Juvenile obesity enhances emotional memory and amygdala plasticity through glucocorticoids.
In addition to metabolic and cardiovascular disorders, obesity is associated with adverse cognitive and emotional outcomes. Its growing prevalence during adolescence is particularly alarming since recent evidence indicates that obesity can affect hippocampal function during this developmental period. Adolescence is a decisive period for maturation of the amygdala and the hypothalamic-pituitary-adrenal (HPA) stress axis, both required for lifelong cognitive and emotional processing. However, little data are available on the impact of obesity during adolescence on amygdala function. Herein, we therefore evaluate in rats whether juvenile high-fat diet (HFD)-induced obesity alters amygdala-dependent emotional memory and whether it depends on HPA axis deregulation. Exposure to HFD from weaning to adulthood, i.e., covering adolescence, enhances long-term emotional memories as assessed by odor-malaise and tone-shock associations. Juvenile HFD also enhances emotion-induced neuronal activation of the basolateral complex of the amygdala (BLA), which correlates with protracted plasma corticosterone release. HFD exposure restricted to adulthood does not modify all these parameters, indicating adolescence is a vulnerable period to the effects of HFD-induced obesity. Finally, exaggerated emotional memory and BLA synaptic plasticity after juvenile HFD are alleviated by a glucocorticoid receptor antagonist. Altogether, our results demonstrate that juvenile HFD alters HPA axis reactivity leading to an enhancement of amygdala-dependent synaptic and memory processes. Adolescence represents a period of increased susceptibility to the effects of diet-induced obesity on amygdala function.
INRA, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, Université de Bordeaux, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France.
Chloé
C
Boitard
Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa 31905, Israel.
Mouna
M
Maroun
INRA, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, Université de Bordeaux, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France.
Frédéric
F
Tantot
INRA, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, Université de Bordeaux, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France.
Amandine
A
Cavaroc
INRA, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, Université de Bordeaux, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France.
Julie
J
Sauvant
CNRS, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, UMR 5287, 33076 Bordeaux, France, and Université de Bordeaux, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, UMR 5287, 33076 Bordeaux, France.
Alain
A
Marchand
INRA, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, Université de Bordeaux, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France.
Sophie
S
Layé
INRA, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, Université de Bordeaux, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France.
Lucile
L
Capuron
INRA, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, Université de Bordeaux, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France.
Muriel
M
Darnaudery
INRA, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, Université de Bordeaux, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France.
Nathalie
N
Castanon
CNRS, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, UMR 5287, 33076 Bordeaux, France, and Université de Bordeaux, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, UMR 5287, 33076 Bordeaux, France.
Etienne
E
Coutureau
CNRS, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, UMR 5287, 33076 Bordeaux, France, and Université de Bordeaux, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, UMR 5287, 33076 Bordeaux, France.
Rose-Marie
http://orcid.org/0000-0001-5535-5448
RM
Vouimba
INRA, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, Université de Bordeaux, Nutrition and Integrative Neurobiology, UMR 1286, 33076 Bordeaux, France, guillaume.ferreira@bordeaux.inra.fr.
Guillaume
G
Ferreira
D000679:Amygdala / Q000503:physiopathology*; D000818:Animals; D001007:Anxiety / Q000523:psychology; D001362:Avoidance Learning; D004644:Emotions; D005239:Fear / Q000523:psychology; D005938:Glucocorticoids / Q000378:metabolism*; D008297:Male; D008568:Memory; D009473:Neuronal Plasticity; D009765:Obesity / Q000503:physiopathology / Q000523:psychology*; D051381:Rats; D017208:Rats, Wistar; D013315:Stress, Psychological / Q000378:metabolism / Q000503:physiopathology
D005938:Glucocorticoids
adolescence; amygdala; emotion; glucocorticoids; memory; obesity