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Review
. 2024 Apr;29(4):982-991.
doi: 10.1038/s41380-023-02386-4. Epub 2024 Jan 4.

Astrocytes in the adult dentate gyrus-balance between adult and developmental tasks

Nicholas Chalmers  1 , Evangelia Masouti  1 , Ruth Beckervordersandforth  2
Affiliations
Review

Astrocytes in the adult dentate gyrus-balance between adult and developmental tasks

Nicholas Chalmers et al. Mol Psychiatry. 2024 Apr.

Abstract

Astrocytes, a major glial cell type in the brain, are indispensable for the integration, maintenance and survival of neurons during development and adulthood. Both life phases make specific demands on the molecular and physiological properties of astrocytes, and most research projects traditionally focus on either developmental or adult astrocyte functions. In most brain regions, the generation of brain cells and the establishment of neural circuits ends with postnatal development. However, few neurogenic niches exist in the adult brain in which new neurons and glial cells are produced lifelong, and the integration of new cells into functional circuits represent a very special form of plasticity. Consequently, in the neurogenic niche, the astrocytes must be equipped to execute both mature and developmental tasks in order to integrate newborn neurons into the circuit and yet maintain overall homeostasis without affecting the preexisting neurons. In this review, we focus on astrocytes of the hippocampal dentate gyrus (DG), and discuss specific features of the astrocytic compartment that may allow the execution of both tasks. Firstly, astrocytes of the adult DG are molecularly, morphologically and functionally diverse, and the distinct astrocytes subtypes are characterized by their localization to DG layers. This spatial separation may lead to a functional specification of astrocytes subtypes according to the neuronal structures they are embedded in, hence a division of labor. Secondly, the astrocytic compartment is not static, but steadily increasing in numbers due to lifelong astrogenesis. Interestingly, astrogenesis can adapt to environmental and behavioral stimuli, revealing an unexpected astrocyte dynamic that allows the niche to adopt to changing demands. The diversity and dynamic of astrocytes in the adult DG implicate a vital contribution to hippocampal plasticity and represent an interesting model to uncover mechanisms how astrocytes simultaneously fulfill developmental and adult tasks.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Astrocyte subtypes in the adult DG are associated to distinct functional compartments.
A Confocal image of the adult DG (blue line) immunostained against SYNAPTOPORIN (magenta) illustrating the distinct layers (hilus, GZ granule zone, iML inner Molecular layer; m/oML medial and outer Molecular layer). B Astrocytes of the adult DG as revealed by GFAP immunostaining (white). C Schematic depicts the compartmentalization of the adult DG. Afferents from the entorhinal cortex form the medial and outer ML, while those from the contralateral DG form the inner ML. The neurogenic lineage (gray) consists of a neural stem cell (NSC) giving rise to actively proliferating intermediate precursor cells (IPCs), which generated neuroblasts (NBs). NBs subsequently mature to granule neurons. D–F Astrocytes reveal a subtype-specific morphology as determined by the expression of enhancedGFP (green) in brain slices of hGFAPeGFP transgenic animals (on the left). The eGFP signal was reconstructed in IMARIS (depicted on the right); different colors highlight branching order (dark blue=primary; light blue=secondary; turquoise=tertiary; green=quaternary; light green=quinary; yellow=septenary; orange=octonary; red = nonary). D Astrocytes of the upper DG compartments (ML and GZ) show a polarized morphology with one primary process emerging from the soma and fanning out into the ML with treetop-like branches. E Hilus astrocytes reveal a bushy morphology with several primary processes pointing in each direction. F SGZ astrocytes are smaller and stretch out one to two primary branches along the SGZ boarder. Scale bar = 100 μm (A, B) and 20 μm (D–F).
Fig. 2
Fig. 2. Ratios of neurogenesis and astrogenesis in the adult DG under different environmental condition and stimuli.
A–C Schematics depict neurogenesis (dark gray) and astrogenesis (green). A Under physiological conditions, the vast majority of newly generated cells are neurons. In contrast to neurons, most adult-generated astrocytes derive from local astrocyte proliferation, and not from a direct NSC-division. B Voluntary physical exercise by running wheel significantly increases the number of newly generated neurons and astrocytes, but does not change the ratio between neuro- and astrogenesis in the adult DG. C From six months of age, the number of newborn neurons is strongly decrease, while new astrocytes are generated until much older ages, leading to a shift in the ratio towards astrogenesis.
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