Chem. Senses 27: 703-709,
2002
© Oxford University Press 2002
Autonomic Nervous System Responses to Odours: the Role of Pleasantness and Arousal
Laboratoire de Neurosciences et Systèmes Sensoriels CNRS UMR 5020 and Université Claude Bernard Lyon 1, 50 avenue Tony Garnier, 69366 Lyon Cedex 07, France
Correspondence to be sent to: M. Bensafi, Laboratoire de Neurosciences et Systèmes Sensoriels CNRS UMR 5020 and Université Claude Bernard Lyon 1, 50 avenue Tony Garnier, 69366 Lyon Cedex 07, France. e-mail: bensafi{at}olfac.univ-lyon1.fr
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Abstract |
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Perception of odours can provoke explicit reactions such as judgements of intensity or pleasantness, and implicit output such as skin conductance or heart rate variations. The main purpose of the present experiment was to ascertain: (i) the correlation between odour ratings (intensity, arousal, pleasantness and familiarity) and activation of the autonomic nervous system, and (ii) the inter-correlation between self-report ratings on intensity, arousal, pleasantness and familiarity dimensions in odour perception. Twelve healthy volunteers were tested in two separate sessions. Firstly, subjects were instructed to smell six odorants (isovaleric acid, thiophenol, pyridine, L-menthol, isoamyl acetate, and 1-8 cineole), while skin conductance and heart rate variations were being measured. During this phase, participants were not asked to give any judgement about the odorants. Secondly, subjects were instructed to rate the odorants on dimensions of intensity, pleasantness, arousal and familiarity (self-report ratings), by giving a mark between 1 (not at all intense, arousing, pleasant or familiar) and 9 (extremely intense, arousing, pleasant or familiar). Results indicated: (i) a pleasantness factor correlated with heart rate variations, (ii) an arousal factor correlated with skin conductance variations, and (iii) a strong correlation between the arousal and intensity dimensions. In conclusion, given that these correlations are also found in other studies using visual and auditory stimuli, these findings provide preliminary information suggesting that autonomic variations in response to olfactory stimuli are probably not modality specific, and may be organized along two main dimensions of pleasantness and arousal, at least for the parameters considered (i.e. heart rate and skin conductance).
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Pleasure and arousal have been identified as the principal dimensions of affective response to the environment (Mehrabian and Russell, 1974
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These authors constructed a set of verbal texts describing different
situations, and a scale for rating them (the Semantic Differential Scale).
When applied to materials describing common events, the first two factors
explaining most of the variance were pleasure and arousal. In this case,
pleasure is defined as the degree to which one has favourable feelings towards
a situation, while arousal is defined as the degree to which one feels excited
in the situation. In order to evoke affective states in a laboratory setting,
some authors have assembled sets of pictures
(Lang et al., 1998a),
sounds (Bradley and Lang,
1999b), odorants (Bensafi,
2001) or words (Bradley and
Lang, 1999a) chosen to elicit a range of positive, neutral or
negative affective states. In such studies, subjects had to rate the pictures,
sounds, odorants or words for pleasure and arousal. Results indicated that the
shape of the distribution is very similar across all sensory modalities:
arousal ratings increase with emotional valence (either positive or negative).
Taken as a whole, the results are consistent with the hypothesis that emotion
stems from two underlying neural systems, appetitive (for positive affective
states) and defensive (for negative affective states), that each vary in
arousal. This organization can be expected to be the same for all modalities.
Besides these subjective evaluations, it is possible to study objectively the
activation (in term of emotional arousal) of these neural subsystems implied
in positive and negative emotions, by recording peripheral and central brain
reactions in response to affective stimuli
(Lang et al.,
1997).
Perception of emotional stimuli can thus lead to explicit reactions such as
verbal responses, and to implicit output such as variations in the autonomic
nervous system. In the visual modality, many studies
(Greenwald et al.,
1989; Lang et al.,
1998b) using affective stimuli showed that skin conductance level
covaries directly with reports of arousal, whatever the sign (positive or
negative) of pleasantness. With regard to heart rate variation, it has been
shown that pleasantness plays a major role in determining cardiac response
during perception (Lang et al.,
1993).
In the olfactory modality, it has been demonstrated that skin conductance
can be modulated by the perception of an odorant
(Van Toller et al.,
1983; Robin et al.,
1999). More specifically, skin conductance variations were found
to be associated with odorant concentration: odorants at weak concentration
evoked lower skin conductance than did more strongly concentrated odorants
(Uryvaev et al.,
1986). In addition, it has been shown in other studies that
electrodermal response variations (skin resistance and ohmic perturbation
duration) could be modulated by odour pleasantness (Alaoui-Ismaïli et
al., 1997a,
b). In these studies, other
dimensions such as the intensity, arousal or familiarity of the odours were
not taken into account. Another study, by Braüchli et al., also
showed a variation in skin conductance level as a function of odour
pleasantness, but not of arousal
(Braüchli et al.
1995). Findings with regard to heart rate variation are similar:
generally, unpleasant odours evoke an increase in heart rate, while pleasant
ones lead to a decrease (Braüchli
et al., 1995; Alaoui-Ismaïli et al.,
1997a,
b).
Even though well established in the visual modality, the link between
self-report ratings (of pleasantness and arousal, for example) and autonomic
variations (such as heart rate and skin conductance) remains unclear in the
olfactory modality. This question was therefore addressed in the present
experiment. Given that the above-mentioned studies have indicated in other
modalities a clear relationship between heart rate variation and pleasantness
on the one hand, and skin conductance variation and arousal on the other [see
also Bradley (Bradley, 2000),
for a review], these were the parameters we chose to measure in our study. As
the perception of an odour can lead to several kinds of judgement, we also
considered assessments of odour intensity and odour familiarity.
The present paper will focus on two objectives. The first concerns the
correlation of self-report ratings of pleasantness, intensity, arousal and
familiarity with variations in autonomic nervous system parameters. In the
olfactory modality, while it seems that pleasantness is a good predictor of
heart rate variation, it is less clear whether skin conductance variation is
influenced by either odour pleasantness or odorant concentration, or both. As
skin conductance variations are modulated by arousal in the visual modality,
such possible interdependence in the olfactory modality was looked for here.
The second objective is related to the correlation between the dimensions of
intensity, arousal, pleasantness and familiarity. The question of the degree
of independence between odour dimensions has been addressed in the literature.
For example, Henion (Henion,
1971) considered the intensity and hedonic dimensions as a single
dimension, while other authors did not go along with this idea (Moskowitz
et al., 1974,
1976;
Doty, 1975). We therefore
analysed the correlations between these dimensions, so as to see whether any
of them varied together.
With this aim, we designed an experiment in which subjects had to smell odorants while skin conductance and heart rate were being recorded. Afterwards, we examined correlations between odour dimensions as given in the subjective reports on the one hand (pleasantness, intensity, arousal and familiarity) and autonomic variations on the other hand (skin conductance and heart rate variations).
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Subjects
The subjects were 12 healthy undergraduate and graduate students (six women and six men, mean age = 26.16 ± 3.07) from the Claude Bernard University of Lyon (France). Five of them were smokers.
As some studies have indicated differences between left-handers and
right-handers during various olfactory tasks
(Toulouse and Vaschide, 1899;
Frye et al., 1992;
Hummel et al., 1998),
only right-handers were tested in this study. Handedness was tested by a
French version of the Edinburgh Laterality Inventory
(Oldfield, 1971). In this
test, subjects were instructed to specify which hand they used in the
following 10 everyday tasks: writing, drawing, sewing, using a pair of
scissors, brushing one's teeth, using a knife, using a spoon, using a broom,
lighting a match and opening a box. To this end, they had to put crosses in
the appropriate column (left hand or right hand) of a form. If they performed
the task usually with this hand, they were to put one cross in the appropriate
column. If they performed the task only with this hand, they were to put two
crosses in the appropriate column. Finally, if they performed the task with
either hand, they were to put a cross in each column.
Before the experiment began, the experimenter explicitly asked the subjects whether they had any olfactory problems, and none declared any. All subjects gave informed consent.
Odours
Six odorants (isovaleric acid, thiophenol, pyridine, L-menthol, isoamyl
acetate, and 1-8 cineole) were used in the experiment. The criteria for
odorant selection were that they should be pure compounds and selected from
among those used in a previous study
(Bensafi et al.,
2001). Five odorants of the set were diluted in mineral oil.
Menthol (crystallized) was diluted in diethylphtalate.
Table 1 indicates the odour
names, their codes and dilutions. In order to have approximately the same
molar concentration for each compound, the dilutions noted in
Table 1 were used.
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The six odorants were presented in 15 ml opaque flasks (aperture diameter: 1.5 cm; 5 ml of solvent). Each odorant was absorbed on a piece of polypropylene (3 x 7 cm) to ensure a better exchange with the air.
Apparatus and data processing
Heart rate and skin conductance were recorded with a PROCOMP+ system
(Thought Technology, Montreal, Canada). A photoplethysmographic probe (3.2
cm/1.8 cm, LED type photodetector), placed on the thumb of the non-dominant
(i.e. left) hand, was used to assess heart rate in beats per minute (bpm).
Skin conductance amplitude in microsiemens (µS) was recorded by two
circular Ag/AgCl electrodes (diameter: 1 cm) placed on the third phalanx of
the forefinger and of the middle finger of the non-dominant hand, according to
previous recommendations (Dawson et
al., 2000). Sampling rate was 4 Hz for heart rate and 32 Hz
for skin conductance. Difference scores were calculated by subtracting the
mean rate for the 1 s preceding flask presentation (baseline) from that for
the 8 s after stimulation. For skin conductance responses, so as to examine
spontaneous fluctuations (especially skin conductance amplitude variations)
during a short 8 s period immediately after presentation of the olfactory
stimuli, tonic rather than phasic recording was used.
Procedure
The study was divided into two parts. Firstly, subjects were instructed to
smell odorants, while autonomic parameters were being recorded. For this,
participants were comfortably seated in a room (7 x 7 x 4 m), in a
semi-reclined position. The room was ventilated prior to the experiment in
order to avoid odorant accumulation. After the recording system had been
installed, the experiment began with a rest period of 3 min. Afterwards, six
odorized flasks were presented. The experimenter instructed the subjects not
to move or to speak during this first session. Their task was only to smell
odorants without any overt response. The inter-trial interval was 2 min. This
range of interval is typically used in studies using odorants and recordings
of autonomic parameters (Robin et
al., 1999; Rousmans
et al., 2000; Brand
and Jacquot, 2001; Bensafi
et al., 2002). Given that six different odorants were
presented, and that each was presented once only, it is very unlikely that any
habituation effect could happen. Flask presentation order was randomized for
each subject. Flasks were presented 1 cm from the right nostril, with a
presentation time of 
1 s. A sniff detector was inserted in the
non-stimulated nostril (which was subsequently closed). Subjects were
instructed to sniff the flask when the experimenter placed it under the open
nostril. When the subject smelt a flask, the sniff detector allowed the time
when the odorant had been smelt to be precisely detected on the autonomic
recordings. Skin conductance and heart rate were recorded concurrently.
We used here single-nostril rather than both-nostril stimulation. It is
likely that the volume of air breathed in is relatively reduced with this
paradigm, and therefore the autonomic responses could be expected to be also
reduced. However, a recent study by Brand and Jacquot indicates that this is
not the case: no difference in skin conductance amplitude variation was
observed whether odorants were presented to one nostril (either the right or
the left) or to both nostrils (Brand and
Jacquot, 2001).
It may be noted that in order to minimize any influence due to the flask being seen by the subjects during the odorant presentation, the experimenter instructed them to focus their attention on a point placed in front of the subject on the wall of the experimental room. As this did not prevent subjects' locating objects in their visual field, the experimenter instructed them to sniff the flask when it was detected under the nostril. A training run before the first session enabled all subjects to manage to sniff at the moment when the experimenter placed the flask under their nostril, without moving their eyes.
Secondly, after the recording session (first session), subjects smelt each flask again and had to evaluate the odour on four dimensions — intensity, arousal, pleasantness and familiarity — by giving a mark between 1 (not at all intense/arousing/pleasant/familiar) and 9 (extremely intense/arousing/pleasant/familiar). It may be noted that, for this session, judgement of arousal refers to the possible effect of the odorant on the subject's own subjective state of arousal. Actually, subjects were instructed to answer the following question: `Please judge your feeling when you smelled the odorant by giving a mark between 1 (not at all arousing) to 9 (extremely arousing)'. Subjects thus smelt the same odorant several times and assessed each dimension separately. As it is very likely that unilateral presentation of odorants can lead to a decrease in the psychological dimension (in particular, perceived intensity), subjects were instructed to smell the odorants with both nostrils.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Two kinds of analyses were performed on the data (processed by odorant). To address the first objective, odour ratings (intensity, arousal, pleasantness and familiarity) were each correlated with heart rate variation on the one hand and skin conductance variation on the other. To fulfil the second objective, we inter-correlated the odour assessments (intensity, arousal, pleasantness and familiarity) provided by the subjects in the second session. A Pearson correlation test on SYSTAT 7.0 (SPSS Inc., Chicago, IL) was used for the analysis. Intensity, arousal, pleasantness and familiarity ratings of odorants given by the subjects during the experimental session are illustrated in Table 2.
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First, with regard to autonomic data, correlations between skin conductance variation and each of the odour dimensions gave the following results: (i) r = -0.452 (n = 6) between pleasantness and skin conductance (P > 0.05); (ii) r = -0.267 (n = 6) between familiarity and skin conductance (P > 0.05); (iii) r = 0.799 (n = 6) between intensity and skin conductance (P = 0.057); (iv) r = 0.862 (n = 6) between arousal and skin conductance (P = 0.027). These results thus indicated that arousal (and maybe intensity) was positively correlated with skin conductance variation: the more arousing (and intense) a stimulus, the more the skin conductance level increased. Figure 1 illustrates this result. Concerning heart rate variations, correlational analysis between heart rate and each of the odour dimensions gave the following results: (i) r = 0.230 (n = 6) between arousal and heart rate (P > 0.05); (ii) r = -0.575 (n = 6) between familiarity and heart rate (P > 0.05); (iii) r = 0.170 (n = 6) between intensity and heart rate (P > 0.05); (iv) r = -0.817 (n = 6) between pleasantness and heart rate (P = 0.047). From these results (illustrated in Figure 2), it seems that pleasantness is the best dimension for predicting heart rate variation. Finally, correlations between heart rate and skin conductance variations indicated a trend for a positive significant correlation (r = 0.754; n = 6; P > 0.05).
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Second, the correlation coefficients between odour dimensions indicated a positive significant correlation between intensity and arousal (r = 0.986, n = 6; P = 0.002). The inter-correlations between pleasantness and familiarity (r = 0.856, n = 6; P > 0.05), intensity and pleasantness (r = -0.6, n = 6; P > 0.05), intensity and familiarity (r = -0.45, n = 6; P > 0.05), arousal and pleasantness (r = -0.620, n = 6; P > 0.05) and arousal and familiarity (r = -0.410, n = 6; P > 0.05) did not reach statistical significance.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The goal of the present study was to determine (i) whether a correlation exists between autonomic variations and subjective reports of odour intensity, arousal, pleasantness and familiarity, and (ii) the relationship between these odour dimensions.
Concerning the first objective, two results are discussed below. The first
finding, which clearly replicated previous results, was that heart rate was
correlated with reports of pleasantness. As noted above, this significant
correlation has also been found in the visual modality, where heart rate is
dependent on stimulus affect value (Lang
et al., 1993). Affective categorization is considered the
most important criterion in odour grouping
(Schiffman, 1974), explaining
why some authors consider odour hedonic tone as the most salient odour
dimension (Ehrlichman and Bastone,
1992). The effects of pleasant and unpleasant odours can lead to
positive and negative affective states, respectively
(Ehrlichman and Halpern,
1988), at different speeds
(Bensafi et al.,
2001), and act differentially on peripheral and central nervous
responses [for a review, see Rouby and Bensafi
(Rouby and Bensafi, 2002)].
Indeed, pleasant and unpleasant odours evoke different electrophysiological
patterns (Kobal et al.,
1992; Kobal, 1994;
Kline et al., 2000)
and activate brain structures differentially
(Zald and Pardo, 1997;
Fulbright et al.,
1998). Finally, further evidence for the existence of different
effects is shown by startle reflex experiments: the amplitude of the reflex
can be increased by unpleasant odours
(Miltner et al.,
1994; Ehrlichman et al.,
1995,
1997) and decreased by
pleasant ones (Ehrlichman et al.,
1997). We found in our study that heart rate was increased in a
context of rejection (due to the presentation of unpleasant odours). This
finding is in line with other studies in the olfactory modality showing heart
rate acceleration when unpleasant odours are presented to human subjects
(Braüchli et al.,
1995; Alaoui-Ismaïli,
1997a,b;
Bensafi et al.,
2002).
Another result of interest was the observation that the arousal dimension
was positively correlated with skin conductance amplitude variation: the more
arousing an odorant, the more the skin conductance amplitude variations
increased. As we have seen previously, this result is in line with other
results that indicate a strong correlation between reports of arousal and skin
conductance level for visual stimuli
(Bradley, 2000). Given that the
electrodermal system is innervated only by the sympathetic nervous system,
this result suggests that these effects may index the reactivity of this
autonomic system, which is greater for arousing than for non-arousing
odorants. Autonomic level activation is very likely related to the activation
of both trigeminal and olfactory nerves. Some odorants used in the present
experiment had a trigeminal component (e.g. pyridine and thiophenol). This
leads us to ask the question whether this autonomic activation was due only to
trigeminal or olfactory nerve stimulation. The answer is probably both given
that pyridine was the less arousing odorant, while thiophenol was the most
arousing.
It has been generally shown in several studies using visual and auditory
stimuli that males are more sensitive than females in their skin conductance
response [for a review, see Bradley
(Bradley, 2000)]: a larger
proportion of males than females showed a significant correlation between
arousal and skin conductance variation in the study by Lang et al.
(Lang et al., 1993).
Given that a small sample of subjects was used in the present study, the
probable gender effect was not analysed, and future experiments are needed to
explore it.
With regard to the second objective, our results indicated no correlation
between intensity, pleasantness and familiarity. These results are at variance
with those of a recent study by Distel et al.
(Distel et al.,
1999), which provided consistent evidence for a positive
correlation between different kinds of judgement: intensity, hedonic strength
and familiarity. The difference between this cross-cultural experiment and our
own study could be due to our limited set of odorants. Of the six odorants
(see Table 2), three were
perceived as unpleasant by the subjects (thiophenol, pyridine and isovaleric
acid) and three as pleasant (L-menthol, isoamyl acetate and 1-8 cineole). The
lack of neutral odours probably increased the variation in emotional valence,
and therefore led to non-significant results. Some of our results, however,
are in accordance with Distel et al.'s study. They define hedonic
strength as absolute ratings of pleasantness without regard to sign, that is
regardless as to whether the odours are pleasant or not. Thus hedonic strength
may refer to the emotional importance of the odour for a subject, something
defined as arousal in our study and in homologous studies in at least three
modalities, showing that arousal ratings increase with hedonic strength:
pleasant and unpleasant pictures (Lang
et al., 1998a), sounds
(Bradley and Lang, 1999b),
odours (Bensafi, 2001) and
words (Bradley and Lang, 1999a)
are usually more arousing than neutral ones. Therefore, the observed
correlation in the study by Distel et al. between intensity and
hedonic strength is in line with our finding of a positive correlation between
inten- sity and arousal, suggesting that these two dimensions tap similar
phenomena in olfaction. The difference between the two judgements may reside
only in the fact that intensity is an external value (an inherent property of
the stimulus), while judgement as to arousal refers to the possible effect of
the odorant on the subjective state.
We did not find any correlation between intensity and pleasantness.
However, a frequent finding in odour hedonic research is an interaction
between intensity and pleasantness: an increase in intensity generally leads
to a decrease in pleasantness rating
(Henion, 1971). Intensity
judgement can be affected by several variables. Zellner and Kautz indicate
that the odour of strawberry was rated as smelling stronger when coloured in
red than when colourless (Zellner and
Kautz, 1990). Hulshoff Pol et al. showed effects of
context on odour intensity judgement: the intensity of odours (either weak or
strong) smelt 25 min earlier influences subsequent odour intensity evaluations
(Hulshoff Pol et al.,
1998). Another example of the influence of external variables is
given by the study by Distel and Hudson
(Distel and Hudson, 2001)
showing that intensity judgement was highest when subjects were given the name
of the odour by the experimenter. An additional variable is probably the
method of odour administration. Indeed, it is very likely that intensity
judgement is affected by single versus double nostril odour administration.
Given that our study used single nostril administration, the volume of air
breathed in was probably relatively reduced, and thus the odorant
concentration delivered to the nose was probably also reduced. Therefore, it
is possible that perceived intensity was likewise reduced, affecting the
perception of pleasant and unpleasant odours differently. It is not, however,
unanimously agreed that odour pleasantness is a linear function of odour
intensity. Indeed, as noted above, Henion
(Henion, 1971) suggested that
odour intensity and odour pleasantness form a single continuum: judgements of
pleasantness and intensity of amyl acetate were highly negatively correlated,
but this hypothesis was untenable when other odorants were considered.
Moskowitz et al., testing the odour of butanol, found that for some
subjects this odour became increasingly pleasant as its concentration rose,
although most participants reported just the opposite
(Moskowitz et al.,
1974). Moreover, Moskowitz et al., using 32 odorants,
suggested that relationships between the two attributes of intensity and
pleasantness are more complex, and depend on the specific odorant used
(Moskowitz et al.,
1976). They found at least four cases: (a) a positive correlation
between inten- sity and pleasantness (e.g. benzaldehyde is neutral at a low
intensity and becomes more pleasant as intensity increases); (b) a negative
correlation (e.g. hexaldehyde, neutral at a low intensity and becoming more
unpleasant as intensity increases); (c) a complex pattern (e.g. 3-hexanol,
which is neutral at low intensity, pleasant at medium intensity, and
unpleasant at high intensity); (d) no correlation between intensity and
pleasantness (e.g. vanillin, pleasant at low, medium and high levels of
intensity). Thus, these studies indicate that odour pleasantness is not always
a function of odour intensity, and that relationships between these two odour
attributes depend on the stimulus and the subject.
Actually, the present study did not test the effect of odour intensity on
odour pleasantness for a given olfactory stimulus. Moreover, in order to
reduce artefacts related to motion and tasks, subjects of this experiment were
instructed to not move and no specific task was given to them immediately
after they smelt the odorants. They were asked to estimate odour dimensions
with both nostrils in a separate session. A future parametric experiment is
therefore needed to explore the effect of the interaction between (i) odour
intensity for a given stimulus, (ii) odour pleasantness, and (iii) the mode of
stimulation, on autonomic variations. In conclusion, our study found strong
correlations between (i) pleasantness and heart rate variation, (ii) arousal
and skin conductance variation, and (iii) the arousal and intensity
dimensions. Given that these correlations have also been found in studies
using visual and auditory stimuli (Bradley,
2000), these results provide preliminary information suggesting
that autonomic variations in response to olfactory stimuli are probably not
modality specific, and may be organized along two main dimensions of
pleasantness and arousal, at least for the parameters considered (i.e. heart
rate and skin conductance).
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Accepted July 19, 2002
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