Chem. Senses 24: 327-335,
1999
© Oxford University Press
Basic Emotions Evoked by Eugenol Odor Differ According to the Dental Experience. A Neurovegetative Analysis
Département de physiologie, Faculté d'Odontologie, Université Claude Bernard, LYON I, rue Guillaume Paradin, F-69372 Lyon Cedex 08, 1 Emotion et Vigilance, LPM, CNRS, INSA Lyon, bâtiment 401, 20 avenue Albert Einstein, F-69621 Villeurbanne Cedex, France 2 Microcapteurs microsystèmes biomédicaux, LPM, CNRS, INSA Lyon, bâtiment 401, 20 avenue Albert Einstein, F-69621 Villeurbanne Cedex, France
Correspondence to be sent to: O. Robin, Faculté d'Odontologie, rue Guillaume Paradin, F-69372 Lyon Cedex 08, France. e-mail:robin{at}laennec.univ-lyon1.fr
| Abstract |
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Subjective individual experiences seem to indicate that odors may form strong connections with memories, especially those charged with emotional significance. In the dental field, this could be the case with the odorant eugenol, responsible for the typical clinging odor impregnating the dental office. The odor of eugenol could evoke memories of unpleasant dental experiences and, therefore, negative feelings such as anxiety and fear, since eugenates (cements containing eugenol) are used in potentially painful restorative dentistry. This hypothesis was tested by evaluating the emotional impact of the odor of eugenol through autonomic nervous system (ANS) analysis. The simultaneous variations of six ANS parameters (two electrodermal, two thermovascular and two cardiorespiratory), induced by the inhalation of this odorant, were recorded on volunteer subjects. Vanillin (a pleasant odorant) and propionic acid (an unpleasant one) served as controls. After the experiment, subjects were asked to rate the pleasantness versus unpleasantness of each odorant on an 11-point hedonic scale. The patterns of autonomic responses, obtained for each odorant and each subject, were transcribed into one of the six basic emotions defined by Ekman et al.
| Introduction |
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Previous studies by Berggren and co-workers (Berggren and Meynert, 1984
It can thus be suggested that eugenol odor could evoke memories of unpleasant dental
experiences and contribute to dental anxiety and fear. This is supported by the results of
Kirk-Smith et al. (1983
), who
demonstrated that if an unfamiliar
odor is associated with
a stressful situation, this odor may, at a later time, elicit concomitant mood and attitudinal
changes. In the case of eugenol, its association with unpleasant dental care experiences could be
explained by the fact that eugenates (cements containing eugenol) are often used in potentially
painful restorative dentistry on vital teeth.
In a recent study (Robin et al.,
1998
), we have evaluated,
through simultaneous
recording of six autonomic nervous system (ANS) parameters, the emotional impact of dental
odorants and especially eugenol, responsible for the typical odor of the dental office. The
variations of the ANS parameters induced by the inhalation of this odorant were compared
between two groups of subjects divided according to their dental experience (fearful and
non-fearful dental care subjects). The results showed that eugenol odor induced significantly
different patterns of ANS responses between the two groups with stronger variations in the
fearful dental subjects. It was suggested that these results reflect the particular significance of this
odor to fearful subjects, evoking unpleasant feelings such as anxiety and fear related to their
dental experience. However, one limitation of this study was that it provided only quantitative
data from the variations of the ANS parameters. Moreover, the stronger differences between the
two groups of subjects were mainly observed through one ANS channel (the electrodermal
channel), so that information obtained through the other ANS channels (thermovascular and
cardiorespiratory) could not be taken into account for the data analysis. The same conclusion was
made by AlaouiIsmaïli et al. (1997a
), who studied the
relation between the
hedonic valence of five odorants and the autonomic parameter variations induced by the
inhalation
of these odorants. A significant correlation between autonomic responses and the subject's
hedonic estimation for all the odorants was obtained only through the skin resistance and heart
rate parameters. It was concluded that it would be more interesting to consider the global pattern
of ANS responses rather than each parameter separately. Such an approach can be realize if each
ANS pattern is transcribed into a basic emotion, allowing a qualitative analysis of the response in
addition to the quantitative one (Vernet-Maury et
al., 1995a
).
Defined by Ekman et al. (1983
),
basic emotions (happiness,
surprise, sadness, fear,
anger and disgust) can be considered as psychophysiological entities that are behaviorally
observed and cross-culturally distinguished. They are characterized by a rapid onset, a short
duration and a spontaneous occurrence explaining that ANS, a highly and rapidly activated
system, is capable of differentiating among them (Schwartz
et al., 1981
; Ekman et al.,
1983
; Uchiyama, 1992
; Collet et al.,
1997
). Phillips et al.
(1997
) have
even demonstrated, using functional magnetic resonance imaging, the existence of distinct
neural
substrates for perception of disgust, involving primarily the anterior insula, and of fear, involving
the amygdala.
In a recent study (Alaoui-Ismaïli et al.,
1997b
) basic
emotions could be
associated with different odorants from the global autonomic response pattern induced by the
inhalation of each odorant. This approach allowed us to demonstrate that pleasantly connoted
odorants were mainly associated with `positive' emotions (happiness and
surprise),
whereas unpleasantly connoted odorants were associated with `negative' emotions,
mainly disgust and anger.
The purpose of this study was to transcribe the global ANS pattern induced by the inhalation
of the odorant eugenol into a basic emotion and to compare the distribution of the basic emotions
between fearful and non-fearful dental subjects. It was expected that the basic emotions
associated
with eugenol odor could differ between these two groups of subjects in relation to their dental
experience. A pleasant odorant (vanillin) and an unpleasant one (propionic acid) were used as
controls. In addition to ANS (unconscious) basic emotions, the distribution of verbal
(self-estimated, conscious) emotions was also reported since differences from these two methods
of evaluation were previously observed concerning, especially, unpleasant odors
(Alaoui-Ismaïli et al., 1997b
)
| Materials and methods |
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Subjects and odorants
Forty-four healthy, non-smoker volunteer students (20 males and 24 females) served as subjects. Their mean age was 25 years, ranging from 20 to 28 years. All subjects participated as part of practical works of applied physiology (University Lyon I) after providing informed consent to the protocol.
The three diluted odorants in ethanol 95 (eugenol 0.15%, vanillin 1% and propionic acid 0.015%) were delivered in a randomized order and were always preceded by a pleasant odorant (lavender 1%) in order to suppress the surprise effect induced by the first stimulus. The concentration of each odorant was adjusted to be clearly recognizable without stimulating the trigeminal nerve endings (no pungent sensation in the nose).
Procedure
Subjects were individually involved in an olfactory test session lasting ~40 min. Odorants
were delivered from an olfactometer where compressed air (5.1 l/min), purified by passing
through different kinds of filters, fed the glass flasks containing the odorants. Two clips placed
on
the rubber tube at the entrance and the exit of each flask permitted the delivery of odors to the
subjects through a two-outflow glass tube fixed under the nostrils (Alaoui-Ismaïli et al., 1997b
) An output from the polygraph enabled
the experimenter to synchronize odor
presentation with the inhaling part of the breathing cycle.
Prior to experimental sessions, subjects were informed verbally about the procedure. They were made aware that an odorant was to be delivered but they did not know when. During the test, subjects were alone in the experiment room (temperature = 22°C), isolated from the experimental device. Odorants were delivered for 5 s with variable time intervals of ~2 min, when ANS parameters had recovered their prestimulus basal level after each response.
After the experimental session, the odorants were again delivered to the subjects, who were asked to identify (if possible) each odorant, to situate it on an 11-point hedonic scale (from 0 = highly pleasant to 10 = highly unpleasant) and to associate it to one of the six basic emotions listed on a paper in front of them (verbal or conscious basic emotions).
From the 44 subjects, 19 (6 males and 13 females) identified the odorant eugenol as the
typical odor of the dental office. Each of these subjects was then asked to specify his or her
attitude toward dental care (apprehensive or not) and the feelings associated with this evocation
(unpleasant or not). This allowed us to divide them into two groups: non-fearful dental subjects
(n = 7: 2 males and 5 females), for whom no unpleasant connotation was associated
with
the dental office or dental care, and fearful dental subjects (n = 12: 4 males and 8
females), who reported an aversive attitude toward dental care. Subjects who did not explicitly
associate eugenol with the dentist were not included in this study since their responses could not
be interpreted in terms of dental fear. However, an analysis of the ANS responses of the 44
subjects, induced by the inhalation of different odors (including eugenol), has previously been
performed and discussed according to the hedonic valence of the odorants (Alaoui-Ismaïli et al., 1997b
).
Autonomic nervous system parameters
Throughout the olfactory test, six ANS parameters were simultaneously and continuously recorded with no interference: skin potential (SP) and skin resistance (SR) (electrodermal parameters), skin blood flow (SBF) and skin temperature (ST) (thermovascular parameters), and instantaneous respiratory frequency (IRF) and instantaneous heart rate (IHR) (cardiorespiratory parameters).
Skin resistance
SR was recorded using 25 mm² Ag/AgCl round electrodes (Clark Electromedical
Instruments E 243, Reading, UK), placed on the second phalanx of the index and the third digit
of
the non-dominant hand, held by adhesive tape. Electrode positioning was in compliance with
traditional recommendations (Fowles et al.,
1981
). Resistance
was measured by a 15
µA DC current. As response amplitude depends on the prestimulation value (Wilder,
1962
), a more reliable index was defined: the time during which the subject responds
to the
stimulus without referring to the initial value (or tonic level). This index, called OPD (for ohmic
perturbation duration), was shown to reflect the emotional load of the stimulus (Vernet-Maury et al., 1995b
).
Skin potential
SP was recorded using Beckman 78 mm² electrodes, fixed by double-sided adhesive
tape. Electrode positioning and electrode cream were in compliance with traditional
recommendations (Fowles et al., 1981
).
The active electrode
was
placed on the
hypothenar eminence of the subject's non-dominant hand (after alcoholether
cleaning of the skin). The reference electrode was placed 10 cm higher on the wrist (on the
equidistant line of the median plane and the outer extremity of the forearm). Electrodermal
potential variations were analyzed with the SYDER code (Dittmar et al.,
1995
), which
permits classification of elementary responses according to their form (A, B, C), sign (+ or
) and duration.
Skin blood flow
SBF was assessed using the original Hematron patented sensor (Dittmar, 1989
). The
non-invasive sensor was placed on the skin with adhesive tape (thenar eminence of the
non-dominant hand). The transducer consisted of a disk 25 mm in diameter and 4 mm thick. The
measuring surface in contact with the skin was made up of two parts: the reference area at the
periphery of the disk, and the measurement area at the center of the disk. The temperature
difference between these two areas was measured using 16 thermocouple junctions. A very low
thermal inertia flat heater was located in the central part of the disk. A proportional, integrative
and derivative device controlled the heating power in order to maintain a constant temperature
difference of 2°C between the central area and the periphery. The size and shape of the
heater were designed in such a manner that a thermal field was induced in the capillary network.
The power necessary to maintain the temperature difference constant depends on SBF: heat is
transferred through the skin and washed out by the blood flow. At all times, electric power is
proportional to the heat evacuated by the tissue blood flow (Dittmar, 1989
).
Blood flow in capillaries is submitted to microchanges reflecting variations of emotional
load.
SBF variations were measured by the duration of the oscillation break period induced by the
stimulus. At rest, SBF recording shows spontaneous and regular oscillations which disappear
when the subject is under the stimulation. The duration of the pertubation of these oscillations is
expressed in seconds through the NOD index (for non-oscillatory duration) (Vernet-Maury et
al., 1991
).
Skin temperature
ST was measured by a slow inertia thermistor (10 K3 MCD2 Betatherm). A 4 mm²
sensor was placed in the middle of the palm of the non-dominant hand with noncaustic glue. A
variation of about one-thousandth of a degree can be detected under such conditions. With regard
to the different subjects' thermal balance, the amplitude variation (positive or negative)
was measured by the difference between the tonic temperature level and the phasic variation,
using the disrupted slope of the graph. For the same reason, duration was measured from the
onset of the phasic response to this disrupted slope of the graph.
Instantaneous respiratory frequency
IRF was recorded from an oblong thermistor (length 10 mm, diameter 3 mm), placed at the
entrance of the left nostril with hypoallergenic adhesive tape. The processed signal gives the IRF
on the basis of the difference in temperature between inhaled and exhaled air.
Instantaneous heart rate
IHR was recorded from three silver electrodes in a precordial position. The D2 derivation
signal (interval between two consecutive R waves) was processed and delivered in the form of
instantaneous heart frequency. The smallest appreciable variation was 0.5 beats/min and the
calibrated scale ranged from 0 to 200 beats/min.
Recording system and signal analysis
The six measured signals were recorded by a 80286 microcomputer (Toshiba T3200). Signal sampling was carried out by a 16-bit data acquisiton card (ADAC 5508HR) at a frequency of 8 Hz. Signals were recorded in parallel by a six-channel potentiometric DC recorder (YTSE 460 type BBC) to allow rapid visual inspection of the recordings and quality control of experimentation.
A special software package was designed and developed for rapid analysis and processing of
the recorded data. The interactive software permits calculation of all indices (including waveform
pattern recognition of SP responses). The software features have other uses, such as amplification
and attenuation of signals and zooming. A digital signal processing library of functions was
designed and added to the software in order to allow processing of all types of artefacts and to
filter random noise whenever present in the recorded signals (Rada et al.,
1995
).
Data analysis and extracted parameters
Data analysis was performed through the five following extracted parameters: (i) the sign (+
or ) and the form of the SP response (A, B or C), according to the SYDER code
(Dittmar et al., 1995
), which reflects the
duration of the response
(the A form corresponds to the
shortest responses and the C form to the longest responses); (ii) the duration of the SR response,
expressed in seconds, with the OPD index (Vernet-Maury
et al., 1995b
); (iii) the
duration of the SBF response, expressed in seconds, corresponding to the non-oscillatory period
induced by the stimulus (NOD index; Vernet-Maury et
al., 1991
); (iv) the amplitude and
the sign (+ or ) of the ST response; and (v) the variation (increase or decrease) of the
IHR response expressed in beats/min. The variations of the respiratory frequency were not taken
into account for the data analysis since the inhalation of the odorants could interfere with the
respiratory response. However, this parameter was useful for controlling the time when the odor
was detected by the subject.
ANS basic emotions
ANS responses were analyzed subject by subject and odorant by odorant. The pattern of ANS
responses, obtained for each odorant, was transcribed into one of the six basic emotions
(happiness, surprise, sadness, fear, anger and disgust) using a decision tree built from different
autonomic analysis, especially those of Ekman et al. (1983
) and
Collet et al.
(1997
) (Figure
1). The responses obtained
through each ANS
parameter were calculated for each
odorant, as previously explained. Their magnitude was then evaluated as strong (+++), medium
(++) or weak (+), from a comparison between all responses of the subject and reported on the
decision tree, allowing the association of each ANS pattern with one of the basic emotions (ANS
basic emotion). This procedure is illustrated by an example in the `Results'
section.
|
Statistical analysis
The following data were statistically compared, for each odorant, between the two groups of subjects (fearful and non-fearful dental subjects): the hedonic scores by a oneway ANOVA and the distribution of verbal and ANS basic emotions with the non-parametric Fisher test. All differences were considered significant at a level of P< 0.05.
| Results |
|---|
|
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Hedonic scores
Comparison of hedonic scores (mean ± SEM) obtained for the three odorants between the two groups of subjects showed that vanillin was rated as pleasant, with no significant difference between the non-fearful (1.9 ± 1.1) and fearful dental subjects (1.9 ± 0.9), and propionic acid as very unpleasant, also with no significant difference between the non-fearful (8.3 ± 0.5) and fearful dental subjects (8.9 ± 0.4). Only eugenol was rated with a significant difference between the two groups: pleasantly by the non-fearful dental subjects (3.4 ± 0.7) and unpleasantly by the fearful dental subjects (7.8 ± 0.6) (F = 21.94, P< 0.001).
Autonomic responses and basic emotions
An example of a simultaneous recording of the six ANS parameters in response to eugenol is presented in Figure 2. In this case, it can be observed that the odor of eugenol induced strong electrodermal (SR: OPD index = 40s ; SP: C+ form) and SBF (NOD index = 30 s) responses, a decrease of the ST and no significant perturbation of the IHR. According to the decision tree (Figure 1), the magnitude of these responses allow the association of this ANS pattern with `disgust' (SR +++, IHR +, ST and SBF ++).
|
The distribution of the verbal and ANS basic emotions associated with each odorant is presented in Figure 3. The number of basic emotions evoked by each of the three odorants is always greater from the autonomic (unconscious) estimation than from the verbal (conscious) estimation (vanillin: 3 verbal versus 6 ANS emotions; eugenol: 6 verbal versus 7 ANS emotions; and propionic acid: 4 verbal versus 6 ANS emotions). The repartition of the verbal as well as the ANS basic emotions is not significantly different between the two groups of subjects for the two non-dental odorants (vanillin: P = 0.64 and 0.36 for the verbal and ANS basic emotions respectively; propionic acid: P = 0.64 and 0.63 for the verbal and ANS basic emotions respectively). The pleasant odorant vanillin was mainly associated with happiness whereas the unpleasant odorant propionic acid was mainly associated with negative basic emotions, especially anger and disgust. By contrast, the odorant eugenol induced two significantly different patterns of verbal (P = 0.036) as well as ANS (P = 0.006) basic emotions between the two groups of subjects, with a greater proportion of positive basic emotions (happiness and surprise) in the non-dental fearful subjects and a greater proportion of negative basic emotions (fear, anger, disgust) in the dental fearful subjects. More particularly, it must be noted that the basic emotion fear was evoked at the conscious (verbal) level, as well as the unconscious (ANS) level, only in the dental fearful subjects.
|
| Discussion |
|---|
|
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The belief that odors may form powerful connections to memories, especially those charged with emotional significance, has been discussed by several authors (Van Toller, 1988
In the dental field, a specific odorant, eugenol, could be potentially charged with a high
emotional significance. The clinging odor of eugenol, which often impregnates the dental office,
could evoke memories of unpleasant dental experiences, since eugenates (cements containing
eugenol) are used in restorative dentistry on vital teeth. The operative procedures can be carried
out on anesthetized or nonanesthetized teeth. However, the use of the drill, in addition to the
sight
of the anesthetic needle in the first case and the fear of pain in the second, represent the greatest
sources of fear and anxiety in dental treatments (Kleinknecht et al., 1973
).
This hypothesis was examined in a previous study by evaluating the quantitative variations of
five autonomic parameters induced by the inhalation of the odor of eugenol (Robin et al.,
1998
). These variations were compared between fearful and non-fearful dental
subjects and
showed that eugenol odor induced two significantly different patterns of ANS responses, mainly
observed through the electrodermal channel. However, one limitation of this study was that it
provided only quantitative data without taking into account the global pattern of the ANS
responses, which has been shown to be more informative when it is transcribed into a basic
emotion (Vernet-Maury et al., 1995a
;
Alaoui-Ismaïli et al., 1997b
).
In this study, the patterns of the ANS responses induced by the inhalation of three odorants
(eugenol, vanillin and propionic acid) were transcribed into one of the basic emotions and their
distribution compared between fearful and non-fearful dental subjects. In both groups, basic
emotions (ANS as well as verbal emotions) evoked by the pleasant odorant vanillin (mainly
happiness) and by the unpleasant one propionic acid (mainly disgust and anger) probably reflect
the hedonic valence of these two odors. It has been shown that the magnitude of the
physiological
responses induced by odorants partially depend on their hedonic tone, pleasant odors inducing
lower responses than unpleasant ones (Kobal et al.,
1991
;
Miltner et al., 1994
;
Brauchli et al., 1995
, Vernet-Maury et al.,
1995a
). By contrast, the distribution
of the basic emotions evoked by the inhalation of the odor of eugenol differs according to the
dental experience. For the non-fearful dental subjects, this odor was mainly associated with
positive basic emotions (happiness and surprise) and, for the fearful dental subjects, this odorant
evoked negative emotions (fear, anger and disgust).
Two main differences emerge from the comparison between the verbal (self-reported or
conscious) evaluation of the basic emotions and the ANS (unconscious) one. The first is the
greatest number of basic emotions found from the ANS evaluation, indicating that such
estimation
is probably more informative, reflecting more various emotional states. The second concerns the
basic emotion anger, which is rarely expressed through the verbal channel whereas the ANS
evaluation revealed a higher occurrence of this emotion. This phenomenon, previously observed
in
a greater number of subjects (Alaoui-Ismaïli et
al., 1997b
),
was also reported by
other authors, in particular the confusion between anger and disgust (Bullock and
Russel, 1986
).
For Vrana (1993
), both the disgust and anger
situations are predicted to
produce self-reported
judgements of `disgusting' because one common-language meaning of disgust is
disapproval of another's actions or principles, which is semantically similar to being
cheated, a common anger theme.
Our results indicate that, at the conscious level (verbal estimation), the emotional state induced by an unpleasant odor (propionic acid) or by an odor evoking negative and aversive feelings (eugenol) is more easily expressed in terms of disgust. At the unconscious level (ANS estimation), this emotional state can always be traduced in terms of disgust, but also in terms of anger. Even though this phenomenon still remains poorly explained, one explanation of the nonverbalization of anger in an experimental context could be the result of a social inhibition.
If the high percentage of disgust, obtained in response to the propionic acid odor and, to a
lesser degree, to the eugenol odor, may traduce an avoidance behavior toward an unpleasant
odor, it cannot be the case for the basic emotion fear, which is rarely evoked by the propionic
acid
odorant yet judged as very unpleasant. Fear is characterized by a strong tachycardia, a decrease in
ST, a moderate variation of the SR and SBF parameters and, especially, negative SP responses,
which have been shown to characterize stimuli with a high emotional load (Vernet-Maury et al., 1996
). The distribution of the
verbal as well as the
ANS basic emotions
revealed that fear
was almost exclusively evoked by the odor of eugenol and only in fearful dental subjects,
probably
reflecting the negative dental experience of these subjects. The influence of general emotional
factors on the apparition of dental fear has been questioned in several studies (Berggren and
Carlsson, 1985
; Kleinhauz et al.,
1992
) which
showed that the initial dental fear seems to
be only weakly related to patients' general emotional reactions. Berggren et
al. (1997
) recently confirmed that most
psychometrically assessed
emotional reactions of
patients
suffering from severe dental fear were within the normal range, especially general anxiety and
depression. Thus, it seems reasonable to relate dental fear to past negative dental experiences
rather than to a personality trait. It can thus be suggested that the odor of eugenol, spontaneously
identified as the typical odor of the dental office, evokes unpleasant feelings such as anxiety, fear
or pain, experienced during painful (or potentially painful) dental care on vital teeth.
In conclusion, the results of this study demonstrate that the transcription of the patterns of
ANS responses induced by the inhalation of odors allows the association of an olfactory
sensation
to a basic emotion, confirming the strong relationship between olfaction and emotion.
Concerning
eugenol, this odorant was shown to evoke negative basic emotions, especially fear, in dental
fearful subjects, thus confirming the potential role of odors as elicitors of emotional memories.
This study also supports the possible influence of the ambient odor, due to eugenol, impregnating
the dental office in strengthening negative conditioning toward dental care. This could be avoid
by
eliminating the odor of eugenol in the dental office. The possibility of masking it by a pleasant
and
relaxing odor, such as lavender (Ludvigson and Rottman,
1989
; Lawless, 1991
), should be
considered.
| Acknowledgments |
|---|
This research was supported by the Danone Institute, France. The authors are very grateful to Sophie Rousmans for her technical assistance in the preparation of the manuscript.
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Accepted February 9, 1999
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) and fearful (
) dental care subjects. The
comparison of these distributions between the two groups of subjects shows significant
differences only for eugenol (verbal emotions: P = 0.036; ANS emotions: P =
0.006) (H = happiness, Su = surprise, Sa = sadness, F = fear, A = anger, D = disgust).
