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. 2020 Apr 7;8:211. doi: 10.3389/fcell.2020.00211

TABLE 1.

Proliferative activation of stem and progenitor cells of the adult and aged dentate gyrus by different neurogenic stimuli.

System (dentate gyrus) Neurogenic stimulus Activation of stem cells (type-1; BrdU+ GFAP+ nestin+ Sox2+) Activation of progenitor cells (type-2-3) Cognitive effects References
Adult Running NO YES Rescue of contextual memory Suh et al., 2007; Farioli-Vecchioli et al., 2014; Kronenberg et al., 2003; Steiner et al., 2008; Brandt et al., 2010;
Running YES (Hes5+) Lugert et al., 2010
Fluoxetine NO YES (and increased neuron survival) Encinas et al., 2006; Micheli et al., 2017, 2018a;
Fluoxetine (after global ischemia) YES YES Couillard-Despres et al., 2009; Khodanovich et al., 2018
Learning (enriched environment) NO NO (but increased survival of neurons) Improved spatial learning Kronenberg et al., 2003; Kempermann et al., 1997;
Learning (enriched environment preceded or not by hypoxia) YES YES (and increased number of neurons) Improved spatial learning Salmaso et al., 2012
Learning (spatial learning) YES (BrdU+) (but increased survival of neurons) Gould et al., 1999; Ambrogini et al., 2000; Döbrössy et al., 2003; Epp et al., 2007
Nutrient: Hydroxytyrosol NO* NO (but increased survival of new neurons) D’Andrea et al., 2020
Nutrient: Luteolin (in mouse model of Down syndrome and Alzheimer disease Ts65Dn) YES*** YES Improved spatial learning and object recognition Zhou et al., 2019
Nutrient: Caffeoylquinic acid (in senescence-accelerated prone 8 mouse [SAMP8]) YES – (increased generation of new neurons BrdU+NeuN+) Improved spatial memory Sasaki et al., 2019
Nutrient: Astragaloside VI (after ischemia) YES Rescue of spatial memory Chen et al., 2019
Nutrient: n-3 PUFA YES Improved spatial memory Cutuli et al., 2014
Electromagnetic fields YES YES Improved spatial learning Leone et al., 2014
Adult (after corticosterone-induced depression-like state) Running YES Rescue of spatial memory Yau et al., 2012
Aged Nutrient: Hydroxytyrosol YES** YES (and increased survival of neurons) D’Andrea et al., 2020
Running NO YES Rescue of place recognition memory Siette et al., 2013; Micheli et al., 2019
Fluoxetine NO NO (and no increase of neuron survival) No rescue of visuospatial deficit; enhancement of contextual memory and spine density Micheli et al., 2018a; Couillard-Despres et al., 2009; Li et al., 2015; McAvoy et al., 2015
Learning (enriched environment) NO (increased survival of neurons) No improved spatial learning Kempermann et al., 1998

*Ki67+Sox2+GFAP+ **Ki67+Sox2+ (Type-1-2a) ***Nestin+ (Type-1-2ab) or GFAP+.