A physiological increase of insulin in the olfactory bulb decreases detection of a learned aversive odor and abolishes food odor-induced sniffing behavior in rats

• Published in: PloS one 2012-12, Vol.7 (12), p.e51227-e51227
• Main Authors: Aimé, Pascaline, Hegoburu, Chloé, Jaillard, Tristan, Degletagne, Cyril, Garcia, Samuel, Messaoudi, Belkacem, Thevenet, Marc, Lorsignol, Anne, Duchamp, Claude, Mouly, Anne-Marie, Julliard, Andrée Karyn
• Format: Article
• Language: English
• Subjects: Acetic acid; Animals; Aversion; Avoidance Learning; Base Sequence; Behavior, Animal; Binding sites; Biodiversity and Ecology; Biology; Blood Glucose - metabolism; Blood-brain barrier; Body weight; Brain; Conditioning; Diabetes mellitus; DNA Primers; Energy balance; Environmental Sciences; Food; Food intake; Glucose; Homeostasis; Information processing; Injection; Injections, Intraventricular; Insulin; Insulin - administration & dosage; Insulin - blood; Insulin - metabolism; Insulin receptors; Isoamyl acetate; Kinases; Male; Metabolic disorders; Mitral cells; Neurons; Neurosciences; Obesity; Odor; Odorants; Odors; Olfaction; Olfactory bulb; Olfactory Bulb - metabolism; Phosphorylation; Physiological aspects; Physiology; Potassium; Rats; Rats, Wistar; Receptors; Regulatory mechanisms (biology); Rodents; Senses; Smell; Sniffing behavior
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0051227

Insulin is involved in multiple regulatory mechanisms, including body weight and food intake, and plays a critical role in metabolic disorders such as obesity and diabetes. An increasing body of evidence indicates that insulin is also involved in the modulation of olfactory function. The olfactory bulb (OB) contains the highest level of insulin and insulin receptors (IRs) in the brain. However, a role for insulin in odor detection and sniffing behavior remains to be elucidated. Using a behavioral paradigm based on conditioned olfactory aversion (COA) to isoamyl-acetate odor, we demonstrated that an intracerebroventricular (ICV) injection of 14 mU insulin acutely decreased olfactory detection of fasted rats to the level observed in satiated animals. In addition, whereas fasted animals demonstrated an increase in respiratory frequency upon food odor detection, this effect was absent in fasted animals receiving a 14 mU insulin ICV injection as well as in satiated animals. In parallel, we showed that the OB and plasma insulin levels were increased in satiated rats compared to fasted rats, and that a 14 mU insulin ICV injection elevated the OB insulin level of fasted rats to that of satiated rats. We further quantified insulin receptors (IRs) distribution and showed that IRs are preferentially expressed in the caudal and lateral parts of the main OB, with the highest labeling found in the mitral cells, the main OB projection neurons. Together, these data suggest that insulin acts on the OB network to modulate olfactory processing and demonstrate that olfactory function is under the control of signals involved in energy homeostasis regulation and feeding behaviors.