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. 2015 Nov;23(11):2157-64.
doi: 10.1002/oby.21306.

Maternal high-fat diet and obesity impact palatable food intake and dopamine signaling in nonhuman primate offspring

Heidi M Rivera  1 , Paul Kievit  1 , Melissa A Kirigiti  1 , Leigh Ann Bauman  1 , Karalee Baquero  1 , Peter Blundell  1 , Tyler A Dean  1 , Jeanette C Valleau  1 , Diana L Takahashi  1 , Tim Frazee  1 , Luke Douville  1   2 , Jordan Majer  1 , M Susan Smith  1 , Kevin L Grove  1 , Elinor L Sullivan  1   2   3
Affiliations

Maternal high-fat diet and obesity impact palatable food intake and dopamine signaling in nonhuman primate offspring

Heidi M Rivera et al. Obesity (Silver Spring). 2015 Nov.

Abstract

Objective: To utilize a nonhuman primate model to examine the impact of maternal high-fat diet (HFD) consumption and pre-pregnancy obesity on offspring intake of palatable food and to examine whether maternal HFD consumption impaired development of the dopamine system, critical for the regulation of hedonic feeding.

Methods: The impact of exposure to maternal HFD and obesity on offspring consumption of diets of varying composition was assessed after weaning. The influence of maternal HFD consumption on the development of the prefrontal cortex-dopaminergic system at 13 months of age was also examined.

Results: During a preference test, offspring exposed to maternal HFD consumption and obesity displayed increased intake of food high in fat and sugar content relative to offspring from lean control mothers. Maternal HFD consumption suppressed offspring dopamine signaling (as assessed by immunohistochemistry) relative to control offspring. Specifically, there was decreased abundance of dopamine fibers and of dopamine receptor 1 and 2 proteins.

Conclusions: This study reveals that offspring exposed to both maternal HFD consumption and maternal obesity during early development are at increased risk for obesity due to overconsumption of palatable energy-dense food, a behavior that may be related to reduced central dopamine signaling.

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Conflict of interest statement

Conflict of Interest: All other authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Maternal obesity, not maternal HFD consumption, altered offspring body weight at weaning. A) There was a main effect of maternal obesity (p<0.05) but not a main effect of maternal HFD consumption (p=0.88). Posthoc test results demonstrated that offspring from CTR-obese mothers weighed more than controls (offspring from CTR-lean mothers, p<0.05). Offspring from HFD-lean (p=0.69) and HFD-obese (p=0.10) mothers were not significantly different than controls. + Main effect of maternal obesity. * Greater than controls. B) Maternal pre-pregnancy body fat was positively correlated with offspring weight (p<0.05). Sample sizes for offspring from CTR-lean mothers n = 5 (n = 2 females; n = 3 males), offspring from CTR-obese mothers n = 9 (n = 5 females; n = 4 males), offspring from HFD-lean mothers n = 5 (n = 1 female; n = 4 males), and offspring from HFD-obese mothers n = 13 (n = 8 females; n = 5 males). Data shown as mean ± SEM.
Figure 2
Figure 2
Both maternal HFD consumption and obesity impaired offspring absolute intake of palatable food at weaning. A) Offspring from HFD-obese mothers displayed increased consumption of palatable, energy-dense food (high-fat/sucrose) relative to offspring from CTR-lean mothers. Bars labeled with different letters indicate a significant difference (p<0.05), while bars with the same letter are not significantly different. B) Diet preference of each offspring group. C) No significant differences were apparent in total caloric intake between offspring groups. D) Maternal pre-pregnancy body fat was positively correlated with offspring intake of high-fat/sucrose (p<0.05). E) Offspring weight was positively correlated with offspring intake for high-fat/sucrose (p<0.01). Sample sizes for offspring from CTR-lean mothers n = 5, offspring from CTR-obese mothers n = 9, offspring from HFD-lean mothers n = 5, and offspring from HFD-obese mothers n = 13. Data shown as mean ± SEM.
Figure 3
Figure 3
Maternal HFD consumption decreased DA fiber projections to PFC. A) DA fibers were concentrated in superficial and deep layers, but sparse in the medial layer. PFC diagram showing region analyzed (adapted from (40)). B) Representative images reveal a robust amount of TH-positive fibers in offspring from mothers consuming a HFD, but a comparative reduction in offspring from mothers consuming a CTR diet. Scale bar in image = 400 μm. C) Offspring from mothers consuming a HFD (p<0.001) exhibited a decrease in the abundance of TH-positive fibers (density) in the superficial layer, but not in the medial (p=0.29) or deep (p=0.13) layers. * Less than offspring from mothers consuming a CTR diet. Sample sizes for offspring from CTR mothers n = 6 (3 females; 3 males) and offspring from HFD mothers n = 6 (3 females; 3 males). Data shown as mean ± SEM.
Figure 4
Figure 4
Maternal HFD consumption decreased dopamine receptor proteins (D1 and D2) in the PFC. A) D1- and D2-positive cells were evident in both medial and deep layers, but not in the superficial layer. PFC diagram showing region analyzed (adapted from (40)). B) Representative images reveal a robust amount of D1-positive cells in offspring from mothers consuming a CTR diet but a comparative reduction in offspring from mothers consuming a HFD. Scale bar in image = 100 μm. C) Offspring from mothers consuming a HFD (p<0.05) displayed a decrease in the abundance of D1-positive cells (density) in the deep layer, but not in the medial layer (p=0.20). * Less than offspring from mothers consuming a CTR diet. D) Offspring from mothers consuming a HFD displayed a decrease in the percent of cells stained with D1 in the medial (p<0.05) and deep (p<0.05) layers. * Less than offspring from mothers consuming a CTR diet. E) No group difference was observed in total number of cells in medial (p=0.14) or deep (p=0.24) layers. Sample sizes for offspring from CTR mothers n = 6 and offspring from HFD mothers n = 6. Data shown as mean ± SEM.
Figure 5
Figure 5
Maternal HFD consumption decreased D2 proteins in the PFC. A) Representative images reveal a robust amount of D2-positive cells in offspring from mothers consuming a CTR diet but a comparative reduction in offspring consuming a HFD. Scale bar in image = 100 μm. B) No group difference was observed in density in medial (p=0.63) or deep (p=0.56) layers. C) Offspring from mothers consuming a HFD displayed a decrease in the percent of cells stained with D2 in the deep (p<0.05), but not medial (p=0.71) layer. D) Offspring from mothers consuming a HFD displayed an increased total number of cells in the deep (p<0.005), but not medial (p=0.10) layer. * Greater than offspring from mothers consuming a CTR diet. Sample sizes for offspring from CTR mothers n = 6 and offspring from HFD mothers n = 6. Data shown as mean ± SEM.
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