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Odour liking physiological indices: a correlation of sensory and electrophysiological responses to odour
Food Quality and Preference 13 (2002) 307–316 www.elsevier.com/locate/foodqual
Odour liking physiological indices: a correlation of sensory and electrophysiological responses to odour C.M. Owen*, J. Patterson Sensory Neuroscience Laboratory, School of Biophysical Sciences and Electrical Engineering, Swinburne University of Technology, PO Box 218, Hawthorn, Vic 3122, Australia Received 25 January 2001; received in revised form 21 September 2001; accepted 2 April 2002
Abstract The perception of smell is dominated by an hedonic dimension, with changes in left and right orbitofrontal activation evident in responses to odours of different valence. Electrophysiological (EEG) recordings were used to investigate differences in hemispheric activation associated with different hedonic responses to a low concentration of a single compound (damascenone: fruity, berry smell). Stimulus delivery (air, or air with odour) was synchronised with inspiration using a continuous respiration olfactometer. EEG responses were analysed using traditional power spectrum techniques to determine the relationship of the brain activity to the reported odour liking responses. Differences in response to the odour were evident in comparison with air, and also between response groups. Using the same odour to evoke different hedonic responses, power spectrum analysis revealed a non-significant trend for left frontal differences in EEG associated with different liking responses to damascenone. This demonstrated quantification of the neurophysiological effects associated with odour liking. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Odour liking; Hedonic; Olfactory; EEG; Frequency; Damascenone
1. Introduction The physiological effect of the emotional experience has for years been the focus of research, utilising psychophysiological, electrophysiological and neuroimaging techniques and clinical studies to investigate theories of the physiological organisation of emotion. Davidson (1987, 1992) proposed a theory of hemispheric specialisation for approach and withdrawal processes, evident in changes in anterior activation of the electroencephalogram (EEG). This theory and subsequent evidence has provided a framework for predictions of differences in brain activity responses associated with stimuli perceived as positive and negative, with the left hemisphere specialised for approach and the right hemisphere for withdrawal (Davidson, 1992; Davidson, Ekman, Saron, Senulis & Friesen, 1990; Davidson & Sutton, 1995; Sutton, & Davidson, 2000). Cortical activation of the left hemisphere has been identified with * Corresponding author. Tel.: +61-3-9214-8580; fax: +61-3-98190856. E-mail address: [email protected] (C.M. Owen).
positive emotions and the right with negative emotions (Dimond, Farrington, & Johnson, 1976; Kline, Blackhart, Woodward, Williams, & Schwartz, 2000; Miltner & Braun, 1993; Sutton & Davidson, 2000; Wheeler, Davidson, & Tomarken, 1993). Electrophysiological evidence has demonstrated arousal of approach-related positive affect associated with left anterior cortical activation and arousal of withdrawal-related negative affect associated with right anterior activation (Davidson, 1992; Lane et al., 1997; Sutton & Davidson, 2000). These results support the idea that some aspects of emotional responses are encoded in left/right hemispheric processing. Relatively little olfactory research has been carried out which has delved into the organisation of emotion associated with odour responses. Odour experience is naturally hedonistic; the primary response to odour is liking or disliking, with the most salient attribute of odours being pleasantness or unpleasantness (Ehrlichman & Halpern, 1988). In an evolutionary sense, the olfactory system is one of the most primitive systems in the human body, the importance of which is often underestimated in modern society. Along with the visual system, the olfactory
0950-3293/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S0950-3293(02)00043-5
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system has a short pathway into the brain. Furthermore, it has relatively direct connections to the limbic system, which may be associated with its strong affective and emotional connections (Kline et al., 2000; Marieb, 1998). These connections have been demonstrated in psychophysiological studies revealing physiological changes associated with exposure to pleasant and unpleasant odours (Alaoui-Ismaili, Vernet-Maury, Dittmar, Delhomme, & Chanel, 1997; Brauchli, Ruegg, Etzweiler, & Zeier, 1995; Ehrlichman, Brown, Zhu, & Warrenburg, 1995; Miltner & Braun, 1993; Miltner, Matjak, Braun, Diekmann, & Brody, 1994). Odour places few demands on complex cognitive and attentional processes, and could therefore provide a means for eliciting affective experiences without the interpretative problems accompanying more cognitively saturated techniques such as those using visual or auditory stimuli. The ability of odours to produce pleasant or unpleasant experiences with little cognitive mediation suggests the potential for using odours in research into the differential involvement of the left and right hemispheres in emotional responses (Ehrlichman & Bastone, 1992). The perception of smell is dominated by an hedonic dimension, with exposure to odorants producing robust approach and withdrawal responses (Zald & Pardo, 1997), evident in changes in left and right orbitofrontal activation associated with responses to odours with different valence (Kline et al., 2000). Considerable olfactory research has been conducted investigating responses to different odours using psychophysiological and neurophysiological methods, and to differences in the hedonic response to the test odours, demonstrating the different emotional qualities of odours recognised as positive and negative stimuli (Miltner et al., 1994; Royet et al., 2001; Van Toller, 1988). Recent studies have shown differences in brain electrical activity associated with odour detection responses, with distinct differences in regional brain activity evident for odours of varying valence, even when the odour was not consciously detected (Owen, 1998; Owen & Patterson, 2000). This supported previous reports of changes in regional activation related to hedonic responses (Brauchli et al., 1995; Klemm, Lutes, Hendrix, & Warrenburg, 1992). These findings suggest the potential of the technique to reveal differences in liking responses, even when the odour is at very low concentrations (at or near threshold level), consequently overcoming some of the difficulties associated with the subjective reporting of odour responses. EEG activity has been found to differ significantly between odorant conditions, supporting the hypothesis that odours existing in concentrations at a low or very low level of awareness can affect brain activity and may thus influence mood and behaviour. The principal basis of this study was to investigate trends in hemispheric activation associated with hedonic
responses to a low concentration odour, delivered during natural respiration. The breathing techniques used during odour administration can influence the recording of olfactory responses (Lorig, Matia, Peszka, & Bryant, 1996; Prah, Sears, & Walker, 1995) with nostril flowrate effecting the detection of odorous stimuli (Laing, 1983; Sobel, Khan, Hartley, Sullivan, & Gabrieli, 2000). Human olfactory research has not typically involved the measurement of sniffing or breathing parameters, however, evidence has suggested that variations in these parameters may influence measures of odour perception (Pause, Krauel, Sojka, & Ferstl, 1999; Prah et al., 1995). The odour delivery system used while determining these dynamic brain processes must provide precise temporal presentation of the odour and avoid concomitant excitation of other sensory systems (Kobal & Hummel, 1994) and the use of artificial methods for administering odorous stimuli (such as odorant pulses or ‘blast’ olfactometry) avoided in view of the possible interaction with tactile trigeminal components of sensation (pain or irritation) (Evans, Kobal, Lorig, & Prah, 1993). The adoption of specific breathing techniques can also introduce the confounding effect of divided attention, with the subject attending to breathing instructions and techniques rather than to odour presentation (Pause et al., 1999). EEG responses may be effected by the method of odour administration, with findings of differences in EEG amplitudes and latencies associated with passive breathing and active breathing techniques such as sniffing or velopharyngeal closure (Laing, 1983; Pause et al., 1999; Prah et al., 1995). The potential benefit of synchronising odour stimulus delivery with natural respiration has been recognised and confirmed by research demonstrating the effect of odorants on respiratory behaviour and the importance of monitoring possible respiratory changes during olfactory stimulation (Lorig, 1989; Lorig, Schwartz, Herman, & Lane, 1988; Plattig & Kobal, 1979; Warren, Walker, Drake, & Lutz, 1990; Walker, Kendal-Reed, Hall, Morgan, Polyakov, & Lutz, 2001; Walker, Kurtz, Shore, Ogden, & Reynolds, 1990). The bulk of the research investigating hedonic odour responses has focussed on comparisons of brain activity between pleasant and unpleasant odours (Brauchli et al., 1995; Ehrlichman et al., 1995; Kobal, Hummel, & Van Toller, 1992; Kobal & Kettenmann, 2000; Roescher, Guera, & Kobal, 1998), such as the comparison of responses to pleasant (vanilla), neutral (water) and unpleasant (valerian) odours undertaken by Kline et al. (2000). This research supported left-frontal involvement in positive/approach-related emotion, finding increased left frontal activation associated with the pleasant odour, but failing to demonstrate the expected right frontal effect associated with the unpleasant odour. The authors proposed that the lack of unpleasant response might be partly related to the duration of the FFT
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analysis (over a 1-min period) which may have failed to capture the phasic change in right frontal activation during behavioural withdrawal. Studies such as this comparison of frontal activation in response to odours of different valence have supported the hypothesis of left frontal activation in response to pleasant versus unpleasant stimuli, however little research has examined differences in frontal activation associated with different responses (pleasant versus unpleasant) to the same odour. The current research was designed to use electrophysiological techniques to further investigate hemispheric differences in responses between those who ‘‘liked’’ a compound compared with those who ‘‘disliked’’ the compound. Subjective odour liking responses were correlated with the objective physiological (EEG) responses to investigate differences in perceptual responses to a low concentration odour delivered during natural respiration. The system used in this study incorporated a respiratory monitoring system to permit odour or air delivery synchronous with respiration during the recording of periods of electrical activity associated with the odour response for comparison with electrical activity associated with breathing odour-free air.
2. Method 2.1. Code of conduct and ethics assurance All research was conducted within the parameters and procedures established by the Swinburne University of Technology’s policies on Code of Conduct, Human Experimental Ethics Clearances and Intellectual Property. 2.2. Subjects Thirty-six subjects (males=18, females=18) participated in the study, with a mean age of 24.03 ( 6.59: range 15–43 years). All were right handed, as assessed using the Edinburgh Handedness Inventory (Oldfield, 1971). All subjects were profiled using the Sniffin’ Sticks Test of Olfactory Performance (Burghart, Wedel, Germany). This test of olfactory performance consists of a basic screening test and an advanced test. The screening test includes a basic smell identification task. The advanced test is composed of three sub-tests: odour identification, odour discrimination and a butanol threshold test (Hummel, Sekinger, Wolf, Pauli, & Kobal, 1997). The scores from the Threshold, Discrimination and Identification tests were summed to form the TDI score, with a total maximum score out of 48. Subjects were divided into Liking groups, based on rating responses obtained during the EEG
Table 1 Demographic details and Sniffin’ Sticks TDI scores ( standard deviation) for the Total Group and liking response sub-groups: Like, Neutral and Dislike
Mean age Age range Gender Males Females TDI score
Group (n=36)
Like (n=15)
Neutral (n=13)
Dislike (n=8)
24.036.59 15–43
24.536.89 15–43
23.77 5.97 18–39
23.507.76 18–36
18 18 34.343.72
7 8 35.103.29
8 5 31.90 3.35
3 5 36.563.22
recording. This is further described in the following section. Liking group demographic details and Sniffin’ Sticks Olfactory Performance TDI scores are presented in Table 1. 2.3. Odour liking and strength ratings During the EEG recordings, each participant completed a psychometric rating of the odour (hedonic or emotional response and perceived strength) after each odour delivery trial. These ratings were based on simple 10 cm Likert scales: Liking (strong like=0; strong dislike=10) and Strength (very weak=0; very strong=10). Subjects also provided descriptions of the odour and any associated responses or reactions. Liking ratings were then grouped according to these rating levels: Like (< 4), Neutral (4–6) and Dislike (> 6). 2.4. Odour stimulus preparation The test odour was beta-damascenone (C13H18O; a sweet, fruity, rose, berry odour). A gas form of the odour stimulus was obtained from a pure liquid source (Product Makers; Melbourne, Australia) by bubbling room air through 8 ml of liquid in a 20 ml glass vial sealed by a rubber stopper. The rubber stopper was pierced by two blunt 18 G hypodermic needles (Terumo; Melbourne, Australia), sealed by three-way disposable stopcocks (Discofix#; Braun; Melsungen) fitted with Luer lock terminations. A 2-m length of TygonTM tubing was fitted to the taps by ways of plastic tubing adapters and then inserted into the pump head of a Cole-PalmerTM roller pump. Air was then pumped and recirculated through the liquid for 20 min. At the conclusion of the recirculation, the air was removed from the tubing into a teflon gas sample bag and the tubing flushed out with 350 ml of room air using plastic 50 ml Luer syringes. In this way odour-rich air was prepared for the damascenone stimulus. In GC/MS analysis, the concentration of the odorous gas was determined to be 1.99 ppm (reported threshold: 0.009 ppm; Ohloff, 1994).
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2.5. Odour delivery Odour was delivered using a continuous respiration olfactometer (CRO). The odour syringe was filled with 50 ml of the damascenone gas sample, and similar volume of room air filled the control air syringe. The CRO delivers odour during normal respiration by closely monitoring the subject’s natural respiratory cycle using a pneumotachograph mounted on the facemask with a two-way non-rebreathing valve. Delivery of odour or air is then timed to the subject’s inspiration. The outlet tubing from the computer-controlled delivery syringes was inserted into separate ports in the facemask. The apparatus is described in detail elsewhere (Owen, Patterson, Silberstein, Simpson, Neild, & Pipingas, 1997; Patterson, Owen, Silberstein, Simpson, Pipingas, & Neild, 1998; Owen, Patterson, & Simpson, 1999). Either 1 ml of odour, or 1 ml of air, is delivered into each inspiratory air flow (taking approximately 500 ms/delivery) using a pseudo-random sequence at an air: odour ratio of 3:1, with a minimum of two air delivery between odour deliveries. For this study’s group of participants, there was an average breath duration of 4.9 s ( 0.25), resulting in an average inter-stimulus interval (ISI) of 10–25 s. This delivery ratio is supported by the evidence of the number of air and odour deliveries analysed with each 20 min recording in the current study: Air: M=164 ( 55), range 90–319; Odour: M=55 ( 19), range 29–108. With repeated exposure to odour stimuli, there is a possible habituation effect. However, this possible effect was reduced through the combination of the use of the 3:1 air: odour delivery ratio, the low concentration odour stimulus delivered by the CRO, and the introduction of rest periods between each five minute recording period. 2.6. EEG recordings Brain electrical activity was recorded with a 64-channel ElectroGeodesic Inc (EGI) EEG sensor system (saline electrodes), referenced at Cz channel, with a sample rate of 500 samples/s, and high and low-pass filter settings of 200 and 0.1 Hz, respectively. Stimulus presentation records were achieved by triggering the EGI through its interface port between the acquisition and task computers. The source of the trigger was a pair of specific outputs indicating syringe drive from the CRO, marking the EGI-EEG record when odour, or air, was delivered. 2.7. Procedure All subjects were screened using the Sniffin’ Sticks Test of Olfactory Performance prior to attending an EEG recording session. EEG during stimulus delivery (air or odour) was recorded for 5-min trials, and each
subject participated in four repeated trials resulting in a total of 20 min of EEG recorded. Following each trial, participants completed a rating sheet, using a 10-point Likert scale to indicate their perceived liking and strength ratings, and describing the odour they detected during the recording. Using the CRO delivery technique with the EEG system, differences caused by the test odours in comparison to air without test odours were recorded and analysed, correlating the odour nature with the hedonic/emotive responses. 2.8. Data processing and statistical analysis The EEG data obtained in the 20 min of recording were epoched for 1024 ms periods around the stimulus point for air or odour delivery (100 ms pre-delivery and 924 ms post-delivery), and averaged for air or odour. This resulted in an average of 164 air epochs and 55 odour epochs for averaging. During off-line analysis, the EEG signals were processed for artefact reduction and digitally filtered using a 45 Hz low-pass filter to reduce electrical noise contamination (50 Hz mains). In addition to studying the EEG signals at specific anterior electrode sites, the signals were averaged for left and right frontal electrode sites (grouped at sites equating to around F3 and F4 in the 10/20 system). The raw signals thus collated were exported to ExcelTM and the time series data graphed for the averaged frontal sites and for individual electrodes for the condition, and for liking responses to each cheese odour. The averaged signals for each subject were also subjected to FFT analysis for the 1024 ms epoch period (512 samples). Following the FFT analysis, each subject’s air averages and odour averages were normalised such that the total power in each set totalled 100%. Relative % power was then obtained for the frequency bins of interest (1–4, 4–8, 8–12 Hz) for each condition odour vs air. The use of relative % power in this study was justified due to the protocol adopted, which incorporated both air and odour stimuli randomised throughout the same time frames (each 5-min recording period). It could therefore be assumed that within each time frame the total power for each epoch would remain relatively constant. In view of the use of a no-odour control (air stimulus only), the relative % power was also calculated for the odour–air difference, based on the assumption that such a calculation would account for any common brain responses, and isolate the odourrelated responses. From Excel, graphs of the various frequency bins were prepared and comparisons made between the left and right frontal regions relative to the different liking response groups, and subjected to statistical analysis. Statistical analysis was conducted using SPSS (version 10.0 for Macintosh; Release 10.0.7a; SPSS Inc., 2000). Analysis of variance (ANOVA) was used, with the
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Newman–Keuls post-hoc test and P < 0.05 for identifying significant results.
3. Results 3.1. Olfactory performance The mean TDI score of the Sniffin’ Sticks Test of Olfactory Performance screening test (M=34.34 3.72; range 22.25–40.50) indicated that all subjects were within the range for normal olfactory function (Kobal et al., 2000). One-way ANOVA with Liking Group (Like, Neutral, Dislike) as the between-subjects factor was conducted for each olfactory performance task. Results revealed that the Threshold scores differed significantly across liking groups [F (2,33)=3.644, P < 0.01] and there was a significant difference in the TDI scores across liking sub-groups [F (2,33)=5.751, P < 0.05], but there was no significant difference in the mean scores of the liking sub-groups for the Discrimination and Identification tasks. Newman–Keuls post-hoc comparisons revealed that the mean Threshold and TDI scores for the Neutral response group were significantly lower than the scores for both the Like and Dislike response groups, as seen in Table 2. 3.2. Odour liking The mean liking responses were calculated from the subjective odour ratings provided following each EEG recording trial, where the participants had to rate their liking for the odour on a scale of 0 (strong like) to 10 (strong dislike). Liking sub-groups were formed based
Table 2 Mean Sniffin’ Sticks sub-test and TDI scores ( standard deviation) for the liking response sub-groups: Like, Neutral and Dislike
Threshold Discrimination Identification TDI Score
Like (n=15)
Neutral (n=13)
Dislike (n=8)
8.70 12.80 13.60 35.10
6.98 11.85 13.08 31.90
9.81 13.13 13.50 36.56
( 2.35) ( 1.47) ( 1.50) ( 3.30)
( 2.34) ( 2.73) ( 1.19) ( 3.35)
( 2.75) ( 1.73) ( 1.31) ( 3.22)
Table 3 Mean Liking and Strength response ratings ( standard deviation) for the liking response sub-groups: Like, Neutral and Dislike
Liking Mean Liking Range Strength Mean Strength Range
Like (n=15)
Neutral (n=13)
Dislike (n=8)
2.64 ( 0. 91) (0.6–3.7) 4.15 ( 1.99) (0.7–7.38)
4.99 ( 0.58) (4.1–5.8) 4.40 ( 1.50) (0.8–6.35)
7.05 ( 1.06) (6.0–9.2) 5.54 ( 1.65) (3.28–8.70)
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on the mean liking score for all four trials, with mean liking ratings for each sub-groups summarised in Table 3. Independent groups One-Way ANOVAs with Liking Group (Like, Neutral, Dislike) as the between-subjects factor were computed for the mean Liking and Strength responses, revealing significant differences in mean Liking scores between the designated sub-groups [F(2,33)=75.778, P < 0.001, Z2=0.82]. There was no significant difference in Strength scores between the three Liking sub-groups [F(2,33)=1.703, P > 0.05]. Newman–Keuls post-hoc comparisons showed that the Like group had significantly lower Liking scores than the Neutral group, which had significantly lower scores than the Dislike group, as shown in Table 3. This analysis supported the post-hoc formation of these Liking sub-groups. 3.3. EEG responses In the interest of exploring the effect of liking responses to an odour, frequency and frontal EEG responses were examined for each liking response group. A 3 3 2 mixed design ANOVA was conducted on the Odour relative % power responses, with Liking group (Like, Neutral, Dislike) as a between subjects factor, and with frequency range (1–4, 4–8, and 8– 12 Hz) and frontal location (Left, Right) as within subject factors. As could be predicted in consideration of the relative % power frequency groupings applied here, there was a significant within subject effect for frequency [F(2,66)=200.501, P < 0.001, 2=0.86], with significant differences in mean relative % frequencies across all liking groups for 1–4 Hz range (68.55 2.42), 4–8 Hz rang (11.23 1.06) and 8–12 Hz range (5.28 2.64). However, there was no significant interaction between frequency and liking group [F(4,66)=0.11, P > 0.05]. There was no significant within subject effect for frontal location [F(1,33)=0.115, P > 0.05]. There was no significant interaction between liking group, frequency and frontal location [F(4, 66)=2.433, P=0.098, 2=0.13]. Fig. 1 depicts the means for the relative % power odour responses for the three frequency bands for liking sub-groups and left versus right frontal responses. Although there were no significant differences associated with frontal region of activation in these frequency bands, a study of the means reveals a trend associated with liking group responses for left versus right frontal locations, as shown in Table 4. In the 1–4 Hz (delta) range, there was a trend for slightly greater left frontal activation cf. right frontal activation for the Like group, and a stronger reverse trend for the Dislike group, with little difference evident between 1 and 4 Hz frontal responses for the Neutral group. Similarly, in the 4–8 Hz (theta) and 8–12 Hz (alpha) ranges,
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Fig. 1. Relative percent power (with standard error bars) for the 1–4, 4–8, and 8–12 Hz power bands in response to the odour stimulus (damascenone) for liking response sub-groups: Like (n=15), Neutral (n=13) and Dislike (n=8). The columns represent Left (white) and Right (black) frontal activation. The Y-axis shows power normalised as a relative percentage. In the 4–8 and 8–12 Hz bands there was a trend for reduced left frontal activation for the Like and Neutral groups and increased activation for the Dislike group relative to the right frontal activation. (Note the different Y-axis values for the 1–4 Hz range in comparison to the 4–8 Hz and 8–12 Hz ranges.).
Table 4 Frontal (Left vs Right) mean relative % power odour responses ( SD), grouped in frequency bins, for the odour liking response subgroups: Like, Neutral and Dislike Relative% power odour response
Like (n=15)
1–4 Hz Left mean 1–4 Hz Right mean
67.20 ( 5.84) 71.86 ( 6.28) 65.20 ( 5.53) 70.20 ( 5.94)
62.38 ( 8.00) 74.43 ( 7.57)
4–8 Hz Left mean 4–8 Hz Right mean
9.69 ( 2.41) 10.13 ( 2.59) 10.59 ( 2.45) 12.47 ( 2.64)
14.99 ( 3.30) 9.94 ( 3.59)
8–12 Hz Left mean 8–12 Hz Right mean
2.83 ( 1.22) 2.37 ( 1.21)
Neutral (n=13) Dislike (n=8)
5.58 ( 1.32) 5.13 ( 1.30)
8.95 ( 1.68) 6.82 ( 1.65)
there was little difference between left and right frontal odour responses in the Like responses or in the Neutral responses but the Dislike group trend was reversed with greater right frontal 4–8 and 8–12 Hz activation. In general, there was an increase in theta activity in the left frontal location and an increase in alpha activity in the both the left and right frontal locations associated with Dislike for the odour (cf. Like or Neutral responses).
Relative % power was also calculated for the odourair difference, to determine if the significant differences observed for the odour responses were consistent across the odour-air difference condition. A 3 3 2 mixed design ANOVA was conducted on the relative % power difference (Odour minus Air) responses, with Liking group (Like, Neutral, Dislike) as a between subjects factor, and with frequency range (1–4, 4–8, and 8–12 Hz) and frontal location (Left, Right) as within subject factors. There were no significant within or between subject effects for frontal location or frequency range for the liking groups (P > 0.05). However, the mean responses for the difference frequency ranges in the left versus right frontal locations suggested a trend in difference (odour-air) responses associated with liking group. In the 1–4 Hz (delta) range, there was little difference in left frontal odour-related activation associated with the odour cf. right frontal activation for the Like group, a slight increase in odour-related activation in the left cf. right frontal for the Neutral group, and a trend for a decrease in odour-related activation in the left cf. right frontal location for the Dislike group. In the 4–8 Hz (theta) range, there was a trend for a slight decrease in
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activation associated with the left frontal odour-related difference responses for the Like and Neutral groups, but an increase in left frontal odour-related activation cf. right frontal activation for the Dislike group. The increase in theta activity in the left frontal location and an increase in alpha activity in the both the left and right frontal locations associated with Dislike for the odour (cf. Like or Neutral responses), observed for the odour responses, was again evident in the difference responses.
4. Discussion Although there were no significant interactions between liking responses, frontal location and relative% power evident in the current study, there was evidence of a trend for differences in left and right frontal power differences associated with Like or Dislike for the odour. Although there was little difference in left vs right frontal responses for the Like and Neutral groups, there was a trend for greater right frontal activation in the 1–4 Hz range and greater left frontal activation in the 4–8 and 8–12 Hz ranges for the Dislike group. In addition, there was evidence to suggest an increase in theta activity in the left frontal location and an increase in alpha activity in the both the left and right frontal locations associated with Dislike for the odour (cf. Like or Neutral responses). The hedonic effect of odours on brain electrical activity has been described in the literature as differences in anterior brain activity associated with pleasant and unpleasant odours (Brauchli et al., 1995; Ehrlichman et al., 1995; Kobal et al., 1992; Roescher et al., 1998). A particular association between left frontal activation and pleasant odours has been described (Kline et al., 2000), supporting previous studies of positive emotional responses activating the left frontal region (Davidson, 1992; Lane et al., 1997; Sutton & Davidson, 2000). This study approached this research question from a different direction by investigating different liking (pleasant, unpleasant) responses to one particular odour. While failing to find significant differences in the relative power of frontal responses associated with reported like or dislike for the odour, there was a trend for differences in theta and alpha responses for Dislike group cf. the Like and Neutral groups, particularly in the left frontal location. The presentation of damascenone resulted in a lower relative power (non-significant) for those who reported liking the odour and higher relative power for those who disliked the odour when compared to those with a neutral response. This extends previous findings from electrophysiological and neuroimaging studies (Klemm et al., 1992; Kline et al., 2000; Kobal et al., 1992; Kobal & Kettenmann, 2000) which reported differences in left frontal activation associated with
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stimulation by a pleasant odour in comparison with stimulation by an unpleasant odour. The trend for reduced left frontal activation in the 4–8 Hz or theta range associated with a like response also support previous findings of reduced theta activity in response to pleasant food odours such as chocolate (synthetic and real), spearmint (synthetic) and spiced apple (Lorig & Schwartz, 1988; Lorig, Herman, Schwartz, & Cain, 1990; Martin, 1998). However, it has been proposed that the effect of odours on theta activity may actually be a reflection of the odour’s ability to attract or distract and therefore reflect shifts in attention associated with the emotional reaction to the odour (Martin, 1998). This has been supported previously by findings of an apparent association between changes in theta activity and self-reports of tension and anxiety responses (Lorig & Schwartz, 1988). It has also been proposed that the olfactory effects on theta may be specific to different odours possessing similar psychological properties (Martin, 1998). In the current study, the evidence (non-significant) of increased theta activity in the left frontal region evident in the Dislike responses in comparison with the Like and Neutral responses may reflect the shift in attention associated with a dislike response common to different cheese odours and associated with the similar psychological (hedonic) response to the odours. As cortical alpha power has reported to be inversely related to cortical activity (Coan, Allen, & HarmonJones, 2001), suppression of alpha activity has been equated to an increase in activation in response to stimulation. This has been demonstrated in response to visual and auditory stimulation (Brauchli et al., 1995) and has more recently been reported by EEG studies in response to olfactory stimulation (Brauchli et al., 1995; Lorig, 1994; Lorig et al., 1990; Lorig, Huffman, DeMartino, & De Marco, 1991; Schwartz, Wright, Polak, Kline, & Dikman, 1992; Van Toller et al., 1993). Due to the protocol used in the current study, it may have been expected that there would be an increase in alpha due to the test conditions (darkened room, calming breathing), similar to the increase in alpha associated with a ‘restful’ state (Klemm et al., 1992). Such an effect would be common to both the air and odour conditions due to the experimental design. Although it was not significant, the consistent trend in alpha band left frontal decreases associated with liking for an odour (cf. dislike) was found in both the relative % power of the odour responses and the odour–air differences, suggesting the validity of the assumption that these decreases are related to the odour stimulus. The focus of previous research on electrophysiological changes associated with hedonic responses to different odours has introduced potentially confounding issues associated with the different odour stimuli used. The possible intranasal trigeminal stimulation associated
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with the unpleasant odours used may have caused the effects seen in some studies to be related to differences in sensory perception (Brauchli et al., 1995). A study by Brauchli et al. (1995) demonstrated an increased autonomic arousal in response to the unpleasant odour. The authors reported a greater increase in alpha power in response to the unpleasant odour in comparison to the pleasant odour. Decreases in alpha are common in EEG research, and are taken to be suggestive of cognitive activity, but are more commonly associated with cortical arousal due to sensory stimulation (Lorig et al., 1990). This was interpreted as suggesting that stimulation with an unpleasant odour may lead to stronger cortical deactivation than stimulation with a pleasant odour, as also suggested by previous research (Ehrlichman & Bastone, 1992; Miltner et al., 1994). Evidence from the current study can only suggest the existence of a trend towards decreased alpha associated with a liking response, but has contributed to and extended this research direction by demonstrating this hedonic effect using an odour stimulus that evoked different hedonic effects in the subject population. The approach-withdrawal theory (Davidson, 1987, 1992) proposed that approach-related positive responses would be evident in changes in anterior EEG activation in the left frontal region, seen as decreased alpha activation (increased arousal or attention) in response to the positive stimuli and a corresponding increased alpha activation in response to negative stimuli. Changes in right anterior activation would be predicted with withdrawal-related negative responses, seen in decreased alpha activation right frontal response to negative stimuli, and a corresponding increased alpha activation right frontal response to positive arousal. Although there was evidence of a trend in alpha changes associated with like vs dislike, the current study did not find the significant differences in left or right frontal activation predicted by the approach-withdrawal theory. This may have been due in part to the range of hedonic responses evoked by the odour, and in particular to the degree of negativity involved in the hedonic response. The perceived Dislike response to the test odour was possibly a less potent negative response than that used in the emotional studies. This may therefore have reduced the effect of the negative response which was predicted by the approach-withdrawal theory (Davidson, 1987, 1992). A lack of significant right frontal differences was also reported by Kline et al. (2000), with a possible explanation offered associated with the period of the FFT was computed—over an entire minute— which may have caused the phasic right frontal activation during behavioural withdrawal to be missed. In the current study, the FFT was computed over a 900 ms post-stimulus period in an attempt to analyse the cortical arousal due to sensory stimulation, and again the right frontal activation did not reveal the negative
withdrawal response. It would therefore appear that the duration of the FFT analysis, as proposed by Kline et al. (2000), may be a potential dominant contributor to this lack of right frontal negative effect. While not fully supporting the predictions for hedonic-related EEG changes, this study has extended olfactory research by demonstrating the consistency of the left frontal response associated with liking an odour. In taking a different approach and using the same odour to evoke different hedonic responses, these results have provided further non-significant evidence of changes in left frontal activation associated with the hedonic response. Future studies with greater numbers of subjects and different odours (particularly using odours which may evoke stronger negative reactions) will provide evidence of the significance or robustness of these changes in frontal activation associated with the hedonic response. This application of objective physiological techniques to sensory studies has the potential to contribute to an understanding of the sensory qualities associated with odour perception and liking.
Acknowledgements This work was conducted in collaboration with the Australian Grape and Wine Research and Development Corporation, with additional support from the Cooperative Research Centre for International Food Manufacture and Packaging Science. References Alaoui-Ismaili, O., Vernet-Maury, E., Dittmar, A., Delhomme, G., & Chanel, J. (1997). Odor hedonics: connection with emotional response estimated by autonomic parameters. Chemical Senses, 22, 237–248. Brauchli, P., Ruegg, P. B., Etzweiler, F., & Zeier, H. (1995). Electrocortical and autonomic alteration by administration of a pleasant and an unpleasant odor. Chemical Senses, 20, 505–515. Coan, J. A., Allen, J. J. B., & Harmon-Jones, E. (2001). Voluntary facial expression and hemispheric asymmetry over the frontal cortex. Psychophysiology, 38, 912–925. Davidson, R. J. (1987). Cerebral asymmetry and the nature of emotion: implications for the study of individual differences and psychopathology. In R. Takahashi, P. Flor-Henry, J. Gruzelier, & S. Niwa (Eds.), Cerebral dynamics, laterality and psychophathology (pp. 71–83). Netherlands: Elsevier Science. Davidson, R. J. (1992). Anterior cerebral asymmetry and the nature of emotion. Brain and Cognition, 20, 125–151. Davidson, R. J., Ekman, P., Saron, C. D., Senulis, J. A., & Friesen, W. V. (1990). Approach- withdrawal and cerebral asymmetry: emotional expression and brain physiology I. Journal of Personality and Social Psychology, 58(2), 330–341. Davidson, R. J., & Sutton, S. K. (1995). Affective neuroscience: the emergence of a discipline. Current Opinions in Neurobiology, 5, 217–224. Dimond, S. J., Farrington, L., & Johnson, P. (1976). Differing emotional response from right and left hemispheres. Nature, 261, 690–692. Ehrlichman, H., & Bastone, L. (1992). Olfaction and emotion. In M. J. Serby, & K. L. Chobor (Eds.), Science of olfaction (pp. 410– 438). New York: Springer-Verlag.
C.M. Owen, J. Patterson / Food Quality and Preference 13 (2002) 307–316 Ehrlichman, H., Brown, S., Zhu, J., & Warrenburg, S. (1995). Startle reflex modulation during exposure to pleasant and unpleasant odors. Psychophysiology, 32, 150–154. Ehrlichman, H., & Halpern, J. N. (1988). Affect and memory: effects of pleasant and unpleasant odors on retrieval of happy and unhappy memories. Journal of Personality and Social Psychology, 55(5), 769–779. Evans, W. J., Kobal, G., Lorig, T. S., & Prah, J. D. (1993). Suggestions for collection and reporting of chemosensory (olfactory) eventrelated potentials. Chemical Senses, 18, 751–756. Hummel, T., Sekinger, B., Wolf, S. R., Pauli, E., & Kobal, G. (1997). ‘‘Sniffin’ Sticks’’: olfactory performance assessed by the combined testing of odor identification, odor discrimination, and olfactory thresholds. Chemical Senses, 22, 39–52. Klemm, W. R., Lutes, S. D., Hendrix, D. V., & Warrenburg, S. (1992). Topographical EEG maps of human responses to odors. Chemical Senses, 17(3), 347–361. Kline, J. P., Blackhart, G. C., Woodward, K. M., Williams, S. R., & Schwartz, G. E. R. (2000). Anterior electroencephalographic asymmetry changes in elderly women in response to a pleasant and unpleasant odor. Biological Psychology, 52, 241–250. Kobal, G., & Hummel, T. (1994). Olfactory (chemosensory) eventrelated potentials. Toxicology and Industrial Health, 10, 587–596. Kobal, G., Hummel, T., & Van Toller, S. (1992). Differences in human chemosensory evoked potentials to olfactory and somatosensory chemical stimuli presented to left and right nostrils. Chemical Senses, 17, 233–244. Kobal, G., & Kettenmann, B. (2000). Olfactory functional imaging and physiology. International Journal of Psychophysiology, 36, 157– 163. Kobal, G., Klimek, L., Wolfensberger, M., Gudziol, H., Temmel, A., Owen, C. M., Seeber, H., Pauli, E., & Hummel, T. (2000). Multicenter investigation of 1,036 subjects using a standardized method for the assessment of olfactory function combining tests of odor identification, odor discrimination, and olfactory thresholds. European Archives of Otorhinolaryngology, 257, 205–211. Laing, D. G. (1983). Natural sniffing gives optimum odour perception for humans. Perception, 12, 99–117. Lane, R. D., Reiman, E. M., Bradley, M. M., Lang, P. J., Ahern, G. L., Davidson, R. J., & Schwartz, G. E. (1997). Neuroanatomical correlates of pleasant and unpleasant emotion. Neuropsychologia, 35(11), 1437–1444. Lorig, T. S. (1989). Human EEG and odor response. Progress in Neurobiology, 33, 387–398. Lorig, T. S. (1994). EEG and ERP studies using low-level odor exposure in normal subjects. Toxicology & Industrial Health, 10, 579–586. Lorig, T. S., Herman, K. B., Schwartz, G. E., & Cain, W. S. (1990). EEG activity during administration of low-concentration odors. Bulletin of the Psychonomic Society, 28(5), 405–408. Lorig, T. S., Huffman, E., DeMartino, A., & DeMarco, J. (1991). The effects of low concentration odors on EEG activity and behaviour. Journal of Psychophysiology, 5, 69–77. Lorig, T. S., Matia, D. C., Peszka, J., & Bryant, D. N. (1996). The effects of active and passive stimulation on chemosensory eventrelated potentials. International Journal of Psychophysiology, 23, 199–205. Lorig, T. S., & Schwartz, G. E. (1988). EEG activity during administration of undetected odors. Chemical Senses, 13, 710. Lorig, T. S., Schwartz, G. E., Herman, K. B., & Lane, R. D. (1988). Brain and odor: II EEG activity during nose and mouth breathing. Psychophysiology, 16, 285–287. Marieb, E. (1998). Human anatomy and physiology (4th ed.). Menlo Park, California: Addison Wesley Longman. Martin, G. N. (1998). Human electroencephalographic (EEG) response to olfactory stimulation: two experiments using the aroma of food. International Journal of Psychophysiology, 30, 287– 302.
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Odour liking physiological indices: a correlation of sensory and electrophysiological responses to odour C.M. Owen*, J. Patterson Sensory Neuroscience Laboratory, School of Biophysical Sciences and Electrical Engineering, Swinburne University of Technology, PO Box 218, Hawthorn, Vic 3122, Australia Received 25 January 2001; received in revised form 21 September 2001; accepted 2 April 2002
Abstract The perception of smell is dominated by an hedonic dimension, with changes in left and right orbitofrontal activation evident in responses to odours of different valence. Electrophysiological (EEG) recordings were used to investigate differences in hemispheric activation associated with different hedonic responses to a low concentration of a single compound (damascenone: fruity, berry smell). Stimulus delivery (air, or air with odour) was synchronised with inspiration using a continuous respiration olfactometer. EEG responses were analysed using traditional power spectrum techniques to determine the relationship of the brain activity to the reported odour liking responses. Differences in response to the odour were evident in comparison with air, and also between response groups. Using the same odour to evoke different hedonic responses, power spectrum analysis revealed a non-significant trend for left frontal differences in EEG associated with different liking responses to damascenone. This demonstrated quantification of the neurophysiological effects associated with odour liking. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Odour liking; Hedonic; Olfactory; EEG; Frequency; Damascenone
1. Introduction The physiological effect of the emotional experience has for years been the focus of research, utilising psychophysiological, electrophysiological and neuroimaging techniques and clinical studies to investigate theories of the physiological organisation of emotion. Davidson (1987, 1992) proposed a theory of hemispheric specialisation for approach and withdrawal processes, evident in changes in anterior activation of the electroencephalogram (EEG). This theory and subsequent evidence has provided a framework for predictions of differences in brain activity responses associated with stimuli perceived as positive and negative, with the left hemisphere specialised for approach and the right hemisphere for withdrawal (Davidson, 1992; Davidson, Ekman, Saron, Senulis & Friesen, 1990; Davidson & Sutton, 1995; Sutton, & Davidson, 2000). Cortical activation of the left hemisphere has been identified with * Corresponding author. Tel.: +61-3-9214-8580; fax: +61-3-98190856. E-mail address: [email protected] (C.M. Owen).
positive emotions and the right with negative emotions (Dimond, Farrington, & Johnson, 1976; Kline, Blackhart, Woodward, Williams, & Schwartz, 2000; Miltner & Braun, 1993; Sutton & Davidson, 2000; Wheeler, Davidson, & Tomarken, 1993). Electrophysiological evidence has demonstrated arousal of approach-related positive affect associated with left anterior cortical activation and arousal of withdrawal-related negative affect associated with right anterior activation (Davidson, 1992; Lane et al., 1997; Sutton & Davidson, 2000). These results support the idea that some aspects of emotional responses are encoded in left/right hemispheric processing. Relatively little olfactory research has been carried out which has delved into the organisation of emotion associated with odour responses. Odour experience is naturally hedonistic; the primary response to odour is liking or disliking, with the most salient attribute of odours being pleasantness or unpleasantness (Ehrlichman & Halpern, 1988). In an evolutionary sense, the olfactory system is one of the most primitive systems in the human body, the importance of which is often underestimated in modern society. Along with the visual system, the olfactory
0950-3293/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S0950-3293(02)00043-5
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system has a short pathway into the brain. Furthermore, it has relatively direct connections to the limbic system, which may be associated with its strong affective and emotional connections (Kline et al., 2000; Marieb, 1998). These connections have been demonstrated in psychophysiological studies revealing physiological changes associated with exposure to pleasant and unpleasant odours (Alaoui-Ismaili, Vernet-Maury, Dittmar, Delhomme, & Chanel, 1997; Brauchli, Ruegg, Etzweiler, & Zeier, 1995; Ehrlichman, Brown, Zhu, & Warrenburg, 1995; Miltner & Braun, 1993; Miltner, Matjak, Braun, Diekmann, & Brody, 1994). Odour places few demands on complex cognitive and attentional processes, and could therefore provide a means for eliciting affective experiences without the interpretative problems accompanying more cognitively saturated techniques such as those using visual or auditory stimuli. The ability of odours to produce pleasant or unpleasant experiences with little cognitive mediation suggests the potential for using odours in research into the differential involvement of the left and right hemispheres in emotional responses (Ehrlichman & Bastone, 1992). The perception of smell is dominated by an hedonic dimension, with exposure to odorants producing robust approach and withdrawal responses (Zald & Pardo, 1997), evident in changes in left and right orbitofrontal activation associated with responses to odours with different valence (Kline et al., 2000). Considerable olfactory research has been conducted investigating responses to different odours using psychophysiological and neurophysiological methods, and to differences in the hedonic response to the test odours, demonstrating the different emotional qualities of odours recognised as positive and negative stimuli (Miltner et al., 1994; Royet et al., 2001; Van Toller, 1988). Recent studies have shown differences in brain electrical activity associated with odour detection responses, with distinct differences in regional brain activity evident for odours of varying valence, even when the odour was not consciously detected (Owen, 1998; Owen & Patterson, 2000). This supported previous reports of changes in regional activation related to hedonic responses (Brauchli et al., 1995; Klemm, Lutes, Hendrix, & Warrenburg, 1992). These findings suggest the potential of the technique to reveal differences in liking responses, even when the odour is at very low concentrations (at or near threshold level), consequently overcoming some of the difficulties associated with the subjective reporting of odour responses. EEG activity has been found to differ significantly between odorant conditions, supporting the hypothesis that odours existing in concentrations at a low or very low level of awareness can affect brain activity and may thus influence mood and behaviour. The principal basis of this study was to investigate trends in hemispheric activation associated with hedonic
responses to a low concentration odour, delivered during natural respiration. The breathing techniques used during odour administration can influence the recording of olfactory responses (Lorig, Matia, Peszka, & Bryant, 1996; Prah, Sears, & Walker, 1995) with nostril flowrate effecting the detection of odorous stimuli (Laing, 1983; Sobel, Khan, Hartley, Sullivan, & Gabrieli, 2000). Human olfactory research has not typically involved the measurement of sniffing or breathing parameters, however, evidence has suggested that variations in these parameters may influence measures of odour perception (Pause, Krauel, Sojka, & Ferstl, 1999; Prah et al., 1995). The odour delivery system used while determining these dynamic brain processes must provide precise temporal presentation of the odour and avoid concomitant excitation of other sensory systems (Kobal & Hummel, 1994) and the use of artificial methods for administering odorous stimuli (such as odorant pulses or ‘blast’ olfactometry) avoided in view of the possible interaction with tactile trigeminal components of sensation (pain or irritation) (Evans, Kobal, Lorig, & Prah, 1993). The adoption of specific breathing techniques can also introduce the confounding effect of divided attention, with the subject attending to breathing instructions and techniques rather than to odour presentation (Pause et al., 1999). EEG responses may be effected by the method of odour administration, with findings of differences in EEG amplitudes and latencies associated with passive breathing and active breathing techniques such as sniffing or velopharyngeal closure (Laing, 1983; Pause et al., 1999; Prah et al., 1995). The potential benefit of synchronising odour stimulus delivery with natural respiration has been recognised and confirmed by research demonstrating the effect of odorants on respiratory behaviour and the importance of monitoring possible respiratory changes during olfactory stimulation (Lorig, 1989; Lorig, Schwartz, Herman, & Lane, 1988; Plattig & Kobal, 1979; Warren, Walker, Drake, & Lutz, 1990; Walker, Kendal-Reed, Hall, Morgan, Polyakov, & Lutz, 2001; Walker, Kurtz, Shore, Ogden, & Reynolds, 1990). The bulk of the research investigating hedonic odour responses has focussed on comparisons of brain activity between pleasant and unpleasant odours (Brauchli et al., 1995; Ehrlichman et al., 1995; Kobal, Hummel, & Van Toller, 1992; Kobal & Kettenmann, 2000; Roescher, Guera, & Kobal, 1998), such as the comparison of responses to pleasant (vanilla), neutral (water) and unpleasant (valerian) odours undertaken by Kline et al. (2000). This research supported left-frontal involvement in positive/approach-related emotion, finding increased left frontal activation associated with the pleasant odour, but failing to demonstrate the expected right frontal effect associated with the unpleasant odour. The authors proposed that the lack of unpleasant response might be partly related to the duration of the FFT
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analysis (over a 1-min period) which may have failed to capture the phasic change in right frontal activation during behavioural withdrawal. Studies such as this comparison of frontal activation in response to odours of different valence have supported the hypothesis of left frontal activation in response to pleasant versus unpleasant stimuli, however little research has examined differences in frontal activation associated with different responses (pleasant versus unpleasant) to the same odour. The current research was designed to use electrophysiological techniques to further investigate hemispheric differences in responses between those who ‘‘liked’’ a compound compared with those who ‘‘disliked’’ the compound. Subjective odour liking responses were correlated with the objective physiological (EEG) responses to investigate differences in perceptual responses to a low concentration odour delivered during natural respiration. The system used in this study incorporated a respiratory monitoring system to permit odour or air delivery synchronous with respiration during the recording of periods of electrical activity associated with the odour response for comparison with electrical activity associated with breathing odour-free air.
2. Method 2.1. Code of conduct and ethics assurance All research was conducted within the parameters and procedures established by the Swinburne University of Technology’s policies on Code of Conduct, Human Experimental Ethics Clearances and Intellectual Property. 2.2. Subjects Thirty-six subjects (males=18, females=18) participated in the study, with a mean age of 24.03 ( 6.59: range 15–43 years). All were right handed, as assessed using the Edinburgh Handedness Inventory (Oldfield, 1971). All subjects were profiled using the Sniffin’ Sticks Test of Olfactory Performance (Burghart, Wedel, Germany). This test of olfactory performance consists of a basic screening test and an advanced test. The screening test includes a basic smell identification task. The advanced test is composed of three sub-tests: odour identification, odour discrimination and a butanol threshold test (Hummel, Sekinger, Wolf, Pauli, & Kobal, 1997). The scores from the Threshold, Discrimination and Identification tests were summed to form the TDI score, with a total maximum score out of 48. Subjects were divided into Liking groups, based on rating responses obtained during the EEG
Table 1 Demographic details and Sniffin’ Sticks TDI scores ( standard deviation) for the Total Group and liking response sub-groups: Like, Neutral and Dislike
Mean age Age range Gender Males Females TDI score
Group (n=36)
Like (n=15)
Neutral (n=13)
Dislike (n=8)
24.036.59 15–43
24.536.89 15–43
23.77 5.97 18–39
23.507.76 18–36
18 18 34.343.72
7 8 35.103.29
8 5 31.90 3.35
3 5 36.563.22
recording. This is further described in the following section. Liking group demographic details and Sniffin’ Sticks Olfactory Performance TDI scores are presented in Table 1. 2.3. Odour liking and strength ratings During the EEG recordings, each participant completed a psychometric rating of the odour (hedonic or emotional response and perceived strength) after each odour delivery trial. These ratings were based on simple 10 cm Likert scales: Liking (strong like=0; strong dislike=10) and Strength (very weak=0; very strong=10). Subjects also provided descriptions of the odour and any associated responses or reactions. Liking ratings were then grouped according to these rating levels: Like (< 4), Neutral (4–6) and Dislike (> 6). 2.4. Odour stimulus preparation The test odour was beta-damascenone (C13H18O; a sweet, fruity, rose, berry odour). A gas form of the odour stimulus was obtained from a pure liquid source (Product Makers; Melbourne, Australia) by bubbling room air through 8 ml of liquid in a 20 ml glass vial sealed by a rubber stopper. The rubber stopper was pierced by two blunt 18 G hypodermic needles (Terumo; Melbourne, Australia), sealed by three-way disposable stopcocks (Discofix#; Braun; Melsungen) fitted with Luer lock terminations. A 2-m length of TygonTM tubing was fitted to the taps by ways of plastic tubing adapters and then inserted into the pump head of a Cole-PalmerTM roller pump. Air was then pumped and recirculated through the liquid for 20 min. At the conclusion of the recirculation, the air was removed from the tubing into a teflon gas sample bag and the tubing flushed out with 350 ml of room air using plastic 50 ml Luer syringes. In this way odour-rich air was prepared for the damascenone stimulus. In GC/MS analysis, the concentration of the odorous gas was determined to be 1.99 ppm (reported threshold: 0.009 ppm; Ohloff, 1994).
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2.5. Odour delivery Odour was delivered using a continuous respiration olfactometer (CRO). The odour syringe was filled with 50 ml of the damascenone gas sample, and similar volume of room air filled the control air syringe. The CRO delivers odour during normal respiration by closely monitoring the subject’s natural respiratory cycle using a pneumotachograph mounted on the facemask with a two-way non-rebreathing valve. Delivery of odour or air is then timed to the subject’s inspiration. The outlet tubing from the computer-controlled delivery syringes was inserted into separate ports in the facemask. The apparatus is described in detail elsewhere (Owen, Patterson, Silberstein, Simpson, Neild, & Pipingas, 1997; Patterson, Owen, Silberstein, Simpson, Pipingas, & Neild, 1998; Owen, Patterson, & Simpson, 1999). Either 1 ml of odour, or 1 ml of air, is delivered into each inspiratory air flow (taking approximately 500 ms/delivery) using a pseudo-random sequence at an air: odour ratio of 3:1, with a minimum of two air delivery between odour deliveries. For this study’s group of participants, there was an average breath duration of 4.9 s ( 0.25), resulting in an average inter-stimulus interval (ISI) of 10–25 s. This delivery ratio is supported by the evidence of the number of air and odour deliveries analysed with each 20 min recording in the current study: Air: M=164 ( 55), range 90–319; Odour: M=55 ( 19), range 29–108. With repeated exposure to odour stimuli, there is a possible habituation effect. However, this possible effect was reduced through the combination of the use of the 3:1 air: odour delivery ratio, the low concentration odour stimulus delivered by the CRO, and the introduction of rest periods between each five minute recording period. 2.6. EEG recordings Brain electrical activity was recorded with a 64-channel ElectroGeodesic Inc (EGI) EEG sensor system (saline electrodes), referenced at Cz channel, with a sample rate of 500 samples/s, and high and low-pass filter settings of 200 and 0.1 Hz, respectively. Stimulus presentation records were achieved by triggering the EGI through its interface port between the acquisition and task computers. The source of the trigger was a pair of specific outputs indicating syringe drive from the CRO, marking the EGI-EEG record when odour, or air, was delivered. 2.7. Procedure All subjects were screened using the Sniffin’ Sticks Test of Olfactory Performance prior to attending an EEG recording session. EEG during stimulus delivery (air or odour) was recorded for 5-min trials, and each
subject participated in four repeated trials resulting in a total of 20 min of EEG recorded. Following each trial, participants completed a rating sheet, using a 10-point Likert scale to indicate their perceived liking and strength ratings, and describing the odour they detected during the recording. Using the CRO delivery technique with the EEG system, differences caused by the test odours in comparison to air without test odours were recorded and analysed, correlating the odour nature with the hedonic/emotive responses. 2.8. Data processing and statistical analysis The EEG data obtained in the 20 min of recording were epoched for 1024 ms periods around the stimulus point for air or odour delivery (100 ms pre-delivery and 924 ms post-delivery), and averaged for air or odour. This resulted in an average of 164 air epochs and 55 odour epochs for averaging. During off-line analysis, the EEG signals were processed for artefact reduction and digitally filtered using a 45 Hz low-pass filter to reduce electrical noise contamination (50 Hz mains). In addition to studying the EEG signals at specific anterior electrode sites, the signals were averaged for left and right frontal electrode sites (grouped at sites equating to around F3 and F4 in the 10/20 system). The raw signals thus collated were exported to ExcelTM and the time series data graphed for the averaged frontal sites and for individual electrodes for the condition, and for liking responses to each cheese odour. The averaged signals for each subject were also subjected to FFT analysis for the 1024 ms epoch period (512 samples). Following the FFT analysis, each subject’s air averages and odour averages were normalised such that the total power in each set totalled 100%. Relative % power was then obtained for the frequency bins of interest (1–4, 4–8, 8–12 Hz) for each condition odour vs air. The use of relative % power in this study was justified due to the protocol adopted, which incorporated both air and odour stimuli randomised throughout the same time frames (each 5-min recording period). It could therefore be assumed that within each time frame the total power for each epoch would remain relatively constant. In view of the use of a no-odour control (air stimulus only), the relative % power was also calculated for the odour–air difference, based on the assumption that such a calculation would account for any common brain responses, and isolate the odourrelated responses. From Excel, graphs of the various frequency bins were prepared and comparisons made between the left and right frontal regions relative to the different liking response groups, and subjected to statistical analysis. Statistical analysis was conducted using SPSS (version 10.0 for Macintosh; Release 10.0.7a; SPSS Inc., 2000). Analysis of variance (ANOVA) was used, with the
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Newman–Keuls post-hoc test and P < 0.05 for identifying significant results.
3. Results 3.1. Olfactory performance The mean TDI score of the Sniffin’ Sticks Test of Olfactory Performance screening test (M=34.34 3.72; range 22.25–40.50) indicated that all subjects were within the range for normal olfactory function (Kobal et al., 2000). One-way ANOVA with Liking Group (Like, Neutral, Dislike) as the between-subjects factor was conducted for each olfactory performance task. Results revealed that the Threshold scores differed significantly across liking groups [F (2,33)=3.644, P < 0.01] and there was a significant difference in the TDI scores across liking sub-groups [F (2,33)=5.751, P < 0.05], but there was no significant difference in the mean scores of the liking sub-groups for the Discrimination and Identification tasks. Newman–Keuls post-hoc comparisons revealed that the mean Threshold and TDI scores for the Neutral response group were significantly lower than the scores for both the Like and Dislike response groups, as seen in Table 2. 3.2. Odour liking The mean liking responses were calculated from the subjective odour ratings provided following each EEG recording trial, where the participants had to rate their liking for the odour on a scale of 0 (strong like) to 10 (strong dislike). Liking sub-groups were formed based
Table 2 Mean Sniffin’ Sticks sub-test and TDI scores ( standard deviation) for the liking response sub-groups: Like, Neutral and Dislike
Threshold Discrimination Identification TDI Score
Like (n=15)
Neutral (n=13)
Dislike (n=8)
8.70 12.80 13.60 35.10
6.98 11.85 13.08 31.90
9.81 13.13 13.50 36.56
( 2.35) ( 1.47) ( 1.50) ( 3.30)
( 2.34) ( 2.73) ( 1.19) ( 3.35)
( 2.75) ( 1.73) ( 1.31) ( 3.22)
Table 3 Mean Liking and Strength response ratings ( standard deviation) for the liking response sub-groups: Like, Neutral and Dislike
Liking Mean Liking Range Strength Mean Strength Range
Like (n=15)
Neutral (n=13)
Dislike (n=8)
2.64 ( 0. 91) (0.6–3.7) 4.15 ( 1.99) (0.7–7.38)
4.99 ( 0.58) (4.1–5.8) 4.40 ( 1.50) (0.8–6.35)
7.05 ( 1.06) (6.0–9.2) 5.54 ( 1.65) (3.28–8.70)
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on the mean liking score for all four trials, with mean liking ratings for each sub-groups summarised in Table 3. Independent groups One-Way ANOVAs with Liking Group (Like, Neutral, Dislike) as the between-subjects factor were computed for the mean Liking and Strength responses, revealing significant differences in mean Liking scores between the designated sub-groups [F(2,33)=75.778, P < 0.001, Z2=0.82]. There was no significant difference in Strength scores between the three Liking sub-groups [F(2,33)=1.703, P > 0.05]. Newman–Keuls post-hoc comparisons showed that the Like group had significantly lower Liking scores than the Neutral group, which had significantly lower scores than the Dislike group, as shown in Table 3. This analysis supported the post-hoc formation of these Liking sub-groups. 3.3. EEG responses In the interest of exploring the effect of liking responses to an odour, frequency and frontal EEG responses were examined for each liking response group. A 3 3 2 mixed design ANOVA was conducted on the Odour relative % power responses, with Liking group (Like, Neutral, Dislike) as a between subjects factor, and with frequency range (1–4, 4–8, and 8– 12 Hz) and frontal location (Left, Right) as within subject factors. As could be predicted in consideration of the relative % power frequency groupings applied here, there was a significant within subject effect for frequency [F(2,66)=200.501, P < 0.001, 2=0.86], with significant differences in mean relative % frequencies across all liking groups for 1–4 Hz range (68.55 2.42), 4–8 Hz rang (11.23 1.06) and 8–12 Hz range (5.28 2.64). However, there was no significant interaction between frequency and liking group [F(4,66)=0.11, P > 0.05]. There was no significant within subject effect for frontal location [F(1,33)=0.115, P > 0.05]. There was no significant interaction between liking group, frequency and frontal location [F(4, 66)=2.433, P=0.098, 2=0.13]. Fig. 1 depicts the means for the relative % power odour responses for the three frequency bands for liking sub-groups and left versus right frontal responses. Although there were no significant differences associated with frontal region of activation in these frequency bands, a study of the means reveals a trend associated with liking group responses for left versus right frontal locations, as shown in Table 4. In the 1–4 Hz (delta) range, there was a trend for slightly greater left frontal activation cf. right frontal activation for the Like group, and a stronger reverse trend for the Dislike group, with little difference evident between 1 and 4 Hz frontal responses for the Neutral group. Similarly, in the 4–8 Hz (theta) and 8–12 Hz (alpha) ranges,
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Fig. 1. Relative percent power (with standard error bars) for the 1–4, 4–8, and 8–12 Hz power bands in response to the odour stimulus (damascenone) for liking response sub-groups: Like (n=15), Neutral (n=13) and Dislike (n=8). The columns represent Left (white) and Right (black) frontal activation. The Y-axis shows power normalised as a relative percentage. In the 4–8 and 8–12 Hz bands there was a trend for reduced left frontal activation for the Like and Neutral groups and increased activation for the Dislike group relative to the right frontal activation. (Note the different Y-axis values for the 1–4 Hz range in comparison to the 4–8 Hz and 8–12 Hz ranges.).
Table 4 Frontal (Left vs Right) mean relative % power odour responses ( SD), grouped in frequency bins, for the odour liking response subgroups: Like, Neutral and Dislike Relative% power odour response
Like (n=15)
1–4 Hz Left mean 1–4 Hz Right mean
67.20 ( 5.84) 71.86 ( 6.28) 65.20 ( 5.53) 70.20 ( 5.94)
62.38 ( 8.00) 74.43 ( 7.57)
4–8 Hz Left mean 4–8 Hz Right mean
9.69 ( 2.41) 10.13 ( 2.59) 10.59 ( 2.45) 12.47 ( 2.64)
14.99 ( 3.30) 9.94 ( 3.59)
8–12 Hz Left mean 8–12 Hz Right mean
2.83 ( 1.22) 2.37 ( 1.21)
Neutral (n=13) Dislike (n=8)
5.58 ( 1.32) 5.13 ( 1.30)
8.95 ( 1.68) 6.82 ( 1.65)
there was little difference between left and right frontal odour responses in the Like responses or in the Neutral responses but the Dislike group trend was reversed with greater right frontal 4–8 and 8–12 Hz activation. In general, there was an increase in theta activity in the left frontal location and an increase in alpha activity in the both the left and right frontal locations associated with Dislike for the odour (cf. Like or Neutral responses).
Relative % power was also calculated for the odourair difference, to determine if the significant differences observed for the odour responses were consistent across the odour-air difference condition. A 3 3 2 mixed design ANOVA was conducted on the relative % power difference (Odour minus Air) responses, with Liking group (Like, Neutral, Dislike) as a between subjects factor, and with frequency range (1–4, 4–8, and 8–12 Hz) and frontal location (Left, Right) as within subject factors. There were no significant within or between subject effects for frontal location or frequency range for the liking groups (P > 0.05). However, the mean responses for the difference frequency ranges in the left versus right frontal locations suggested a trend in difference (odour-air) responses associated with liking group. In the 1–4 Hz (delta) range, there was little difference in left frontal odour-related activation associated with the odour cf. right frontal activation for the Like group, a slight increase in odour-related activation in the left cf. right frontal for the Neutral group, and a trend for a decrease in odour-related activation in the left cf. right frontal location for the Dislike group. In the 4–8 Hz (theta) range, there was a trend for a slight decrease in
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activation associated with the left frontal odour-related difference responses for the Like and Neutral groups, but an increase in left frontal odour-related activation cf. right frontal activation for the Dislike group. The increase in theta activity in the left frontal location and an increase in alpha activity in the both the left and right frontal locations associated with Dislike for the odour (cf. Like or Neutral responses), observed for the odour responses, was again evident in the difference responses.
4. Discussion Although there were no significant interactions between liking responses, frontal location and relative% power evident in the current study, there was evidence of a trend for differences in left and right frontal power differences associated with Like or Dislike for the odour. Although there was little difference in left vs right frontal responses for the Like and Neutral groups, there was a trend for greater right frontal activation in the 1–4 Hz range and greater left frontal activation in the 4–8 and 8–12 Hz ranges for the Dislike group. In addition, there was evidence to suggest an increase in theta activity in the left frontal location and an increase in alpha activity in the both the left and right frontal locations associated with Dislike for the odour (cf. Like or Neutral responses). The hedonic effect of odours on brain electrical activity has been described in the literature as differences in anterior brain activity associated with pleasant and unpleasant odours (Brauchli et al., 1995; Ehrlichman et al., 1995; Kobal et al., 1992; Roescher et al., 1998). A particular association between left frontal activation and pleasant odours has been described (Kline et al., 2000), supporting previous studies of positive emotional responses activating the left frontal region (Davidson, 1992; Lane et al., 1997; Sutton & Davidson, 2000). This study approached this research question from a different direction by investigating different liking (pleasant, unpleasant) responses to one particular odour. While failing to find significant differences in the relative power of frontal responses associated with reported like or dislike for the odour, there was a trend for differences in theta and alpha responses for Dislike group cf. the Like and Neutral groups, particularly in the left frontal location. The presentation of damascenone resulted in a lower relative power (non-significant) for those who reported liking the odour and higher relative power for those who disliked the odour when compared to those with a neutral response. This extends previous findings from electrophysiological and neuroimaging studies (Klemm et al., 1992; Kline et al., 2000; Kobal et al., 1992; Kobal & Kettenmann, 2000) which reported differences in left frontal activation associated with
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stimulation by a pleasant odour in comparison with stimulation by an unpleasant odour. The trend for reduced left frontal activation in the 4–8 Hz or theta range associated with a like response also support previous findings of reduced theta activity in response to pleasant food odours such as chocolate (synthetic and real), spearmint (synthetic) and spiced apple (Lorig & Schwartz, 1988; Lorig, Herman, Schwartz, & Cain, 1990; Martin, 1998). However, it has been proposed that the effect of odours on theta activity may actually be a reflection of the odour’s ability to attract or distract and therefore reflect shifts in attention associated with the emotional reaction to the odour (Martin, 1998). This has been supported previously by findings of an apparent association between changes in theta activity and self-reports of tension and anxiety responses (Lorig & Schwartz, 1988). It has also been proposed that the olfactory effects on theta may be specific to different odours possessing similar psychological properties (Martin, 1998). In the current study, the evidence (non-significant) of increased theta activity in the left frontal region evident in the Dislike responses in comparison with the Like and Neutral responses may reflect the shift in attention associated with a dislike response common to different cheese odours and associated with the similar psychological (hedonic) response to the odours. As cortical alpha power has reported to be inversely related to cortical activity (Coan, Allen, & HarmonJones, 2001), suppression of alpha activity has been equated to an increase in activation in response to stimulation. This has been demonstrated in response to visual and auditory stimulation (Brauchli et al., 1995) and has more recently been reported by EEG studies in response to olfactory stimulation (Brauchli et al., 1995; Lorig, 1994; Lorig et al., 1990; Lorig, Huffman, DeMartino, & De Marco, 1991; Schwartz, Wright, Polak, Kline, & Dikman, 1992; Van Toller et al., 1993). Due to the protocol used in the current study, it may have been expected that there would be an increase in alpha due to the test conditions (darkened room, calming breathing), similar to the increase in alpha associated with a ‘restful’ state (Klemm et al., 1992). Such an effect would be common to both the air and odour conditions due to the experimental design. Although it was not significant, the consistent trend in alpha band left frontal decreases associated with liking for an odour (cf. dislike) was found in both the relative % power of the odour responses and the odour–air differences, suggesting the validity of the assumption that these decreases are related to the odour stimulus. The focus of previous research on electrophysiological changes associated with hedonic responses to different odours has introduced potentially confounding issues associated with the different odour stimuli used. The possible intranasal trigeminal stimulation associated
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with the unpleasant odours used may have caused the effects seen in some studies to be related to differences in sensory perception (Brauchli et al., 1995). A study by Brauchli et al. (1995) demonstrated an increased autonomic arousal in response to the unpleasant odour. The authors reported a greater increase in alpha power in response to the unpleasant odour in comparison to the pleasant odour. Decreases in alpha are common in EEG research, and are taken to be suggestive of cognitive activity, but are more commonly associated with cortical arousal due to sensory stimulation (Lorig et al., 1990). This was interpreted as suggesting that stimulation with an unpleasant odour may lead to stronger cortical deactivation than stimulation with a pleasant odour, as also suggested by previous research (Ehrlichman & Bastone, 1992; Miltner et al., 1994). Evidence from the current study can only suggest the existence of a trend towards decreased alpha associated with a liking response, but has contributed to and extended this research direction by demonstrating this hedonic effect using an odour stimulus that evoked different hedonic effects in the subject population. The approach-withdrawal theory (Davidson, 1987, 1992) proposed that approach-related positive responses would be evident in changes in anterior EEG activation in the left frontal region, seen as decreased alpha activation (increased arousal or attention) in response to the positive stimuli and a corresponding increased alpha activation in response to negative stimuli. Changes in right anterior activation would be predicted with withdrawal-related negative responses, seen in decreased alpha activation right frontal response to negative stimuli, and a corresponding increased alpha activation right frontal response to positive arousal. Although there was evidence of a trend in alpha changes associated with like vs dislike, the current study did not find the significant differences in left or right frontal activation predicted by the approach-withdrawal theory. This may have been due in part to the range of hedonic responses evoked by the odour, and in particular to the degree of negativity involved in the hedonic response. The perceived Dislike response to the test odour was possibly a less potent negative response than that used in the emotional studies. This may therefore have reduced the effect of the negative response which was predicted by the approach-withdrawal theory (Davidson, 1987, 1992). A lack of significant right frontal differences was also reported by Kline et al. (2000), with a possible explanation offered associated with the period of the FFT was computed—over an entire minute— which may have caused the phasic right frontal activation during behavioural withdrawal to be missed. In the current study, the FFT was computed over a 900 ms post-stimulus period in an attempt to analyse the cortical arousal due to sensory stimulation, and again the right frontal activation did not reveal the negative
withdrawal response. It would therefore appear that the duration of the FFT analysis, as proposed by Kline et al. (2000), may be a potential dominant contributor to this lack of right frontal negative effect. While not fully supporting the predictions for hedonic-related EEG changes, this study has extended olfactory research by demonstrating the consistency of the left frontal response associated with liking an odour. In taking a different approach and using the same odour to evoke different hedonic responses, these results have provided further non-significant evidence of changes in left frontal activation associated with the hedonic response. Future studies with greater numbers of subjects and different odours (particularly using odours which may evoke stronger negative reactions) will provide evidence of the significance or robustness of these changes in frontal activation associated with the hedonic response. This application of objective physiological techniques to sensory studies has the potential to contribute to an understanding of the sensory qualities associated with odour perception and liking.
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