Modulation of spontaneous and odorant-evoked activity of rat olfactory sensory neurons by two anorectic peptides, insulin and leptin.
In mammals, the sense of smell is modulated by the status of satiety, which is mainly signaled by blood-circulating peptide hormones. However, the underlying mechanisms linking olfaction and food intake are poorly understood. Here we investigated the effects of two anorectic peptides, insulin and leptin, on the functional properties of olfactory sensory neurons (OSNs). Using patch-clamp recordings, we analyzed the spontaneous activity of rat OSNs in an in vitro intact epithelium preparation. Bath perfusion of insulin and leptin significantly increased the spontaneous firing frequency in 91.7% (n = 24) and 75.0% (n = 24) of the cells, respectively. When the activity was electrically evoked, both peptides shortened the latency to the first action potential by approximately 25% and decreased the interspike intervals by approximately 13%. While insulin and leptin enhanced the electrical excitability of OSNs in the absence of odorants, they surprisingly reduced the odorant-induced activity in the olfactory epithelium. Insulin and leptin decreased the peak amplitudes of isoamyl acetate-induced electroolfactogram (EOG) signals to 46 and 38%, respectively. When measured in individual cells by patch-clamp recordings, insulin and leptin decreased odorant-induced transduction currents and receptor potentials. Therefore by increasing the spontaneous activity but reducing the odorant-induced activity of OSNs, an elevated insulin and leptin level (such as after a meal) may result in a decreased global signal-to-noise ratio in the olfactory epithelium, which matches the smell ability to the satiety status.
Savigner
Agnès
A
Université de Lyon, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5020, Neurosciences Sensorielles, Comportement, Cognition, Lyon, France. savigner@mail.med.upenn.edu
Duchamp-Viret
Patricia
P
Grosmaitre
Xavier
X
Chaput
Michel
M
Garcia
Samuel
S
Ma
Minghong
M
Palouzier-Paulignan
Brigitte
B
D000200:Action Potentials / Q000187:drug effects*; D000818:Animals; D000831:Animals, Newborn; D004558:Electric Stimulation / Q000379:methods; D066298:In Vitro Techniques; D007328:Insulin / Q000494:pharmacology*; D020738:Leptin / Q000494:pharmacology*; D009812:Odorants; D009830:Olfactory Bulb / Q000166:cytology*; D018408:Patch-Clamp Techniques / Q000379:methods; D051381:Rats; D011930:Reaction Time / Q000187:drug effects; D011984:Sensory Receptor Cells / Q000187:drug effects*
D007328:Insulin; D020738:Leptin