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Retronasal perception of odors
Physiology & Behavior 107 (2012) 484–487
Contents lists available at SciVerse ScienceDirect
Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Retronasal perception of odors Viola Bojanowski, Thomas Hummel ⁎ Smell and Taste Clinic, Department of Otorhinolaryngology, Technical University of Dresden Medical School, Fetscherstrasse 74, 01307 Dresden, Germany
a r t i c l e Keywords: Nose Smell Taste Flavor
i n f o
a b s t r a c t We perceive odors orthonasally during sniffing; in contrast, we perceive odors retronasally during eating when they enter the nose through the pharynx. There are clear differences between orthonasal and retronasal olfaction in neuronal processing and perception, so that these two pathways convey two distinct sensory signals. The perception of foods is based on the interaction between ortho- and retronasal smell, taste, trigeminal activation and texture, so it is difficult to investigate one of these factors in isolation. Specific clinical aspects include effects of retronasal olfaction on satiation and swallowing. © 2012 Elsevier Inc. All rights reserved.
1. Introduction Odors reach the olfactory epithelium by two pathways: via the nostrils, during sniffing, and via the mouth, during eating or drinking (Fig. 1). These two pathways are referred to as orthonasal and retronasal olfaction [1,2]. As retronasal sensations are frequently referred to as ‘taste’ so that smell–taste confusions have been described frequently (e.g., [3,4]). In fact, when people lose their sense of smell they would often describe their smell loss as a ‘loss of taste function’ [5]. In addition, the smell–taste confusions are so profound that there are even languages (e.g., Swiss German) that do not have a proper word for ‘smelling’ but largely refer to it as ‘tasting’. This is despite the fact that there are major differences between orthonasal and retronasal perception of odors, which are also reflected in the different cortical processing of ortho- or retronasal activation.
2. Various methods to investigate retronasal olfaction There are diverse psychophysical, electrophysiological, and imaging methods to test retronasal olfaction function. They allow to examine deficits in retronasal olfactory function, differences to orthonasal olfaction, interactions with other senses, and the clinical aspects of retronasal olfaction. Psychophysical tests to explore retronasal olfactory function include, for example, flavor identification tests like the “taste powders” (Schmeckpulver; Fig. 2)” or the “candy smell test” (CST). Taste powders are a test kit with 20 grocery-available foods. The powders are administered to the middle of the tongue by using squeezable plastic vials. Using a multiple forced choice procedure, subjects are asked to identify the “taste” then from a list of one of four items [6]. The CST ⁎ Corresponding author at: Tel.: + 49 351 458 4189; fax: + 49 351 458 7130. E-mail address: [email protected] (T. Hummel). 0031-9384/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2012.03.001
addresses the retronasal application of odors, typical for food aroma effects during mastication and swallowing [7]. Both tests are easy to handle; they are reliable methods for the clinical routine. In order to investigate differences between orthonasal and retronasal perception of odors, presentation of odorous stimuli is a key issue. Halpern pointed out that ortho- and retronasal stimuli should reach the olfactory mucosa by the two distinct pathways, without producing additional gustatory or mechanical stimuli [8]. Thus, studies based on the application of liquid or solid stimuli to the oral cavity cannot allow direct comparisons to stimuli that are presented in front of the nose, simply because the oral administration of odors may produce gustatory, thermal, and mechanical sensations which may interact with olfactory mediated sensations [9,10]. To avoid this situation, some researchers placed odors in containers presented to the oral cavity (e.g. [11]), while others asked subjects to sniff the headspace of an odorous liquid or inhale the same headspace through the mouth followed by nasal exhalation [12] (cf. [13,14]). The perception of retronasal olfaction starts milliseconds after expiration onset [15]. A major limitation of these methods is the unknown odor concentration in the oral cavity and the mechanical stimulation of intraoral surfaces [10]. To allow for a more defined retronasal stimulation, a device was developed [16] which allows the release of odors directly into the epipharynx above the soft palate. This avoids concomitant oral gustatory, thermal and mechanical stimulation, thus permitting the study of ortho- or retronasal olfaction in isolation. Two plastic tubes are placed in the nasal cavity under endoscopic control such that the opening of one of the tubes is just beyond the nasal valve and the opening of the other tube is in the epipharynx. For stimulus presentation, the tubes are connected to outlets of a computer-controlled air-dilution olfactometer. Mechanical stimulation is avoided by embedding the stimuli into a constant flow of odorless, humidified air of controlled temperature [17]. Odors presented through either tube reach the olfactory epithelium at approximately the same concentration and with the same time course [18].
V. Bojanowski, T. Hummel / Physiology & Behavior 107 (2012) 484–487
Fig. 1. There are two pathways for odors to reach the olfactory epithelium. The orthonasal red route is used during sniffing, for example, to identify odors like rose, smoke, or other odorants in the environment. Through the retronasal blue route the flavor of foods can be perceived.
3. Differences between orthonasal and retronasal olfaction Results from psychophysical, electrophysiological, and imaging studies suggest that there are clear differences in the perception and processing of ortho- and retronasal stimuli. Food odors may produce different sensations when presented in front of the nose or intraorally, when eaten, e.g., cheeses, coffee, or flowery odors like lavender. There are numerous possible reasons for these phenomena. Differences in airflow patterns are thought to contribute to perceptual differences between ortho- and retronasal presentation of odors [19]; in fact, the direction of odor movement across the olfactory epithelium could lead to differences in the processing of odorous information. This hypothesis is supported by work emphasizing the significance of nasal airflow on the perception of odors [20–24]. Differences between ortho- and retronasal olfactory functions are also emphasized by differences in the salivary response if an odor is repeatedly presented. The response decreases until a new food odor
485
is presented. The same effect is found if the route of administration is changed from orthonasal to retronasal or vice versa. Thus, presenting the same odor via different pathways represents a distinct sensory signal which can also be shown on a behavioral level [25]. With regard to this findings it is no surprise that there are patients with an isolated smell deficit only for one route of olfaction whereas the other route shows normal function. Better retronasal than orthonasal olfactory function, meaning impaired smell with preserved flavor perception, has been reported in patients with nasal polyposis [28]. This is thought to be related, at least in part, to the presence of mechanical obstruction in the anterior portion of the olfactory cleft [29], whereas odors could still reach the olfactory epithelium through the retronasal route. In addition, orthonasal olfactory loss with little or no changes in retronasal odor perception has been reported even in the absence of nasal polyposis (e.g. [30,31]). There were also studies which have described a retronasal smell loss in the absence of orthonasal deficits. [26,27]. Orthonasal and retronasal olfaction differ in terms of threshold, rated odor intensity, ability to localize an odor, and the neuronal processing of either signal. Thresholds to orthonasal stimuli are typically lower compared to retronasal thresholds [12]. On a suprathreshold level it has also been reported [32] that the ability to identify odors is less efficient when stimuli are presented retronasally [14]. Using olfactory threshold measurements, greater impairment has been reported for retronasal than for orthonasal perception in elderly people [13]. Numerous studies indicate that olfactory stimuli cannot be lateralized when the stimulus is applied to one of the two nostrils [33,34]. Interestingly, subjects are able to localize ortho- and retronasal presentation of an odorant. As expected, the trigeminal stimulus CO2 can be localized and lateralized, but also the pure olfactory stimuli H2S and in most cases PEA, a rose-like odorant, cannot be lateralized but are clearly localizable [35]. Cortical responses reflect differences between ortho- and retronasal stimuli. EEG-derived event-related potentials indicated that, when an odorant unrelated to food (e.g., lavender) was presented in a contextually unusual site, i.e. retronasally, the response was larger compared to the presentation of the same odorant at an orthonasal site [36]. This was the other way around for a food-related odor (e.g., chocolate). These findings clearly indicate contextual differences of information processing depending on the route of odor presentation. Orthonasal and retronasal stimuli produce different patterns of brain activation. Specifically, imaging techniques like functional
Fig. 2. Taste powders (“Schmeckpulver”) – photograph of the psychophysical investigation of retronasal olfactory perception. Powders like cacao, paprika or garlic are applied to the middle of the tongue. Subjects have to select one of four items that best describes the flavor (Heilmann et al. 2002).
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V. Bojanowski, T. Hummel / Physiology & Behavior 107 (2012) 484–487
magnetic resonance imaging (fMRI) allow to investigate differences between ortho- and retronasal olfactory activation at a cerebral level [37,38]. Activation due to retronasal stimulation was found at the base of the central sulcus, corresponding to the primary representation of the oral cavity [39], possibly reflecting that retronasal odors are referred to the mouth. Small and colleagues reported activation in different brain areas in response to taste and orthonasally/retronasally presented stimuli [40,41]. They observed deactivation in the orbitofrontal cortex, insula, and anterior cingulate cortex for taste-orthonasal stimulus association, and supra-additive responses at the same regions for the combination of taste and retronasal stimuli. These results clearly indicate that the neural processing of an odor is influenced by route of administration. 4. Interactions between retronasal olfaction and gustatory / tactile influences During oral processing of foods and swallowing the senses interact in a non-linear way. This means that texture or taste of foods influences the perception of odors (e.g. [42–44]. For example, retronasally applied odor of benzaldehyde (smell of almonds/marzipan) is enhanced by the sweet taste of sucrose. This is not the case if the stimulus is a different, contextually incongruent taste, like water or umami [45]. In contrast, there seems to be a relatively weaker enhancement of taste by odors [46]. Faster processing of an olfactory stimulus was induced by an incongruent simultaneous taste. For example there were shorter latencies of EEG-derived olfactory eventrelated potentials in the combination “vanilla odor and sour taste” compared to “vanilla odor and sweet taste” [47]. With regard to the trigeminal activation induced by most odorants [49] there is also the possibility that the interaction between the trigeminal and the olfactory system relates to the differential perception of ortho- and retronasal stimuli [50–52]. To be specific, there is evidence indicating that the sensitivity for chemosensory stimuli is higher in the anterior compared to the posterior portion of the nose while this is the other way around for mechanical stimuli [53] (but see also [54]). Results obtained by Visschers et al. [55] suggest that the intensity of aroma decreased with increasing consistency of the consumed food. In addition, it has been shown that retronasal odorous stimuli increase the intensities of thickness and creaminess of oral stimuli [56]. Importantly, this interaction was strongest when the presentation of the odor coincided with swallowing indicating that also temporal issues feed into the interaction between these sensory channels. These details help to explain some interesting findings how the senses influence each other, with most interactions taking place in the central nervous system. It is important to note that context plays a very strong role in the perception of foods. If a fruit does not have the expected taste or texture, this food probably is not eaten. The tight interaction between the various sensory channels also becomes clear when we describe odors with terms of taste qualities with these taste-like qualities of odors probably being learned [48]. 5. Clinical aspects of retronasal olfaction As an interesting aspect regarding the biological role of retronasal odor perception, recent work suggests that perceived satiation is modulated by the extent of retronasal aroma release. The extent of aroma release depends on personal and product differences. People differ in oral processing, bite size, duration of processing and meal duration. Small bite sizes and longer duration of oral processing favor a higher aroma release. Product properties like solid consistency, a high protein percentage and a multi-component aroma may also enhance satiation which, in turn could prevent consumers from overeating (reviewed in [57]).
Another clinical aspect is the swallowing inducing effect of retronasal stimulation. Retronasal stimulation seems to facilitate swallowing. Compared to orthonasal stimulation swallowing occurs significantly faster and more frequently when odors are presented retronasally [58]. Other factors with a modulating effect on swallowing include bolus size, texture, orthonasally presented odors, saliva or muscular abilities. At the moment retronasal stimulation is only one possibility to trigger the swallowing reflex. But still, it may become a clinical option to coordinate swallowing, aiming to prevent aspiration, for example in stroke patients with swallowing disorders (review by [59]). References [1] Rozin P. "Taste–smell confusions" and the duality of the olfactory sense. Percept Psychophys 1982;31:397–401. [2] Shepherd GM. Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Ann N Y Acad Sci 2007;1121:87–101. [3] Murphy C, Cain WS. Taste and olfaction: independence vs interaction. Physiol Behav 1980;24:601–5. [4] Murphy C, Cain WS, Bartoshuk LM. Mutual action of taste and olfaction. Sens Processes 1977;1:204–11. [5] Deems DA, Doty RL, Settle RG, Moore-Gillon V, Shaman P, Mester AF, et al. Smell and taste disorders, a study of 750 patients from the University of Pennsylvania Smell and Taste Center. Arch Otolaryngol Head Neck Surg 1991;117:519–28. [6] Heilmann S, Strehle G, Rosenheim K, Damm M, Hummel T. Clinical assessment of retronasal olfactory function. Arch Otolaryngol Head Neck Surg 2002;128:414–8. [7] Haxel BR, Bertz-Duffy S, Faldum A, Trellakis S, Stein B, Renner B. et al The Candy Smell Test in clinical routine. Am J Rhinol Allergy 2011;25:e145–8. [8] Halpern BP. Retronasal and orthnasal smelling. Chemo Sense 2004;6:1–7. [9] Welge-Lussen A, Drago J, Wolfensberger M, Hummel T. Gustatory stimulation influences the processing of intranasal stimuli. Brain Res 2005;1038:69–75. [10] Land DG. Perspectives on the effects of interactions on flavor perception: an overview. In: McGorrin RJ, Leland J, editors. Flavor–Food Interactions. Washington D.C: ACS Symposium Series; 1994. p. 2–11. [11] Sun BC, Halpern BP. Identification of air phase retronasal and orthonasal odorant pairs. Chem Senses 2005;30:693–706. [12] Voirol E, Daget M. Comparative study of nasal and retronasal olfactory perception. Food Sci Technol 1986;19:316–9. [13] Duffy VB, Cain WS, Ferris AM. Measurement of sensitivity to olfactory flavor: application in a study of aging and dentures. Chem Senses 1999;24:671–7. [14] Burdach KJ, Kroeze JH, Koster EP. Nasal, retronasal, and gustatory perception: an experimental comparison. Percept Psychophys 1984;36:205–8. [15] Masaoka Y, Satoh H, Akai L, Homma I. Expiration: the moment we experience retronasal olfaction in flavor. Neurosci Lett 2010;473:92–6. [16] Heilmann S, Hummel T. A new method for comparing orthonasal and retronasal olfaction. Behav Neurosci 2004;118:412–9. [17] Kobal G. Elektrophysiologische Untersuchungen des menschlichen Geruchssinns Stutgart: Thieme Verlag; 1981. [18] Small DM, Prescott J. Odor/taste integration and the perception of flavor. Exp Brain Res 2005;166:345–57. [19] Mozell MM. Evidence for sorption as a mechanism of the olfactory analysis of vapours. Nature 1964;203:1181–2. [20] Leopold DA. The relationship between nasal anatomy and human olfaction. Laryngoscope 1988;98:1232–8. [21] Sobel N, Khan RM, Saltman A, Sullivan EV, Gabrieli JD. The world smells different to each nostril. Nature 1999;402:35. [22] Damm M, Vent J, Schmidt M, Theissen P, Eckel HE, Lotsch J, et al. Intranasal volume and olfactory function. Chem Senses 2002;27:831–9. [23] Kubie J, Mackay-Sim A, Moulton DG. Inherent spatial patterning of respoinses to odorants in the salamander olfactory epithelium. In: Scott JW, Acevedo HP, Sherrill L, Phan M, Van der Starre H, editors. Olfaction and Taste VII. London: IRL Press Ltd; 1980. p. 163–6. [24] Scott JW, Acevedo HP, Sherrill L, Phan M. Responses of the rat olfactory epithelium to retronasal air flow. J Neurophysiol 2007;97:1941–50. [25] Bender G, Hummel T, Negoias S, Small DM. Separate signals for orthonasal vs. retronasal perception of food but not nonfood odors. Behav Neurosci 2009;123:481–9. [26] Cowart BJ, Halpern BP, Varga EK. A clinical Test of retronasal olfactory function. Chem Senses 1999;24:608. [27] Cowart BJ, Halpern BP, Rosen D, klock CT, Pribitkin ED. Differential loss of retronasal relative to orthonasal olfaction in a clinical population. Chem Senses 2003: A65. [28] Landis BN, Giger R, Ricchetti A, Leuchter I, Hugentobler M, Hummel T, et al. Retronasal olfactory function in nasal polyposis. Laryngoscope 2003;113:1993–7. [29] Pfaar O, Landis BN, Frasnelli J, Huttenbrink KB, Hummel T. Mechanical obstruction of the olfactory cleft reveals differences between orthonasal and retronasal olfactory functions. Chem Senses 2006;31:27–31. [30] Ogle W. Anosmia, or cases illustrating the physiology and pathology of the sense of smell. Med Chir Trans 1870;53:263–90. [31] Cerf-Ducastel B, Murphy C. fMRI activation in response to odorants orally delivered in aqueous solutions. Chem Senses 2001;26:625–37. [32] Pierce J, Halpern BP. Orthonasal and retronasal odorant identification based upon vapor phase input from common substances. Chem Senses 1996;21:529–43.
V. Bojanowski, T. Hummel / Physiology & Behavior 107 (2012) 484–487 [33] von Skramlik E. Über die Lokalisation der Empfindungen bei den niederen Sinnen. Zeitschrift für Sinnesphysiologie 1924;56:69. [34] Porter J, Anand T, Johnson B, Khan RM, Sobel N. Brain mechanisms for extracting spatial information from smell. Neuron 2005;47:581–92. [35] Hummel T. Retronasal perception of odors. Chem Biodivers 2008;5:853–61. [36] Hummel T, Heilmann S. Olfactory event-related potentials in response to orthoand retronasal stimulation with odors related or unrelated to foods. Int Dairy J 2008;18:874–8. [37] Small DM, Gerber JC, Mak YE, Hummel T. Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 2005;47: 593–605. [38] Small DM, Zatorre RJ, Jones-Gotman M. Increased intensity perception of aversive taste following right anteromedial temporal lobe removal in humans. Brain 2001;124:1566–75. [39] Yamashita H, Kumamoto Y, Nakashima T, Yamamoto T, Inokuchi A, Komiyama S. Magnetic sensory cortical responses evoked by tactile stimulations of the human face, oral cavity and flap reconstructions of the tongue. Eur Arch Otorhinolaryngol 1999;256(Suppl. 1):S42–6. [40] Small DM, Jones-Gotman M, Zatorre RJ, Petrides M, Evans AC. Flavor processing: more than the sum of its parts. Neuroreport 1997;8:3913–7. [41] Small DM, Voss J, Mak YE, Simmons KB, Parrish T, Gitelman D. Experience-dependent neural integration of taste and smell in the human brain. J Neurophysiol 2004;92: 1892–903. [42] Stevenson RJ, Prescott J, Boakes RA. Confusing tastes and smells: how odours can influence the perception of sweet and sour tastes. Chem Senses 1999;24:627–35. [43] Hollowood TA, Linforth RS, Taylor AJ. The effect of viscosity on the perception of flavour. Chem Senses 2002;27:583–91. [44] Weel KG, Boelrijk AE, Alting AC, Van Mil PJ, Burger JJ, Gruppen H, et al. Flavor release and perception of flavored whey protein gels: perception is determined by texture rather than by release. J Agric Food Chem 2002;50:5149–55. [45] Dalton P, Doolittle N, Nagata H, Breslin PA. The merging of the senses: integration of subthreshold taste and smell. Nat Neurosci 2000;3:431–2. [46] Green BG, Nachtigal D, Hammond S, Lim J. Enhancement of retronasal odors by taste. Chem Senses 2012;37:77–86.
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[47] Welge-Lussen A, Husner A, Wolfensberger M, Hummel T. Influence of simultaneous gustatory stimuli on orthonasal and retronasal olfaction. Neurosci Lett 2009;454:124–8. [48] Gautam SH, Verhagen JV. Evidence that the sweetness of odors depends on experience in rats. Chem Senses 2010;35:767–76. [49] Elsberg CA, Levy I, Brewer ED. A new method for testing the sense of smell and for the establishment of olfactory values of odorous substances. Science 1936;83: 211–2. [50] Cain WS, Murphy CL. Interaction between chemoreceptive modalities of odour and irritation. Nature 1980;284:255–7. [51] Hummel T, Livermore A. Intranasal chemosensory function of the trigeminal nerve and aspects of its relation to olfaction. Int Arch Occup Environ Health 2002;75:305–13. [52] Frasnelli J, Hummel T. Interactions between the chemical senses: trigeminal function in patients with olfactory loss. Int J Psychophysiol 2007;65:177–81. [53] Frasnelli J, Heilmann S, Hummel T. Responsiveness of human nasal mucosa to trigeminal stimuli depends on the site of stimulation. Neurosci Lett 2004;362:65–9. [54] Melzner J, Bitter T, Guntinas-Lichius O, Gottschall R, Walther M, Gudziol H. Comparison of the orthonasal and retronasal detection thresholds for carbon dioxide in humans. Neurosci Lett 2011;36:435–41. [55] Visschers RW, Jacobs MA, Frasnelli J, Hummel T, Burgering M, Boelrijk AE. Crossmodality of texture and aroma perception is independent of orthonasal or retronasal stimulation. J Agric Food Chem 2006;54:5509–15. [56] Bult JH, de Wijk RA, Hummel T. Investigations on multimodal sensory integration: texture, taste, and ortho- and retronasal olfactory stimuli in concert. Neurosci Lett 2007;411:6–10. [57] Ruijschop RM, Boelrijk AE, de Graaf C, Westerterp-Plantenga MS. Retronasal aroma release and satiation: a review. J Agric Food Chem 2009;57:9888–94. [58] Welge-Lussen A, Ebnother M, Wolfensberger M, Hummel T. Swallowing is differentially influenced by retronasal compared with orthonasal stimulation in combination with gustatory stimuli. Chem Senses 2009;34:499–502. [59] Ryan C, Hummel T. Principles of deglutition: a multidisciplinary text for swallowing and its disorders and manual of diagnostic and therapeutic techniques for disorders of deglutition. In: Shaker RPG, Belafsky P, Easterling C, editors. in press.
Contents lists available at SciVerse ScienceDirect
Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Retronasal perception of odors Viola Bojanowski, Thomas Hummel ⁎ Smell and Taste Clinic, Department of Otorhinolaryngology, Technical University of Dresden Medical School, Fetscherstrasse 74, 01307 Dresden, Germany
a r t i c l e Keywords: Nose Smell Taste Flavor
i n f o
a b s t r a c t We perceive odors orthonasally during sniffing; in contrast, we perceive odors retronasally during eating when they enter the nose through the pharynx. There are clear differences between orthonasal and retronasal olfaction in neuronal processing and perception, so that these two pathways convey two distinct sensory signals. The perception of foods is based on the interaction between ortho- and retronasal smell, taste, trigeminal activation and texture, so it is difficult to investigate one of these factors in isolation. Specific clinical aspects include effects of retronasal olfaction on satiation and swallowing. © 2012 Elsevier Inc. All rights reserved.
1. Introduction Odors reach the olfactory epithelium by two pathways: via the nostrils, during sniffing, and via the mouth, during eating or drinking (Fig. 1). These two pathways are referred to as orthonasal and retronasal olfaction [1,2]. As retronasal sensations are frequently referred to as ‘taste’ so that smell–taste confusions have been described frequently (e.g., [3,4]). In fact, when people lose their sense of smell they would often describe their smell loss as a ‘loss of taste function’ [5]. In addition, the smell–taste confusions are so profound that there are even languages (e.g., Swiss German) that do not have a proper word for ‘smelling’ but largely refer to it as ‘tasting’. This is despite the fact that there are major differences between orthonasal and retronasal perception of odors, which are also reflected in the different cortical processing of ortho- or retronasal activation.
2. Various methods to investigate retronasal olfaction There are diverse psychophysical, electrophysiological, and imaging methods to test retronasal olfaction function. They allow to examine deficits in retronasal olfactory function, differences to orthonasal olfaction, interactions with other senses, and the clinical aspects of retronasal olfaction. Psychophysical tests to explore retronasal olfactory function include, for example, flavor identification tests like the “taste powders” (Schmeckpulver; Fig. 2)” or the “candy smell test” (CST). Taste powders are a test kit with 20 grocery-available foods. The powders are administered to the middle of the tongue by using squeezable plastic vials. Using a multiple forced choice procedure, subjects are asked to identify the “taste” then from a list of one of four items [6]. The CST ⁎ Corresponding author at: Tel.: + 49 351 458 4189; fax: + 49 351 458 7130. E-mail address: [email protected] (T. Hummel). 0031-9384/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2012.03.001
addresses the retronasal application of odors, typical for food aroma effects during mastication and swallowing [7]. Both tests are easy to handle; they are reliable methods for the clinical routine. In order to investigate differences between orthonasal and retronasal perception of odors, presentation of odorous stimuli is a key issue. Halpern pointed out that ortho- and retronasal stimuli should reach the olfactory mucosa by the two distinct pathways, without producing additional gustatory or mechanical stimuli [8]. Thus, studies based on the application of liquid or solid stimuli to the oral cavity cannot allow direct comparisons to stimuli that are presented in front of the nose, simply because the oral administration of odors may produce gustatory, thermal, and mechanical sensations which may interact with olfactory mediated sensations [9,10]. To avoid this situation, some researchers placed odors in containers presented to the oral cavity (e.g. [11]), while others asked subjects to sniff the headspace of an odorous liquid or inhale the same headspace through the mouth followed by nasal exhalation [12] (cf. [13,14]). The perception of retronasal olfaction starts milliseconds after expiration onset [15]. A major limitation of these methods is the unknown odor concentration in the oral cavity and the mechanical stimulation of intraoral surfaces [10]. To allow for a more defined retronasal stimulation, a device was developed [16] which allows the release of odors directly into the epipharynx above the soft palate. This avoids concomitant oral gustatory, thermal and mechanical stimulation, thus permitting the study of ortho- or retronasal olfaction in isolation. Two plastic tubes are placed in the nasal cavity under endoscopic control such that the opening of one of the tubes is just beyond the nasal valve and the opening of the other tube is in the epipharynx. For stimulus presentation, the tubes are connected to outlets of a computer-controlled air-dilution olfactometer. Mechanical stimulation is avoided by embedding the stimuli into a constant flow of odorless, humidified air of controlled temperature [17]. Odors presented through either tube reach the olfactory epithelium at approximately the same concentration and with the same time course [18].
V. Bojanowski, T. Hummel / Physiology & Behavior 107 (2012) 484–487
Fig. 1. There are two pathways for odors to reach the olfactory epithelium. The orthonasal red route is used during sniffing, for example, to identify odors like rose, smoke, or other odorants in the environment. Through the retronasal blue route the flavor of foods can be perceived.
3. Differences between orthonasal and retronasal olfaction Results from psychophysical, electrophysiological, and imaging studies suggest that there are clear differences in the perception and processing of ortho- and retronasal stimuli. Food odors may produce different sensations when presented in front of the nose or intraorally, when eaten, e.g., cheeses, coffee, or flowery odors like lavender. There are numerous possible reasons for these phenomena. Differences in airflow patterns are thought to contribute to perceptual differences between ortho- and retronasal presentation of odors [19]; in fact, the direction of odor movement across the olfactory epithelium could lead to differences in the processing of odorous information. This hypothesis is supported by work emphasizing the significance of nasal airflow on the perception of odors [20–24]. Differences between ortho- and retronasal olfactory functions are also emphasized by differences in the salivary response if an odor is repeatedly presented. The response decreases until a new food odor
485
is presented. The same effect is found if the route of administration is changed from orthonasal to retronasal or vice versa. Thus, presenting the same odor via different pathways represents a distinct sensory signal which can also be shown on a behavioral level [25]. With regard to this findings it is no surprise that there are patients with an isolated smell deficit only for one route of olfaction whereas the other route shows normal function. Better retronasal than orthonasal olfactory function, meaning impaired smell with preserved flavor perception, has been reported in patients with nasal polyposis [28]. This is thought to be related, at least in part, to the presence of mechanical obstruction in the anterior portion of the olfactory cleft [29], whereas odors could still reach the olfactory epithelium through the retronasal route. In addition, orthonasal olfactory loss with little or no changes in retronasal odor perception has been reported even in the absence of nasal polyposis (e.g. [30,31]). There were also studies which have described a retronasal smell loss in the absence of orthonasal deficits. [26,27]. Orthonasal and retronasal olfaction differ in terms of threshold, rated odor intensity, ability to localize an odor, and the neuronal processing of either signal. Thresholds to orthonasal stimuli are typically lower compared to retronasal thresholds [12]. On a suprathreshold level it has also been reported [32] that the ability to identify odors is less efficient when stimuli are presented retronasally [14]. Using olfactory threshold measurements, greater impairment has been reported for retronasal than for orthonasal perception in elderly people [13]. Numerous studies indicate that olfactory stimuli cannot be lateralized when the stimulus is applied to one of the two nostrils [33,34]. Interestingly, subjects are able to localize ortho- and retronasal presentation of an odorant. As expected, the trigeminal stimulus CO2 can be localized and lateralized, but also the pure olfactory stimuli H2S and in most cases PEA, a rose-like odorant, cannot be lateralized but are clearly localizable [35]. Cortical responses reflect differences between ortho- and retronasal stimuli. EEG-derived event-related potentials indicated that, when an odorant unrelated to food (e.g., lavender) was presented in a contextually unusual site, i.e. retronasally, the response was larger compared to the presentation of the same odorant at an orthonasal site [36]. This was the other way around for a food-related odor (e.g., chocolate). These findings clearly indicate contextual differences of information processing depending on the route of odor presentation. Orthonasal and retronasal stimuli produce different patterns of brain activation. Specifically, imaging techniques like functional
Fig. 2. Taste powders (“Schmeckpulver”) – photograph of the psychophysical investigation of retronasal olfactory perception. Powders like cacao, paprika or garlic are applied to the middle of the tongue. Subjects have to select one of four items that best describes the flavor (Heilmann et al. 2002).
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magnetic resonance imaging (fMRI) allow to investigate differences between ortho- and retronasal olfactory activation at a cerebral level [37,38]. Activation due to retronasal stimulation was found at the base of the central sulcus, corresponding to the primary representation of the oral cavity [39], possibly reflecting that retronasal odors are referred to the mouth. Small and colleagues reported activation in different brain areas in response to taste and orthonasally/retronasally presented stimuli [40,41]. They observed deactivation in the orbitofrontal cortex, insula, and anterior cingulate cortex for taste-orthonasal stimulus association, and supra-additive responses at the same regions for the combination of taste and retronasal stimuli. These results clearly indicate that the neural processing of an odor is influenced by route of administration. 4. Interactions between retronasal olfaction and gustatory / tactile influences During oral processing of foods and swallowing the senses interact in a non-linear way. This means that texture or taste of foods influences the perception of odors (e.g. [42–44]. For example, retronasally applied odor of benzaldehyde (smell of almonds/marzipan) is enhanced by the sweet taste of sucrose. This is not the case if the stimulus is a different, contextually incongruent taste, like water or umami [45]. In contrast, there seems to be a relatively weaker enhancement of taste by odors [46]. Faster processing of an olfactory stimulus was induced by an incongruent simultaneous taste. For example there were shorter latencies of EEG-derived olfactory eventrelated potentials in the combination “vanilla odor and sour taste” compared to “vanilla odor and sweet taste” [47]. With regard to the trigeminal activation induced by most odorants [49] there is also the possibility that the interaction between the trigeminal and the olfactory system relates to the differential perception of ortho- and retronasal stimuli [50–52]. To be specific, there is evidence indicating that the sensitivity for chemosensory stimuli is higher in the anterior compared to the posterior portion of the nose while this is the other way around for mechanical stimuli [53] (but see also [54]). Results obtained by Visschers et al. [55] suggest that the intensity of aroma decreased with increasing consistency of the consumed food. In addition, it has been shown that retronasal odorous stimuli increase the intensities of thickness and creaminess of oral stimuli [56]. Importantly, this interaction was strongest when the presentation of the odor coincided with swallowing indicating that also temporal issues feed into the interaction between these sensory channels. These details help to explain some interesting findings how the senses influence each other, with most interactions taking place in the central nervous system. It is important to note that context plays a very strong role in the perception of foods. If a fruit does not have the expected taste or texture, this food probably is not eaten. The tight interaction between the various sensory channels also becomes clear when we describe odors with terms of taste qualities with these taste-like qualities of odors probably being learned [48]. 5. Clinical aspects of retronasal olfaction As an interesting aspect regarding the biological role of retronasal odor perception, recent work suggests that perceived satiation is modulated by the extent of retronasal aroma release. The extent of aroma release depends on personal and product differences. People differ in oral processing, bite size, duration of processing and meal duration. Small bite sizes and longer duration of oral processing favor a higher aroma release. Product properties like solid consistency, a high protein percentage and a multi-component aroma may also enhance satiation which, in turn could prevent consumers from overeating (reviewed in [57]).
Another clinical aspect is the swallowing inducing effect of retronasal stimulation. Retronasal stimulation seems to facilitate swallowing. Compared to orthonasal stimulation swallowing occurs significantly faster and more frequently when odors are presented retronasally [58]. Other factors with a modulating effect on swallowing include bolus size, texture, orthonasally presented odors, saliva or muscular abilities. At the moment retronasal stimulation is only one possibility to trigger the swallowing reflex. But still, it may become a clinical option to coordinate swallowing, aiming to prevent aspiration, for example in stroke patients with swallowing disorders (review by [59]). References [1] Rozin P. "Taste–smell confusions" and the duality of the olfactory sense. Percept Psychophys 1982;31:397–401. [2] Shepherd GM. Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Ann N Y Acad Sci 2007;1121:87–101. [3] Murphy C, Cain WS. 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