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Front. Biol.    2016, Vol. 11 Issue (3) : 193-213    https://doi.org/10.1007/s11515-016-1403-5
REVIEW
Distribution and fate of DCX/PSA-NCAM expressing cells in the adult mammalian cortex: A local reservoir for adult cortical neuroplasticity?
Richard König1,2,Bruno Benedetti3,Peter Rotheneichner1,4,Anna O′ Sullivan1,4,5,Christina Kreutzer1,4,Maria Belles6,Juan Nacher6,Thomas M. Weiger7,Ludwig Aigner1,2,*(),Sébastien Couillard-Després1,4,*()
1. Spinal Cord Injury and Tissue Regeneration Center Salzburg (SCI-TReCS), Paracelsus Medical University, Salzburg, Austria
2. Institute of Molecular Regenerative Medicine, Paracelsus Medical University, Salzburg, Austria
3. Department of Physiology and Medical Physics, Innsbruck Medical University, Innsbruck, Austria
4. Institute of Experimental Neuroregeneration, Paracelsus Medical University, Salzburg, Austria
5. Department of Otorhinolaryngology, Head and Neck Surgery, Paracelsus Medical University Salzburg, Salzburg, Austria
6. Neurobiology Unit, Interdisciplinary Research Structure for Biotechnology and Biomedicine Valencia, Universitat de Valencia, Comunitat Valenciana, Spain
7. Division of Cellular and Molecular Neurobiology, Department of Cell Biology, University of Salzburg, Salzburg, Austria
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Abstract

The expression of early developmental markers such as doublecortin (DCX) and the polysialylated-neural cell adhesion molecule (PSA-NCAM) has been used to identify immature neurons within canonical neurogenic niches. Additionally, DCX/PSA-NCAM+ immature neurons reside in cortical layer II of the paleocortex and in the paleo- and entorhinal cortex of mice and rats, respectively. These cells are also found in the neocortex of guinea pigs, rabbits, some afrotherian mammals, cats, dogs, non-human primates, and humans. The population of cortical DCX/PSA-NCAM+ immature neurons is generated prenatally as conclusively demonstrated in mice, rats, and guinea pigs. Thus, the majority of these cells do not appear to be the product of adult proliferative events. The immature neurons in cortical layer II are most abundant in the cortices of young individuals, while very few DCX/PSA-NCAM+ cortical neurons can be detected in aged mammals. Maturation of DCX/PSA-NCAM+ cells into glutamatergic and GABAergic neurons has been proposed as an explanation for the age-dependent reduction in their population over time. In this review, we compile the recent information regarding the age-related decrease in the number of cortical DCX/PSA-NCAM+ neurons. We compare the distribution and fates of DCX/PSA-NCAM+ neurons among mammalian species and speculate their impact on cognitive function. To respond to the diversity of adult neurogenesis research produced over the last number of decades, we close this review by discussing the use and precision of the term “adult non-canonical neurogenesis.”
Keywords aging      cognition      doublecortin      piriform cortex      plasticity      neurogenesis     
Corresponding Author(s): Ludwig Aigner,Sébastien Couillard-Després   
Just Accepted Date: 01 June 2016   Online First Date: 21 June 2016    Issue Date: 05 July 2016
 Cite this article:   
Richard König,Bruno Benedetti,Peter Rotheneichner, et al. Distribution and fate of DCX/PSA-NCAM expressing cells in the adult mammalian cortex: A local reservoir for adult cortical neuroplasticity?[J]. Front. Biol., 2016, 11(3): 193-213.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-016-1403-5
https://academic.hep.com.cn/fib/EN/Y2016/V11/I3/193
Fig.1  Schematic representation of the proliferative neurogenic sites within the adult mouse brain. Adult-born neurons generated in the subventricular zone migrate dorsally to the olfactory bulb to mature and integrate as inhibitory neurons. In the dentate gyrus, newly born neuroblasts differentiate locally into granular cells. In light blue presumptive regions supporting low-level adult neurogenesis are marked (reviewed in: (Gould, 2007)), defined as regions were proliferation markers co-occur in immunohistologically labelled neurons. The piriform cortex, which is part of the paleocortex, is highlighted in green.
Fig.2  In the young adult mouse brain, immature neurons are most abundant in the canonical neurogenic niches and within paleocortical regions. Transgenic DCX-CreERT2 mouse line allowed for the detection of DCX/PSA-NCAM IN. In this picture, immature neurons expressing the transgene under the DCX promoter are visualized by 3,3'-Diaminobenzidine (DAB) staining. The amount of DAB positive cells is the highest within the dentate gyrus (DG), the lateral ventricular (LV) wall, and the posterior part of the piriform cortex layer II. In the piriform cortex most DAB positive cells are accumulated in the posterior part, extending into the amygdaloidal transitional area (CxA), and the ventral claustrum (VEn). It was demonstrated that most immature neurons in the layer II of the murine piriform cortex do express PSA-NCAM (Rubio et al., 2015). In contrast, the evenly distributed DAB positive cells present throughout all cortical regions, co-express the NG2 antigen, but mostly lack PSA-NCAM expression (own observation). Abbreviations: agranular insular cortex dorsal part (AID), agranular insular corte, ventral part (AIV), basolateral amygdaloid nucleus anterior part (BLA), basolateral amygdaloid nucleus posterior part (BLP), basomedial amygdaloid nucleus anterior part (BMA), basomedial amygdaloid nucleus posterior part (BMP), field cornu ammonis (CA) 1 of the hippocampus (CA1), field CA2 of the hippocampus (CA2), field CA3 of the hippocampus (CA3), corpus callosum (cc), caudomedial entorhinal cortex (CEnt), claustrum (Cl), caudate putamen (CPu), crus 1 of the ansiform lobule (Crus1), crus 2 of the ansiform lobule (Crus2), cortex-amygdala transition zone (CxA), dorsal endopiriform claustrum (DEn), dysgranular insular cortex (DI), dorsolateral entorhinal cortex (DLEnt), dorsal subiculum (DS), fimbria of the hippocampus (fi), flocculus (Fl), granular insular cortex (GI), dentate gyrus (DG), globus pallidus (GP), internal capsule (ic), lateral ventricle (LV), paraflocculus (PFl), posterolateral cortical amygdaloid area (PLCo), paramedian lobule (PM), posteriormedial cortical amygdaloid area (PMCo), presubiculum (PrS), parietal cortex, posterior area dorsalis (PtPD), parietal cortex, posterior area rostralis (PtPR), rhinal fissure (rf), primary somatosensory cortex (S1), primary somatosensory cortex, barrel field (S1BF), primary somatosensory cortex, jaw region (S1J), primary somatosensory cortex, upper lip region (S1ULp), simple lobule (Sim), primary visual cortex (V1), ventral endopiriform claustrum (VEn), ventral subiculum (VS); (Paxinos and Franklin, 2012).
Fig.3  Schematic cytoarchitecture of the piriform cortex. (a) GFP/DCX positive cell in the piriform cortex of a mouse stained for PSA-NCAM (yellow). Most of these cells show small soma size and lack synaptic input. (b) Transgenic DCX-CreERT2 mouse line allowed for the detection of DCX/PSA-NCAM IN which predominantly resided in the layer IIa of the mouse piriform cortex. This mouse model enables fate mapping of DCX expressing cells (Zhang et al., 2010). (c) SL and SP have their somata concentrated in layers IIa and IIb, respectively. DP and MS are found at lower density in layer II. (d) GABA-releasing interneurons are distributed more sparsely and uniformly, but are less abundant in layer II. (e) Detection of the cell layer of the piriform cortex by DAPI (blue) staining. Main (f) output and (g) input regions of the piriform cortex. Abbreviations: superficial pyramidal cells (SP), semilunar cells (SL), multipolar spiny cells (MS), deep pyramidal cells (DP), bitufted cells (BT), fast spiking cells (FS), chandelier cells (CH), regular-spiking cells (RS), neuroglial-like cells (NL), lateral olfactory tract (LOT); nomenclature following (Bekkers and Suzuki, 2013).
Mammal Location Expected fate Are-related reduction? Overlap with fate-specific or mature neural markers? Prenatal birth dating? Antigens Proliferationin the adult? Morphologies Reference
Mouse Piriform cortex (posterior) Glutamatergic n.a. DCX expression overlapped with Tbr1. No co-expression with interneuronal markers n.a. Ki67; TUJ1;NeuN; DCX; PSA-NCAM; Parvalbumin; Somatostatin; Calbindin; GABA); GAD67; pan DLL; Lhx6; Tbr1; BrdU No adult DNA synthesis DCX/PSA-NCAM:Type 1 cells: bipolar and relatively smallType 2 cells: larger cell bodies; wide and well-developed dendritic arborisation; referred as “extraverted neurons” (Nieuwenhuys, 1994; Sanides and Sanides, 1972) Luzzati et al., 2009
Piriform cortex n.a. Reduction of DCX-DsRed cell number following bulbectomy DCX-DsRed expression overlapped with NeuN n.a. BrdU; DCX; PSA-NCAM; NeuN; Iba-1;Transgenic mice expressing red fluorescent protein (DsRed) under the control of the DCX promoter [C57BL/6J-Tg(DCX-DsRed)14Qlu/J n.a.in transgenic mice n.a. Rossi et al., 2014
Piriform cortex Glutamatergic n.a. PSA-NCAM expression overlapped with Tbr1 (77.7%). No co-expression with interneuronal markers Mainly in E13.5-E14.5 BrdU; DCX; GAD67); GFAP; Ki67; NeuN; NG2; PSA-NCAM; RIP; Tbr1 Prenatal DNA-synthesis, and no adult DNA synthesis DCX/PSA-NCAM:Small cells (6.21µm) – “Tangled Cells”Larger cells (9.64µm) – “semilunar-pyramidal transitional neurons”10% of all cells in layer II of the piriform cortex did express PSA-NCAM Rubio et al., 2015
Rat Piriform cortex and entorhinal cortex(perirhinal cortex, agranular insular, ectorhinal cortices) n.a.(Suggested by the authors: Glutamatergic fate) n.a. PSA-NCAM expression in larger cells overlapped with faint NeuN expression, and the expression of the NR1 subunit of the NMDA receptor. No co-expression with interneuronal markers Mainly in E15.5 Alpha-actinin, Arc, GABA, BrdU, CaMKII, Calbindin, Calretinin, c-Fos, Cholecytstokinin; CNGA-3, DCX, GFAP, Glucocorticoid receptor, GAD-67, MAP2, NG2, Nestin, NeuN, Neuropeptide Y; NMDA receptor 1; Parvalbumin; Pax6; Phospho-CREB, RIP; PSA-NCAM; Somatostatin; TUC-4; Vasoactive intestinal peptide Prenatal DNA-synthesis, and no adult or perinatal DNA synthesis DCX/PSA-NCAM:Small cells (soma diameter 8.9µm) – “Tangled Cells”Small cells mostly co-expressed DCX, TUC-4, CNGA-3, which is strongly expressed by migrating neuroblasts of the rostral migratory stream (Guiterrez-Mecinas et al., 2007), and p-CREB, a molecule expressed transiently in differentiating granule neurons the adult hippocampus (Nakagawa et al., 2002)Larger cells (14.8µm) – “semilunar-pyramidal transitional neurons” Gomez-Climent et al., 2008
Piriform cortex (DCX staining mostly present in the part of the piriform cortex) Scarce DCX expressing cells in the neocortex Glutamatergic n.a. DCX expression overlapped with Tbr1. No co-expression with interneuronal markers n.a. Ki67; TUJ1;NeuN; DCX; PSA-NCAM; Parvalbumin; Somatostatin; Calbindin; GABA); GAD67; pan DLL; Lhx6; Tbr1; BrdU No adult DNA synthesis DCX/PSA-NCAM:Type 1 cells: bipolar and relatively smallType 2 cells: larger cell bodies; wide and well-developed dendritic arborisation; referred as “extraverted neurons” (Nieuwenhuys, 1994; Sanides and Sanides, 1972) Luzzati et al., 2009
Piriform cortex n.a. n.a. BrdU overlapped with NeuN, but no BrdU/NeuN positive cells 12 weeks after BrdU administration n.a. BrdU; NeuN; PSA-NCAM; DCX; TUC-4 Adult-born NeuN expressing cells that do not survive Pyramidal morphology of BrdU/NeuN positive cells in layer II Pekcec et al., 2006
Allocortex, medial prefontal cortex, and (Amygdala) n.a.(Suggested by the authors: Glutamatergic fate) Age related reduction of “s cells” (small PSA-NCAM expressing cells) but not of “L cells” n.a. n.a. PSA-NCAM n.a. PSA-NCAM:Smaller PSA-NCAM expressing cells (“s cells”) were found only in the dentate gyrus, and only in the layer II of the piriform, entorhinal, perirhinal and insular cortices. “L cells” with comparatively larger soma, found in the hippocampus, the entorhinal and piriform cortices, and in all the extension of the neocortex and in different amygdaloid nucleus. The L cells were not present within the layer II of the piriform cortex. Number of “L cells” did not decrease dramatically in adulthood. Varea et al., 2009
Afrotherian mammals (hottentot golden mole, rock hyrax, eastern rock sengi, four toed sengi) Allocortex andneocortex n.a. n.a. n.a. n.a. DCX; Ki-67 No Ki67 immunoreactivity of DCX expressing cells in cortical layer II DCX:Mostly bipolar or multi-polar in shape, occasionally unipolar DCX expressing cells in cortical layer II Patzke et al., 2014
Guinea Pig Allocortex and neocortex with a dorsal to ventral high to low gradient;(Amygdala) n.a. n.a. n.a. E21-28 in the piriform cortex, E35 in the neocortex DCX, BrdU Only scare DNA-synthesis in DCX expressing cortical layer II cells DCX:Comparable to Xiong et al., 2008 Yang et al., 2015
Paleocortex n.a. n.a. n.a. n.a. DCX, NeuN n.a. He et al., 2014
Allocortex and neocortex GABAergic From 3 month to 3 years of age DCX+ cell number decreased about 50% for all observed areas (piriform, entorhinal, temporal, and parietal cortex) DCX/PSA-NCAM/TuJ1 in small cellsDCX/NeuN in large cells; subpopulation of DCX+ cells showed weak to moderate GABA labelling; large cells with faint DCX expression showed robust GAD67, GAD65/67; some larger DCX+ cells co-expressed NADPH-D or NOS n.a. DCX; PSA-NCAM; beta tubulin III; NeuN; GFAP; Reelin; GABA; GAD67; GAD 65/67; Calbindin; Calretinin; Neurogranin; Nitric oxidase); TuJ n.a. DCX:Small DCX expressing cells:(5µm soma diameter) with no/one/two processes that extended from one or opposite poles of the somata (most abundant DCX+ cell type)Medium-sized DCX expressing cells:(5-10µm) displayed moderate to heavy DCX reactivity and 2-4 processes radiating from the somataLarge-sized DCX expressing cells: (10-20µm in soma diameter) had branched dendrite-like processes for several hundred micrometres Xiong et al., 2008
Piriform cortex, neocortex, amigdalo-pyriform transition area(Amygdala) Glutamatergic n.a. DCX expression overlapped with Tbr1. No co-expression with interneuronal markers n.a. Ki67; TUJ1;NeuN; DCX; PSA-NCAM; Parvalbumin; Somatostatin; Calbindin; GABA); GAD67; pan DLL; Lhx6; Tbr1; BrdU No adult DNA synthesis DCX/PSA-NCAM:Type 1 cells: bipolar and relatively smallType 2 cells: larger cell bodies; wide and well-developed dendritic arborisation; referred as “extraverted neurons” (Nieuwenhuys, 1994; Sanides and Sanides, 1972) Luzzati et al., 2009
Rabbit Piriform cortex, neocortex, amygdalo-piriform transition area(Amygdala) Glutamatergic n.a. DCX expression overlapped with Tbr1. No co-expression with interneuronal markers n.a. Ki67; TUJ1;NeuN; DCX; PSA-NCAM; Parvalbumin; Somatostatin; Calbindin; GABA); GAD67; pan DLL; Lhx6; Tbr1; BrdU No adult DNA synthesis DCX/PSA-NCAM:Type 1 cells: bipolar and relatively smallType 2 cells: larger cell bodies; wide and well-developed dendritic arborisation; referred as “extraverted neurons” (Nieuwenhuys, 1994; Sanides and Sanides, 1972) Luzzati et al., 2009
Cat Allocortex and neocortex; ventrodorsal high to low gradient Glutamatergic n.a. PSA-NCAM expression overlapped with Tbr1 in small cells. No co-expression with interneuronal markers n.a. PSA-NCAM; NeuN; GAD67; DCX; CNGA3; CaMKII; Tbr1; Calbindin; Calretinin; Parvalbumin; Cholecystokinin; Vasoactive Intestinal Peptide; Neuropeptide Y; Somatostatin; Nitric Oxide Synthase Neural No adult DNA synthesis PSA-NCAM:“S” cells (small) PSA-NCAM/DCX/TBR1/CNGA3 (12 µm soma size), present in layer II of various cortices“L” cells (large) PSA-NCAM/NeuN(Gad67/CB/CR) (21 µm soma size), not present within the layer II Varea et al., 2011
Allocortex and neocortex; ventrodorsal high to low gradient GABAergic E.g. entorhinal cortex: Are-related reduction in cell number of about 60% (young=1.5 years; old=4.5 years) In small cells of the layer II: DCX is coexpressed with PSA-NCAM and TuJ1; In larger cells: DCX is co-expressed with NeuN, and different interneuron markers n.a. DCX; PSA-NCAM; Tuj-1); NeuN; GFAP; Oligodendrocyte Protein; OX42; Neurogranin; GABA; GAD67; Calbindin; Parvalbumin; Calretinin; Somatostatin; nNOS n.a. DCX:Heterogenic population, ranging from small DCX expressing cells (5µm) up to larger cells (20µm) Cai et al., 2009
Dog Paleocortex, neocortex (mostly frontal), (and cerebellum) n.a. Age-related reduction (from 3 month to 5 year and 17 year old lupines) in DCX expressing cell number in the layer II of the frontal neocortex, paleocortex and piriform lobe. n.a. n.a. DCX; Nucleostemin; tubulin beta III; NeuN; GFAP n.a. DCX:Irregular cells having a small cellular body and short extensions, but with more mature morphologies in neocortical layer II De Nevi et al., 2013
Hesus monkey Neocortex, entorhinal cortex, (and amygdala)ventrodorsal high to low gradient;only occasionally detected DCX expressing cells in primary motor and sensory cortical areas GABAergic Age-related reduction (from 12 to 21 and 31 years): 32%, and 13% Partial co-localisation of DCX/NeuN, DCX/GABA, and DCX/TH n.a. DCX; PSA-NCAM; NeuN; GABA; TyrosinHydroxilase (TH) n.a. Most DCX expressing cells were small and bipolar, often arranged in clusters (like observed within all species investigated so far (Gomez-Climent et al., 2008; Marti-Mengual et al., 2013; Nacher et al., 2001; Varea et al., 2011); complete co-localization of DCX with PSA-NCAMA few relatively large cells with reduced DCX reactivity were present in layer II/III in temporal lobe cortical areas Zhang et al., 2009
Allocortex and neocortex; ventrodorsal high to low gradient n.a.(Suggested by the authors: GABAergic fate) n.a. n.a. n.a. DCX n.a. DCX: Most DCX expressing cells in layer II/III were bipolar, while some appeared to be multipolar. Cai et al., 2009
Human n.a. Age-related reduction (from 1 year to 3.7, and 6 years of age) n.a. n.a. DCX, GAD65/67; PSA-NCAM, NeuN Either DCX, or PSA-NCAMDCX: Small cells (8µm diameter) with mostly one/two long processes were present in layer II of the cortex in the principal sulcus, gyrus rectus and, most abundantly, around the inferior arcuate sulcus and lateral orbital sulcus. While these layer II DCX expressing cells were present in the neonatal rhesus macaque brain, and in the 1 month old brain, the density of these cells were reduced in 3.7 and 6 year old monkeys. PSA-NCAM:Heterogeneous population; co-expression of GAD65/67 in some cortical layers Srikandarajah et al., 2009
Entorhinal cortex (Hippocampus) n.a. n.a. (for the entorhinal cortex) n.a. n.a. PSA-NCAM n.a. In the hippocampal formation,immunoreactivity was occasionally observed as a band of cells in the entorhinal cortex, in 7 month old humans. Ni Dhuill et al., 1999
Neocortex (temporal and frontal lopes) n.a.(Suggested by the authors: GABAergic fate) n.a. n.a. n.a. DCX n.a. DCX: DCX expressing cells varied in soma size, shape, staining intensity and neuritic appearance. Anyhow, many small cells showed small bipolar and a few multipolar cells exhibiting heavy reactivity Medium-sized cells with weak to moderate DCX reactivity Cai et al., 2009
Neocortex (undifferentiated) n.a. n.a. n.a. n.a. BrdU (mouse igG, M0744); DCX (rabbit IgG, ab18723; goat IgG, Sc-8066; guinea pig IgG, AB2253; guinea pig IgG, AB5910); GFAP (mouse IgG1, G3893; chicken IgY, AB5541; rabbit IgG, Z0334); Nestin (rabbit IgG, AB5922; mouse IgG1, MAB377); vimentin (IgG1, M0725); NeuN, Iba-1; n.a. DCX:DCX was found in the cerebral cortex, highly localized at the glia limitans, layer II and layer V (non-human primate, and humans); 4.55+/− 1.58% of total cells expressed DCX in the neocortex in nonhuman primates; DCX-positive cells with long processes were observed in the glia limitans and in the layer I;DCX-positive cells with pyramidal cell bodies were stained in layer II;DCX-positive cells with small stellar morphology were located at the limit between GM and WMSmall cells, negative for Nestin, NeuN, GFAP, Iba-1, and vimentin, represented about 18% of the total DCX-positive cells in the cortex. Larger DCX-positive cells were either described to express NeuN (26%), with the shape of Cajal-Retzius cells, or to express GFAP (26%), or are positive or DCX/NeuN/GFAP (30%).DCX-positive cells in adult brain cell cultures from human brain biopsies:In-vitro 9.8% of cortical cells in-cooperated BrdU at day 35, and nearly all of the BrdU-positive cells expressed DCX/GFAP. Bloch et al., 2011
Tab.1  An overview of the various reports on cortical layer II immature neurons
Fig.4  Box 1Do different fates and distributions of DCX/PSA-NCAM IN reflect phylogenetic adaptations and are therefore species-specific? The fate of DCX/PSA-NCAM IN is not resolved yet, current reports are inconsistent. Species-specific variation in fate and distribution of DCX/PSA-NCAM IN may reflect phylogenetic differences in corticogenesis and/or cortical network physiology. The distribution of DCX/PSA-NCAM IN (green) and the locations of the canonical neurogenic niches (red) are schematically shown in different mammalian species. The order of the illustrated species reflects absolute cortical volume, but not the taxonomy of the listed mammals. While DCX/PSA-NCAM IN in mammals with relatively smaller cortices are mostly limited to allocortical regions, the numbers of DCX/PSA-NCAM IN and the number of regions bearing these cells in mammals with comparatively bigger cerebrums are higher. Since about 10% of all the cells in the layer II of the posterior piriform cortex in young adult mice are described as PSA-NCAM expressing cells with immature morphology (Rubio et al., 2015), it is suggested that the overall number of DCX/PSA-NCAM IN in mammals with large neocortical lobes is scaling proportional with bigger cortices and therefore the functional relevance of DCX/PSA-NCAM IN upon maturation is expected to be higher for large-brained species. Despite maturation, it is unresolved whether DCX/PSA-NCAM IN develop into GABAergic neurons in some species and glutamatergic neurons in others, or if both fates are covered in some species. We can speculate that these variances reflect species-specific assignments of DCX/PSA-NCAM IN. Alternatively, different types of neurons hypothetically originate from DCX/PSA-NCAM IN in mammals with large cerebrum, as opposed to those with small cerebrums. Nevertheless, it is also possible that the reported discrepancy in the fate of these cortical progenitors is a matter of unstandardized fixation, staining, counting, and fate-mapping methods.
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