Insulin modulates network activity in olfactory bulb slices: impact on odour processing. (21st May 2014)

• Record Type: Journal Article
• Authors: Kuczewski, Nicola; Fourcaud‐Trocmé, Nicolas; Savigner, Agnès; Thevenet, Marc; Aimé, Pascaline; Garcia, Samuel; Duchamp‐Viret, Patricia; Palouzier‐Paulignan, Brigitte
• Is Part Of: Journal of physiology. Volume 592:Number 13(2014:Jul.)
• Page Start: 2751
• Page End: 2769
• Publication Date: 2014-05-21
• Subjects: Physiology -- Periodicals; 612.005
• DOI: 10.1113/jphysiol.2013.269639
• Languages: English
• ISSNs: 0022-3751

Abstract

<abstract abstract-type="main"> <title> <x xml:space="preserve">Abstract</x> </title> <sec id="tjp6177-sec-0010" sec-type="section"> <title>Key points</title> <p> <list id="tjp6177-list-0001" list-type="bullet"> <list-item> <p>Olfactory function is largely under metabolic influence.</p> </list-item> <list-item> <p>Insulin, one of the major players between food intake and energy balance, is known to act at both central and peripheral levels.</p> </list-item> <list-item> <p>The present study assesses the action of insulin in olfactory bulb slices by using patch‐clamp recordings in young rats.</p> </list-item> <list-item> <p>The results show that insulin can alter both spontaneous and olfactory nerve‐induced firing activities in most of the main ouput neurons, this action being differentially exerted in two opposite directions.</p> </list-item> <list-item> <p>A mathematical model demonstrates that insulin, by acting in this way, could impact odour detection and discrimination mechanisms. Such an impact could be hypothesized as being exerted according to pertinent ecological characteristics, such as the alimentary/ethological valence of odour.</p> </list-item> </list> </p> </sec> <sec id="tjp6177-sec-0020" sec-type="section"> <title>Abstract</title> <p>Odour perception depends closely on nutritional status, in animals as in humans. Insulin, the principal anorectic hormone, appears to be one of the major candidates for ensuring the link between olfactory abilities and nutritional status, by modifying processing in the olfactory bulb (OB), one of its main central targets. The present study investigates whether and how insulin can act in OB, by evaluating its action on the main output neurons activities, mitral cells (MCs), in acute rat OB slices. Insulin was found to act at two OB network levels: (1) on MCs, by increasing their excitability, probably by inhibiting two voltage‐gated potassium (K<sup>+</sup>) channels; (2) on interneurons by modifying the GABAergic and on glutamatergic synaptic activity impinging on MCs, mainly reducing them. Insulin also altered the olfactory nerve (ON)‐evoked excitatory postsynaptic currents in 60% of MCs. Insulin decreased or increased the ON‐evoked responses in equal proportion and the direction of its effect depended on the initial neuron ON‐evoked firing rate. Indeed, insulin tended to decrease the high and to increase the low ON‐evoked firing rates, thereby reducing inter‐MC response firing variability. Therefore, the effects of insulin on the evoked firing rates were not carried out indiscriminately in the MC population. By constructing a mathematical model, the impact of insulin complex effects on OB was assessed at the population activity level. The model shows that the reduction of variability across cells could affect MC detection and discrimination abilities, mainly by decreasing and, less frequently, increasing them, depending on odour quality. Thus, as previously proposed, this differential action of insulin on MCs across odours would allow this hormone to put the olfactory function under feeding signal control, given the discerning valence of an odour as a function of nutritional status.</p> </sec> </abstract>