidae Ilede-France sheep 147 days Born with open eyes 10–12 yrs       AD [10] AD [10]     HTH, 18–24 mth [56]
Carnivora/Felidae Domestic cat 64 days P7–P10 12–18 yrs             18–24 mth [8] CTX, EC 18–24 mth [8]
Carnivora/Canidae Domestic dog 61 days P10–P14 10–13 yrs         2–6 yrs [7][70]      
Carnivora/Mustelidae Ferret 42 days P32 5–12 yrs     P4, P21 [71]          
Scandentia/Tupaiidae Tree shrew 46 days P21 12 yrs       2 mth-6 yrs [15] AD [14]   2 mth -6 yrs [15] BLA 2 mth-6 yrs [15]
Chiroptera Microchiroptera bats 44–180 days P1–P2 20 yrs     AD [72] AD [18]   AD [72] AC, BLA [72]
Megachiroptera bats 4–6 m P1–P2 20 yrs     AD [73] AD [19][73] AD [73] AD [73] BrSt, Tectum, AD [73]
Primates/(New World monkey) Callitrichidae Common marmoset 151 days Born with open eyes 12 yrs up to P30 [74]       1.5–7 yrs [75]
4 yrs [74][76]		     CTX, CC, AMG
4 yrs [76]
Primates/(New World monkey) Cebidae Squirrel monkey 160–170 days Born with open eyes 21 yrs       4–6 yrs [77] 7–10 yrs [78]   3-6 yrs [79] CTX, BLA 3-6 yrs [79]
Primates/(Old World monkey)
Cercopithecidae		 Rhesus monkey 165 days Born with open eyes 30 yrs         12, 21, 31 yrs [80]     CTX, BLA 12, 21, 31 yrs [80]]
Macaque monkey 162 days E125 25 yrs         5–23 yrs [21]   6-12 yrs [79] CTX AD [81], BLA6-12 yrs [79]
Primates/Hominidae Humans 280 days E195 75–80 yrs   3 wk-1 yr [82][83] up to 5 mth [83]   16-69 yrs [84] 23–72 yrs [22]
AD [85][86][87]
14–79 yrs [86]		     STR 3–79 yrs [88] AMG 24–67 yrs [89]

2. Adult Neurogenesis in the Subventricular Zone/Olfactory Bulb 

Progenitor cells leave the SVZ after division and migrate long distances. Numerous papers have reported that in various mammals, including marsupials, the majority of proliferated cells of the SVZ migrate through the rostral migratory stream (RMS) and mature in the olfactory bulb (OB). These data are presented in Table 1. The OB is a relay structure of the brain for the olfactory system. In the glomerulus of the OB, information is selectively modulated by GABAergic and dopaminergic interneurons forming the periglomerular inhibitory network. The second inhibitory network is formed by GABAergic granule cells of the OB. This two-layered lateral inhibition enhances odor discrimination to make information more specific, and then the axons of mitral cells send it to the olfactory cortex (for review, see [90]). In mice, progenitor cells of the SVZ undergo asymmetric divisions generating neuroblasts that migrate along the RMS to reach the OB [91]. Most of them differentiate into granule or periglomerular neurons using a neurotransmitter, either GABA (the majority) or dopamine [92].
A large number of studies have revealed that new neurons are critical for odor detection and discrimination and olfactory learning and memory [93][94][95]. Newly generated granule cells participate in odor–reward association [96]. The elimination of adult-born neurons or inhibition of the rate of neurogenesis in the OB affects odor detection and odor discrimination regardless of the methods used [97][98]. In addition, adult-born granule neurons are involved in the regulation of mitral cell activity; that is, adult-born young neurons incorporated into the neuronal circuit of the OB enhance odor-induced responses of mitral cells, improving their power to discriminate between odors [99]. This effect is diminished as adult-born neurons become mature.
However, people's knowledge about the function of adult-born granule cells of the OB is far from complete. It has become obvious that there are two different populations of granule cells in the OB. One population of granule neurons of the OB is generated during the embryonic development of mice, while a second population of granule neurons, consisting of the majority, is generated in postnatal life [100]. Data related to the function of these neuron populations are controversial. On the one hand, Sakamoto et al. [100] have revealed that inhibition or activation of interneurons activity in the adult OB of genetically-manipulated mice does not affect behavioral tasks requiring olfactory perception. However, Takahashi et al. [95] have reported that granule cells derived from postnatal neurogenesis are required for odor detection. More recent research has demonstrated that preexisting neurons are involved in complex learned discrimination only, whereas adult-born neurons are engaged in both simple and complex learned discrimination [101].
In humans, the presence of newborn neurons in the SVZ/OB remains controversial. First, Eriksson et al. [22] described the progenitor cells in the SVZ adjacent to the caudate nucleus in humans using BrdU. Furthermore, adult neurogenesis in the human SVZ has been examined by other markers [84][102]. The progenitor cells of the rostral subependymal layer (known as the SVZ) adjacent to the caudate nucleus were co-expressed with the polysialic acid form of neural cell adhesion molecule (PSA-NCAM, a marker for migrating cells) or class III β-tubulin or Hu proteins which are specific for neuroblasts/neurons [103]. Other markers, such as the proliferating cell nuclear antigen (PCNA, a cell cycle marker), Olig2, and DCX, a marker for migrating immature neurons, were also used to determine proliferating cells in the SVZ [104]. However, Sanai et al. [105] have demonstrated that newly proliferated cells in the SVZ and RMS are present only until 18 months of age, and they are absent in the adult human brain. In addition, cells expressing DCX and PSA-NCAM are not located in the OB, but they migrate to the striatum [88]. One of the mechanisms identified to regulate adult neurogenesis in the striatum of humans is Notch-signaling, which inhibits the generation of neurons [106]. Adult neurogenesis in the striatum of rodents (mice, rat, and rabbit) and monkeys has been reported, although its function is not well known.
In marsupials, as in laboratory rodents, adult neurogenesis persists in the SVZ, and the majority of neuroblasts migrate to reach the OB [1]. In the opossum Monodelphis domestica, adult neurogenesis appears to have typical properties. That is, the number of newly generated neurons can be regulated by pharmacological interventions or other factors, for example, aging, which is a physiological process. It has been shown that buspirone, a partial 5-HT1A receptor agonist provides an increase in proliferation, while aging reduces the proliferation of progenitor cells [1]. Furthermore, the olfactory discrimination test performed on opossums revealed that the performance in a behavioral test is associated with the number of adult-born neurons of the OB. Opossums with a low number of newborn neurons of the OB reached significantly worse results in the olfactory-guided behavioral test [107]. This paper suggests that in the opossum, newly generated neurons are integrated into existing circuits of the OB and are required for learning and memory of new odors.
Overall, the OB is known as one of few structures of the brain that displays neuroplasticity in both eutherians and marsupials.

3. Does Adult Neurogenesis Occur in the Piriform Cortex?

Information from the OB reaches directly via the lateral olfactory tract to the olfactory cortex. The main areas of the olfactory cortex are the anterior olfactory nucleus, olfactory tubercle, entorhinal cortex, and piriform cortex. The piriform cortex is the largest region among olfactory cortical areas. Apart from the OB input, the piriform cortex also receives afferents from the amygdala and orbitofrontal cortex [108]. Nacher et al. [109] demonstrated that some cells in the piriform cortex of adult mice express DCX, indicating the presence of immature neurons. These neurons become mature, as shown by BrdU and the NeuN double labeling method [50][79]. However, further papers have highlighted that DCX-expressing cells are generated during embryonic development of the piriform cortex and express DCX for a long period (2–3 months after birth) [109][110]. During embryonic development, DCX is expressed in progenitor cells and migrating neuronal-lineage cells, while in adult brains, transient expression of DCX is present in immature neurons. Once these cells become mature neurons, which takes 2–3 weeks, DCX expression disappears.
The time of origin of DCX-expressing cells has been studied in the piriform cortex of the young adult guinea pig following prenatal BrdU injections [110]. Prenatal neurogenesis has been shown to occur from E21 to E28 in the piriform cortex of the guinea pig. A number of newly generated BrdU-labeled cells were colocalized with DCX-expressing cells in the piriform cortex of the young guinea pig, indicating that immature neurons were present over 2 months. When DCX-expressing immature neurons of the piriform cortex mature, they structurally integrate into the existing neuronal network, serving as a source of plasticity. This shows that structures involved in olfaction, from the neuroepithelium through the OB and piriform cortex, are required to reorganize neuronal networks for proper olfaction function. Adult-born neurons of the OB or the piriform cortex neurons that express immature cell markers are appropriate candidates for establishing structural and functional synapses.
Our preliminary and unpublished data demonstrated that DCX-expressing cells were distributed in the piriform cortex of young, sexually immature male opossums. DCX-expressing cells disappeared from the piriform cortex cells in sexually mature male opossums (about 7 months of age). Based on these data, researchers hypothesized that DCX immature neurons in the piriform cortex might be involved in sexual development, contributing to the formation of stable neuronal connections during the sexual maturation period and promoting neuroplasticity at this stage of development.
Collectively, a large body of evidence suggests that immature neurons in the piriform cortex of young animals provide a specific form of plasticity. In particular, most of these cells remain immature for more than 2–3 months and, if necessary, they reorganize their phenotype, become mature, and incorporate into the preexisting neuronal network.

4. Adult-Born Neurons of the Dentate Gyrus (DG)

Anatomically, the hippocampal formation consists of the hippocampus proper, DG, subiculum, and entorhinal cortex [111]. The dentate gyrus (DG) is not included in the hippocampus proper, but the term “hippocampal adult neurogenesis” only refers to adult neurogenesis of the DG. Cells are proliferated in the hilus and subgranular layer of the DG. After proliferation, one-half of these newly proliferated cells die quickly [112]. Surviving neurons reach the granule cell layer of the DG and make the first synapses. The axons of newly generated granule neurons form synaptic connections with the CA3 pyramidal neurons. In this way, they integrate into the existing neural network and mature further [33][113][114]. It takes 8 weeks for newly generated neurons to fully mature [115].
Adult neurogenesis in the DG is conserved across mammals and declines with age in almost all investigated species (Table 1). In the DG of aged rodents, neurogenesis is still ongoing, albeit at a lower level. It has been shown that the number of adult-born neurons was considerably lower in the DG of middle-aged rats (12 months) compared to young animals [37]. In older rats (21 months), the number of adult-born neurons was reduced by 90% compared to juvenile rats. Interestingly, in some species of shrews, neurogenesis completely ceases in the DG of aged animals [11]. In the common shrew (Sorex araneus), the highest rate of hippocampal neurogenesis was observed 1 month after birth. The rate of neurogenesis increased in the following months of young animals and diminished at the age of 10-month-old shrews [11]. Amrein et al. found that adult hippocampal neurogenesis was absent in nine tropical bat species (Glossophaga soricina, Carollia perspicillata, Phyllostomus discolor, Nycteris macrotis, Nycteris thebaica, Hipposideros cyclops, Neoromicia rendalli, Pipistrellus guineensis, and Scotophilus leucogaster) throughout life [65].
In humans, newly generated cells have been first reported in the DG of old individuals (57 to 72 years) [22]. Further papers have confirmed these data, reporting that adult neurogenesis persists in the human DG from birth to old age, even in a centenarian [116]. On the other hand, several papers have demonstrated very low numbers of adult-born neurons in the DG of individuals whose ages ranged from 7 to 77 years [82]. Accordingly, the concept of adult neurogenesis in the DG of humans has been questioned, and this has sparked a debate [83][117][118][119].
A decrease in the rate of hippocampal neurogenesis has also been demonstrated in two aged marsupial species, the fat tail dunnart and Monodelphis opossum, which have been examined so far [1][2].
Despite many studies, the role of neurogenesis in the adult mammalian brain has not yet been fully elucidated. According to some research, the presence of a new pool of neurons may play an important role in hippocampal-dependent memory function, in particular, in spatial memory [120][121][122]. In laboratory rodents, spatial hippocampal memory has been widely studied using behavioral tests, particularly the water maze test (for review, see [123]). Mice with enhanced adult neurogenesis localized the hidden platform in less time than control mice in the water maze test [124][125], while mice with reduced neurogenesis had impaired learning and memory functions [126]. Further research has demonstrated that learning effects on the development of newborn neurons’ dendritic tree [127], indicating that adult neurogenesis maintains hippocampal plasticity. However, there are many papers that did not find any correlation between the number of newborn neurons in the DG and learning and memory function [128][129][130].
The paper by Tepper et al. highlighted behavior and adult neurogenesis in young opossums at the age of 6 months and aged opossums at the age of 21 months [131]. The number of newly generated cells in the DG of young opossums was almost 3.5 times more than aged opossums. Since aging is a dynamic process that takes place over time, the number of newborn neurons in the DG of opossums declines individually depending on the stage of aging. There was a 2.5-fold difference in the number of DCX-labeled cells in the DG among 21-month-old opossums. In addition, the study indicates a correlation between the number of DCX-expressing neurons and behavior. Aged opossums with high numbers of DCX cells made fewer errors, achieving high performance levels in the water maze task.
In summary, adult hippocampal neurogenesis is a common feature of mammals that exists across mammals and declines with age in almost all investigated species, including marsupials. The water maze test makes it possible to study learning and memory function in marsupials. There is only one work in marsupials indicating that adult-born neurons contribute to learning and memory. Further research is needed to understand the role of adult neurogenesis in marsupials.

This entry is adapted from the peer-reviewed paper 10.3390/cells11172735

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