Research report
Fasting increases and satiation decreases olfactory detection for a neutral odor in rats

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Abstract

Olfaction plays a fundamental role in feeding behavior, but changes in olfactory acuity according to feeding states have never been precisely demonstrated in animals. The present study assesses the olfactory detection performance of fasted or satiated rats placed under a strictly controlled food-intake regimen. We did this using a conditioned odor aversion (COA) protocol which induced in rats an almost total aversion to an ISO-odorized drink at 10−5 (1 μl in 100 ml of water). The rats (either fasted or satiated) were then presented with different concentrations of ISO-odorized water to compare their ability to detect and so avoid the ISO drink. In both states, the rats consumed significantly larger volumes of ISO at 10−10, 10−9 and 10−8 than at 10−5, suggesting lower detection at these three concentrations, although the fasted rats consumed significantly less ISO drink than did the satiated ones, showing better ISO detection at these concentrations.

These experiments provide original data demonstrating the expected fact that olfactory sensitivity increases in fasted animals. Since these results were obtained using a neutral odor, we suggest that olfactory acuity increases during fasting, enabling animals to more easily detect both food and environmental odors such as those of predators. This would have an obvious eco-ethological role by increasing the relevance of olfactory inputs when seeking food.

Introduction

Olfaction is a sensory dimension that is an integral part of food intake. Many animals rely on odor to determine the location of their food sources and to discriminate and identify them. Although odors are not contingent on the nutritive properties of food, they are always associated with them, and are the major determinant of the palatability of food items [29], [31] and essential to control of food intake [23], [24], [27], [28], [30], [43]. The question of the effect of the nutritional state of an organism on odor perception (olfactory sensitivity) gave rise to several studies on humans at the beginning of the 20th century. The question is once more of interest because of the increased public health concerns regarding obesity. Since satiety towards a specific odor can be obtained only by smelling or chewing a food without swallowing it [40], it appears crucial to determine the implications of olfaction in the control of food intake. Some pathophysiological feeding behavior may be partly related to differences in the olfactory perception of foods, and thus in evaluating their palatability [34], [46].

In humans, olfactory sensitivity has been shown to change extensively after lunch [15], [16], [17], [18], [23], [26], [50], [52]. However, because these studies utilized experimental paradigms that focused on different parameters, their results are highly discrepant and do not allow definitive conclusions. For example, in the most recent of these studies, Koelega [26], studying the olfactory sensitivity of subjects to a neutral odor, concluded that there are no consistent changes in sensitivity related to food intake. He however chipped away at his conclusion by underlining that his experiments may have had some drawbacks attributable to a non strict control of the diet composition and size, to a lack of real knowledge of the internal nutritional status of his subjects, and to the fact that changes in olfactory sensitivity linked to feeding states could be very subtle.

In animals, the interactions between olfaction and food intake have been known for decades but the mechanisms underlying modifications of olfactory activity with the nutritional state remain unknown. The neural processing of olfactory information has been shown to be closely linked to the physiological and nutritional status of the organism. The olfactory system is more reactive to odors under starvation conditions, and its activity is reduced after satiation [1], [37]. Moreover, olfactory bulb reactivity is selectively increased by an odor known to be palatable [36]. To our knowledge the changes in olfactory detection ability caused by the food status have never been precisely studied in animals using a specific paradigm focusing on olfactory performance dissociated from food intake. Obtaining such information in strict experimental conditions is an essential prerequisite for initiating further research dealing with the neural communication processes occurring between the hypothalamic feeding centers and the olfactory system. Knowledge of the natural modulation of the olfactory function by nutritional states will be especially useful for assessing the respective roles in odor processing of neuropeptides like orexin, leptin, or insulin (for a review see Ref. [32]), which are described as neurochemical signatures of the fasted and satiated states. This is why the question of whether odor sensitivity changes with the nutritional state was studied using a conditioned odor aversion (COA) protocol. This behavioral paradigm was devoted to comparing the olfactory detection abilities of fasted and satiated rats made aversive to a neutral odor.

Section snippets

Animals

Experiments were carried out in accordance with the European Community Council Directive of November 24th, 1986 (86/609/EEC) for the care and use of laboratory animals. Experimental protocols were approved by the Comité d’Expérimentation Animale de l’Université Claude Bernard–Lyon1.

Ten male Wistar rats were used in each COA based experiment and eight as controls of fluid intake during the COA protocol. They were purchased from Charles River. They were 2-months old and weighed 250–260 g at the

COA: establishment and stability

In both experiments as in control, the rats readily accepted to drink ISO 10−5-odorized water from its first presentation. Because they were satiated in the baseline experiment and fasted in the detection experiment, this acceptance suggests that the feeding state did not change the rat's drinking behavior regarding an eventual repulsion or preference for ISO.

Fig. 3 shows the mean volume of odorized water drunk by the rats as a function of the training progress. By contrast to control rats the

Discussion

The two behavioral experiments are based on COA. The baseline experiment tested the assumption that the ability of rats to avoid the odorized water as a function of ISO concentrations would not change when the same concentrations were presented twice. Because the rats did not show habituation, a second experiment where the rats were presented with the same concentrations during two daily sessions was performed to determine the influence of fasting and satiation on avoidance of the odorized

Conclusion

The interaction between the olfactory system and the hypothalamic feeding centers involves neurochemical and neuroanatomical substrates. A direct centrifugal pathway has been described between the feeding centers and the olfactory bulb [6], [8], [9], [38]. This centrifugal pathway allows orexin, an orexygenic peptide, to modulate the activity of neurons in the olfactory bulb [5], [20]. Furthermore, the olfactory structures, from the periphery to the center, are rich in food-intake control

Acknowledgements

The authors are grateful to Dr. Barbara Ferry (CNRS, UMR7521, Laboratoire de neurosciences comportementales et cognitives, Strasbourg, France) Pr. Edwin Griff (University of Cincinnati) for their critical reading and to Wanda Lipski (English training service) for English language correction of this paper. The authors would like to thank Bernard Bertrand and Samuel Garcia for their technical assistance. This work was supported by the Centre National de la Recherche (CNRS) and the Claude Bernard

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