02/02/2009
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Quality of Life in Olfactory Dysfunction



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Mediating Factors:  Caveats, Context, Expectation and Verbal Illusions
Caveats:  At least two caveats to the assertion that all olfactory hedonic responses are learned must be mentioned.  One is the issue of trigeminal stimulation.  Trigeminal stimulation is responsible for the tactile (burning, cooling) and irritating component of odor perception.  Although the trigeminal system is separate from the olfactory system, subjective experience is not distinct and it is often very difficult to dissociate the olfactory from the trigeminal aspects of a scent (e.g., gasoline).   Odors vary greatly in the degree to which they stimulate the trigeminal nerve and in many cases this aspect is negligible (Doty et al., 1978).   However, trigeminally irritating odors may elicit immediate avoidance responses on the basis of their trigeminal component and thus odors that cause trigeminal irritation do not require learning to be considered unpleasant.   This is adaptive for us as well as many toxic substances are strongly trigeminal.      

A second consideration is the individual variability that may exist in specific genes and pseudogenes for olfactory perception across individuals.  It is known that of the 1,000 genes coding for olfactory receptors, only a subset of them (between 300-400) are functional (e.g., Malnic et al., 2004).   It is quite likely given the variability in the number of functional genes reported, that there is also variability between individuals in what those functional genes are.  Thus, it may be the case that a person who likes the smell of skunk does so in part because they are missing receptors for detecting some of the more pungent volatiles, while another who is repulsed by this scent is endowed with a greater number of receptors that are keenly attuned to the mercaptan and sulphide aspects of this bouquet.  In particular, it appears that a genetic case can be made for the spice cilantro.  Cilantro elicits strong and polarizing hedonic responses.  Current research by Chuck Wysocki has shown that identical twins always have the same immediate hedonic response to cilantro (either loving it or hating it) while fraternal twins do not (see the Monell Connection newsletter, winter 2003, for more details).   It is not yet known what olfactory receptors or genes account for these differences, however it appears that genetic/receptor mechanisms mediate perception of this specific spice.   Very recent molecular research also suggests that the timing of the turning on or off of certain genes that govern specific olfactory receptors causes changes to our sense of smell throughout life (Stuart Firestein, personal communication, January 9, 2004).   That is, the way a rose smelled to us at 2 yrs of age, at 20 yrs of age and at 50 yrs of age may not be the same.   It would be interesting to examine how genetic effects and aging interact with susceptibility for odor-associative learning.   Perhaps someone who is genetically endowed to dislike cilantro will still be able to become fond of it if their first true love is a Mexican chef.  Further exploration and understanding of the role of genetics in odor preferences will be very fruitful and future research should investigate individual genetic differences and aging as covariates to susceptibility for odor-associative learning.

Context, Expectation and Verbal Illusions:  In addition to the power of emotion and associative learning for odor preference formation, there are several other factors that mediate odor preference perception, in particular: context, expectation and language. 

A context is a state or situation (mental or physical) or environment that induces a set of preconceptions and expectations.   Context can be a powerful mediator of odor hedonic perception.  For example, if you are walking by a garbage dumpster and you smell a particular scent with a few sharp notes, you are likely to perceive the smell as unpleasant, however, that exact same chemical composition hovering above the cheese plate at a French restaurant might inspire salivation.  Thus, the preconceptions and expectations elicited by the physical context in which you are exposed to an odor can be a strong determinant of its hedonic meaning.   A poignant literary example of the influence of expectation on olfaction was described in Mark Twain’s The Invalid’s Tale.   A stowaway on a train car jumps to what becomes the cause of his untimely death, because he convinces himself that the sack beside him contains a dead body, when in fact all it contained was “a lot of innocent cheese.”   This anecdote describes a visual context (a burlap sack of a particular shape) that created a set of expectations that powerfully influenced odor hedonic perception.   No experiments to date have investigated visual context effects on odor perception, however, verbal contexts have been well studied and appear to be very influential for altering odor perception (Herz & von Clef, 2001; Herz, 2003). 

My laboratory has found that verbal expectation effects are so great that they can cause olfactory illusions to be induced by words alone (Herz & von Clef, 2001).   Using the definition that an illusion is created when a physical stimulus remains invariant but its context alters perception, we investigated whether verbal context could produce olfactory illusions.  We examined five ambiguous odors.3  The odors were: violet leaf, patchouli, pine oil, menthol, and a 1:1 mixture of isovaleric + butyric acid.   Participants sniffed each odor at two different sessions separated by one week.   At each session an odor was given a different verbal label, either positive or negative (for example, iso-valeric + butyric acid was alternately called “vomit” or “parmesan cheese,” and pine oil was called “disinfectant” or “Christmas tree”).   Participants then gave ratings to the odors on several hedonic scales and provided motivational and interpretative responses to them.  Results showed that the hedonic perception of all of the odors could be significantly influenced by the label provided for it.  When the label was positive each odorant was evaluated as more pleasant and familiar than when that same odorant was given a negative label.  Moreover, motivational responses were entirely different as a function of label.   For example, when isovaleric + butyric acid was called “parmesan cheese” it inspired participants to say they would like to eat it, while when it was given the negative label (“vomit”) it provoked the wish to escape from it.   The effect was so strong for certain odors, that participants could not believe that the same odorant had been presented to them at both sessions.  This dramatic alteration of the perception of an odor by words alone is the first empirical demonstration of olfactory illusions.

In another study, the concepts of ‘synthetic’ and ‘natural’ were examined as mediators of odor preference (Herz, 2003).   Eight common positive and negative odors (rose, vanilla, lemon, peppermint, fish, sweat, bad breath and rotten egg) were presented in their natural and synthetic forms and verbal labels designating name and source (natural, synthetic) information were either: explicitly given, self-generated, falsely provided, or not provided.  Results showed that when an odor was believed to be “synthetic” it was given lower hedonic evaluations than when the same odorant was believed to be “natural,” regardless of whether or not the odorant was truly natural or synthetic.  It also didn’t matter whether an odor was actually present, or whether the scent was positive or negative.  That is, using the label “natural vanilla” resulted in higher pleasantness and familiarity ratings than the label “synthetic vanilla” even when there was no accompanying smell.  And “natural” was evaluated as superior for negative odors as much as the positive odors (i.e., “natural” bad breath was preferred to “synthetic bad breath”).   Notably, if the participant believed the odorant to be comprised of “both natural and synthetic” components (this was actually never the case) it was given equally positive ratings as the same odorant believed to be 100% natural.   Furthermore, participants were objectively unable to discriminate between natural and synthetic versions of the same scents, and without any labels truly natural and synthetic odorants were given either equivalent evaluations or in some cases the synthetic versions were actually preferred. 

Together these studies show that the connotation of words can have a tremendous impact on how well liked an odor will be, independent of how it was originally learned.  For example, parmesan cheese may be associated with the comfort and pleasure of eating pasta, but a chemical that could be parmesan cheese if believed to be something quite different (e.g., vomit) will utterly negate the past positive association.   Thus, words provide a context in which an odor is interpreted, and how that interpretation fits with past experiences will determine how it will be evaluated.

Sex Differences?
Women have been shown to be more sensitive to odors than men under some conditions.  In particular when an odorant is at sub-threshold concentration, women are more likely to report detecting a scent before a man (Whisman et al., 1978).  However, at or above average threshold concentration there are typically no differences between men and women in their odor sensitivity.   Menstrual cycle phase also plays an important role in women’s odor detection abilities.  During ovulation, women are especially sensitive to odors, however during the menses stage of their cycle women are equivalent or may even be less sensitive than the average male to any given scent (Doty et al., 1981). 

Given that odor intensity is related to odor hedonic perception, it is worth considering whether there are any preference differences between men and women.  No systematic test of this question has been conducted that is not restricted to body-odor, and conclusions from this area of work are confounded by heterosexual attraction mechanisms.   Nevertheless, in the many studies I have conducted and the numerous others that I have read, I have never observed any systematic sex differences in basic odor preference evaluations.  To the extent that familiarity plays a role in odor hedonic judgments, Cain (1982) showed that women were more familiar with and better able to name many common odors than men, but at closer inspection this familiarity bias was due to cultural exposure effects.  That is, women were more familiar with cooking and cosmetic odors, while men were more familiar with outdoors and mechanical odors.  

The personality predisposition of being particularly interested in and attentive to scent is related to odor preferences and may be mediated to some degree by sex.  People who pay attention to and care about smell tend to be more favorably predisposed to odors in general, and therefore will like more odors than someone who is uninterested in scent.   Wrzesniewski, McCauley and Rozin (1999) developed a questionnaire to assess the degree to which people are interested in and pay attention to odors.  The higher the score on this questionnaire the greater the importance of odors to that individual.  Wrzesniewski et al. (1999) did not obtain sex differences in their data, however, a non-significant trend for women to score higher on this questionnaire has been observed (Herz, 2004), suggesting that women may like odors more or have more odor preferences than men.

I would like to end the topic of sex differences by discussing a condition where many anecdotal reports of temporarily altered odor preferences among women exist; the state of pregnancy.   In addition to surprising food cravings like pickles and ice-cream, sudden food/odor preferences and aversions are also often reported.  In many cases, the suddenly repulsive food/odor was very well liked prior to pregnancy; for example fried chicken, or pizza (Pope et al., 1992).   Folklore has received much more attention than science in this domain so we tend to believe that something about pregnancy (e.g., hormonal state) alters women’s odor preferences.  But what is the scientific evidence? 

Several recent studies have examined olfactory sensitivity changes during pregnancy, focusing both on the first trimester, where there is much anecdotal report of increased sensitivity to smells, as well as the entire period of pregnancy.  A review of this literature shows that no systematic changes in odor sensitivity were found at any point of pregnancy and pregnant women are no more sensitive to odors than their non-pregnant peers (Kobel et al, 1991: Hummel et al., 2002; Lashka et al., 1996).  Odor induced nausea is also seen during pregnancy and has been experimentally investigated in relation to olfactory sensitivity, but the data suggest that feeling sick from smelling fried chicken is due to how the odor is psychologically perceived and not due to any changes in olfactory sensitivity or hormonal changes due to pregnancy (Bayley et al., 2002; Hummel et al., 2002).   In other words, the olfactory-food oddities that are reported during pregnancy seem to be idiosyncratic and psychological rather than physiological.  It is possible that women who experience pregnancy as a psychologically heightened emotional state, may be more susceptible to developing new emotional associations during this time and hence new cravings and aversions (i.e., hedonic responses) appear.  It is also conceivable that because there is so much popular lore about food and odor changes during pregnancy that much of the alterations in preferences reported are a function of and perpetuated by cultural suggestion; that is, culturally induced associative learning (see Carruth & Skinner, 1991 and Pope et al., 1992).

(3) Ambiguous odors are those with minimally fixed sources and can thus be interpreted with various hedonic connotations.

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