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Hard-diet feeding recovers neurogenesis in the subventricular zone and olfactory functions of mice impaired by soft-diet feeding.

Utsugi C, Miyazono S, Osada K, Sasajima H, Noguchi T, Matsuda M, Kashiwayanagi M - PLoS ONE (2014)

Bottom Line: Recent studies have shown that a reduction of mastication impairs both neurogenesis in the hippocampus and brain functions.Avoidance of butyric acid was reduced by the soft-diet feeding.The present results suggest that feeding with a hard diet improves neurogenesis in the SVZ, which in turn enhances olfactory function at the OB.

View Article: PubMed Central - PubMed

Affiliation: Department of Oral and Maxillofacial Surgery, Asahikawa Medical University, Asahikawa, Japan; Department of Sensory Physiology, Asahikawa Medical University, Asahikawa, Japan.

ABSTRACT
The subventricular zone (SVZ) generates an immense number of neurons even during adulthood. These neurons migrate to the olfactory bulb (OB) and differentiate into granule cells and periglomerular cells. The information broadcast by general odorants is received by the olfactory sensory neurons and transmitted to the OB. Recent studies have shown that a reduction of mastication impairs both neurogenesis in the hippocampus and brain functions. To examine these effects, we first measured the difference in Fos-immunoreactivity (Fos-ir) at the principal sensory trigeminal nucleus (Pr5), which receives intraoral touch information via the trigeminal nerve, when female adult mice ingested a hard or soft diet to explore whether soft-diet feeding could mimic impaired mastication. Ingestion of a hard diet induced greater expression of Fos-ir cells at the Pr5 than did a soft diet or no diet. Bromodeoxyuridine-immunoreactive (BrdU-ir) structures in sagittal sections of the SVZ and in the OB of mice fed a soft or hard diet were studied to explore the effects of changes in mastication on newly generated neurons. After 1 month, the density of BrdU-ir cells in the SVZ and OB was lower in the soft-diet-fed mice than in the hard-diet-fed mice. The odor preferences of individual female mice to butyric acid were tested in a Y-maze apparatus. Avoidance of butyric acid was reduced by the soft-diet feeding. We then explored the effects of the hard-diet feeding on olfactory functions and neurogenesis in the SVZ of mice impaired by soft-diet feeding. At 3 months of hard-diet feeding, avoidance of butyric acid was reversed and responses to odors and neurogenesis were recovered in the SVZ. The present results suggest that feeding with a hard diet improves neurogenesis in the SVZ, which in turn enhances olfactory function at the OB.

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BrdU-ir cells in the SVZ and OB of mice fed a hard or soft diet.Sagittal sections of the SVZ (A–D) and OB (E–H) of mice fed a hard diet (A, B, E and F) or soft diet (C, D, G and H) for 1 month. Scale bar: 500 µm (C and G), 200 µm (D and H); I: the numbers of BrdU-ir cells at 600 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the SVZ to the lateral side of mice fed the hard diet (black column; n = 3) or soft diet (white column; n = 4). J: the number of BrdU-ir cells at 300 µm thickness from the section from Figure 108 of the mouse atlas (lateral 0.84 mm) of the OB to the lateral side of mice fed the hard diet (black column; n = 5) or soft diet (white column; n = 5). *: p<0.05; **: p<0.01.
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pone-0097309-g001: BrdU-ir cells in the SVZ and OB of mice fed a hard or soft diet.Sagittal sections of the SVZ (A–D) and OB (E–H) of mice fed a hard diet (A, B, E and F) or soft diet (C, D, G and H) for 1 month. Scale bar: 500 µm (C and G), 200 µm (D and H); I: the numbers of BrdU-ir cells at 600 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the SVZ to the lateral side of mice fed the hard diet (black column; n = 3) or soft diet (white column; n = 4). J: the number of BrdU-ir cells at 300 µm thickness from the section from Figure 108 of the mouse atlas (lateral 0.84 mm) of the OB to the lateral side of mice fed the hard diet (black column; n = 5) or soft diet (white column; n = 5). *: p<0.05; **: p<0.01.

Mentions: Neurogenesis occurs robustly in the hippocampus and SVZ even in adulthood [13], [22]. In the present study, as shown in Figure 1A and B, there were many BrdU-ir cells in the SVZ of mice fed the normal hard diet. However, there were fewer BrdU-ir cells in the SVZ of mice fed the soft diet (powdered food) for 1 month (Figure 1C and D). Newly generated cells at the SVZ migrate to the OB via the RMS [8]. Many BrdU-ir cells were observed in the OB of mice fed the normal hard diet (Figure 1E and F), however, fewer BrdU-ir cells were observed in the OB of mice fed the soft diet for 1 month (Figure 1G and H). The data from each group were cast into a two-factor ANOVA as follows: diet (hard or soft) and regions (SVZ or OB). This analysis revealed a main effect of diet (F(1, 13) = 33.38, p<0.0001). An interaction between diet and regions were also found to be significant (F(1, 13) = 14.989, p<0.005). Fisher's PLSD post-hoc testing indicated that the number of BrdU-ir cells in hard diet fed mice was higher than that in soft diet fed mice (p<0.05). The number of BrdU-ir cells at the SVZ in mice fed the hard diet was higher than that of mice fed the soft diet (p<0.01), suggesting that a powdered diet led to a decrease in neurogenesis activity at the SVZ (Figure 1I). This would suggest that fewer cells migrated from the SVZ to the OB in the soft-diet-fed mice than in the hard diet-fed mice. Figure 1J shows the quantity of BrdU-ir cells at the OB of mice fed the soft or hard diet for 1 month. The numbers of BrdU-ir cells at the granule cell layer of the OB of mice fed the soft diet were lower than those of mice fed the hard diet for 1 month. The density of BrdU-ir cells in mice fed the soft diet was lower than that of mice fed the hard diet (p<0.05).


Hard-diet feeding recovers neurogenesis in the subventricular zone and olfactory functions of mice impaired by soft-diet feeding.

Utsugi C, Miyazono S, Osada K, Sasajima H, Noguchi T, Matsuda M, Kashiwayanagi M - PLoS ONE (2014)

BrdU-ir cells in the SVZ and OB of mice fed a hard or soft diet.Sagittal sections of the SVZ (A–D) and OB (E–H) of mice fed a hard diet (A, B, E and F) or soft diet (C, D, G and H) for 1 month. Scale bar: 500 µm (C and G), 200 µm (D and H); I: the numbers of BrdU-ir cells at 600 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the SVZ to the lateral side of mice fed the hard diet (black column; n = 3) or soft diet (white column; n = 4). J: the number of BrdU-ir cells at 300 µm thickness from the section from Figure 108 of the mouse atlas (lateral 0.84 mm) of the OB to the lateral side of mice fed the hard diet (black column; n = 5) or soft diet (white column; n = 5). *: p<0.05; **: p<0.01.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4016307&req=5

pone-0097309-g001: BrdU-ir cells in the SVZ and OB of mice fed a hard or soft diet.Sagittal sections of the SVZ (A–D) and OB (E–H) of mice fed a hard diet (A, B, E and F) or soft diet (C, D, G and H) for 1 month. Scale bar: 500 µm (C and G), 200 µm (D and H); I: the numbers of BrdU-ir cells at 600 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the SVZ to the lateral side of mice fed the hard diet (black column; n = 3) or soft diet (white column; n = 4). J: the number of BrdU-ir cells at 300 µm thickness from the section from Figure 108 of the mouse atlas (lateral 0.84 mm) of the OB to the lateral side of mice fed the hard diet (black column; n = 5) or soft diet (white column; n = 5). *: p<0.05; **: p<0.01.
Mentions: Neurogenesis occurs robustly in the hippocampus and SVZ even in adulthood [13], [22]. In the present study, as shown in Figure 1A and B, there were many BrdU-ir cells in the SVZ of mice fed the normal hard diet. However, there were fewer BrdU-ir cells in the SVZ of mice fed the soft diet (powdered food) for 1 month (Figure 1C and D). Newly generated cells at the SVZ migrate to the OB via the RMS [8]. Many BrdU-ir cells were observed in the OB of mice fed the normal hard diet (Figure 1E and F), however, fewer BrdU-ir cells were observed in the OB of mice fed the soft diet for 1 month (Figure 1G and H). The data from each group were cast into a two-factor ANOVA as follows: diet (hard or soft) and regions (SVZ or OB). This analysis revealed a main effect of diet (F(1, 13) = 33.38, p<0.0001). An interaction between diet and regions were also found to be significant (F(1, 13) = 14.989, p<0.005). Fisher's PLSD post-hoc testing indicated that the number of BrdU-ir cells in hard diet fed mice was higher than that in soft diet fed mice (p<0.05). The number of BrdU-ir cells at the SVZ in mice fed the hard diet was higher than that of mice fed the soft diet (p<0.01), suggesting that a powdered diet led to a decrease in neurogenesis activity at the SVZ (Figure 1I). This would suggest that fewer cells migrated from the SVZ to the OB in the soft-diet-fed mice than in the hard diet-fed mice. Figure 1J shows the quantity of BrdU-ir cells at the OB of mice fed the soft or hard diet for 1 month. The numbers of BrdU-ir cells at the granule cell layer of the OB of mice fed the soft diet were lower than those of mice fed the hard diet for 1 month. The density of BrdU-ir cells in mice fed the soft diet was lower than that of mice fed the hard diet (p<0.05).

Bottom Line: Recent studies have shown that a reduction of mastication impairs both neurogenesis in the hippocampus and brain functions.Avoidance of butyric acid was reduced by the soft-diet feeding.The present results suggest that feeding with a hard diet improves neurogenesis in the SVZ, which in turn enhances olfactory function at the OB.

View Article: PubMed Central - PubMed

Affiliation: Department of Oral and Maxillofacial Surgery, Asahikawa Medical University, Asahikawa, Japan; Department of Sensory Physiology, Asahikawa Medical University, Asahikawa, Japan.

ABSTRACT
The subventricular zone (SVZ) generates an immense number of neurons even during adulthood. These neurons migrate to the olfactory bulb (OB) and differentiate into granule cells and periglomerular cells. The information broadcast by general odorants is received by the olfactory sensory neurons and transmitted to the OB. Recent studies have shown that a reduction of mastication impairs both neurogenesis in the hippocampus and brain functions. To examine these effects, we first measured the difference in Fos-immunoreactivity (Fos-ir) at the principal sensory trigeminal nucleus (Pr5), which receives intraoral touch information via the trigeminal nerve, when female adult mice ingested a hard or soft diet to explore whether soft-diet feeding could mimic impaired mastication. Ingestion of a hard diet induced greater expression of Fos-ir cells at the Pr5 than did a soft diet or no diet. Bromodeoxyuridine-immunoreactive (BrdU-ir) structures in sagittal sections of the SVZ and in the OB of mice fed a soft or hard diet were studied to explore the effects of changes in mastication on newly generated neurons. After 1 month, the density of BrdU-ir cells in the SVZ and OB was lower in the soft-diet-fed mice than in the hard-diet-fed mice. The odor preferences of individual female mice to butyric acid were tested in a Y-maze apparatus. Avoidance of butyric acid was reduced by the soft-diet feeding. We then explored the effects of the hard-diet feeding on olfactory functions and neurogenesis in the SVZ of mice impaired by soft-diet feeding. At 3 months of hard-diet feeding, avoidance of butyric acid was reversed and responses to odors and neurogenesis were recovered in the SVZ. The present results suggest that feeding with a hard diet improves neurogenesis in the SVZ, which in turn enhances olfactory function at the OB.

Show MeSH
Related in: MedlinePlus