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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 of mice fed a hard diet for 1 or 3 months after being fed a soft diet.Sagittal sections of the SVZ of mice fed only a hard diet (A and D), only a soft diet (B and E), or a hard diet for 1 (C) or 3 months (F) after a soft diet for 1 month. Sagittal sections of the OB of mice fed only a hard diet (G), only a soft diet (H), and a hard diet for 3 months after a soft diet for 1 month (I). Scale bar: 200 µm (F and I); J and K: The numbers of BrdU-ir cells in 600 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the SVZ to the lateral side of mice fed only the hard diet (black column), only the soft diet (white column), or the hard diet for 1 month (J) or 3 months (K) after the soft diet (gray column). n = 4 without white column in K, n = 5 for white column in K. L: The number of BrdU-ir cells in 300 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the OB to the lateral side of mice fed only the hard diet (black column; n = 4), only the soft diet (white column; n = 5), or the hard diet for 3 months after the soft diet for 1 month (gray column; n = 4). *: p<0.05; **: p<0.01; ***: p<0.0001.
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pone-0097309-g004: BrdU-ir cells in the SVZ of mice fed a hard diet for 1 or 3 months after being fed a soft diet.Sagittal sections of the SVZ of mice fed only a hard diet (A and D), only a soft diet (B and E), or a hard diet for 1 (C) or 3 months (F) after a soft diet for 1 month. Sagittal sections of the OB of mice fed only a hard diet (G), only a soft diet (H), and a hard diet for 3 months after a soft diet for 1 month (I). Scale bar: 200 µm (F and I); J and K: The numbers of BrdU-ir cells in 600 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the SVZ to the lateral side of mice fed only the hard diet (black column), only the soft diet (white column), or the hard diet for 1 month (J) or 3 months (K) after the soft diet (gray column). n = 4 without white column in K, n = 5 for white column in K. L: The number of BrdU-ir cells in 300 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the OB to the lateral side of mice fed only the hard diet (black column; n = 4), only the soft diet (white column; n = 5), or the hard diet for 3 months after the soft diet for 1 month (gray column; n = 4). *: p<0.05; **: p<0.01; ***: p<0.0001.

Mentions: We next explored the effect of hard-diet feeding on neurogenesis at the SVZ and the number of newly generated cells at the OB in mice fed the soft diet for 1 month. Figure 4 shows BrdU-ir cells at the SVZ of mice fed only the hard diet, only the soft diet, or the hard diet for 1 or 3 months after the soft diet for 1 month. The expression of BrdU immunoreactivity at the SVZ of mice fed only the soft diet (B) was similar to that of mice fed the hard diet for 1 month after the soft diet for 1 month (C). However, the expression of the BrdU immunoreactivity of mice fed the hard diet for 3 months after the soft diet for 1 month (F) was higher than that of mice fed only the soft diet (E). At the SVZ, the data from each group were cast into a two-factor ANOVA as follows: hard, soft, or hard after soft diet and the period of hard-diet feeding. The main effect of diet was found to be significant (F (2, 19) = 28.928, p<0.0001). In mice given 1 month of a hard diet after 1 month of a soft diet, the number of BrdU-ir cells at the SVZ was similar to that of mice fed only the soft diet (Figure 4J). The number of BrdU-ir cells in mice given 3 months of a hard diet after 1 month of a soft diet was still smaller than that of mice fed only the hard diet (Figure 4K; p<0.0001), but it was significantly larger than that of mice fed only the soft diet (p<0.05). The number of BrdU-immunoreactive signals surrounded with doublecortin (DCX)-immunoreactive signals at the SVZ of mice fed a hard-diet after feeding with a soft-diet was higher than that of mice fed a soft-diet alone (Figure S2), suggesting that the reduced neurogenesis by soft-diet feeding was recovered by hard-diet feeding for 3 months.


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 of mice fed a hard diet for 1 or 3 months after being fed a soft diet.Sagittal sections of the SVZ of mice fed only a hard diet (A and D), only a soft diet (B and E), or a hard diet for 1 (C) or 3 months (F) after a soft diet for 1 month. Sagittal sections of the OB of mice fed only a hard diet (G), only a soft diet (H), and a hard diet for 3 months after a soft diet for 1 month (I). Scale bar: 200 µm (F and I); J and K: The numbers of BrdU-ir cells in 600 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the SVZ to the lateral side of mice fed only the hard diet (black column), only the soft diet (white column), or the hard diet for 1 month (J) or 3 months (K) after the soft diet (gray column). n = 4 without white column in K, n = 5 for white column in K. L: The number of BrdU-ir cells in 300 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the OB to the lateral side of mice fed only the hard diet (black column; n = 4), only the soft diet (white column; n = 5), or the hard diet for 3 months after the soft diet for 1 month (gray column; n = 4). *: p<0.05; **: p<0.01; ***: p<0.0001.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
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pone-0097309-g004: BrdU-ir cells in the SVZ of mice fed a hard diet for 1 or 3 months after being fed a soft diet.Sagittal sections of the SVZ of mice fed only a hard diet (A and D), only a soft diet (B and E), or a hard diet for 1 (C) or 3 months (F) after a soft diet for 1 month. Sagittal sections of the OB of mice fed only a hard diet (G), only a soft diet (H), and a hard diet for 3 months after a soft diet for 1 month (I). Scale bar: 200 µm (F and I); J and K: The numbers of BrdU-ir cells in 600 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the SVZ to the lateral side of mice fed only the hard diet (black column), only the soft diet (white column), or the hard diet for 1 month (J) or 3 months (K) after the soft diet (gray column). n = 4 without white column in K, n = 5 for white column in K. L: The number of BrdU-ir cells in 300 µm thickness from Figure 108 of the mouse atlas (lateral 0.84 mm) of the OB to the lateral side of mice fed only the hard diet (black column; n = 4), only the soft diet (white column; n = 5), or the hard diet for 3 months after the soft diet for 1 month (gray column; n = 4). *: p<0.05; **: p<0.01; ***: p<0.0001.
Mentions: We next explored the effect of hard-diet feeding on neurogenesis at the SVZ and the number of newly generated cells at the OB in mice fed the soft diet for 1 month. Figure 4 shows BrdU-ir cells at the SVZ of mice fed only the hard diet, only the soft diet, or the hard diet for 1 or 3 months after the soft diet for 1 month. The expression of BrdU immunoreactivity at the SVZ of mice fed only the soft diet (B) was similar to that of mice fed the hard diet for 1 month after the soft diet for 1 month (C). However, the expression of the BrdU immunoreactivity of mice fed the hard diet for 3 months after the soft diet for 1 month (F) was higher than that of mice fed only the soft diet (E). At the SVZ, the data from each group were cast into a two-factor ANOVA as follows: hard, soft, or hard after soft diet and the period of hard-diet feeding. The main effect of diet was found to be significant (F (2, 19) = 28.928, p<0.0001). In mice given 1 month of a hard diet after 1 month of a soft diet, the number of BrdU-ir cells at the SVZ was similar to that of mice fed only the soft diet (Figure 4J). The number of BrdU-ir cells in mice given 3 months of a hard diet after 1 month of a soft diet was still smaller than that of mice fed only the hard diet (Figure 4K; p<0.0001), but it was significantly larger than that of mice fed only the soft diet (p<0.05). The number of BrdU-immunoreactive signals surrounded with doublecortin (DCX)-immunoreactive signals at the SVZ of mice fed a hard-diet after feeding with a soft-diet was higher than that of mice fed a soft-diet alone (Figure S2), suggesting that the reduced neurogenesis by soft-diet feeding was recovered by hard-diet feeding for 3 months.

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