Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus

Jabès, Adeline; Lavenex, Pamela Banta; Amaral, David G.; Lavenex, Pierre

doi:10.1111/j.1460-9568.2009.07061.x

Cited by 114 publications

(147 citation statements)

References 67 publications

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“…Interestingly, however, whereas the hippocampus is not activated during such context conditioning in 21-day-old rats, it is activated in 24-dayolds (Raineki et al, 2010). The emergence of contextual conditioning is thus likely related to the maturation of both the hippocampus, which also exhibits a delayed developmental profile (Bekenstein and Lothman, 1991;Jabès et al, 2010Jabès et al, , 2011Nurse and Lacaille, 1999;Swann et al, 1990), and the basolateral complex of the amygdala, which likely is insufficiently mature to integrate such contextual information until the beginning of the third week of life.…”

Section: Functional Considerationsmentioning

confidence: 99%

Postnatal development of the amygdala: A stereological study in rats

Chareyron

Lavenex

2012

J of Comparative Neurology

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The amygdala is the central component of a functional brain system regulating fear and emotional behaviors. Studies of the ontogeny of fear behaviors reveal the emergence of distinct fear responses at different postnatal ages. Here, we performed a stereological analysis of the rat amygdala to characterize the cellular changes underlying its normal structural development. Distinct amygdala nuclei exhibited different patterns of postnatal development, which were largely similar to those we have previously shown in monkeys. The combined volume of the lateral, basal, and accessory basal nuclei increased by 113% from 1 to 3 weeks of age and by an additional 33% by 7 months of age. The volume of the central nucleus increased only 37% from 1 to 2 weeks of age and 38% from 2 weeks to 7 months. At 1 week of age, the medial nucleus was 77% of the 7-monthold's volume and exhibited a constant, marginal increase until 7 months. Neuron number did not differ in the amygdala from 1 week to 7 months of age. In contrast, astrocyte number decreased from 3 weeks to 2 months of age in the whole amygdala. Oligodendrocyte number increased in all amygdala nuclei from 3 weeks to 7 months of age. Our findings revealed that distinct amygdala nuclei exhibit different developmental profiles and that the rat amygdala is not fully mature for an extended period postnatally. We identified different periods of postnatal development of distinct amygdala nuclei and cellular components, which are concomitant with the ontogeny of different fear and emotional behaviors.

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Section: Functional Considerationsmentioning

confidence: 99%

Postnatal development of the amygdala: A stereological study in rats

Chareyron

Lavenex

2012

J of Comparative Neurology

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“…Recent work in our laboratory has shown that the monkey dentate gyrus, in which nearly 40% of the neurons found in the adult are generated postnatally (Jabès, Banta Lavenex, Amaral, & Lavenex, 2010), exhibits a late and protracted development, and has not yet reached an adult volume at one year of age (which corresponds to approximately 4 years of age in humans). This lead us to hypothesize that the improvement in allocentric spatial memory capacities with age might result from the gradual functional maturation of the dentate gyrus and trisynaptic hippocampal pathway, which contribute to improved spatial pattern separation abilities from 2 to 6 years of life in humans.…”

Section: Improved Allocentric Spatial Processing After 2 Years Of Agementioning

confidence: 99%

“…The encoding of autobiographical memories, by definition, requires rapid, single-trial contextual learning. We therefore propose that it is the immaturity of the dentate gyrus (Jabès et al, 2010(Jabès et al, , 2011 that underlies the phenomenon of childhood amnesia, and the gradual maturation of the trisynaptic hippocampal pathway subserves the gradual improvement, from 2 to 7 years of age, in our ability to create autobiographical memories that can be recalled later in life.…”

Section: The Emergence Of Autobiographical Memory In 2-year-old Childrenmentioning

confidence: 99%

Development of allocentric spatial memory abilities in children from 18 months to 5 years of age

Ribordy¹,

Jabès²,

Lavenex³

et al. 2013

Cognitive Psychology

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Episodic memories for autobiographical events that happen in unique spatiotemporal contexts are central to defining who we are. Yet, before 2 years of age, children are unable to form or store episodic memories for recall later in life, a phenomenon known as infantile amnesia. Here, we studied the development of allocentric spatial memory, a fundamental component of episodic memory, in two versions of a real-world memory task requiring 18 month-to 5-year-old children to search for rewards hidden beneath cups distributed in an open-field arena. Whereas children 25-42-months-old were not capable of discriminating three reward locations among 18 possible locations in absence of local cues marking these locations, children older than 43 months found the reward locations reliably. These results support previous findings suggesting that allocentric spatial memory, if present, is only rudimentary in children under 3.5 years of age. However, when tested with only one reward location among four possible locations, children 25-39-months-old found the reward reliably in absence of local cues, whereas 18-23-month-olds did not. Our findings thus show that the ability to form a basic allocentric representation of the environment is present by 2 years of age, and its emergence coincides temporally with the offset of infantile amnesia. However, the ability of children to distinguish and remember closely related spatial locations improves from 2 to 3.5 years of age, a developmental period marked by persistent deficits in long-term episodic E-mail address: pierre.lavenex@unifr.ch (P. Lavenex).memory known as childhood amnesia. These findings support the hypothesis that the differential maturation of distinct hippocampal circuits contributes to the emergence of specific memory processes during early childhood.

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“…For example, nestin marks stem cells (Lendahl et al, 1990) and is expressed in both type 1 (GFAP + ) and type 2 (GFAP -) progenitor cells in the SGZ (Ming and Song, 2011). Ki-67 (also known as MKI67) specifically labels proliferating cells over the whole cell cycle from G1 to M phases (Jabès et al, 2010). CD24 marks differentiating post-mitotic neurons (Calaora et al, 1996), whereas doublecortin (Dcx) (Brown et al, 2003) and Sox11 (Mu et al, 2012) show high expression in proliferating progenitor cells and newly generated neuroblasts but have sharply decreased expression as neurons mature.…”

Section: Introductionmentioning

confidence: 99%

Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates

et al. 2013

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The neurogenic potential of the subgranular zone (SGZ) of the hippocampal dentate gyrus is likely to be regulated by molecular cues arising from its complex heterogeneous cellular environment. Through transcriptome analysis using laser microdissection coupled with DNA microarrays, in combination with analysis of genome-wide in situ hybridization data, we identified 363 genes selectively enriched in adult mouse SGZ. These genes reflect expression in the different constituent cell types, including progenitor and dividing cells, immature granule cells, astrocytes, oligodendrocytes and GABAergic interneurons. Similar transcriptional profiling in the rhesus monkey dentate gyrus across postnatal development identified a highly overlapping set of SGZ-enriched genes, which can be divided based on temporal profiles to reflect maturation of glia versus granule neurons. Furthermore, we identified a neurogenesis-related gene network with decreasing postnatal expression that is highly correlated with the declining number of proliferating cells in dentate gyrus over postnatal development. Many of the genes in this network showed similar postnatal downregulation in mouse, suggesting a conservation of molecular mechanisms underlying developmental and adult neurogenesis in rodents and primates. Conditional deletion of Sox4 and Sox11, encoding two neurogenesis-related transcription factors central in this network, produces a mouse with no hippocampus, confirming the crucial role for these genes in regulating hippocampal neurogenesis.

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Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus

Cited by 114 publications

References 67 publications

Postnatal development of the amygdala: A stereological study in rats

Postnatal development of the amygdala: A stereological study in rats

Development of allocentric spatial memory abilities in children from 18 months to 5 years of age

Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates

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