Abstract
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.
Highlights
The physiological regulation of food intake and body weight relies on endocrine signals, such as insulin, continuously informing the central nervous system (CNS) about the circulating and stored levels of nutrients in the organism
We observed that insulin receptors (IRs) are preferentially expressed in the caudal and lateral parts of the main olfactory bulb (OB), with the highest labeling found in the mitral cells, the main OB projection neurons
We demonstrated that insulin ICV injection in fasted adult rats decreased olfactory detection of a learned aversive odor and abolished sniffing behavior during food odor presentation
Summary
The physiological regulation of food intake and body weight relies on endocrine signals, such as insulin, continuously informing the central nervous system (CNS) about the circulating and stored levels of nutrients in the organism. Third ventricular injections of insulin decrease food intake and body weight [8], [9,10], [11], [12], [13], and the selective depletion of insulin receptors (IRs) in neurons results in hyperphagia leading to obesity [14]. A 48 h starvation increases exploratory and sniffing behaviors as well as c-fos activation in the mitral and granular cell layers of the olfactory bulb (OB) in response to food odors [16]. OB mitral cell reactivity is increased by short-term starvation and insulininduced hypoglycemia and decreased by re-feeding and gastric distension [17], [18], [19], [20]. It has been previously reported that repeated intranasal insulin administrations lead to the functional activation of downstream effectors of IRs in the OB and the modulation of several behaviors, including changes in olfactory discrimination [27]
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