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      Repeated exposure to odors induces affective habituation of perception and sniffing

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          Abstract

          Olfactory perception, and especially hedonic evaluation of odors, is highly flexible, but some mechanisms involved in this flexibility remain to be elucidated. In the present study we aimed at better understanding how repeated exposure to odors can affect their pleasantness. We tested the hypothesis of an affective habituation to the stimuli, namely a decrease of emotional intensity over repetitions. More specifically, we tested whether this effect is subject to inter-individual variability and whether it can also be observed at the olfactomotor level. Twenty-six participants took part in the experiment during which they had to smell two odorants, anise and chocolate, presented 20 times each. On each trial, sniff duration and volume were recorded and paired with ratings of odor pleasantness and intensity. For each smell, we distinguished between “likers” and “dislikers,” namely individuals giving positive and negative initial hedonic evaluations. Results showed a significant decrease in pleasantness with time when the odor was initially pleasant (“likers”), while unpleasantness remained stable or slightly decreased when the odor was initially unpleasant (“dislikers”). This deviation toward neutrality was interpreted as affective habituation. This effect was all the more robust as it was observed for both odors and corroborated by sniffing, an objective measurement of odor pleasantness. Affective habituation to odors can be interpreted as an adaptive response to stimuli that prove over time to be devoid of positive or negative outcome on the organism. This study contributes to a better understanding of how olfactory preferences are shaped through exposure, depending on the individual's own initial perception of the odor.

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          Most cited references43

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          Changes in brain activity related to eating chocolate: from pleasure to aversion.

          D M Small (2001)
          We performed successive H(2)(15)O-PET scans on volunteers as they ate chocolate to beyond satiety. Thus, the sensory stimulus and act (eating) were held constant while the reward value of the chocolate and motivation of the subject to eat were manipulated by feeding. Non-specific effects of satiety (such as feelings of fullness and autonomic changes) were also present and probably contributed to the modulation of brain activity. After eating each piece of chocolate, subjects gave ratings of how pleasant/unpleasant the chocolate was and of how much they did or did not want another piece of chocolate. Regional cerebral blood flow was then regressed against subjects' ratings. Different groups of structures were recruited selectively depending on whether subjects were eating chocolate when they were highly motivated to eat and rated the chocolate as very pleasant [subcallosal region, caudomedial orbitofrontal cortex (OFC), insula/operculum, striatum and midbrain] or whether they ate chocolate despite being satiated (parahippocampal gyrus, caudolateral OFC and prefrontal regions). As predicted, modulation was observed in cortical chemosensory areas, including the insula and caudomedial and caudolateral OFC, suggesting that the reward value of food is represented here. Of particular interest, the medial and lateral caudal OFC showed opposite patterns of activity. This pattern of activity indicates that there may be a functional segregation of the neural representation of reward and punishment within this region. The only brain region that was active during both positive and negative compared with neutral conditions was the posterior cingulate cortex. Therefore, these results support the hypothesis that there are two separate motivational systems: one orchestrating approach and another avoidance behaviours.
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            Genetic variation in a human odorant receptor alters odour perception.

            Human olfactory perception differs enormously between individuals, with large reported perceptual variations in the intensity and pleasantness of a given odour. For instance, androstenone (5alpha-androst-16-en-3-one), an odorous steroid derived from testosterone, is variously perceived by different individuals as offensive ("sweaty, urinous"), pleasant ("sweet, floral") or odourless. Similar variation in odour perception has been observed for several other odours. The mechanistic basis of variation in odour perception between individuals is unknown. We investigated whether genetic variation in human odorant receptor genes accounts in part for variation in odour perception between individuals. Here we show that a human odorant receptor, OR7D4, is selectively activated in vitro by androstenone and the related odorous steroid androstadienone (androsta-4,16-dien-3-one) and does not respond to a panel of 64 other odours and two solvents. A common variant of this receptor (OR7D4 WM) contains two non-synonymous single nucleotide polymorphisms (SNPs), resulting in two amino acid substitutions (R88W, T133M; hence 'RT') that severely impair function in vitro. Human subjects with RT/WM or WM/WM genotypes as a group were less sensitive to androstenone and androstadienone and found both odours less unpleasant than the RT/RT group. Genotypic variation in OR7D4 accounts for a significant proportion of the valence (pleasantness or unpleasantness) and intensity variance in perception of these steroidal odours. Our results demonstrate the first link between the function of a human odorant receptor in vitro and odour perception.
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              Cognitive modulation of olfactory processing.

              We showed how cognitive, semantic information modulates olfactory representations in the brain by providing a visual word descriptor, "cheddar cheese" or "body odor," during the delivery of a test odor (isovaleric acid with cheddar cheese flavor) and also during the delivery of clean air. Clean air labeled "air" was used as a control. Subjects rated the affective value of the test odor as significantly more unpleasant when labeled "body odor" than when labeled "cheddar cheese." In an event-related fMRI design, we showed that the rostral anterior cingulate cortex (ACC)/medial orbitofrontal cortex (OFC) was significantly more activated by the test stimulus and by clean air when labeled "cheddar cheese" than when labeled "body odor," and the activations were correlated with the pleasantness ratings. This cognitive modulation was also found for the test odor (but not for the clean air) in the amygdala bilaterally.
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                Author and article information

                Contributors
                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                10 April 2014
                2014
                : 8
                : 119
                Affiliations
                Centre National de la Recherche Scientifique UMR5292, INSERM U1028, Centre de Recherche en Neurosciences de Lyon, Université Claude Bernard Lyon 1 Lyon, France
                Author notes

                Edited by: Donald A. Wilson, New York University School of Medicine, USA

                Reviewed by: Ilona Croy, University of Gothenburg, Sweden; Monique A. Smeets, Utrecht University, Netherlands

                *Correspondence: Camille Ferdenzi, Centre National de la Recherche Scientifique UMR5292, INSERM U1028, Centre de Recherche en Neurosciences de Lyon, Université Claude Bernard Lyon 1, 50 Avenue Tony Garnier, F-69366 Lyon Cedex 07, France e-mail: cferdenzi@ 123456crnl.cnrs.fr

                This article was submitted to the journal Frontiers in Behavioral Neuroscience.

                Article
                10.3389/fnbeh.2014.00119
                3989720
                24782728
                76e763c0-168a-4acb-969e-bdba04c232f1
                Copyright © 2014 Ferdenzi, Poncelet, Rouby and Bensafi.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 11 February 2014
                : 21 March 2014
                Page count
                Figures: 4, Tables: 1, Equations: 0, References: 50, Pages: 10, Words: 6749
                Categories
                Neuroscience
                Original Research Article

                Neurosciences
                pleasantness,smell,repeated exposure,sniff,habituation
                Neurosciences
                pleasantness, smell, repeated exposure, sniff, habituation

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