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      Dissociated Representations of Pleasant and Unpleasant Olfacto-Trigeminal Mixtures: An fMRI Study

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          Abstract

          How the pleasantness of chemosensory stimuli such as odorants or intranasal trigeminal compounds is processed in the human brain has been the focus of considerable recent interest. Yet, so far, only the unimodal form of this hedonic processing has been explored, and not its bimodal form during crossmodal integration of olfactory and trigeminal stimuli. The main purpose of the present study was to investigate this question. To this end, functional magnetic resonance imaging (fMRI) was used in an experiment comparing brain activation related to a pleasant and a relatively unpleasant olfacto-trigeminal mixture, and to their individual components (CO 2 alone, Orange alone, Rose alone). Results revealed first common neural activity patterns in response to both mixtures in a number of regions: notably the superior temporal gyrus and the caudate nucleus. Common activations were also observed in the insula, although the pleasant mixture activated the right insula whereas the unpleasant mixture activated the left insula. However, specific activations were observed in anterior cingulate gyrus and the ventral tegmental area only during the perception of the pleasant mixture. These findings emphasized for the firs time the involvement of the latter structures in processing of pleasantness during crossmodal integration of chemosensory stimuli.

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          Most cited references32

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          Pain and emotion interactions in subregions of the cingulate gyrus.

          Brent Vogt (2005)
          Acute pain and emotion are processed in two forebrain networks, and the cingulate cortex is involved in both. Although Brodmann's cingulate gyrus had two divisions and was not based on any functional criteria, functional imaging studies still use this model. However, recent cytoarchitectural studies of the cingulate gyrus support a four-region model, with subregions, that is based on connections and qualitatively unique functions. Although the activity evoked by pain and emotion has been widely reported, some view them as emergent products of the brain rather than of small aggregates of neurons. Here, we assess pain and emotion in each cingulate subregion, and assess whether pain is co-localized with negative affect. Amazingly, these activation patterns do not simply overlap.
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            Crossmodal processing in the human brain: insights from functional neuroimaging studies.

            Modern brain imaging techniques have now made it possible to study the neural sites and mechanisms underlying crossmodal processing in the human brain. This paper reviews positron emission tomography, functional magnetic resonance imaging (fMRI), event-related potential and magnetoencephalographic studies of crossmodal matching, the crossmodal integration of content and spatial information, and crossmodal learning. These investigations are beginning to produce some consistent findings regarding the neuronal networks involved in these distinct crossmodal operations. Increasingly, specific roles are being defined for the superior temporal sulcus, the inferior parietal sulcus, regions of frontal cortex, the insula cortex and claustrum. The precise network of brain areas implicated in any one study, however, seems to be heavily dependent on the experimental paradigms used, the nature of the information being combined and the particular combination of modalities under investigation. The different analytic strategies adopted by different groups may also be a significant factor contributing to the variability in findings. In this paper, we demonstrate the impact of computing intersections, conjunctions and interaction effects on the identification of audiovisual integration sites using existing fMRI data from our own laboratory. This exercise highlights the potential value of using statistical interaction effects to model electrophysiological responses to crossmodal stimuli in order to identify possible sites of multisensory integration in the human brain.
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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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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                12 June 2012
                : 7
                : 6
                : e38358
                Affiliations
                [1 ]Lyon Neuroscience Research Center, CNRS, UMR5292, University Lyon, Lyon, France
                [2 ]Department of Otorhinolaryngology, Smell & Taste Clinic, University of Dresden Medical School, Dresden, Germany
                [3 ]Department of Neuroradiology, University of Dresden Medical School, Dresden, Germany
                French National Centre for Scientific Research, France
                Author notes

                Conceived and designed the experiments: MB TH. Performed the experiments: MB EI JP SH JG CR TH. Analyzed the data: MB EI TH. Wrote the paper: MB TH.

                Article
                PONE-D-11-19050
                10.1371/journal.pone.0038358
                3373527
                22701631
                56cf4ef8-6737-4f57-ba14-7094bea7417c
                Bensafi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 28 September 2011
                : 3 May 2012
                Page count
                Pages: 6
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Neurological System
                Biochemistry
                Neurochemistry
                Neuroscience
                Neurochemistry
                Neurochemicals
                Neuroimaging
                Fmri
                Sensory Systems
                Olfactory System
                Cognitive Neuroscience
                Neuropsychology
                Social and Behavioral Sciences
                Psychology
                Cognitive Psychology
                Sensory Perception

                Uncategorized
                Uncategorized

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