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Chemosensory interaction: acquired olfactory impairment is associated with decreased taste function

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Abstract

Olfaction, taste and trigeminal function are three distinct modalities. However, in daily life they are often activated concomitantly. In health and disease, it has been shown that in two of these senses, the trigeminal and olfactory senses, modification of one sense leads to changes in the other sense and vice versa. The objective of the study was to investigate whether and (if so) how, the third modality, taste, is influenced by olfactory impairment. We tested 210 subjects with normal (n = 107) or impaired (n = 103) olfactory function for their taste identification capacities. Validated tests were used for olfactory and gustatory testing (Sniffin’ Sticks, Taste Strips). In an additional experiment, healthy volunteers underwent reversible olfactory cleft obstruction to investigate short-time changes of gustatory function after olfactory alteration. Mean gustatory identification (taste strip score) for the subjects with impaired olfaction was 19.4 ± 0.6 points and 22.9 ± 0.5 points for those with normal olfactory function (t = 4.6, p < 0.001). The frequencies of both, smell and taste impairments interacted significantly (Chi2, F = 16.4, p < 0.001), and olfactory and gustatory function correlated (r 210 = 0.30, p < 0.001). Neither age nor olfactory impairment cause effects interfered with this olfactory–gustatory interaction. In contrast, after short-lasting induced olfactory decrease, gustatory function remained unchanged. The present study suggests that longstanding impaired olfactory function is associated with decreased gustatory function. These findings seem to extend previously described mutual chemosensory interactions also to smell and taste. It further raises the question whether chemical senses in general decrease mutually after acquired damage.

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References

  1. Albrecht J, Kopietz R, Frasnelli J, Wiesmann M, Hummel T, Lundstrom JN (2010) The neuronal correlates of intranasal trigeminal function—an ALE meta-analysis of human functional brain imaging data. Brain Res Rev 62(2):183–196

    Google Scholar 

  2. Buchel C, Price C, Frackowiak RS, Friston K (1998) Different activation patterns in the visual cortex of late and congenitally blind subjects. Brain 121(Pt 3):409–419

    Article  PubMed  Google Scholar 

  3. Cain WS (1974) Contribution of the trigeminal nerve to perceived odor magnitude. Ann N Y Acad Sci 237:28–34

    Article  CAS  PubMed  Google Scholar 

  4. Cain WS, Murphy CL (1980) Interaction between chemoreceptive modalities of odour and irritation. Nature 284:255–257

    Article  CAS  PubMed  Google Scholar 

  5. Collignon O, Voss P, Lassonde M, Lepore F (2009) Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects. Exp Brain Res 192:343–358

    Article  PubMed  Google Scholar 

  6. Cruz A, Green BG (2000) Thermal stimulation of taste. Nature 403:889–892

    Article  CAS  PubMed  Google Scholar 

  7. Dalton P, Doolittle N, Nagata H, Breslin PA (2000) The merging of the senses: integration of subthreshold taste and smell. Nat Neurosci 3:431–432

    Article  CAS  PubMed  Google Scholar 

  8. Doty RL, Bartoshuk LM, Snow JBJ (1991) Causes of olfactory and gustatory disorders. In: Getchell TV, Doty RL, Bartoshuk LM, Snow JBJ (eds) Smell and taste in health and disease. Raven Press, New York, pp 449–462

    Google Scholar 

  9. Doty RL, Shah M, Bromley SM (2008) Drug-induced taste disorders. Drug Saf 31:199–215

    Article  CAS  PubMed  Google Scholar 

  10. Finger TE, Bottger B, Hansen A, Anderson KT, Alimohammadi H, Silver WL (2003) Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc Natl Acad Sci USA 100:8981–8986

    Article  CAS  PubMed  Google Scholar 

  11. Fortis-Santiago Y, Rodwin BA, Neseliler S, Piette CE, Katz DB (2010) State dependence of olfactory perception as a function of taste cortical inactivation. Nat Neurosci 13:158–159

    Article  CAS  PubMed  Google Scholar 

  12. Frasnelli J, Schuster B, Hummel T (2007) Subjects with congenital anosmia have larger peripheral but similar central trigeminal responses. Cereb Cortex 17:370–377

    Article  CAS  PubMed  Google Scholar 

  13. Gilliland AR (1921) The taste sensitivity of an anosmic subject. J Exp Psychol 4:318–326

    Article  Google Scholar 

  14. Gulbransen B, Silver W, Finger TE (2008) Solitary chemoreceptor cell survival is independent of intact trigeminal innervation. J Comp Neurol 508:62–71

    Article  PubMed  Google Scholar 

  15. Hasan KS, Reddy SS, Barsony N (2007) Taste perception in Kallmann syndrome, a model of congenital anosmia. Endocr Pract 13:716–720

    PubMed  Google Scholar 

  16. Heckmann JG, Stossel C, Lang CJ, Neundorfer B, Tomandl B, Hummel T (2005) Taste disorders in acute stroke: a prospective observational study on taste disorders in 102 stroke patients. Stroke 36:1690–1694

    Article  PubMed  Google Scholar 

  17. Hummel T, Barz S, Lotsch J, Roscher S, Kettenmann B, Kobal G (1996) Loss of olfactory function leads to a decrease of trigeminal sensitivity. Chem Senses 21:75–79

    Article  CAS  PubMed  Google Scholar 

  18. Hummel T, Kobal G, Gudziol H, Mackay-Sim A (2007) Normative data for the “Sniffin’ Sticks” including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur Arch Otorhinolaryngol 264:237–243

    Article  CAS  PubMed  Google Scholar 

  19. Iannilli E, Del Gratta C, Gerber JC, Romani GL, Hummel T (2008) Trigeminal activation using chemical, electrical, and mechanical stimuli. Pain 139:376–388

    Article  CAS  PubMed  Google Scholar 

  20. Kobal G, Hummel C (1988) Cerebral chemosensory evoked potentials elicited by chemical stimulation of the human olfactory and respiratory nasal mucosa. Electroencephalogr Clin Neurophysiol 71:241–250

    Article  CAS  PubMed  Google Scholar 

  21. Kobal G, Klimek L, Wolfensberger M, Gudziol H, Temmel A, Owen CM, Seeber H, Pauli E, Hummel T (2000) Multicenter investigation of 1, 036 subjects using a standardized method for the assessment of olfactory function combining tests of odor identification, odor discrimination, and olfactory thresholds. Eur Arch Otorhinolaryngol 257:205–211

    Article  CAS  PubMed  Google Scholar 

  22. Landis BN, Hummel T, Lacroix JS (2005) Basic and clinical aspects of olfaction. Adv Tech Stand Neurosurg 30:69–105

    Article  CAS  PubMed  Google Scholar 

  23. Landis BN, Welge-Luessen A, Bramerson A, Bende M, Mueller CA, Nordin S, Hummel T (2009) “Taste Strips”—a rapid, lateralized, gustatory bedside identification test based on impregnated filter papers. J Neurol 256:242–248

    Article  PubMed  Google Scholar 

  24. Merabet LB, Hamilton R, Schlaug G, Swisher JD, Kiriakopoulos ET, Pitskel NB, Kauffman T, Pascual-Leone A (2008) Rapid and reversible recruitment of early visual cortex for touch. PLoS One 3:e3046

    Article  PubMed  Google Scholar 

  25. Mueller C, Kallert S, Renner B, Stiassny K, Temmel AF, Hummel T, Kobal G (2003) Quantitative assessment of gustatory function in a clinical context using impregnated “taste strips”. Rhinology 41:2–6

    CAS  PubMed  Google Scholar 

  26. Pfaar O, Landis BN, Frasnelli J, Huttenbrink KB, Hummel T (2006) Mechanical obstruction of the olfactory cleft reveals differences between orthonasal and retronasal olfactory functions. Chem Senses 31:27–31

    Article  PubMed  Google Scholar 

  27. Rolls ET (2005) Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiol Behav 85:45–56

    Article  CAS  PubMed  Google Scholar 

  28. Rolls ET, Baylis LL (1994) Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J Neurosci 14:5437–5452

    CAS  PubMed  Google Scholar 

  29. Schaefer ML, Bottger B, Silver WL, Finger TE (2002) Trigeminal collaterals in the nasal epithelium and olfactory bulb: a potential route for direct modulation of olfactory information by trigeminal stimuli. J Comp Neurol 444:221–226

    Article  PubMed  Google Scholar 

  30. Shepherd GM (2006) Smell images and the flavour system in the human brain. Nature 444:316–321

    Article  CAS  PubMed  Google Scholar 

  31. Small DM, Jones-Gotman M, Zatorre RJ, Petrides M, Evans AC (1997) Flavor processing: more than the sum of its parts. Neuroreport 8:3913–3917

    Article  CAS  PubMed  Google Scholar 

  32. Todrank J, Bartoshuk LM (1991) A taste illusion: taste sensation localized by touch. Physiol Behav 50:1027–1031

    Article  CAS  PubMed  Google Scholar 

  33. Vennemann MM, Hummel T, Berger K (2008) The association between smoking and smell and taste impairment in the general population. J Neurol 255:1121–1126

    Article  PubMed  Google Scholar 

  34. Voss P, Lassonde M, Gougoux F, Fortin M, Guillemot JP, Lepore F (2004) Early- and late-onset blind individuals show supra-normal auditory abilities in far-space. Curr Biol 14:1734–1738

    Article  CAS  PubMed  Google Scholar 

  35. Whitehead MC, Beeman CS, Kinsella BA (1985) Distribution of taste and general sensory nerve endings in fungiform papillae of the hamster. Am J Anat 173:185–201

    Article  Google Scholar 

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Acknowledgments

We would like to thank Gerd Kobal, Stefan Kallert and Christian Mueller for their helpful advice concerning production and use of the “Taste Strips”. The study was supported by a Grant of the Swiss National Fund for Scientific Research [SSMBS grant no. PASMA-119579/1] to BNL. Parts of this work have been published previously as Abstract (see Hummel et al., Chemical Senses 2001, 26, 1118).

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Authors and Affiliations

  1. Smell and Taste Clinic, Department of Otorhinolaryngology, University of Dresden Medical School, Technische Universität Dresden, Fetscherstrasse 74, 01307, Dresden, Germany

    Basile N. Landis, Mandy Scheibe, Cornelia Weber, Robert Berger & Thomas Hummel

  2. Division of Otorhinolaryngology-Head and Neck Surgery, Department of Clinical Neurosciences, Geneva Neuroscience Center, University of Geneva Medical School, Geneva, Switzerland

    Basile N. Landis

  3. Department of Otorhinolaryngology, Central Hospital, Skövde, Sweden

    Annika Brämerson & Mats Bende

  4. Department of Psychology, University of Umea, Umeå, Sweden

    Steven Nordin

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  1. Basile N. Landis
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  2. Mandy Scheibe
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  3. Cornelia Weber
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  8. Thomas Hummel
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Correspondence to Basile N. Landis.

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Landis, B.N., Scheibe, M., Weber, C. et al. Chemosensory interaction: acquired olfactory impairment is associated with decreased taste function. J Neurol 257, 1303–1308 (2010). https://doi.org/10.1007/s00415-010-5513-8

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  • DOI: https://doi.org/10.1007/s00415-010-5513-8

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