Advertisement

Retronasal Habituation: Characterization and Impact on Flavor Perception Using Time-Intensity

  • Robert Pellegrino
  • Addison Atchley
  • Simrah Ali
  • Joel Shingleton
  • Curtis R. LuckettEmail author
Article

Abstract

Introduction

Olfactory habituation results from prolonged exposure to an odor, leading to perceptual changes defined by several characteristics. To date, human habituation research has focused on orthonasal olfaction which is perceived externally while ignoring internal routes of odor perception related to flavor. In our study, we conducted two experiments to characterize retronasal olfactory habituation and measured its impact on flavor perception.

Methods

In Experiment 1, participants were presented a food odor and non-food odor retronasally, using an orally adhered strip. Each participant rated the odor intensity using a time-intensity procedure. After exposure, the participants ate a lime-flavored gummy and rated the lime flavor. In experiment 2, the same procedure was performed for a low-level lime odor, a simple (lime oil) and complex (lime oil + sucrose + citric acid) beverage as the flavor stimuli.

Results

Our results demonstrated two known principles of habituation for retronasally presented odors: (1) prolonged exposure leads to decreased perception and (2) weaker stimuli lead to more rapid habituation. Additionally, we found that the non-food odor habituated slower than the food odor; however, the participants seemed to recover simultaneously upon food and beverage consumption leading to no change in flavor perception.

Conclusion

The findings of this study give evidence that we habituate to different odors at different rates; more specifically, we provide evidence that differentiates between odor origin and concentration.

Implications

This is the first time-intensity characterization of retronasal odor habituation. Additionally, a novel method of administering retronasal odors is presented.

Keywords

Habituation Retronasal Odor Flavor Time-Intensity Desensitization 

Notes

Acknowledgements

The authors would like to thank Sara Burns for her work organizing the logistics of the studies.

Author Contributions

C.R.L. and R.P designed the studies, constructed the manuscript and performed the data analysis. J.S., A.A., and S.A. constructed and administered the stimuli and contributed to the manuscript preparation.

Compliance with Ethical Standards

Funding

This study had no direct funding sources.

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

This study was conducted according to the Declaration of Helsinki for studies on human subjects. The protocol used in this study was approved by the Institutional Review Board of the University of Tennessee (Knoxville, TN).

Informed Consent

Before publication, the experimental procedure was explained to all participants and a written informed consent was obtained from each.

References

  1. ASTM International (2017) Standard Guide for Time-Intensity Evaluation of Sensory Attributes. Retrieved from.  https://doi.org/10.1520/E1909-13R17
  2. Berglund B, Engen T (1993) A comparison of self-adaptation and cross-adaptation to odorants presented singly and in mixtures. Perception 22:103–111.  https://doi.org/10.1068/p220103 CrossRefPubMedGoogle Scholar
  3. Bojanowski V, Hummel T (2012) Retronasal perception of odors. Physiol Behav 107:484–487.  https://doi.org/10.1016/j.physbeh.2012.03.001 CrossRefPubMedGoogle Scholar
  4. Cain W (1974) Perception of odor intensity and the time-course of olfactory adaptation. ASHRAE Trans 80:53–75Google Scholar
  5. Cain W, Polak E (1992) Olfactory adaptation as an aspect of odor similarity. Chem Senses 17:481–491.  https://doi.org/10.1093/chemse/17.5.481 CrossRefGoogle Scholar
  6. Chaput MA, Panhuber H (1982) Effects of long duration odor exposure on the unit activity of olfactory bulb cells in awake rabbits. Brain Res 250:41–52.  https://doi.org/10.1016/0006-8993(82)90951-9 CrossRefPubMedGoogle Scholar
  7. Chaput MA, Buonviso N, Berthommier F (1992) Temporal patterns in spontaneous and odour-evoked mitral cell discharges recorded in anaesthetized freely breathing animals. Eur J Neurosci 4:813–822.  https://doi.org/10.1111/j.1460-9568.1992.tb00191.x CrossRefPubMedGoogle Scholar
  8. Dalton P (1996) Odor perception and beliefs about risk. Chem Senses 21:447–458.  https://doi.org/10.1093/chemse/21.4.447 CrossRefPubMedGoogle Scholar
  9. Dalton P (1999) Cognitive influences on health symptoms from acute chemical exposure. Health Psychol 18:579–590CrossRefGoogle Scholar
  10. Dalton P (2000) Psychophysical and behavioral characteristics of olfactory adaptation. Chem Senses 25:487–492.  https://doi.org/10.1093/chemse/25.4.487 CrossRefPubMedGoogle Scholar
  11. Dalton P, Dilks D, Ruberte J (1999) Effects of social cues on perceived odor, irritation and health symptoms from solvent exposure. Proc Abs Annu Meet East Psychol Associ 70:135Google Scholar
  12. de Wijk RA (1989) Temporal factors in human olfactory perception. Doctoral dissertation, University of UtrechtGoogle Scholar
  13. Foster DH (2003) Does colour constancy exist? Trends Cogn Sci. 7(10):439–443CrossRefGoogle Scholar
  14. Gagnon P, Mergler D, Lapare S (1994) Olfactory adaptation, threshold shift and recovery at low levels of exposure to methyl isobutyl ketone (MIBK). Neurotoxicology 15:637–642PubMedGoogle Scholar
  15. Gottfried JA (2010) Central mechanisms of odour object perception. Nat Rev Neurosci 11:628–641.  https://doi.org/10.1038/nrn2883 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Green BG, Dalton P, Cowart B, Shaffer G, Rankin K, Higgins J (1996) Evaluating the “labeled magnitude scale” for measuring sensations of taste and smell. Chem Senses 21:323–334.  https://doi.org/10.1093/chemse/21.3.323 CrossRefPubMedGoogle Scholar
  17. Heilmann S, Hummel T (2004) A new method for comparing orthonasal and retronasal olfaction. Behav Neurosci 118:412–419.  https://doi.org/10.1037/0735-7044.118.2.412 CrossRefPubMedGoogle Scholar
  18. Hummel T, Sekinger B, Wolf SR, Pauli E, 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.  https://doi.org/10.1093/chemse/22.1.39 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hummel T, Seo H-S, Pellegrino R, Heilmann S (2016) Electro-olfactograms in humans in response to ortho- and retronasal chemosensory stimulation. Chemosens Percept 10:1–5.  https://doi.org/10.1007/s12078-016-9217-z CrossRefGoogle Scholar
  20. Kadohisa M, Wilson DA (2006) Olfactory cortical adaptation facilitates detection of odors against background. J Neurophysiol 95:1888–1896.  https://doi.org/10.1152/jn.00812.2005 CrossRefPubMedGoogle Scholar
  21. Kobayashi T, Sakai N, Kobayakawa T, Akiyama S, Toda H, Saito S (2007) Effects of cognitive factors on perceived odor intensity in adaptation/habituation processes: from 2 different odor presentation methods. Chem Senses 33:163–171.  https://doi.org/10.1093/chemse/bjm075 CrossRefPubMedGoogle Scholar
  22. Köster EP, de Wijk RA (1991) Olfactory adaptation. In: Laing DG, Doty RL, Breipohl W (eds) The human sense of smell. Springer, Berlin, Heidelberg, pp 199–215CrossRefGoogle Scholar
  23. Laing DG, Legha PK, Jinks AL, Hutchinson I (2003) Relationship between molecular structure, concentration and odor qualities of oxygenated aliphatic molecules. Chem Senses 28:57–69CrossRefGoogle Scholar
  24. Larson-Powers N, Pangborn RM (1978) Descriptive analysis of the sensory properties of beverages and gelatins containing sucrose or synthetic sweeteners. J Food Sci 43:47–51.  https://doi.org/10.1111/j.1365-2621.1978.tb09733.x CrossRefGoogle Scholar
  25. Leathers TD (2003) Biotechnological production and applications of pullulan. Appl Microbiol Biotechnol 62:468–473.  https://doi.org/10.1007/s00253-003-1386-4 CrossRefPubMedGoogle Scholar
  26. Lim J, Johnson MB (2012) The role of congruency in retronasal odor referral to the mouth. Chem Senses 37:515–522.  https://doi.org/10.1093/chemse/bjs003 CrossRefPubMedGoogle Scholar
  27. Linster C, Henry L, Kadohisa M, Wilson DA (2007) Synaptic adaptation and odor-background segmentation. Neurobiol Learn Mem 87:352–360.  https://doi.org/10.1016/j.nlm.2006.09.011 CrossRefPubMedGoogle Scholar
  28. Mozell MM, Smith BP, Smith PE, Sullivan RL, Swender P (1969) Nasal chemoreception in flavor identification. Arch Otolaryngol Head Neck Surg 90:367–373.  https://doi.org/10.1001/archotol.1969.00770030369020 CrossRefGoogle Scholar
  29. Pellegrino R, Sinding C, de Wijk RA, Hummel T (2017) Habituation and adaptation to odors in humans. Physiol Behav 177:13–19.  https://doi.org/10.1016/j.physbeh.2017.04.006 CrossRefPubMedGoogle Scholar
  30. Philpott CM, Wolstenholme CR, Goodenough PC, Clark A, Murty GE (2008) Olfactory clearance: what time is needed in clinical practice? J Laryngol Otol 122:912–917.  https://doi.org/10.1017/S0022215107000977 CrossRefPubMedGoogle Scholar
  31. Pierce AM, Simons CT (2018) Olfactory adaptation is dependent on route of delivery. Chem Senses 43:197–203.  https://doi.org/10.1093/chemse/bjy007 CrossRefPubMedGoogle Scholar
  32. Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, McSweeney FK, Wilson DA, Wu CF, Thompson RF (2010) Habituation revisited: an updated and revised description of the behavioral characteristics of habituation 92:135–138. doi:  https://doi.org/10.1016/j.nlm.2008.09.012.Habituation
  33. Rozin P (1982) “Taste-smell confusions” and the duality of the olfactory sense. Percept Psychophys 31:397–401.  https://doi.org/10.3758/BF03202667 CrossRefPubMedGoogle Scholar
  34. Schiet FT, Cain WS (1990) Odor intensity of mixed and unmixed stimuli under environmentally realistic conditions. Perception 19:123–132.  https://doi.org/10.1068/p190123 CrossRefPubMedGoogle Scholar
  35. Scott JW, Sherrill L, Jiang J, Zhao K (2014) Tuning to odor solubility and sorption pattern in olfactory epithelial responses. J Neurosci 34:2025–2036.  https://doi.org/10.1523/JNEUROSCI.3736-13.2014 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Sinding C, Valadier F, Al-Hassani V et al (2017) New determinants of olfactory habituation. Sci Rep 7:41047.  https://doi.org/10.1038/srep41047 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Small DM, Voss J, Mak YE, Simmons KB, Parrish T, Gitelman D (2004) Experience-dependent neural integration of taste and smell in the human brain. J Neurophysiol 92:1892–1903CrossRefGoogle Scholar
  38. Small DM, Gerber JC, Mak YE, Hummel T (2005) Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 47:593–605.  https://doi.org/10.1016/j.neuron.2005.07.022 CrossRefPubMedGoogle Scholar
  39. Smith DW, Gamble KR, Heil TA (2010) A novel psychophysical method for estimating the time course of olfactory rapid adaptation in humans. Chem Senses 35:717–725.  https://doi.org/10.1093/chemse/bjq073 CrossRefPubMedGoogle Scholar
  40. Stevenson RJ, Boakes RA, Prescott J (1998) Changes in odor sweetness resulting from implicit learning of a simultaneous odor-sweetness association: an example of learned synesthesia. Learn Motiv 29:113–132.  https://doi.org/10.1006/lmot.1998.0996 CrossRefGoogle Scholar
  41. Stevenson RJ, Prescott J, Boakes RA (1999) Confusing tastes and smells: how odours can influence the perception of sweet and sour tastes. Chem Senses 24:627–635.  https://doi.org/10.1093/chemse/24.6.627 CrossRefPubMedGoogle Scholar
  42. Stone H, Pryor GT, Steinmetz G (1972) A comparison of olfactory adaptation among seven odorants and their relationship with several physicochemical properties. Percept Psychophys 12:501–504.  https://doi.org/10.3758/BF03210944 CrossRefGoogle Scholar
  43. Stuck BA, Fadel V, Hummel T, Sommer JU (2013) Subjective olfactory desensitization and recovery in humans. Chem Senses 39:151–157.  https://doi.org/10.1093/chemse/bjt064 CrossRefPubMedGoogle Scholar
  44. Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16–43CrossRefGoogle Scholar
  45. Todrank J, Wysock CJ, Beauchamp GK (1991) The effects of adaptation on the perception of similar and dissimilar odors. Chem Senses 16:467–482.  https://doi.org/10.1093/chemse/16.5.467 CrossRefGoogle Scholar
  46. Uchida N, Kepecs A, Mainen ZF (2006) Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making. Nat Rev Neurosci 7:485–491.  https://doi.org/10.1038/nrn1933 CrossRefPubMedGoogle Scholar
  47. Welge-Lussen A, Ebnother M, Wolfensberger M, Hummel T (2009) Swallowing is differentially influenced by retronasal compared with orthonasal stimulation in combination with gustatory stimuli. Chem Senses 34:499–502.  https://doi.org/10.1093/chemse/bjp024 CrossRefPubMedGoogle Scholar
  48. Wilson DA (1998) Habituation of odor responses in the rat anterior Piriform cortex. J Neurophysiol 79:1425–1440CrossRefGoogle Scholar
  49. Wilson D (2010) Olfactory adaptation. In: Goldstein EB (ed) Encyclopedia of Perception. SAGE, Thousand Oaks, CA, pp 676–679Google Scholar
  50. Yang GC, Scherer PW, Zhao K, Mozell MM (2007) Numerical modeling of odorant uptake in the rat nasal cavity. Chem Senses 32:273–284.  https://doi.org/10.1093/chemse/bjl056 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Food Science, Institute of AgricultureUniversity of TennesseeKnoxvilleUSA
  2. 2.Smell & Taste Clinic, Department of OtorhinolaryngologyTU DresdenDresdenGermany

Personalised recommendations