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Prenatal stress inhibits hippocampal neurogenesis but spares olfactory bulb neurogenesis.

Belnoue L, Grosjean N, Ladevèze E, Abrous DN, Koehl M - PLoS ONE (2013)

Bottom Line: It is clearly established that these newborn neurons are implicated in specific functions sustained by these regions and that different factors can influence neurogenesis in both structures.Among these, life events, particularly occurring during early life, were shown to profoundly affect adult hippocampal neurogenesis and its associated functions like spatial learning, but data regarding their impact on adult bulbar neurogenesis are lacking.However, it decreases cell proliferation and neurogenesis in the DG of the hippocampus, thus confirming previous reports on rats.

View Article: PubMed Central - PubMed

Affiliation: Inserm U862, Bordeaux, France.

ABSTRACT
The dentate gyrus (DG) and the olfactory bulb (OB) are two regions of the adult brain in which new neurons are integrated daily in the existing networks. It is clearly established that these newborn neurons are implicated in specific functions sustained by these regions and that different factors can influence neurogenesis in both structures. Among these, life events, particularly occurring during early life, were shown to profoundly affect adult hippocampal neurogenesis and its associated functions like spatial learning, but data regarding their impact on adult bulbar neurogenesis are lacking. We hypothesized that prenatal stress could interfere with the development of the olfactory system, which takes place during the prenatal period, leading to alterations in adult bulbar neurogenesis and in olfactory capacities. To test this hypothesis we exposed pregnant C57Bl/6J mice to gestational restraint stress and evaluated behavioral and anatomic consequences in adult male offspring. We report that prenatal stress has no impact on adult bulbar neurogenesis, and does not alter olfactory functions in adult male mice. However, it decreases cell proliferation and neurogenesis in the DG of the hippocampus, thus confirming previous reports on rats. Altogether our data support a selective and cross-species long-term impact of prenatal stress on neurogenesis.

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Prenatal stress does not disturb adult bulbar neurogenesis.(A) Illustration of Ki67-IR cells in the SVZ. (B) Sagittal view of the olfactory bulb. (C) High magnification of the granule cell layer of the olfactory bulb with 5-week-old CldU-IR cells. (D) Number of Ki67-IR cells in the dorsolateral corner of the SVZ, n = 9–12 per group. (E) Volume of the granule cell layer of the OB, n = 10–14 per group. (F) Number of 5-week-old CldU-IR cells in the GCL, n = 10–14 per group. (G) Illustration of CldU-NeuN-IR cells (white arrow) and of CldU-S100-IR cells (white star). (H) Percentage of CldU-NeuN-IR cells in the GCL, n = 5 per group. (I) Percentage of CldU-S100-IR cells in the GCL, n = 5 per group. Scale bars = 100 µm, 100 µm, 80 µm, and 20 µm for A, B, C, and G, respectively.
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pone-0072972-g002: Prenatal stress does not disturb adult bulbar neurogenesis.(A) Illustration of Ki67-IR cells in the SVZ. (B) Sagittal view of the olfactory bulb. (C) High magnification of the granule cell layer of the olfactory bulb with 5-week-old CldU-IR cells. (D) Number of Ki67-IR cells in the dorsolateral corner of the SVZ, n = 9–12 per group. (E) Volume of the granule cell layer of the OB, n = 10–14 per group. (F) Number of 5-week-old CldU-IR cells in the GCL, n = 10–14 per group. (G) Illustration of CldU-NeuN-IR cells (white arrow) and of CldU-S100-IR cells (white star). (H) Percentage of CldU-NeuN-IR cells in the GCL, n = 5 per group. (I) Percentage of CldU-S100-IR cells in the GCL, n = 5 per group. Scale bars = 100 µm, 100 µm, 80 µm, and 20 µm for A, B, C, and G, respectively.

Mentions: To first determine a potential effect of prenatal stress on the olfactory bulb, we evaluated cell proliferation in the dorso-lateral subventricular zone, where we could not evidence any effect of prenatal stress (Fig. 2A,D; t19 = 0.93, p = ns). We then determined whether long-term cell survival was affected by evaluating the number of 5-week old CldU-IR cells in the granule cell layer (GCL). As for cell proliferation, cell survival was unaffected by prenatal stress (Fig. 2C,F; t19 = 0.37, p = ns) and as a consequence the volume of the granule cell layer (GCL) was identical between groups (Fig. 2B,E t22 = 0.68, p = ns). Finally, we determined whether prenatal stress had an impact on neuronal or astroglial differentiation but no difference could be detected between NS and PS mice in the percentage of newborn cells endorsing a neuronal phenotype (CldU-NeuN-IR cells, Fig. 2G,H; t8 = 0.47, p = ns) or an astroglial phenotype (CldU-S100-IR cells; Fig. 2G,I; t8 = 0.07, p = ns).


Prenatal stress inhibits hippocampal neurogenesis but spares olfactory bulb neurogenesis.

Belnoue L, Grosjean N, Ladevèze E, Abrous DN, Koehl M - PLoS ONE (2013)

Prenatal stress does not disturb adult bulbar neurogenesis.(A) Illustration of Ki67-IR cells in the SVZ. (B) Sagittal view of the olfactory bulb. (C) High magnification of the granule cell layer of the olfactory bulb with 5-week-old CldU-IR cells. (D) Number of Ki67-IR cells in the dorsolateral corner of the SVZ, n = 9–12 per group. (E) Volume of the granule cell layer of the OB, n = 10–14 per group. (F) Number of 5-week-old CldU-IR cells in the GCL, n = 10–14 per group. (G) Illustration of CldU-NeuN-IR cells (white arrow) and of CldU-S100-IR cells (white star). (H) Percentage of CldU-NeuN-IR cells in the GCL, n = 5 per group. (I) Percentage of CldU-S100-IR cells in the GCL, n = 5 per group. Scale bars = 100 µm, 100 µm, 80 µm, and 20 µm for A, B, C, and G, respectively.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3756947&req=5

pone-0072972-g002: Prenatal stress does not disturb adult bulbar neurogenesis.(A) Illustration of Ki67-IR cells in the SVZ. (B) Sagittal view of the olfactory bulb. (C) High magnification of the granule cell layer of the olfactory bulb with 5-week-old CldU-IR cells. (D) Number of Ki67-IR cells in the dorsolateral corner of the SVZ, n = 9–12 per group. (E) Volume of the granule cell layer of the OB, n = 10–14 per group. (F) Number of 5-week-old CldU-IR cells in the GCL, n = 10–14 per group. (G) Illustration of CldU-NeuN-IR cells (white arrow) and of CldU-S100-IR cells (white star). (H) Percentage of CldU-NeuN-IR cells in the GCL, n = 5 per group. (I) Percentage of CldU-S100-IR cells in the GCL, n = 5 per group. Scale bars = 100 µm, 100 µm, 80 µm, and 20 µm for A, B, C, and G, respectively.
Mentions: To first determine a potential effect of prenatal stress on the olfactory bulb, we evaluated cell proliferation in the dorso-lateral subventricular zone, where we could not evidence any effect of prenatal stress (Fig. 2A,D; t19 = 0.93, p = ns). We then determined whether long-term cell survival was affected by evaluating the number of 5-week old CldU-IR cells in the granule cell layer (GCL). As for cell proliferation, cell survival was unaffected by prenatal stress (Fig. 2C,F; t19 = 0.37, p = ns) and as a consequence the volume of the granule cell layer (GCL) was identical between groups (Fig. 2B,E t22 = 0.68, p = ns). Finally, we determined whether prenatal stress had an impact on neuronal or astroglial differentiation but no difference could be detected between NS and PS mice in the percentage of newborn cells endorsing a neuronal phenotype (CldU-NeuN-IR cells, Fig. 2G,H; t8 = 0.47, p = ns) or an astroglial phenotype (CldU-S100-IR cells; Fig. 2G,I; t8 = 0.07, p = ns).

Bottom Line: It is clearly established that these newborn neurons are implicated in specific functions sustained by these regions and that different factors can influence neurogenesis in both structures.Among these, life events, particularly occurring during early life, were shown to profoundly affect adult hippocampal neurogenesis and its associated functions like spatial learning, but data regarding their impact on adult bulbar neurogenesis are lacking.However, it decreases cell proliferation and neurogenesis in the DG of the hippocampus, thus confirming previous reports on rats.

View Article: PubMed Central - PubMed

Affiliation: Inserm U862, Bordeaux, France.

ABSTRACT
The dentate gyrus (DG) and the olfactory bulb (OB) are two regions of the adult brain in which new neurons are integrated daily in the existing networks. It is clearly established that these newborn neurons are implicated in specific functions sustained by these regions and that different factors can influence neurogenesis in both structures. Among these, life events, particularly occurring during early life, were shown to profoundly affect adult hippocampal neurogenesis and its associated functions like spatial learning, but data regarding their impact on adult bulbar neurogenesis are lacking. We hypothesized that prenatal stress could interfere with the development of the olfactory system, which takes place during the prenatal period, leading to alterations in adult bulbar neurogenesis and in olfactory capacities. To test this hypothesis we exposed pregnant C57Bl/6J mice to gestational restraint stress and evaluated behavioral and anatomic consequences in adult male offspring. We report that prenatal stress has no impact on adult bulbar neurogenesis, and does not alter olfactory functions in adult male mice. However, it decreases cell proliferation and neurogenesis in the DG of the hippocampus, thus confirming previous reports on rats. Altogether our data support a selective and cross-species long-term impact of prenatal stress on neurogenesis.

Show MeSH
Related in: MedlinePlus