Cross-modal integration of emotions in the chemical senses

Frontiers in Human Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Bensafi, Moustafa ^a   Iannilli, Emilia ^b   Schriever, Valentin A ^b   Poncelet, Johan ^a   Seo, Han Seok ^c   Gerber, Johannes ^b   Rouby, Catherine ^a   Hummel, Thomas ^b  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITY OF DRESDEN MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Congruency; Emotion; Fmri; Olfaction; Trigeminal

Indexed keywords

CARBON DIOXIDE;

ADULT; ANTERIOR CINGULATE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONDITIONED EMOTIONAL RESPONSE TEST; EMOTION; EVENT RELATED POTENTIAL; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; NERVE STIMULATION; NORMAL HUMAN; ODOR RECOGNITION TEST; OLFACTORY DISCRIMINATION; OLFACTORY STIMULUS; ORANGE (FRUIT); ROSE; SENSORY STIMULATION; STIMULUS RESPONSE; TRIGEMINAL NERVE;

EID: 84891049687     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00883     Document Type: Article

References (50)

1. Albrecht, J., Kopietz, R., Frasnelli, J., Wiesmann, M., Hummel, T., and Lundstrom, J. N. (2010). The neuronal correlates of intranasal trigeminal function-an ALE meta-analysis of human functional brain imaging data. Brain Res. Rev. 62, 183-196. doi: 10.1016/j.brainresrev.2009.11.001
2. Anderson, A. K., Christoff, K., Stappen, I., Panitz, D., Ghahremani, D. G., Glover, G., et al. (2003). Dissociated neural representations of intensity and valence in human olfaction. Nat. Neurosci. 6, 196-202. doi: 10.1038/nn1001
3. Ashburner, J., and Friston, K. (2003). "Spatial normalization using basis function," in Human Brain Function 2nd Edn., ed R. S. J. Frackowiak (Amsterdam: Academic Press), 655-672.
4. Barkat, S., Poncelet, J., Landis, B. N., Rouby, C., and Bensafi, M. (2008). Improved smell pleasantness after odor-taste associative learning in humans. Neurosci. Lett. 434, 108-112. doi: 10.1016/j.neulet.2008.01.037
5. Bensafi, M., Croy, I., Phillips, N., Rouby, C., Sezille, C., Gerber, J., et al. (2013). The effect of verbal context on olfactory neural responses. Hum. Brain Mapp. doi: 10.1002/hbm.22215. [Epub ahead of print].
6. Bensafi, M., Frasnelli, J., Reden, J., and Hummel, T. (2007a). The neural representation of odor is modulated by the presence of a trigeminal stimulus during odor encoding. Clin. Neurophysiol. 118, 696-701. doi: 10.1016/j.clinph.2006.10.022
7. Bensafi, M., Rinck, F., Schaal, B., and Rouby, C. (2007b). Verbal cues modulate hedonic perception of odors in 5-year-old children as well as in adults. Chem. Senses 32, 855-862. doi: 10.1093/chemse/bjm055
8. Bensafi, M., Iannilli, E., Gerber, J., and Hummel, T. (2008). Neural coding of stimulus concentration in the human olfactory and intranasal trigeminal systems. Neuroscience 154, 832-838. doi: 10.1016/j.neuroscience.2008.03.079
9. Bensafi, M., Iannilli, E., Poncelet, J., Seo, H. S., Gerber, J., Rouby, C., et al. (2012). Dissociated representations of pleasant and unpleasant olfacto-trigeminal mixtures: an FMRI study. PLoS ONE 7:e38358. doi: 10.1371/journal.pone. 0038358
10. Boyle, J. A., Frasnelli, J., Gerber, J., Heinke, M., and Hummel, T. (2007a). Cross-modal integration of intranasal stimuli: a functional magnetic resonance imaging study. Neuroscience 149, 223-231. doi: 10.1016/j.neuroscience.2007.06.045
11. Boyle, J. A., Heinke, M., Gerber, J., Frasnelli, J., and Hummel, T. (2007b). Cerebral activation to intranasal chemosensory trigeminal stimulation. Chem. Senses 32, 343-353. doi: 10.1093/chemse/bjm004
12. Dalton, P., Doolittle, N., Nagata, H., and Breslin, P. A. (2000). The merging of the senses: integration of subthreshold taste and smell. Nat. Neurosci. 3, 431-432. doi: 10.1038/74797
13. De Araujo, I. E., Rolls, E. T., Kringelbach, M. L., McGlone, F., and Phillips, N. (2003). Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur. J. Neurosci. 18, 2059-2068. doi: 10.1046/j.1460-9568.2003.02915.x
14. De Araujo, I. E., Rolls, E. T., Velazco, M. I., Margot, C., and Cayeux, I. (2005). Cognitive modulation of olfactory processing. Neuron 46, 671-679. doi: 10.1016/j.neuron.2005.04.021
15. Eichenbaum, H., Yonelinas, A. P., and Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30, 123-152. doi: 10.1146/annurev.neuro.30.051606.094328
16. Goodrich-Hunsaker, N. J., Gilbert, P. E., and Hopkins, R. O. (2009). The role of the human hippocampus in odor-place associative memory. Chem. Senses 34, 513-521. doi: 10.1093/chemse/bjp026
17. Gottfried, J. A., and Dolan, R. J. (2003). The nose smells what the eye sees: cross-modal visual facilitation of human olfactory perception. Neuron 39, 375-386. doi: 10.1016/S0896-6273(03)00392-1
18. Herz, R. S. (2003). The effect of verbal context on olfactory perception. J. Exp. Psychol. Gen. 132, 595-606. doi: 10.1037/0096-3445.132.4.595
19. Hummel, T., Iannilli, E., Frasnelli, J., Boyle, J., and Gerber, J. (2009a). Central processing of trigeminal activation in humans. Ann. N. Y. Acad. Sci. 1170, 190-195. doi: 10.1111/j.1749-6632.2009.03910.x
20. Hummel, T., Oehme, L., Van Den Hoff, J., Gerber, J., Heinke, M., Boyle, J. A., et al. (2009b). PET-based investigation of cerebral activation following intranasal trigeminal stimulation. Hum. Brain Mapp. 30, 1100-1104. doi: 10.1002/hbm.20573
21. Hummel, T., and Kobal, G. (2001). "Olfactory event-related potentials," in Methods and Frontiers in Chemosensory Research, eds S. A. Simon and M. A. Nicolelis (Boca Raton, FL: CRC press), 429-464.
22. Hummel, T., Sekinger, B., Wolf, S. R., Pauli, E., and Kobal, G. (1997). 'Sniffin' sticks': olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem. Senses 22, 39-52. doi: 10.1093/chemse/22.1.39
23. Iannilli, E., Gerber, J., Frasnelli, J., and Hummel, T. (2007). Intranasal trigeminal function in subjects with and without an intact sense of smell. Brain Res. 1139, 235-244. doi: 10.1016/j.brainres.2006.12.082
24. Kjelvik, G., Evensmoen, H. R., Brezova, V., and Haberg, A. K. (2012). The human brain representation of odor identification. J. Neurophysiol. 108, 645-657. doi: 10.1152/jn.01036.2010
25. Klasen, M., Kenworthy, C. A., Mathiak, K. A., Kircher, T. T., and Mathiak, K. (2011). Supramodal representation of emotions. J. Neurosci. 31, 13635-13643. doi: 10.1523/JNEUROSCI.2833-11.2011
26. Kobal, G. (1981). Elektrophysiologische Untersuchungen des Menschlichen Geruchssinns. Stuttgart: Thieme Verlag.
27. Kupers, R., Beaulieu-Lefebvre, M., Schneider, F. C., Kassuba, T., Paulson, O. B., Siebner, H. R., et al. (2011). Neural correlates of olfactory processing in congenital blindness. Neuropsychologia 49, 2037-2044. doi: 10.1016/j.neuropsychologia. 2011.03.033
28. Kutas, M., and Federmeier, K. D. (2011). Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). Annu. Rev. Psychol. 62, 621-647. doi: 10.1146/annurev.psych.093008.131123
29. Lundstrom, J. N., Boesveldt, S., and Albrecht, J. (2011). Central processing of the chemical senses: an overview. ACS Chem. Neurosci. 2, 5-16. doi: 10.1021/ cn1000843
30. Lundstrom, J. N., Seven, S., Olsson, M. J., Schaal, B., and Hummel, T. (2006). Olfactory event-related potentials reflect individual differences in odor valence perception. Chem. Senses 31, 705-711. doi: 10.1093/chemse/ bjl012
31. Maldjian, J. A., Laurienti, P. J., Kraft, R. A., and Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 1233-1239. doi: 10.1016/S1053-8119(03)00169-1
32. Osterbauer, R. A., Matthews, P. M., Jenkinson, M., Beckmann, C. F., Hansen, P. C., and Calvert, G. A. (2005). Color of scents: chromatic stimuli modulate odor responses in the human brain. J. Neurophysiol. 93, 3434-3441. doi: 10.1152/jn.00555.2004
33. Pause, B. M., and Krauel, K. (2000). Chemosensory event-related potentials (CSERP) as a key to the psychology of odors. Int. J. Psychophysiol. 36, 105-122. doi: 10.1016/S0167-8760(99)00105-1
34. Penny, W. D., Holmes, A. P., and Friston, K. J. (2003). "Random effects analysis," in Human Brain Function, eds R. S. J. Frackowiak, K. J. Friston, C. Frith, R. Dolan, C. J. Price, S. Zeki, et al. (New York, NY: Academic Press).
35. Poncelet, J., Rinck, F., Bourgeat, F., Schaal, B., Rouby, C., Bensafi, M., et al. (2010). The effect of early experience on odor perception in humans: psychological and physiological correlates. Behav. Brain Res. 208, 458-465. doi: 10.1016/j.bbr.2009.12.011
36. Rinck, F., Barkat-Defradas, M., Chakirian, A., Joussain, P., Bourgeat, F., Thevenet, M., et al. (2011). Ontogeny of odor liking during childhood and its relation to language development. Chem. Senses 36, 83-91. doi: 10.1093/chemse/bjq101
37. Rozin, P., Ebert, L., and Schull, J. (1982). Some like it hot: a temporal analysis of hedonic responses to chili pepper. Appetite 3, 13-22. doi: 10.1016/S0195-6663(82)80033-0
38. Schifferstein, H. N., and Verlegh, P. W. (1996). The role of congruency and pleasantness in odor-induced taste enhancement. Acta Psychol. (Amst.) 94, 87-105. doi: 10.1016/0001-6918(95)00040-2
39. Seo, H. S., Arshamian, A., Schemmer, K., Scheer, I., Sander, T., Ritter, G., et al. (2010). Cross-modal integration between odors and abstract symbols. Neurosci. Lett. 478, 175-178. doi: 10.1016/j.neulet.2010.05.011
40. Seo, H. S., and Hummel, T. (2011). Auditory-olfactory integration: congruent or pleasant sounds amplify odor pleasantness. Chem. Senses 36, 301-309. doi: 10.1093/chemse/bjq129
41. Seubert, J., Freiherr, J., Djordjevic, J., and Lundstrom, J. N. (2012). Statistical localization of human olfactory cortex. Neuroimage 66C, 333-342. doi: 10.1016/j.neuroimage.2012.10.030
42. Small, D. M., Gregory, M. D., Mak, Y. E., Gitelman, D., Mesulam, M. M., and Parrish, T. (2003). Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39, 701-711. doi: 10.1016/S0896-6273(03)00467-7
43. Small, D. M., and Prescott, J. (2005). Odor/taste integration and the perception of flavor. Exp. Brain Res. 166, 345-357. doi: 10.1007/s00221-005-2376-9
44. Small, D. M., Voss, J., Mak, Y. E., Simmons, K. B., Parrish, T., and Gitelman, D. (2004). Experience-dependent neural integration of taste and smell in the human brain. J. Neurophysiol. 92, 1892-1903. doi: 10.1152/jn.00050.2004
45. Smitka, M., Puschmann, S., Buschhueter, D., Gerber, J. C., Witt, M., Honeycutt, N., et al. (2012). Is there a correlation between hippocampus and amygdala volume and olfactory function in healthy subjects? Neuroimage 59, 1052-1057. doi: 10.1016/j.neuroimage.2011.09.024
46. Squire, L. R., Stark, C. E., and Clark, R. E. (2004). The medial temporal lobe. Annu. Rev. Neurosci. 27, 279-306. doi: 10.1146/annurev.neuro.27.070203.144130
47. Staresina, B. P., Gray, J. C., and Davachi, L. (2009). Event congruency enhances episodic memory encoding through semantic elaboration and relational binding. Cereb. Cortex 19, 1198-1207. doi: 10.1093/cercor/bhn165
48. Veldhuizen, M. G., Shepard, T. G., Wang, M. F., and Marks, L. E. (2011). Coactivation of gustatory and olfactory signals in flavor perception. Chem. Senses 35, 121-133. doi: 10.1093/chemse/bjp089
49. Vogt, B. A. (2005). Pain and emotion interactions in subregions of the cingulate gyrus. Nat. Rev. Neurosci. 6, 533-544. doi: 10.1038/nrn1704
50. Yeomans, M. R. (2006). Olfactory influences on appetite and satiety in humans. Physiol. Behav. 87, 800-804. doi: 10.1016/j.physbeh.2006.01.029