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Odors Are More Sensitive to Evaluative Conditioning than Sounds

  • Anika Pützer
  • Tobias Otto
  • Oliver T. WolfEmail author
Article
  • 108 Downloads

Abstract

Introduction

Stimuli of different modalities can acquire an affective value via evaluative conditioning. This process describes a shift in perceived affective quality of a neutral stimulus towards the hedonics of an associated affective stimulus. The olfactory system, as compared to other modalities, might be especially prone to attributing affective value to an odor due to its close neuroanatomical connectivity with brain regions processing emotion.

Methods

In the present study, we investigated whether perceived affective quality of odors is more sensitive to evaluative conditioning than that of sounds. For this purpose, 48 healthy participants (50% male) rated unfamiliar and emotionally neutral odors and sounds before and after pairing with either aversive or neutral pictures.

Results

Our results show a stronger decrease in odor valence and stronger increases in arousal and dominance ratings for odors paired with aversive compared to neutral pictures. For sounds, ratings of valence, arousal, and dominance were independent of picture emotionality.

Conclusion

Odors appear to be more sensitive to evaluative conditioning than sounds. Our findings extend existing modality comparisons mainly focusing on characteristics of odor-associated memories by specifically looking at affective quality of the odor itself in associative learning.

Implications

Perceived affective quality of a stimulus goes along with the tendency to approach or avoid this stimulus. For odors, it is especially prone to change into an aversive direction. This may have implications for food and fragrance choices but also for the understanding of clinical conditions in which odors become highly aversive, such as post-traumatic stress disorder.

Keywords

Evaluative conditioning Associative learning Affective quality Odor Sound Modality comparison 

Notes

Acknowledgements

This work was supported by the German Research foundation (DFG) project B4 of the Collaborative Research Center (SFB) 874 “Integration and Representation of Sensory processes.”

We would like to thank Claire Sulmont-Rossé for providing us with the odorant ratings obtained in her 2012 study and the authors of the Nencki Affective Picture System for making the pictures available to us. We gratefully acknowledge the help of Jonas Chan in proofreading and Dennis Pomrehn, Lea-Marie Knöppel, Viviane Gallus, and Melanie Stockmann in data acquisition.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the local ethics committee of the Faculty of Psychology.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

12078_2018_9255_MOESM1_ESM.pdf (1011 kb)
ESM 1 (PDF 0.98 MB)

References

  1. Alaoui-Ismaïli O, Robin O, Rada H, Dittmar A, Vernet-Maury E (1997) Basic emotions evoked by odorants. Physiol Behav 62:713–720.  https://doi.org/10.1016/S0031-9384(97)90016-0 CrossRefGoogle Scholar
  2. Baeyens F, Wrzesniewski A, De Houwer J, Eelen P (1996) Toilet rooms, body massages, and smells: two field studies on human evaluative odor conditioning. Curr Psychol 15:77–96.  https://doi.org/10.1007/BF02686936 CrossRefGoogle Scholar
  3. Balch WR, Bowman K, Mohler L (1992) Music-dependent memory in immediate and delayed word recall. Mem Cogn 20:21–28.  https://doi.org/10.3758/BF03208250 CrossRefGoogle Scholar
  4. Bliss-Moreau E, Owren MJ, Barrett LF (2010) I like the sound of your voice: Affective learning about vocal signals. J Exp Soc Psychol 46:557–563.  https://doi.org/10.1016/j.jesp.2009.12.017
  5. Bolders AC, Band GPH, Stallen PJ (2012) Evaluative conditioning induces changes in sound valence. Front Psychol 3:1–12.  https://doi.org/10.3389/fpsyg.2012.00106 CrossRefGoogle Scholar
  6. Bradley MM, Lang PJ (1994) Measuring emotion: the self-assessment manikin and the semantic differential. J Behav Ther Exp Psychiatry 25:49–59.  https://doi.org/10.1016/0005-7916(94)90063-9 CrossRefGoogle Scholar
  7. Bradley MM, Lang PJ (2007) The International Affective Digitized Sounds (2nd Edition; IADS-2): Affective ratings of sounds and instruction manual. University of Florida, GainesvilleGoogle Scholar
  8. Buck LB (2000) Smell and taste: the chemical senses. In: Kandel ER, Schwartz JR, Jessell TM (eds) Principles of neural science. McGraw-Hill, New York, pp 625–652Google Scholar
  9. Cann A, Ross DA (1989) Olfactory stimuli as context cues in human memory. Am J Psychol 102:91.  https://doi.org/10.2307/1423118 CrossRefGoogle Scholar
  10. Chu S (2000) Odour-evoked autobiographical memories: psychological investigations of Proustian phenomena. Chem Senses 25:111–116.  https://doi.org/10.1093/chemse/25.1.111 CrossRefGoogle Scholar
  11. Chu S, Downes JJ (2002) Proust nose best: odors are better cues of autobiographical memory. Mem Cogn 30:511–518.  https://doi.org/10.3758/BF03194952 CrossRefGoogle Scholar
  12. Coppens E, Vansteenwegen D, Baeyens F, Vandenbulcke M, van Paesschen W, Eelen P (2006) Evaluative conditioning is intact after unilateral resection of the anterior temporal lobe in humans. Neuropsychologia 44:840–843.  https://doi.org/10.1016/J.NEUROPSYCHOLOGIA.2005.06.008 CrossRefGoogle Scholar
  13. Cox SM, Andrade A, Johnsrude IS (2005) Learning to like: a role for human orbitofrontal cortex in conditioned reward. J Neurosci 25:2733–2740.  https://doi.org/10.1523/JNEUROSCI.3360-04.2005 CrossRefGoogle Scholar
  14. Dalton P, Maute C, Oshida A et al (2008) The use of semantic differential scaling to define the multidimensional representation of odors. J Sens Stud 23:485–497.  https://doi.org/10.1111/j.1745-459X.2008.00167.x CrossRefGoogle Scholar
  15. de Bruijn MJ, Bender M (2018) Olfactory cues are more effective than visual cues in experimentally triggering autobiographical memories. Memory 26:547–558.  https://doi.org/10.1080/09658211.2017.1381744 CrossRefGoogle Scholar
  16. De Houwer J, Thomas S, Baeyens F (2001) Association learning of likes and dislikes: a review of 25 years of research on human evaluative conditioning. Psychol Bull 127:853–869.  https://doi.org/10.1037/0033-2909.127.6.853 CrossRefGoogle Scholar
  17. Djordjevic J, Lundstrom JN, Clement F et al (2007) A rose by any other name: would it smell as sweet? J Neurophysiol 99:386–393.  https://doi.org/10.1152/jn.00896.2007 CrossRefGoogle Scholar
  18. Domínguez-Borràs J, Garcia-Garcia M, Escera C (2008) Emotional context enhances auditory novelty processing: behavioural and electrophysiological evidence. Eur J Neurosci 28:1199–1206.  https://doi.org/10.1111/j.1460-9568.2008.06411.x CrossRefGoogle Scholar
  19. Doty RL, Cameron EL (2009) Sex differences and reproductive hormone influences on human odor perception. Physiol Behav 97:213–228.  https://doi.org/10.1016/j.physbeh.2009.02.032 CrossRefGoogle Scholar
  20. Frühholz S, Trost W, Kotz SA (2016) The sound of emotions—towards a unifying neural network perspective of affective sound processing. Neurosci Biobehav Rev 68:96–110.  https://doi.org/10.1016/j.neubiorev.2016.05.002 CrossRefGoogle Scholar
  21. Garcia J, Koelling RA (1966) Relation of cue to consequence in avoidance learning. Psychon Sci 4:123–124.  https://doi.org/10.3758/BF03342209 CrossRefGoogle Scholar
  22. Gerdes ABM, Wieser MJ, Alpers GW (2014) Emotional pictures and sounds: a review of multimodal interactions of emotion cues in multiple domains. Front Psychol 5:1–13.  https://doi.org/10.3389/fpsyg.2014.01351 CrossRefGoogle Scholar
  23. Gottfried JA (2008) Perceptual and neural plasticity of odor quality coding in the human brain. Chemosens Percept 1:127–135.  https://doi.org/10.1007/s12078-008-9017-1 CrossRefGoogle Scholar
  24. Gottfried JA, Dolan RJ (2003) The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron 39:375–386.  https://doi.org/10.1016/S0896-6273(03)00392-1 CrossRefGoogle Scholar
  25. Gottfried JA, Zald DH (2005) On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates. Brain Res Rev 50:287–304.  https://doi.org/10.1016/j.brainresrev.2005.08.004 CrossRefGoogle Scholar
  26. Gottfried JA, O'Doherty J, Dolan RJ (2002) Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging. J Neurosci 22:10829–10837.  https://doi.org/10.1523/JNEUROSCI.22-24-10829.2002 CrossRefGoogle Scholar
  27. Groyecka A, Sorokowska A, Oleszkiewicz A, Hummel T, Łysenko K, Sorokowski P (2018) Similarities in smell and taste preferences in couples increase with relationship duration. Appetite 120:158–162.  https://doi.org/10.1016/j.appet.2017.08.035 CrossRefGoogle Scholar
  28. Herz RS (1998) Are odors the best cues to memory? A cross-modal comparison of associative memory stimuli. Ann N Y Acad Sci 855:670–674.  https://doi.org/10.1111/j.1749-6632.1998.tb10643.x CrossRefGoogle Scholar
  29. Herz RS (2004) A naturalistic analysis of autobiographical memories triggered by olfactory visual and auditory stimuli. Chem Senses 29:217–224.  https://doi.org/10.1093/chemse/bjh025 CrossRefGoogle Scholar
  30. Herz RS (2005) Odor-associative learning and emotion: effects on perception and behavior. Chem Senses 30:i250–i251.  https://doi.org/10.1093/chemse/bjh209 CrossRefGoogle Scholar
  31. Herz RS, Cupchik GC (1992) An experimental characterization of odor-evoked memories in humans. Chem Senses 17:519–528.  https://doi.org/10.1093/chemse/17.5.519 CrossRefGoogle Scholar
  32. Herz RS, Cupchik GC (1995) The emotional distinctiveness of odor-evoked memories. Chem Senses 20:517–528.  https://doi.org/10.1093/chemse/20.5.517 CrossRefGoogle Scholar
  33. Herz RS, Schooler J (2002) A naturalistic study of autobiographical and visual evoked by olfactory memories the Proustian cues: testing hypothesis. Am J Psychol 115:21–32.  https://doi.org/10.2307/1423672 CrossRefGoogle Scholar
  34. Herz RS, Beland SL, Hellerstein M (2004a) Changing odor hedonic perception through emotional associations in humansGoogle Scholar
  35. Herz RS, Eliassen J, Beland S, Souza T (2004b) Neuroimaging evidence for the emotional potency of odor-evoked memory. Neuropsychologia 42:371–378.  https://doi.org/10.1016/j.neuropsychologia.2003.08.009 CrossRefGoogle Scholar
  36. Herz RS, Van Reen E, Barker DH et al (2017) The influence of circadian timing on olfactory sensitivity. Chem Senses 00:1–7.  https://doi.org/10.1093/chemse/bjx067 Google Scholar
  37. Hoenen M, Müller K, Pause BM, Lübke KT (2016) Fancy citrus, feel good: positive judgment of citrus odor, but not the odor itself, is associated with elevated mood during experienced helplessness. Front Psychol 7:74.  https://doi.org/10.3389/fpsyg.2016.00074 CrossRefGoogle Scholar
  38. Hofmann W, De Houwer J, Perugini M et al (2010) Evaluative conditioning in humans: a meta-analysis. Psychol Bull 136:390–421.  https://doi.org/10.1037/a0018916 CrossRefGoogle Scholar
  39. Hummel T, Rosenheim K, Konnerth C-G, Kobal G (2001) Screening of olfactory function with a four-minute odor identification test: reliability, normative data, and investigations in patients with olfactory loss. Ann Otol Rhinol Laryngol 110:976–981.  https://doi.org/10.1177/000348940111001015 CrossRefGoogle Scholar
  40. Kassab A, Schaub F, Vent J, Hüttenbrink KB, Damm M (2009) Effects of short inter-stimulus intervals on olfactory and trigeminal event-related potentials. Acta Otolaryngol 129:1250–1256.  https://doi.org/10.3109/00016480802644605 CrossRefGoogle Scholar
  41. Kattner F, Ellermeier W (2011) Does evaluative learning rely on the perception of contingency? Exp Psychol 58:391–399.  https://doi.org/10.1027/1618-3169/a000108 CrossRefGoogle Scholar
  42. Kattner F, Ellermeier W, Tavakoli P (2012) Both trace and delay conditioning of evaluative responses depend on contingency awareness. Learn Motiv 43:35–47.  https://doi.org/10.1016/j.lmot.2012.01.004 CrossRefGoogle Scholar
  43. Keller A, Zhuang H, Chi Q, Vosshall LB, Matsunami H (2007) Genetic variation in a human odorant receptor alters odour perception. Nature 449:468–472.  https://doi.org/10.1038/nature06162 CrossRefGoogle Scholar
  44. Khan RM, Luk C-H, Flinker A, Aggarwal A, Lapid H, Haddad R, Sobel N (2007) Predicting odor pleasantness from odorant structure: pleasantness as a reflection of the physical world. J Neurosci 27:10015–10023.  https://doi.org/10.1523/JNEUROSCI.1158-07.2007 CrossRefGoogle Scholar
  45. Kumar S, von Kriegstein K, Friston K, Griffiths TD (2012) Features versus feelings: dissociable representations of the acoustic features and valence of aversive sounds. J Neurosci 32:14184–14192.  https://doi.org/10.1523/JNEUROSCI.1759-12.2012 CrossRefGoogle Scholar
  46. LeDoux JE, Sakaguchi A, Reis DJ (1984) Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli. J Neurosci 4:683–698CrossRefGoogle Scholar
  47. LeDoux JE, Farb C, Ruggiero DA (1990) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 10:1043–1054CrossRefGoogle Scholar
  48. Levey AB, Martin I (1975) Classical conditioning of human ‘evaluative’ responses. Behav Res Ther 13:221–226.  https://doi.org/10.1016/0005-7967(75)90026-1 CrossRefGoogle Scholar
  49. Lorig TS, Elmes DG, Zald DH, Pardo JV (1999) A computer-controlled olfactometer for fMRI and electrophysiological studies of olfaction. Behav Res Methods Instrum Comput 31:370–375.  https://doi.org/10.3758/BF03207734 CrossRefGoogle Scholar
  50. Lundström JN, McClintock MK, Olsson MJ (2006) Effects of reproductive state on olfactory sensitivity suggest odor specificity. Biol Psychol 71:244–247.  https://doi.org/10.1016/j.biopsycho.2005.07.001 CrossRefGoogle Scholar
  51. Marchewka A, Zurawski L, Jednoróg K, Grabowska A (2014) The Nencki Affective Picture System (NAPS): introduction to a novel, standardized, wide-range, high-quality, realistic picture database. Behav Res Methods 46:596–610.  https://doi.org/10.3758/s13428-013-0379-1 CrossRefGoogle Scholar
  52. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257–332.  https://doi.org/10.1016/S0301-0082(98)00003-3 CrossRefGoogle Scholar
  53. McGaugh JL (2018) Emotional arousal regulation of memory consolidation. Curr Opin Behav Sci 19:55–60.  https://doi.org/10.1016/j.cobeha.2017.10.003 CrossRefGoogle Scholar
  54. Mehrabian A (1970) A semantic space for nonverbal behavior. J Consult Clin Psychol 35:248–257.  https://doi.org/10.1037/h0030083 CrossRefGoogle Scholar
  55. Mehrabian A (1996) Pleasure-arousal-dominance: a general framework for describing and measuring individual differences in temperament. Curr Psychol 14:261–292.  https://doi.org/10.1007/BF02686918 CrossRefGoogle Scholar
  56. Mutschler I, Wieckhorst B, Speck O, Schulze-Bonhage A, Hennig J, Seifritz E, Ball T (2010) Time scales of auditory habituation in the amygdala and cerebral cortex. Cereb Cortex 20:2531–2539.  https://doi.org/10.1093/cercor/bhq001 CrossRefGoogle Scholar
  57. Osgood CE, suci GJ, Tannenbaum PH (1957) The measurement of meaning. In: Illinois Press. England, OxfordGoogle Scholar
  58. Pellegrino R, Sinding C, De Wijk RA, Hummel T (2017) Habituation and adaptation to odors in humans.  https://doi.org/10.1016/j.physbeh.2017.04.006
  59. Pollatos O, Kopietz R, Linn J, Albrecht J, Sakar V, Anzinger A, Schandry R, Wiesmann M (2007) Emotional stimulation alters olfactory sensitivity and odor judgment. Chem Senses 32:583–589.  https://doi.org/10.1093/chemse/bjm027 CrossRefGoogle Scholar
  60. Renfro KJ, Hoffmann H (2013) The relationship between oral contraceptive use and sensitivity to olfactory stimuli. Horm Behav 63:491–496.  https://doi.org/10.1016/j.yhbeh.2013.01.001 CrossRefGoogle Scholar
  61. Robin O, Alaoui-Ismaili O, Dittmar A, Vernet-Mauy E (1999) Basic emotions evoked by eugenol odor differ according to the dental experience. A neurovegetative analysis. Chem Senses 24:327–335.  https://doi.org/10.1093/chemse/24.3.327 CrossRefGoogle Scholar
  62. Royet J, Zald D, Costes N et al (2000) Emotional responses to pleasant and unpleasant olfactory, visual, and auditory stimuli: a positron emission tomography study. 20:7752–7759Google Scholar
  63. Rozin P, Wrzesniewski A, Byrnes D (1998) The elusiveness of evaluative conditioning. Learn Motiv 29:397–415.  https://doi.org/10.1006/lmot.1998.1012 CrossRefGoogle Scholar
  64. Russell JA, Mehrabian A (1977) Evidence for a three-factor theory of emotions. J Res Pers 11:273–294.  https://doi.org/10.1016/0092-6566(77)90037-X CrossRefGoogle Scholar
  65. Schulze P, Bestgen A, Lech RK et al (2017) Preprocessing of emotional visual information in the human piriform cortex. Sci Rep 7:9191.  https://doi.org/10.1038/s41598-017-09295-x CrossRefGoogle Scholar
  66. Seitz H, Bühringer G (2010) Empfehlungen des wissenschaftlichen Kuratoriums der DHS zu Grenzwerten für den Konsum alkoholischer GetränkeGoogle Scholar
  67. Snodgrass JG, Corwin J (1988) Pragmatics of measuring recognition memory: applications to dementia and amnesia. J Exp Psychol Gen 117:34–50.  https://doi.org/10.1037/0096-3445.117.1.34 CrossRefGoogle Scholar
  68. Soudry Y, Lemogne C, Malinvaud D, Consoli SM, Bonfils P (2011) Olfactory system and emotion: common substrates. Eur Ann Otorhinolaryngol Head Neck Dis 128:18–23.  https://doi.org/10.1016/j.anorl.2010.09.007 CrossRefGoogle Scholar
  69. Stevenson RJ (2009) An initial evaluation of the functions of human olfaction. Chem Senses 35:3–20.  https://doi.org/10.1093/chemse/bjp083 CrossRefGoogle Scholar
  70. Sulmont-Rossé C, Issanchou S, Köster E (2002) Selection of odorants for memory tests on the basis of familiarity, perceived complexity, pleasantness, similarity and identification. Chem Senses 27:307–317.  https://doi.org/10.1093/chemse/27.4.307 CrossRefGoogle Scholar
  71. Tartar JL, de Almeida K, McIntosh RC et al (2012) Emotionally negative pictures increase attention to a subsequent auditory stimulus. Int J Psychophysiol 83:36–44.  https://doi.org/10.1016/j.ijpsycho.2011.09.020 CrossRefGoogle Scholar
  72. Toffolo MBJ, Smeets M a M, van den Hout M a (2012) Proust revisited: odours as triggers of aversive memories. Cogn Emot 26:83–92.  https://doi.org/10.1080/02699931.2011.555475 CrossRefGoogle Scholar
  73. van den Bosch I, van Delft JM, de Wijk RA, de Graaf C, Boesveldt S (2015) Learning to (dis)like: the effect of evaluative conditioning with tastes and faces on odor valence assessed by implicit and explicit measurements. Physiol Behav 151:478–484.  https://doi.org/10.1016/j.physbeh.2015.08.017 CrossRefGoogle Scholar
  74. Watkins OC, Watkins MJ (1975) Buildup of proactive inhibition as a cue-overload effect. J Exp Psychol Hum Learn Mem 1:442–452.  https://doi.org/10.1037/0278-7393.1.4.442 CrossRefGoogle Scholar
  75. Willander J, Larsson M (2006) Smell your way back to childhood: autobiographical odor memory. Psychon Bull Rev 13:240–244.  https://doi.org/10.3758/BF03193837 CrossRefGoogle Scholar
  76. Willander J, Larsson M (2007) Olfaction and emotion: the case of autobiographical memory. Mem Cogn 35:1659–1663.  https://doi.org/10.3758/BF03193499 CrossRefGoogle Scholar
  77. Yamashita H, Okamoto Y, Morinobu S, Yamawaki S, Kähkönen S (2005) Visual emotional stimuli modulation of auditory sensory gating studied by magnetic P50 suppression. Eur Arch Psychiatry Clin Neurosci 255:99–103.  https://doi.org/10.1007/s00406-004-0538-6 CrossRefGoogle Scholar
  78. Yeomans MR, Mobini S, Elliman TD, Walker HC, Stevenson RJ (2006) Hedonic and sensory characteristics of odors conditioned by pairing with tastants in humans. J Exp Psychol Anim Behav Process 32:215–228.  https://doi.org/10.1037/0097-7403.32.3.215 CrossRefGoogle Scholar
  79. Zellner DA (2013) Color–odor interactions: a review and model. Chemosens Percept 6:155–169.  https://doi.org/10.1007/s12078-013-9154-z CrossRefGoogle Scholar
  80. Zellner DA, Rozin P, Aron M, Kulish C (1983) Conditioned enhancement of human’s liking for flavor by pairing with sweetness. Learn Motiv 14:338–350.  https://doi.org/10.1016/0023-9690(83)90021-8 CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Institute of Cognitive Neuroscience, Department of Cognitive PsychologyRuhr University BochumBochumGermany
  2. 2.International Graduate School of NeuroscienceRuhr University BochumBochumGermany

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