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Journal of Sensory Studies ISSN 0887-8250

LEARNING ODORS: THE IMPACT OF VISUAL AND OLFACTORY


MENTAL IMAGERY TRAINING ON ODOR PERCEPTION
S. TEMPERE1,2,6, M.L. HAMTAT3, J.C. BOUGEANT4, G. de REVEL1,2 and G. SICARD5
1
EA 4577, Unité de Recherche Œnologie, Univ. de Bordeaux, ISVV, F-33882 Villenave d’Ornon, France
2
USC 1366, Œnologie, INRA, ISVV, F-33882 Villenave d’Ornon, France
3
EA 4139, Psychologie, Santé et Qualité de Vie, Univ. Bordeaux, Bordeaux, France
4
Laboratoire d’Etude des Mécanismes Cognitifs (EMC), Univ. Lyon, Bron, France
5
UMR 7259, Neurophysiologie des Interactions Cellulaire et Neuropathologie, Univ. Aix-Marseille, F-13331 Marseille, France

6
Corresponding authors. ABSTRACT
TEL: +33557575858;
FAX: +33557575813; Mental imagery has been used successfully in sensorimotor training, but rarely to
EMAIL: sophie.tempere@u-bordeaux.fr. improve sensory skills. Novices, undergraduate enology students (intermediates)
and wine experts were asked to repeatedly imagine the visual images or smells of
Accepted for Publication September 24, 2014
odorant sources presented in picture form. Olfactory abilities, odor sensitivity and
doi:10.1111/joss.12124
identification performance were compared before and after mental training to
check the differential effects of the two types of sensory training. We demonstrated
that, like repeated objective odorant stimulations, repeated imagination of odors
was able to enhance olfactory performance in objective perception. Both odor
detection and identification abilities were improved. However, according to our
results: (1) the effect was odorant specific; and (2) the impact of training on iden-
tification was restricted to wine experts. In addition, interestingly, the experts’
olfactory identification performance apparently deteriorated following specific
visual attention during the training phase.

PRACTICAL APPLICATIONS
One extremely important aspect of sensory evaluation is training panelists to
achieve consistent results. The results demonstrated the effectiveness of olfactory
mental imagery as training strategy. The findings demonstrated that olfactory
mental imagery was able to modify olfactory capabilities of wine professionals,
with results comparable to those obtained using perceptual training. Conse-
quently, olfactory mental imagery is an excellent tool for training the olfactory
capacities of panelists, and may be extended to perfumers, flavorists and tasting
panelists with a view to improving product quality control, without material
stimulus such as chemical supports.

The existence of olfactory imagery is controversial


INTRODUCTION
(Crowder and Schab 1995; Stevenson and Case 2005).
Mental imagery is defined as the creation of a neural repre- However, multiple experiments leave little doubt concern-
sentation in the absence of an external stimulus or event and ing its reality (Djordjevic et al. 2005; Sugiyama et al. 2006;
is accessed from memory (Kosslyn et al. 2001). This phe- Bensafi et al. 2007). In addition, clinical studies reporting
nomenon has been widely studied in the visual, auditory, subjective odor perceptions, i.e., olfactory hallucinations,
tactile and sensory motor domains (Kosslyn and Shwartz may be considered additional proofs of the capacity of the
1977; Aleman et al. 2000; Anema et al. 2012; Bläsing and olfactory system to produce olfactory imagery (Ohayon
Schack 2012). The effectiveness of mental imagery as a 2000). Furthermore, it is even possible to describe interac-
training strategy has been shown in several areas, such as tions between mental imagery and objective perception of
sport and music (Pascual-Leone et al. 1995; Jones and Stuth odors. For example, intermodal interactions of olfactory
1997; Veraksa and Gorovaya 2012). imagery are illustrated by the fact that the intensity of taste

Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc. 435
MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD S. TEMPERE ET AL.

perception may be modified when the participant is asked experts. The impact of OMI training on odor detection and
to create an olfactory mental image: the intensity of the per- identification performance was tested. Visual imagery was
ception of sweet solutions was increased when the subject considered as a control task to assess the specificity impact
simultaneously perceived or imagined the smell of straw- of the training.
berries (Djordjevic et al. 2004a).
The interaction between objective and subjective olfac-
tory experiences has been confirmed by psychometric, neu- EXPERIMENT 1 – IMPACT OF
ropsychological and neurophysiological studies showing OLFACTORY MENTAL TRAINING ON
overlaps in psychophysiological processes (Algom and Cain INDIVIDUAL DETECTION THRESHOLDS
1991; Levy et al. 1999; Bensafi et al. 2003). Other authors In this experiment, we assessed the change in olfactory sen-
have described similar neural substrates evoked during sitivity of enology students following repeated mental
olfactory mental imagery (OMI) and objective olfactory imagery tasks.
perception (Djordjevic et al. 2005; Plailly et al. 2012).
Djordjevic et al. (2004b) reported that an olfactory mental
exercise disrupted olfactory detection tasks. The authors METHODS
showed how detection of weak odors was affected by pre-
ceding olfactory or visual imagery tasks. Participants made Subjects
significantly more mistakes when the imagined odor was A group of 42 volunteer enology students participated in
inconsistent with the one presented in the detection task. In this experiment during the first 6 months of their training:
the same paradigm, visual mental imagery (VMI) had no 21 women and 21 men with an average age of 24 ± 5 years.
effect on performance. Indeed, interactions between olfac- All students reported a normal ability to smell and no respi-
tory imagery and real odor perception have previously been ratory infections or allergies. The study was performed in
reported (Lyman and McDaniel 1990; Carrasco and Ridout accordance with the Declaration of Helsinki on Biomedical
1993). Facilitating or inhibiting effects depend not only on Research involving human subjects and approved by the
the perceived and imagined object but also on the sensory Local Ethics Committee. All participants provided written
modality of the imagery: Lyman and McDaniel (1990) com- informed consent. According to published literature, these
pared OMI and visual imagery to evaluate the effects subjects corresponded more to the definition of “intermedi-
of modality encoding on later stimulus recognition. ates” than novices (Parr et al. 2004).
Intramodal correlations were identified: odor recognition
was enhanced by OMI of congruent odor names while
Olfactory Stimuli
image recognition was enhanced by VMI (The participants
visually imagined items from a word list). Two different key wine compounds were used: diacetyl
On the basis of these data, we hypothesized that olfactory [431-03-8] with a buttery odor (Fluka, Saint-Quentin
mental training would help improve individuals’ olfactory Fallavier, France) and 1-octen-3-one [4312-99-6] reminis-
skills. However, several previous studies had suggested that cent of mushrooms (Lancaster, Alfa Aesar, Schiltigheim,
not all subjects were able to produce olfactory mental France).
images and that this capacity was better developed in sub- In an initial experiment, the odors of both diacetyl and
jects with a sustained practice of smelling particular odors 1-octen-3-one stimuli were considered familiar by 62 and
(Gilbert et al. 1998; Djordjevic et al. 2004b; Plailly et al. 67%, respectively, of a sample of 60 controls. Diacetyl was
2012). Consequently, wine specialists, who use their noses in considered to represent butter “Fairly well to well”, being
their daily work, were included in this study. Wine quality is slightly less typical than the odor of 1-octen-3-one, which
primarily evaluated by experts who use their sensory skills represented mushroom odor “Well to Very well”.
to assess its sensory characteristics. A previous study focus- In order to make each compound soluble, stock solutions
ing on the chemosensory abilities of wine experts evaluated containing an average of 1 g/L in ethanol (HPLC purity,
their sensitivity to wine quality markers (Tempere et al. Merck, Darmstadt, Germany) were prepared and confirmed
2011). A wide dispersion of chemosensory thresholds was by gas chromatography-mass spectrometry. These solutions
found, resembling that of nonexperts. Abnormally low sen- were then diluted in spring water (Volvic, Danone, Paris,
sitivity to certain odorants – specific hyposmia – was even France; pH ± SD = 7.21 ± 0.2). Odor detection thresholds
detected in some experts. Training to enable wine profes- were determined using an ascending procedure with 10
sionals to overcome these specific deficits would be perithreshold concentrations (10 successive twofold dilu-
welcome. The experiments reported in this article addressed tions). Serial dilutions of the two stimuli were prepared the
two dimensions of olfactory perception using OMI training day before the test session to allow time for equilibration of
to improve the olfactory abilities of novices and wine the headspace in testing bottles.

436 Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc.
S. TEMPERE ET AL. MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD

Odorant solutions were presented in randomly coded evocation of olfactory images (Mainland and Sobel
brown bottles (30 mL, open diameter = 2 cm) (Prince 2006).
Emballage, Eysines, France), with phenolic resin caps and
VMI Group. Every day, the subjects spent 2 min visually
polytetrafluoroethylene (PTFE) seals (VWR, Fontenay-
imagining objects corresponding to the odors used in
Sous-Bois, France).
training.
The stimulus concentration ranges to be tested (Table 1)
were determined by analyzing published data and conduct- Control Group without Training. During the first evalua-
ing preliminary experiments. In each case, 10 perithreshold tion session, they were simply informed that they would be
concentrations were prepared, each pair differing by a factor retested with the “butter” and “mushroom” odors during a
of 2. second session.
Odorant Training. The two odors, diacetyl and 1-octen-
Procedure 3-one, and the corresponding pictures were used for
training (Table 1).
Olfactory Detection Measurements. In order to The participants trained once per day for 10 consecutive
evaluate the impact of OMI, the subjects’ sensitivity was days. The task was administered via Internet based on the
assessed twice: before and after training. visual presentation of the photographs of mushrooms and
Sensitivity is usually evaluated by the odor detection butter (Fig. 1). The photographs of odorant sources dis-
threshold, defined as the lowest concentration of an odor played on the screen were 17 × 22.7 cm in size (354 × 472
that can be detected, but not necessarily identified, by a pixels). The pictures were used as support to generate both
sample of subjects. olfactory and visual imageries. Each day, the two items were
Individual olfactory detection thresholds were measured presented in random order. Olfactory or visual imagery
for both compounds. Each subject performed 10 3-AFC training sessions lasted 2 min/day.
ascending detection tests (ISO 13301 2002): for each of the At the end of the training period, the individual detection
10 trials, the participant received a set of three bottles (two threshold measurements were repeated.
blanks of spring water and one with the diluted odorant at 1
Data Analysis and Modeling
of the 10 concentrations) and was asked to sniff each bottle
in the prescribed order and then choose the spiked sample The detection threshold of the group, known as the absolute
in each set of three bottles. The participant indicated the threshold, was defined as the concentration at which the
positive sample on a data sheet (forced choice). spiked sample was detected correctly by 50% of the partici-
pants, corrected by chance. This statistical value was deter-
Experimental Groups and Mental Imagery Tasks.
mined using an adaptation of the ASTM – E1432 method.
The participants were assigned at random to one of the
The psychometric concentration/response function fitted a
three following training groups (14 subjects per group).
sigmoid curve (y = 1/(1 + e(–λx))). Detection probability was
OMI Group. Every day, the subjects spent 2 min imagining corrected using the chance factor (1/3 for 3-AFC). Sigma
specific odors (1 min per item). This group was familiarized Plot (SYSTAT Software INC, London, United Kingdom)
with olfactory imagery practice using the Vividness of software was used for graphic resolution and nonlinear
Olfactory Imagery Questionnaire (VOIQ) and the Vividness regression by analysis of variance (ANOVA) transform to
of Visual Imagery Questionnaire (VVIQ) (Gilbert et al. determine the threshold xo and a second criterion, the slope
1998). These questionnaires introduce the difference b = 1/D. x = xo when P = 0.5. P was the predicted correct
between visual and olfactory imageries requiring subjects to response (Tempere et al. 2011). ANOVA was applied to sta-
mentally evoke objects and activities with visual or olfactory tistical data using XL-STAT (Microsoft Excel, Addinsoft,
cues. Subjects were advised to sniff actively during the train- Paris, France). Duncan’s test was used as a comparison test
ing phase as this sensorimotor activity seems to facilitate the when samples were significantly different after ANOVA.

TABLE 1. PUBLISHED DETECTION THRESHOLDS OF CHEMICALS DILUTED IN WATER, ODOR QUALITIES, CONCENTRATION RANGES USED FOR
DETECTION THRESHOLD MEASUREMENTS, AND THE OLFACTORY ITEMS ASSOCIATED FOR THE OMI TRAINING CONDITIONS AND THE VISUAL
ITEMS USED FOR THE VMI

Published values of detection Our concentration


Compounds Smells threshold in water ranges Pictures
Diacetyl Butter 5 μg/L (Lawless et al. 1994) 0.2–198.4 μg/L
1-Octen-3-one Mushroom 7 ng/L (Buttery et al. 1990) 0.11–108.5 ng/L

Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc. 437
MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD S. TEMPERE ET AL.

FIG. 1. SCHEMATIC REPRESENTATION OF A


TRAINING SESSION ADMINISTERED VIA
INTERNET
A series of screens were displayed at a con-
trolled speed showing digital images of
odorous objects at resolutions of 354 × 472
pixels (17 cm × 22.5 cm). Each day, the two
items were presented in random order.

438 Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc.
S. TEMPERE ET AL. MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD

However, a difference was observed in the training


RESULTS
groups’ initial sensitivity to 1-octen-3-one. The correspond-
The psychometric functions were plotted (Fig. 2) to evalu- ing sigmoid curves exhibit dissimilar slopes (bOMI = 1.14;
ate the impact of the training conditions – two types of bVMI = 3.61; bcontrol = 2.62) and absolute thresholds
mental imagery and controls – on the detection threshold (xoOMI = 25.88 μg/L; xoVMI = 14.36 μg/L; xocontrol = 17.69 μg/
for each compound tested. For diacetyl, pre- and post- L). This difference may originate from sampling.
training performance did not differ significantly between In view of the shape of the control curve, the robustness
the OMI, VMI and control conditions (pre-training values: of the results was checked on a smaller sample: the OMI
xoOMI = 3.86 μg/L, xoVMI = 3.29 μg/L, xocontrol = 3.44 μg/L; training group was reduced to 10 subjects (four less sensi-
post-training values: xoOMI = 3.60 μg/L, xoVMI = 2.91 μg/L, tive subjects were eliminated). A comparison of the sigmoid
xocontrol = 7.49 μg/L). In contrast, OMI training was found to curves confirmed the improvement in performance follow-
have a significant impact on the detection threshold for ing OMI training (Fig. 3). These results confirmed that
1-octen-3-one, which decreased by a factor of 9.4 (pre- OMI training affected the detection threshold. Indeed, the
training values: xoOMI = 25.88 μg/L; post-training values: OMI group’s absolute threshold for 1-octen-3-one was
xoOMI = 2.76 μg/L) (enhancement > intra-individual fluctua- reduced by a factor of 8.39 (enhancement > intra-individual
tion and to one-dilution step; P < 0.1) fluctuation and to one-dilution step; P < 0.05). In contrast,

FIG. 2. IMPACT OF TRAINING ON ABSOLUTE DETECTION THRESHOLDS


Curves represent the sigmoid modeling before (broken lines) and after (solid lines) training. The quality of the fit is given by R2. The detection
threshold was defined as the concentration at which the probability of detection was 50% (indicated by a dotted line at P = 0.5). Three training
groups were formed (14 subjects per group): olfactory mental imagery (OMI), visual mental imagery (VMI) and control. Concentration levels
(expressed as log10) are shown on the horizontal axis and the percentage of positive responses (corrected by chance) on the vertical axis. Upper
section (A): psychometric functions for diacetyl. Lower section (B): psychometric functions for 1-octen-3-one. OMI training had no impact on the
diacetyl curve but reduced the detection threshold of 1-octen-3-one.

Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc. 439
MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD S. TEMPERE ET AL.

emitting source most accurately. On the second time, they


performed a free association task between the suggested
target image and three other pictures presented on the
draughtboard. It was made clear to them that they had to
select the “nearest” images to the target and that they had to
organize their choice in a hierarchy by first indicating the
nearest image to the target, then the second, and then the
third. It was specified that there was no such thing as a right
or wrong answer. The pictures, which were not chosen for
each odorant, were then randomly selected to form a pair of
“unrelated” pictures for the target and for each odorant
stimulus of the test.

METHODS

Subjects
Two groups participated in the study: 20 novices (42 ± 10
years old) and 20 experts (47 ± 9 years old).
Each subject completed a form with regard to the main
criteria (age, gender, smoking habits and health status)
FIG. 3. PSYCHOMETRIC FUNCTIONS FOR THE 10 OMI-TRAINED posited to have an influence on odor perception.
SUBJECTS (OMI GROUP WAS REDUCED TO 10 SUBJECTS. FOUR LESS All experts had wine-tasting qualifications (DNO, Gradu-
SENSITIVE SUBJECTS WERE ELIMINATED) ate Diploma in Oenology, or DUAD, a professional tasting
Concentrations (expressed as log10) are shown on the horizontal axis diploma) and the novices were recruited outside the wine
and the percentage of positive responses (corrected by chance) on the industry. None of the novices had any formal knowledge of
vertical axis. The detection threshold was defined as the concentration
olfactory evaluation criteria. The two groups were sex
at which the probability of detection was 50% (indicated by a dotted
line at P = 0.5). Upper section (A): curves represent the sigmoid model
matched (11 women and 9 men). All novices and experts
before training for total OMI group (dotted line), VMI group (broken reported a normal ability to smell, with no respiratory
line) and control group (solid line). Lower section (B): curves represent infections or allergies.
the sigmoid model for 1-octen-3-one before (broken lines) and after
(solid lines) OMI training for the 10 subjects selected. Stimuli
Forty-seven everyday odors were tested. Some represent also
wine defects, key components of quality or typicality and
no significant difference was found for the other trained non-wine-specific compounds (Table 2).
odor, diacetyl. Briefly, the odorants were diluted in 3 mL mineral oil
(Acros Organics, Geel, Belgium) at concentrations (10−2 to
10−5). Only (±)-geosmin was diluted in spring water to
EXPERIMENT 2 – IMPACT OF
obtain a higher diffusion (-log Kaw = 2.56). The quality of
TRAINING ON OLFACTORY
the smells associated with the compounds did not deterio-
IDENTIFICATION CAPACITIES
rate but remained stable during the testing period (pretest
In this experiment, the olfactory identification ability of in the laboratory with independent groups of novices and
novices and experts was measured and compared using a experts). Each bottle contained a polypropylene pad
forced-choice procedure using a tool with associations (Delahaye Industrie, Saint Aignan de Grand Lieu, France) to
between odors and photographic images which facilitate the absorb the liquid, prevent spilling and enlarge the odorant-
identification for the subjects (Gottfried and Dolan 2003). emitting surface, thus shortening bottle air saturation time.
To build this olfactory-visual test, three preliminary inde- In order to familiarize the subject with the procedure, five
pendent experiments were proposed: (1) to characterize the supplementary odorants (Sigma Aldrich, Saint-Quentin
odorant samples (typicality, familiarity, pleasantness, etc.); Fallavier, France) were prepared: D-limonene [5989-27-5]
and (2) to associate odorants and images. The task associat- (orange), ethyl cinnamate [103-36-6] (strawberry), ethyl
ing odorant stimuli and images involved 105 participants. phenylacetate [557-48-2] (honey), trans-2-cis-6-nonadienal
Individually, they indicate the picture that would enable [110-43-0] (cucumber) and heptan-2-one [107-97-3]
them to imagine the odor of the object and represent the (Roquefort cheese-like odor).

440 Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc.
S. TEMPERE ET AL. MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD

TABLE 2. LIST OF ODORANTS USED IN THE IDENTIFICATION TEST

Familiarity Typicality
No. Odors Chemical names CAS number Suppliers (%) (scale/100) Sets
1 Almond Benzaldehyde 100-57-2 SA 85 45 –
3 Anise Anethol 104-46-1 M 85 53 –
4 Apple Ethyl 2-methylbutyrate 7452-79-1 SA 85 37 –
5 Banana Isoamyl acetate 123-92-2 SA 88 38 –
6 Bell pepper 2-Isobutyl-3-methoxypyrazine 24683-00-9 SA 82 31 –
7 Butter Diacetyl 431-03-8 SA 72 31 2
8 Cabbage Methionol 74-93-1 SA 62 21 2
9 Camembert S-methylthiobutyrate 2432-51-1 SA 77 40 –
10 Caramel Furaneol 3658-77-3 F 63 29 –
11 Cinnamon Cinnamaldehyde 104-55-2 Sr 85 39 2
12 Cloves Eugenol 97-53-0 SA 57 39 –
13 Coconut Whiskey-lactone 39212-23-2 SA 83 42 –
14 Coffee Extract / V 83 33 2
15 Coriander Linalool 78-70-6 F 73 24 1
16 Cork taint 2,4,6-Trichloroanisole 87-40-1 SA 48 19 –
17 Crab stick Dimethylsulfide 75-18-3 SA 75 37 –
18 Earthy (±)-Geosmin 19700-21-1 Su 63 27 –
19 Eucalyptus 1,8-Cineol 470-82-6 SA 87 43 –
20 Feet Isovaleric acid 503-74-2 M 60 47 –
21 Fish 2-Butylamine 13952-84-6 SA 32 17 2
22 Grass Cis-3-hexenol 928-96-1 SA 88 43 –
2 Horse 4-Ethylphenol 123-07-9 L 53 21 –
23 Kiwi Ethyl butyrate 105-54-4 SA 75 29 –
24 Lavender Essential oil / Sn 93 57 –
25 Lemon Citral 5392-40-5 SA 88 52 –
26 Mint Essential oil / Sn 95 50 –
27 Mushroom 1-Octen-3-one 4312-99-6 L 67 36 1
28 Musk Omega-pentadecalactone 106-02-5 SA 57 27 –
29 Onion Ethanethiol 75-08-1 F 70 28 1
30 Orange blossom Methyl anthranilate 134-20-3 E 60 21 2
31 Peach γ-Undecalactone 706-14-9 SA 48 20 1
32 Pear Hexyl acetate 142-92-7 SA 93 45 –
33 Pineapple Allyl hexanoate 123-68-2 SA 68 31 2
34 Plastic Styrene 100-42-5 SA 78 34 2
35 Rose Phenylethanol 60-12-8 M 58 31 1
36 Rubber Benzothiazole 95-16-9 SA 55 31 1
37 Sea Calone 28940-11-6 C 38 19 1
38 Smokey 4-Ethylgaïacol 2785-89-9 L 63 26 1
39 Solvent Nail varnish remover / Re 88 71 –
40 Sweat 3-Sulfanylhexyle acetate 51755-83-0 IC 73 55 2
41 Thyme Thymol 89-83-8 SA 74 34 1
42 Toasted bread 2-Acetylthiazole 24295-03-2 SA 58 21 –
43 Vanilla Aroma / V 87 44 1
44 Vinegar White vinegar / Re 83 46 –
45 Violet β-Ionone 79-77-6 SA 55 25 –
46 Washing powder Aldehyde C12 112-54-9 SA 47 18 –
47 Woody Cedryl acetate P50 61789-42-2 SA 58 21 2

Note: Familiarity and typicality of the smells were measured in a control sample of 60 subjects. The table indicates the percentages of subjects who
considered that the smell was familiar. Typicality is represented by coordinates on an adapted green scale. These are 10-cm-long semilogarithmic
graduated scales annotated with descriptions ranging from “barely identifiable” to “the strongest ever” for intensity or from “very poorly” to “per-
fectly well” for typicality, with which participants checked their answers. Suppliers: Ca, Calchauvet; E, Eastman; F, Fluka; L, Lancaster; M, Merk; Re,
Repère; SA, Sigma Aldrich; Sn, Sanoflor; Sr, Sarsynthèse; Su, Supelco; V, Vahine.

Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc. 441
MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD S. TEMPERE ET AL.

– crab stick – solvent – rose – cloves – smokey – bell pepper


Experimental Design
– almond – rubber – cinnamon – orange blossom – fish –
The experiment consisted of three phases: two identification violet – butter – pear
tests of odor samples separated by a 10-day mental imagery Order 2: the reverse order
training period. The test was individual and the presentation order of the
The olfactory identification test was conducted with the odors was randomized among the subjects in the first
aid of a computer program to regulate the timing (Fig. 4). session and repeated in the same order in the second
Instructions and images were displayed on a computer session.
screen according to a regular schedule; the subjects’ After the first measurement session, each group of sub-
responses were recorded via a keyboard. Subjects were jects (novices and experts) was divided at random into three
assisted by an operator, who presented the odor samples training groups: an OMI group, a VMI group and a control
under their nostrils. This procedure avoided contamination group.
of the odorized bottles (perfume, cigarette, etc.) and stan- The training procedure was identical to that used in
dardized the sampling condition. The 47 odors were pre- experiment 1 except for the length of training. Daily 10-min
sented in turn. After the initial sniffing phase, five pictures sessions (1 minute per item) were guided by a series of
of odorant sources appeared on the screen, including the Internet-based interactive screens (Fig. 1). Novices and
target (most probable odor source or correct answer), two experts were familiarized with olfactory imagery practice
items similar to the target odor (= close answer, “nearby” using the sample given by the VOIQ and the VVIQ. Any
target) and two totally dissimilar items (= distracters). novice reported difficulty with imagery task.
Response time started when the picture was displayed Groups were divided into two subgroups using different
and was unlimited. It was ended by the participant’s sets of 10 training items: set 1 and set 2 (Table 2). Items
response on the keyboard and the elapsed time was were selected to balance the representativeness of the
recorded as the response time. The software that supervised samples. There was no difference between the mean famil-
the experiment processed the answers and determined the iarity percentages of the two samples (U = 41; P = 0.52),
scores – correct, close or wrong answers – and the response with means + SD of 63.3 ± 14.1% and 67.1 ± 15.4%, respec-
time of each subject for each odor. tively. There was no difference on typicality scales:
The five odors presented at the beginning of the experi- 29.3 ± 7.6 mm and 30.3 ± 11.3 mm, respectively (U = 48.5;
ment to familiarize the subjects with the procedure were not P = 0.92).
registered in the results.
The standardized odor samples were presented in one of
Data Analysis
two sequences:
Order 1: pineapple – mushroom – lemon – caramel – Duncan’s test was used as a comparison test when samples
feet – apple – lavender – onion – coconut – mint – cabbage were significantly different after ANOVA. In order to esti-
– kiwi – washing powder – camembert – musk – mate the efficiency of training, three independent variables
banana – vinegar – coriander – woody – horse – anise – were tested: the subjects’ training conditions (OMI and
vanilla – earthy – peach – sea – cork taint – coffee – VMI), the type of items (trained and untrained) and the set
eucalyptus – plastic – thyme – toasted bread – sweat – grass of trained items (set 1 or 2).

FIG. 4. SCHEMATIC REPRESENTATION OF


IDENTIFICATION PROTOCOL
The test began with an initial sniffing phase.
Five pictures were then displayed on the com-
puter screen. The participant had to choose
the corresponding odor source from a set of
photos. For example, when the odorant
tested was ethyl 2-methylbutyrate, the correct
choice was the picture representing an apple.
The nearby responses were pear and peach
and the distracters were coffee and perfume.
Once the subject had entered an answer with
the computer’s numeric keypad, there was a
10-s pause before the next odorant was
presented.

442 Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc.
S. TEMPERE ET AL. MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD

In addition, the time of day of the test (morning versus


RESULTS
afternoon), the presentation order of stimuli and socio-
professional parameters (sex, age, expertise) had no impact
Initial Characteristics of the Training Groups
on scores (ANOVA; P > 0.05).
Factorial ANOVA was used to check whether the composi-
tion of each group of subjects (experts and novices) was
Impact of Mental Imagery on Olfactory
similar in terms of their initial correct identification ability,
Identification Scores
total identification ability (sum of correct and close
responses) and response times. Independent variables were Factorial ANOVA was used to assess the relative impact of
the training conditions (OMI/VMI), the type of items visual/olfactory training, trained/untrained subjects, trained
(trained/untrained items) and the set of trained items (set 1 item sets, measurement sessions and subject groups
or 2). Analysis revealed a significant difference in olfactory (novices or experts) on correct identification scores. The
identification scores between the types of items, F(1, results revealed that OMI training had a significant positive
72) = 11.07; P < 0.01, as well as trained (correct identifica- effect, F(1, 128) = 4.97; P < 0.05. In addition, the analysis
tions: 62.75 ± 2.24) and untrained (correct identifications: revealed an interaction between the five independent vari-
72.03 ± 1.63) items (Fig. 5). Duncan post hoc analysis indi- ables, F(1, 128) = 7.98; P < 0.01. In fact, the increase in
cated a significantly lower score for the trained items. correct identification scores for trained compounds was sig-
However, the test showed an interaction between the types nificantly higher for experts trained with the items in set 2
of items and the sets of trained items. Actually, the differ- only (Fig. 6). Interestingly, with the same set, the experts
ence was only significant for set 2 (P < 0.05). As the initial recorded a significant decrease in identification of trained
identification scores were lower in set 2, there was a slightly stimuli after visual training. No training effect was detected
larger potential for performance enhancement. No signifi- in novices.
cant difference in total scores was observed (P > 0.05) Furthermore, the results revealed a difference between
irrespective of the factor. the two sets of items used, i.e., a significant performance

FIG. 5. COMPARISONS OF THE INITIAL CORRECT IDENTIFICATION SCORES (A) OF STIMULI TO BE INCLUDED IN THE EXPERIMENT AND INITIAL
RESPONSE TIMES (B) ACCORDING TO THE TRAINING CONDITIONS (OMI/VMI), ITEM TYPES (TRAINED OR UNTRAINED) AND TRAINED ITEM SETS (1
OR 2)
Correct identification scores and response times differed between the trained and the untrained items. Asterisks indicate significant differences
(Duncan test; *P < 0.05; **P < 0.01).

Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc. 443
MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD S. TEMPERE ET AL.

FIG. 6. COMPARISON OF PRE- (GRAY) AND POST-TRAINING (BLACK) CORRECT IDENTIFICATION SCORES FOR TRAINED AND UNTRAINED ITEMS
AFTER VISUAL AND OLFACTORY TRAINING IN EXPERTS AND NOVICES
(% means ± standard errors). Asterisks indicate significant differences (Duncan test; *P < 0.05). OMI training had no effect on novices tested with
set 1. In contrast, identification of trained odors improved after OMI training, but only for experts. VMI training had a slight but significant nega-
tive impact on olfactory identification scores in the expert group only.

enhancement for sample set 2 in experts trained by OMI


Measuring the Impact of Mental Imagery on
concerning 7/10 items, but only 2/10 for set 1 (Fig. 7). In
Response Times
the case of set 2, five items where scores improved were
identified by 50% or fewer subjects before training, while The average response times for correct answers were ana-
two were identified correctly by 75% of participants: iden- lyzed for each experimental group (ANOVA). Training was
tification of coffee and pineapple was already high before found to have a significant impact on response times, F(1,
training. In set 1, the identification rate for coriander, 128) = 8.4; P < 0.01, depending on the level of expertise.
like that of fish and the sea, was very low before The decrease was more marked for the experts, but their
training, below 30%, but only that of coriander improved response times in the pre-training phase, 8,126 ± 2,445 ms,
after training. These variations suggest that the starting were longer than those of novices, 7,048 ± 2,520 ms. Post
level does not play an important role, but rather the hoc analysis revealed a significant decrease in the experts’
quality of the items and, more specifically, their times with sample set 2, independent of the type of training
imageability. or item.

444 Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc.
S. TEMPERE ET AL. MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD

FIG. 7. ODOR-SPECIFIC EFFECT OF OMI


TRAINING ON EXPERTS’ CORRECT IDENTIFI-
CATION SCORES WITH TRAINED AND
UNTRAINED ITEMS FROM SETS 1 AND 2
(% means ± standard errors). The results
revealed a significant performance enhance-
ment mainly for experts trained by olfactory
mental imagery (enhancement for 7/10 items)
tested with sample set 2. “+” = items where
performance enhancement was recorded after
training.

ing protocol had lower detection thresholds afterward. No


DISCUSSION
effect was detected with diacetyl, indicating that the increase
This research investigated the possible impact of OMI train- in sensitivity was dependent on the compound tested. The
ing on two aspects of olfactory performance: detection and difference may also have been due to the initial sensitivity
identification. These results provide the first evidence of an levels. A comparison of the initial diacetyl detection thresh-
enhancement of olfactory performance following OMI olds (average 3 μg/L) with published data (12.4 μg/L;
training. Moreover, the proposed training impacted both Tempere et al. 2011), based on the same measurement
aspects. methodology, revealed that the participants were fairly sen-
sitive to this compound (a positive difference greater than
two dilution steps), thus leaving less scope for increasing
Olfactory Sensitivity and Mental Imagery
their sensitivity. Comparing the participants’ initial 1-octen-
The first experiment revealed an enhanced ability to detect 3-one detection thresholds (on average 26 ng/L) with pub-
one of the trained odorants: 1-octen-3-one, reminiscent of lished data (40.8 ng/L; Tempere et al. 2011) revealed a
mushrooms. Participants who followed the imagery train- difference smaller than one-dilution step.

Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc. 445
MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD S. TEMPERE ET AL.

Two alternative, but not mutually exclusive, hypotheses in total identification scores (correct responses plus close
may explain the discrepancy between odorants. First, the responses). Some of the close responses became correct
perception of an object and the ability to imagine its prop- responses. OMI training was expected to facilitate discrimi-
erties depend on familiarity (Carrasco and Ridout 1993). nation among odors in the same perceptual group (i.e.,
Diacetyl odor may be less familiar than that of 1-octen-3- semantically related items).
one and, consequently, more difficult to imagine. This is As in the previous experiment on sensitivity perfor-
unlikely, as the familiarity and typicality data for both mance, the impact of OMI training depended on the
stimuli were at similar levels. Second, the odor sample may odorant chemical species: trained odorant sets 1 and 2 did
not have been perfectly representative of the target item not produce equal results. As stated above, this variation
(although it had previously been validated by 105 subjects). may be explained by differences in the quality of the images
Symmetrically, the imagined odor may have been different representing the odorous materials, the quality of the odor-
from the one perceived in the detection test, with the result ants or visual images used, or the varying difficulty of creat-
that the repeated imagery did not provide effective training. ing mental images corresponding to different odors.
Finally, another possibility is that imagery was as good as The possibility of forming olfactory mental images has
for 1-octen-3-one but without effect (induced no effect) on been questioned (Crowder and Schab 1995; Herz and Engen
diacetyl detection ability. 1996; Herz 2000). Criticisms of the paradigms used in OMI
It is interesting to compare these results with the studies have mainly argued that semantic information is
improvement in the wine experts’ specific sensitivity follow- capable of influencing the odor imagery process (see Elmes
ing repeated exposure to two different key wine com- 1998), implying that imagery may be strictly a sensory (or
pounds: diacetyl and linalool (Tempere et al. 2012). In this depictive) representation. In this regard, it is important to
previous study, trained experts had to smell odor sample note that the experimental psychophysiological or neuro-
bottles once a day for 1 month. As in the present study, the physiological manifestations of so-called “mental imagery”
impact of training on specific sensitivity was assessed by correspond to the subject’s responses to requests for a
measuring changes in olfactory detection thresholds. The mental imagery. Tomiczek and Stevenson (2009) defined
results showed a decrease in the olfactory detection thresh- olfactory imagery as the participant’s response to form a
olds restricted to the trained compounds. While the subjects percept-like representation. To refine this perspective, this
tested had been selected as poorer performers using the representation may or may not be conscious. Gilbert et al.
same method of detection threshold determination (abso- (1998) intended to “measure” this consciousness with the
lute threshold, ASTM – E1432 method), the gains observed VOIQ test, which mimics checking the quality of visual
after perceptual and OMI training were similar, represent- mental images (Marks 1973). However, the consciousness of
ing an average of four binary dilution steps. VMI is consensually accepted but seems problematic in
It is thus possible to conclude that an increase in sensitiv- olfaction. “Measurement” is a subjective concept, with no
ity after olfactory imaging sessions occurred, provided that: clear definition of what is really evaluated by the partici-
(1) initial performance was poor; (2) OMI is inefficient for pant. Olfactory imagery involves physical sensation, seman-
diacetyl odor; and (3) the memory of the training com- tic associations, knowledge (Tomiczek and Stevenson 2009)
pound and the objective perception of the odorant stimulus and even motor representation (Mainland and Sobel 2006).
were consistent. From a physiological standpoint, it was In addition, specific neurological objective perception struc-
unlikely that more effective detection/identification was due tures are actually recruited during OMI experiences or
to an increase in the sensitivity of the olfactory mucosa requested tasks, as demonstrated by neuroimaging studies
(Wang et al. 1993). Indeed, under OMI conditions, without (Djordjevic et al. 2005; Bensafi et al. 2007; Plailly et al.
direct stimulation of the olfactory receptor layer, hypotheses 2012), thus reinforcing the concept that OMI is similar to
focus on either a top-down mechanism (Mainland et al. auditory or VMI (Kosslyn et al. 2001). One aspect that
2002) or a gain in sensitivity supported by central changes. offers promising material for future study is the clear dem-
Note that the hypothesis of an influence on peripheral sen- onstration that some parts of the olfactory (network)
sitivity was not confirmed by recording electro-olfactogram system operate subconsciously (Lorig 1994), suggesting that
responses of the olfactory mucosa (Lapid and Hummel parts of the olfactory mental representation may remain in
2013). the subconscious.
This study provides an additional functional argument in
favor of OMI, as the expected effect of OMI was confirmed
Identification Ability and Imagery
in experts, i.e., it affected their objective olfactory percep-
Identification scores and accuracy were also enhanced by tion. This difference between experts and novices is consis-
OMI training, but only for experts. Indeed, the number of tent with the hypothesis that subjects are not equally able
correct identifications increased, but there was no variation to form olfactory mental images (Gilbert et al. 1998;

446 Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc.
S. TEMPERE ET AL. MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD

Djordjevic et al. 2004a; Bensafi et al. 2005) and that experts’ 2010; Wilson and Rennaker 2010). However, it should be
OMI capabilities are greater than those of novices (Plailly stressed that both types of stimuli are also involved in atten-
et al. 2012; Royet et al. 2013). These findings are also consis- tion processes (e.g., Foxe et al. 2005; Johnson and Zatorre
tent with the analysis of Bende and Nordin (1997), who 2005; Ciaramitaro et al. 2007). In this case, visual pictures
suggested that, in the objective olfactory perception condi- were introduced as mental imagery support in the training
tion, experts do not have a greater detection capacity than procedure and as identifiers of odorant objects used in the
novices, as they do not have specific experiences of the olfactory ability test. In this protocol, therefore, the pictures
detection task. On the contrary, discrimination or identifi- themselves constituted learning targets and acquired certain
cation tasks, which require higher level processing, are sen- properties as perceived objects. These properties may
sitive to mental training. At the same time, some studies include the establishment of attentional cueing (or tagging)
(Djordjevic et al. 2005; Bensafi et al. 2007; Royet et al. 2013) in a specific sensory modality (Mattler 2004). Indeed, when
demonstrated that olfactory networks involving the primary a participant is shown a photograph of an object and
olfactory cortex were activated when novices were requested instructed to form a perceptual copy of that object in his/
to form odor mental images. Moreover, olfactory skills are her mind, the attentional effort may be expected to result in
strongly related to wine professionals’ expertise. In this a suppression of activity or deactivation in brain areas sup-
experiment, their performance as experts was tested which porting nonrelevant sensory modalities (Laurienti et al.
may induce motivational difference with novices. 2002; Johnson and Zatorre 2005). Processing a stimulus in
The response times were relatively long: generally exceed- one sensory modality may result in the suppression of other
ing 4 s. In this experiment, the response time included a sensory-specific activity (e.g., Kawashima et al. 1995;
visual task and a decision guided by olfactory perception. Laurienti et al. 2002; Mozolic et al. 2008). One hypothesis
Each participant scanned the five visual items while remem- arising out of the results presented here is that visual atten-
bering the olfactory sensation or associated perceptive rep- tion may be able to mask an object’s olfactory cues even
resentation of the odorant object, and, finally, made a during mental imagery tasks. This may make it more diffi-
decision. According to a standard hypothesis, the resulting cult to associate subsequent objective odor perception with
response time is the sum of the reaction times for each step a VMI-trained pictorial identifier.
(Sternberg 1969). Olfactory features, or object cueing, thus Our results may be related to mindfulness. This kind of
represented only one part of the task. In fact, response times training is a procedure in which participants simply focus
have rarely been measured in the olfaction field. They vary on a task for a few minutes in silence. This focused attention
according to the experimental paradigm ranging from is sufficient to show large effects on a wide range of physical
600 ms in a detection task (Chen and Dalton 2005) to 1–2 s and cognitive tasks (Hölzel et al. 2011). However, the use of
in a discrimination task (Boesveldt et al. 2010) and 6–10 s different items and the comparison with a control or a VMI
in a retrieval task (Jehl et al. 1997). Nevertheless, it is sug- group indicate the low relation between simple mindfulness
gested here that the longer response times of wine experts training and the effects found after OMI training. Thus, the
were consistent with the idea that they applied an analytical present results depend on the olfactory imaging work
process to the olfactory identification task, while the novices request during OMI. An attention voluntarily oriented on
adopted a heuristic approach. Familiarization with testing olfactory percepts, on the hedonic characteristic or other
conditions may explain the general effect of the session olfactory qualities of odorous objects, seems responsible for
factor observed for novices and experts. the enrichment of the olfactory representation.
One unexpected finding of the study was that VMI train-
ing resulted in lower olfactory identification scores.
Although this effect was of low amplitude and item specific,
CONCLUSION
it deserves a short comment. In this study, olfactory training
and testing involved both olfactory and visual stimuli. At The operationality of mental sensory representations in
first glance, the rich data corpus on sensory cross-modal olfaction is supported by our functional experimental data.
interactions may provide an explanation of the incidental However, the difference detected between novice and expert
result. Reasoning that had mainly been based on visual/ skills reflected a point raised recurrently in the literature.
auditory/touch cross talk between modalities (e.g., Shaw The sensitivity of undergraduate oenology students to
1982; Eimer et al. 2002; Sinnett et al. 2008) was recently OMI-trained samples was enhanced, but, unlike wine
supplemented by functional data, indicating the occurrence experts, the novices did not increase their identification
of perceptual visual-olfactory interactions (Jadauji et al. scores following OMI training. This suggests that the
2012), as well as anatomical or even functional data con- novices lacked a skill that they subsequently acquired. One
firming links between olfactory and visual systems in object pragmatic goal for future study could be: “How to teach
perception (Gottfried and Dolan 2003; Wesson and Wilson novices to learn to use olfactory imaging?”

Journal of Sensory Studies 29 (2014) 435–449 © 2014 Wiley Periodicals, Inc. 447
MENTAL IMAGERY: A NEW OLFACTORY TRAINING METHOD S. TEMPERE ET AL.

unattended sensory information in early visual and auditory


ACKNOWLEDGMENTS human cortex. J. Neurophysiol. 98, 2399–2413.
S. Tempere was supported by a PhD fellowship from the CROWDER, R.G. and SCHAB, F.R. 1995. Imagery for odors. In
Conseil Interprofessionnel du Vin de Bordeaux (Bordeaux, Memory for Odors (F.R. Schab and R.G. Crowder, eds.) pp.
France). M.L. Hamtat was supported by a PhD fellowship 93–107, Erlbaum, Mahwah, NJ.
from the Fondation Edmond Roudnitska (Paris, France). DJORDJEVIC, J., ZATORRE, R. and JONES-GOTMAN, M.
The authors would like to thank these sponsors for their 2004a. Effects of perceived and imagined odors on taste
financial support. detection. Chem. Senses 29, 199–208.
DJORDJEVIC, J., ZATORRE, R., PETRIDES, M. and
JONES-GOTMAN, M. 2004b. The mind’s nose: Effects of
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