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The influence of stimulus duration on odor perception
International Journal of Psychophysiology 62 (2006) 24 – 29 www.elsevier.com/locate/ijpsycho
The influence of stimulus duration on odor perception Johannes Frasnelli *, Christiane Wohlgemuth, Thomas Hummel Smell and Taste Clinic, Department of Otorhinolaryngology, University of Dresden Medical School, Fetscherstr. 74, 01307 Dresden, Germany Received 29 September 2005; received in revised form 11 November 2005; accepted 15 November 2005 Available online 18 January 2006
Abstract Although different parameters are known to alter the shape of olfactory event related potentials (ERP), ERP parameters are generally thought to be independent from stimulus duration. Evidence from recent studies investigating trigeminal ERP indicates that this may not be true. Aim of the present study was to investigate the relationship of stimulus duration and ERP. A total of 20 young healthy subjects participated. Subjects were investigated on 5 occasions on 5 different days. ERP were recorded to olfactory stimuli of two different concentrations and 3 different durations (100 ms, 200 ms, 300 ms). In two sessions olfactory ERP to PEA were recorded, in another two sessions H2S was applied. During the same sessions, intensity ratings were recorded. In the fifth session, subjects were asked to rate the duration of H2S stimuli and PEA stimuli. Whereas at weak stimulus concentrations no effect of stimulus duration could be observed, there was a clear effect of ‘‘duration’’ in ERP amplitudes following stimuli with higher concentrations: the longer the stimulus duration the larger the ERP amplitudes. No effect was found on ERP latencies. With regard to intensity ratings, strong stimuli and longer lasting stimuli lead to higher ratings. Similarly, ratings of stimulus duration were dependent from stimulus concentration and stimulus duration. Results of the present study showed that similar to trigeminal ERP, information about stimulus duration is encoded in olfactory ERP, mainly in amplitudes. D 2005 Elsevier B.V. All rights reserved. Keywords: Olfaction; Duration; Event-related potentials
1. Introduction Chemosensory event-related potentials (CSERP) (Kobal and Hummel, 1988) are a means to investigate chemosensory activation on a central level. In contrast to gustatory ERP (Kobal, 1985), olfactory ERP (OERP) and trigeminal ERP (tERP) (Kobal and Hummel, 1988) are used routinely in both clinical investigations and chemosensory or pain research. CSERP have a typical shape. Following standardized procedures (Evans et al., 1993; Hummel and Kobal, 2002), the first positive peak of the chemosensory ERP is named P1. It typically occurs at latencies later than 200 ms. N1 is the following major negative peak, followed by the late positive complex, the major peak of which is named P2. The early components of ERP are thought to mainly depend on stimulus characteristics (exogenous components), whereas the later * Corresponding author. Tel.: +49 351 458 2268; fax: +49 351 458 4326. E-mail address: [email protected] (J. Frasnelli). 0167-8760/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2005.11.006
components are predominantly a reflection of the interaction between the subject and the stimulus (endogenous components) (Pause and Krauel, 2000). Different parameters are known to alter the shape of olfactory ERP. Increasing concentrations of H2S led to larger amplitudes and shorter latencies of olfactory ERP (Hummel et al., 1998). Similar observations were reported for vanillin, increasing concentrations of which led to shortened ERP latencies, increased ERP amplitudes, and increased ratings (Tateyama et al., 1998). Furthermore, while ERP amplitudes did not significantly increase in response to changes in concentrations of linalool, ERP latencies shortened with higher concentrations of this odor (Pause et al., 1997). In addition, a shortening of ERP latencies was found with higher H2S concentrations although ERP amplitudes did not seem to vary with stimulus concentration (Thiele and Kobal, 1984). Similar results have been found for trigeminal ERP when investigating the impact of stimulus concentration (Anton et al., 1992; Lo¨tsch et al., 1997; Pause et al., 1997; Frasnelli et al., 2003), or
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interstimulus interval (Hummel and Kobal, 1999). Stimulus duration, however, was thought not to affect chemosensory ERP. When stimulus durations from 100 to 700 ms were used (Kobal, 1981), ERP to the mixed trigeminal/ olfactory stimuli isoamylacetate and eucalyptol have been described to remain constant. Based on this observation in 5 subjects, it was hypothesized that olfactory ERP, similar to ERP in other sensory modalities (compare Hummel and Kobal, 2002), would contain mainly information about stimulus onset and stimulus concentration. On a psychophysical level, a number of studies showed a relationship between stimulus duration and perceived stimulus intensity. Longer lasting (up to 1 s) stimuli of isoamylacetate, eucalyptol (Kobal, 1981), linalool, H2S (Strecker, 1983) and amyl acetate (Wang et al., 2002) were perceived as more intense when compared to shorter lasting ones. In addition, with longer lasting stimuli lower perception thresholds were measured for n-butane when compared to stimuli of shorter duration (Schneider et al., 1966). Thus, stimulus duration and stimulus concentration can compensate and reinforce each other in their influence on perceived stimulus intensity. Compared to other sensory modalities, chemosensory ERP have a relatively long latency. Thus, it seems conceivable that – other than previously thought– stimulus duration could have an influence on parameters of chemosensory ERP. The intranasal trigeminal system, which also belongs to the chemosensory system, shares some properties with the olfactory system, e.g. the correlation between stimulus duration and intensity ratings (Anton et al., 1992; Frasnelli et al., 2003; Kobal, 1981). In fact, it was shown that trigeminal ERP also encode information about stimulus duration (Frasnelli et al., 2003). ERP amplitudes at position Cz were linearly related to duration (100 to 300 ms) of the stimulant CO2. Aim of the present study was the investigation of varying stimulus durations and concentrations on ERP parameters, intensity ratings, and duration ratings. It was hypothesized that increase of both stimulus parameters would lead to higher intensity ratings and larger ERP responses. 2. Material and methods A total of 20 subjects participated in the study, 10 of them were women, 10 were men. They were between 20 and 30 years of age. Health and normal olfactory function were ascertained with a detailed medical history, an ENT examination, and the ‘‘Sniffin’ Sticks’’ test (Kobal et al., 1996, 2000). The study was conducted according to the Declaration of Helsinki. Subjects gave written informed consent prior to the study. Using a bio-feedback device, subjects were trained to breathe through their mouth without concomitant nasal airflow (velopharyngeal closure (Kobal, 1981)), which avoided respiratory airflow in the nasal cavity during chemosensory stimulation. Subjects were investigated on 5 occasions. On 4 of these occasions olfactory event-related potentials (OERP) were recorded, using phenyl ethyl alcohol (PEA) and hydrogen
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sulfide (H2S) as stimulants which are known to be pure odorants (Doty et al., 1978; Hummel et al., 1991). In two sessions PEA was used as stimulant, in the other two occasions H2S was applied. Intensity ratings were also recorded during ERP measurements. The sequence of the sessions was pseudorandomized and counterbalanced. In the 5th session, subjects had to rate the duration of H2S stimuli and PEA stimuli. A single session lasted approximately 1 h. Subjects received white noise through headphones in order to mask switching clicks of the stimulation device. To stabilize vigilance, subjects performed a tracking task on a computer screen. Using a joystick, they had to keep a small square inside a larger one, which moved unpredictably (Hummel and Kobal, 2002). Following presentation of each odor stimulus, subjects rated stimulus intensity on a visual analogue scale (Aitken, 1969) displayed on the screen. The left-hand end of the scale was defined as ‘‘no stimulus perceived’’ (0%), the right-hand end as ‘‘extremely strong’’ (100%). Odor stimuli were applied by means of a computercontrolled air-dilution olfactometer (OM2S, Burghart, Wedel, Germany). This stimulator allows application of rectangularshaped chemical stimuli with controlled stimulus onset. Mechanical stimulation is avoided by embedding stimuli into a constant flow of odorless, humidified air of controlled temperature (80% relative humidity, total flow 8 L/min, 36 -C) (Kobal, 1981). Odor stimuli were applied in two different concentrations (weak and strong; H2S at 2 ppm and 8 ppm; PEA at 10% and 40% of saturated air) and 3 stimulus durations (100 ms, 200 ms, 300 ms) resulting in a 6 (2 * 3) conditions paradigm. Within the sessions, each stimulus condition was presented 15 times in a randomized order. The interstimulus interval was approximately 30 s (Hummel and Kobal, 1999; Kobal, 1981). Olfactory ERP were recorded at the position Pz of the 10/20 system (referenced against linked earlobes [A1 + A2]), where olfactory ERP are known to show largest amplitudes (Livermore et al., 1992). Eye blinks were monitored via the Fp2 lead. The sampling frequency was 250 Hz; the pre-trigger period (used for determination of baseline) was 500 ms with a recording time of 2048 ms per record (band pass 0.02– 30 Hz). Recordings were additionally filtered off-line (low-pass 15 Hz). ERP were averaged after records contaminated through motor artifacts or blinks had been discarded. As averages were based on a limited number of single recordings, peak-to-peak amplitude N1P2 was measured in order to obtain stable measures independent of the baseline. Analyses were performed by means of EPEvaluate software (Kobal, Erlangen, Germany). At stimulus duration of 200 ms of the strong H2S stimulus, N1 had a mean latency of 450 ms, and P2’s mean latency was 660 ms. On the fifth session, subjects received the two stimuli (H2S, PEA) at 2 different concentrations: (weak and strong; H2S: 2 ppm and 8 ppm; PEA: 10% and 40% of saturated air) at 4 different stimulus durations (100 ms, 200 ms, 300 ms, 600 ms). The subject’s task was to rate the perceived duration of the
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stimuli on a VAS. The left-hand end of the scale was defined as ‘‘extremely short stimulus’’ (0%), the right-hand end as ‘‘extremely long stimulus’’ (100%). Statistical analyses were performed through SPSS 12.0 for Windowsi (SPSS Inc., Chicago, IL, USA). For variables of interest (ERP parameters, intensity ratings, duration ratings) repeated measures ANOVA were computed (between-subject factor ‘‘sex’’; within-subject factors ‘‘duration’’ (100 ms, 200 ms, 300 ms for the first 4 sessions; 100 ms, 200 ms, 300 ms, 600 ms for the fifth session), ‘‘concentration’’ (weak, strong), ‘‘stimulus’’ (H2S, PEA); Greenhouse-Geisser correction of degrees of freedom; post hoc testing using paired t-tests). The a-level was set at 0.05. 3. Results 3.1. ERP data Grand means of ERP are depicted in Fig. 1. Amplitudes of olfactory ERP were found to change in relation to odor concentration. Strong stimuli evoked responses with larger amplitude (‘‘concentration’’: F[1,17] = 56.3; p < 0.001). The factor ‘‘duration’’ failed to reach significance ( p = 0.062). However, a significant interaction between ‘‘concentration’’ and ‘‘duration’’ was found indicating that varying durations affected ERP amplitudes differently with weak or strong concentrations of the stimulus ( F[2,34] = 6.5; p = 0.004). In fact, when ERP after weak and strong stimuli were analyzed separately, a differentiated picture emerged. Whereas at weak stimulus concentrations no effect of stimulus duration could be observed, there was a clear effect of ‘‘duration’’ in ERP amplitudes following stimuli of strong concentrations ( F[2,34] = 7.4; p = 0.003). Longer stimulus durations led to larger amplitudes (Fig. 2). Stimuli of higher concentrations evoked ERP with shorter latencies of the peaks N1 and P2 (‘‘concentration’’: F[1,17] > 5.84; p < 0.028). Neither an effect of stimulus duration was found on ERP latencies, nor could an interaction between
duration and concentration be detected. With regard to the latency of P2 there was an interaction between ‘‘odor’’ and ‘‘concentration’’ ( F[1,17] = 6.3; p = 0.023) indicating that the relationship between concentration and latency was dependent from the odor used. 3.2. Psychophysical data 3.2.1. Intensity ratings A significant effect of ‘‘concentration’’ was found on intensity ratings ( F[1,18] = 62.7; p = 0.001), with strong stimuli leading to higher ratings. The duration of the stimuli had also an effect on intensity ratings ( F[2,36] = 90.1; p < 0.001). Longer lasting stimuli led to higher intensity ratings (Fig. 3a). There was also an effect of the factor ‘‘sex’’ on intensity ratings ( F[1,18] = 14.3; p = 0.001). Women rated stimuli as more intense than men. In addition, the two odors were rated as differently intense ( F[1,18] = 5.7; p = 0.027), with PEA stimuli being rated as stronger than H2S stimuli. 3.2.2. Duration ratings With regard to ratings of stimulus duration there were significant effects of the factors ‘‘concentration’’ ( F[1,17] = 36.3; p < 0.001) and ‘‘duration’’ ( F[3,51] = 50.6; p < 0.001) on duration ratings of olfactory stimuli. Thus, longer lasting stimuli were rated as longer lasting, but stimuli of higher concentration were also rated as longer lasting (Fig. 3b). In contrast to intensity ratings, no effects of ‘‘sex’’ could be observed for ratings of stimulus duration. The results remained unchanged when only the responses to the stimuli with duration of 100 ms, 200 ms, and 300 ms were included in the statistical analysis. 4. Discussion CSERP have traditionally been thought to be mainly dependent from stimulus concentration and stimulus onset, but to be independent from stimulus duration. For example,
Fig. 1. Grand means of ERP. Results are shown separately for stimulation with weak (upper row) and strong (lower row) stimuli. Responses to H2S are depicted on the left side; responses to PEA are depicted on the right side. Responses to stimuli of 100 ms, 200 ms, 300 ms are shown in black, dark grey and light grey, respectively. Duration and onset of stimulation is represented by bars on the x-axis.
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Fig. 2. Mean (error bars: standard error of mean—SEM) ERP amplitude N1P2 following stimulation with 3 durations (from bright to dark: 100 ms, 200 ms, 300 ms) of 2 concentrations (weak, strong) of phenyl ethyl alcohol (PEA—p) and hydrogen sulfide (H2S—h).
ERP in response to the mixed olfactory/trigeminal stimuli isoamylacetate and eucalyptol appeared to be independent from stimulus duration (Kobal, 1981). However, a recent study showed different results. A positive correlation between stimulus duration and ERP amplitudes has been shown for trigeminal stimuli (Frasnelli et al., 2003). Results of the present study were obtained for ‘‘pure’’ olfactory stimuli. They indicate that olfactory ERP components are dependent from stimulus duration. Another recent study showed similar results. Wang et al. (2002), measured the influence of stimulus ‘‘strength’’ on olfactory ERP. In this
particular study the authors defined the strength of an olfactory stimulus as its width, i.e. its duration. Thus, although they discussed the stimulus concentration being the independent variable, in fact they changed the duration of their stimuli from 35 to 200 ms. They found an effect of stimulus duration on ERP amplitude, but not on latencies. This is in line with the present study, where ERP amplitudes, but not ERP latencies increased with increasing stimulus duration. The present study showed that stronger stimuli evoked ERP with larger amplitudes and shorter latencies. This is in line with previous studies where the relationship between concentration
Fig. 3. (a) Mean (error bars: SEM) intensity ratings following stimulation with 3 durations (from bright to dark: 100 ms, 200 ms, 300 ms) of 2 concentrations (weak, strong) of phenyl ethyl alcohol (PEA—p) and hydrogen sulfide (H2S—h). (b) Mean (error bars: SEM) duration ratings following stimulation with 4 durations (from bright to dark: 100 ms, 200 ms, 300 ms, 600 ms) of 2 concentrations (weak, strong) of phenyl ethyl alcohol (PEA—p) and hydrogen sulfide (H2S—h). Note that stimuli of 400 and 500 ms were not applied.
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of chemosensory stimuli and parameters of ERP components was investigated. In some studies pure olfactory stimuli, e.g. H2S (Hummel et al., 1998; Thiele and Kobal, 1984), vanillin (Tateyama et al., 1998), or linalool (Pause et al., 1997) were applied. In these studies a negative correlation between stimulus concentration and latencies of ERP components could be detected (Pause et al., 1997; Tateyama et al., 1998; Thiele and Kobal, 1984; Hummel et al., 1998). The two studies which investigated a larger number of subjects, in addition, found a positive relationship between stimulus concentration and ERP amplitudes (Hummel et al., 1998; Tateyama et al., 1998). Accordingly, the effect of stimulus concentration is more pronounced on ERP latencies than on ERP amplitudes. The results of the present and prior studies underline the importance of distinguishing between stimulus duration and stimulus concentration. In the literature there is some confusion about these terms (compare Wang et al., 2002). Here, we use the term ‘‘concentration’’, defined as amount per volume, whereas ‘‘duration’’ is defined as the time between beginning and ending of a stimulus. We suggest not to use terms like ‘‘stimulus strength’’, ‘‘stimulus intensity’’ (which are parameters related to perception), and ‘‘stimulus width’’ when describing physical characteristics of chemosensory stimuli. The studies investigating the influence of pure olfactory stimulus parameters on ERP components can be divided into two groups. In a first group of studies the influence of stimulus duration was examined, which was found to exclusively affect ERP amplitudes (Wang et al., 2002, present study). In the second group, the effect of stimulus concentration on ERP components was studied which was found to mainly affect ERP latencies, and, to a lesser degree, also ERP amplitudes (Tateyama et al., 1998; Thiele and Kobal, 1984; Pause et al., 1997; Hummel et al., 1998, present study). The picture is again different when mixed olfactory/trigeminal stimuli are investigated. When applying such stimuli, e.g. toluene (Prah and Benignus, 1992), butanol (Lorig et al., 1993), menthol (Pause et al., 1997), eucalyptol (Kobal, 1981), and citral (Pause et al., 1996), only the latter study showed shorter ERP latencies with stimuli of higher concentrations. However, all authors found a positive correlation between stimulus concentration and ERP amplitudes. Similarly, using the (putatively) pure trigeminal stimulant CO2, ERP amplitudes appeared to be larger in response to stronger stimuli (Frasnelli et al., 2003; Mu¨ller, 1988). Again, as only the latter showed a correlation, an effect on ERP latency was not consistently found. Thus, it seems as in the olfactory system higher stimulus concentrations affect mainly ERP latencies and to a smaller degree ERP amplitudes. In the trigeminal system higher stimulus concentrations have mainly an effect on ERP amplitudes and to a smaller degree on ERP latencies. On the other hand, with regard to stimulus durations the two sensory systems behave similarly. Longer stimulus durations exclusively lead to larger ERP amplitudes, ERP latencies seem to be unaffected. The effect of stimulus duration and stimulus concentration has been studied on a cellular level in both vertebrates and invertebrates. Measuring extracellularly recorded responses from lobster chemoreceptor cells, Gomez and Atema (1996)
found higher odor concentrations, but not longer stimulus duration to lead to shorter first spike latency. With regard to stimulus duration, pheromone-sensitive olfactory neurons have been shown to encode the duration of pheromone pulses with great accuracy in moths (Christensen and Hildebrand, 1997). On the level of the antennal lobe of honeybees, which is the functional analogue of the olfactory bulb, the representation of a particular odor has been shown to change over time. Thus, it is different at the beginning of stimulation when compared to the end of stimulation (Galizia et al., 2000). Finally, also in mammals, activity patterns have been found to change over time in rodents’ olfactory bulb. Higher odor concentrations have been found to lead to shorter response latencies. Longer stimulus durations, on the other hand, were found to have an enlarging effect on the activity of single glomeruli (Spors and Grinvald, 2002). Although both stimulus characteristics lead to higher overall activity, these studies indicate on a cellular level, that stimulus concentration and stimulus duration primarily have differential effects on the olfactory system. Both the olfactory and the trigeminal system seem to integrate information over a longer period of time on a subcortical level (Frasnelli et al., 2003). In a review comparing the perception of odors and language, Lorig stated that ‘‘in order to interpret both olfactory and verbal signals, the nervous system must accumulate the neural code over an epoch, parse the phased but temporally smeared signal and assign the event to some representation’’ (Lorig, 1999). The temporal integration is reflected in the relatively long latencies of chemosensory ERP compared to other sensory modalities. Given this long latency it is conceivable that increasing stimulus duration – leading to a higher total amount of odorous molecules at the olfactory epithelium –leads to a higher degree of activation. This is confirmed by the results of the intensity ratings: not only stimuli with higher concentrations but also longer lasting stimuli lead to higher intensity. This suggests that, similar to the trigeminal system (Cometto-Muniz and Cain, 1984; Frasnelli et al., 2003; Wise et al., 2004), there is a durationconcentration trading in the olfactory system. Longer stimuli are perceived as more intense than shorter ones, although the stimulus concentration is the same; thus, stimuli with lower concentrations are perceived as equally intense as a shorter stimulus with a higher concentration. Therefore, the trigeminal system has been described as a ‘‘mass detector rather than a concentration detector’’ (Cometto-Muniz and Cain, 1984). However, if the olfactory system would be a perfect and pure mass detector, it would be difficult to correctly rate the duration of olfactory stimuli. This was not the case; as subjects could clearly distinguish between different durations of chemosensory stimuli. References Aitken, R.C., 1969. Measurements of feelings using visual analogue scale. Proc. R. Soc. Med. 62, 989 – 996. Anton, F., Euchner, I., Handwerker, H.O., 1992. Psychophysical examination of pain induced by defined CO2 pulses applied to the nasal mucosa. Pain 49, 53 – 60.
J. Frasnelli et al. / International Journal of Psychophysiology 62 (2006) 24 – 29 Christensen, T.A., Hildebrand, J.G., 1997. Coincident stimulation with pheromone components improves temporal pattern resolution in central olfactory neurons. J. Neurophysiol. 77, 775 – 781. Cometto-Muniz, E., Cain, W.S., 1984. Temporal integration of pungency. Chem. Senses 8, 315 – 327. Doty, R.L., Brugger, W.P.E., Jurs, P.C., Orndorff, M.A., Snyder, P.J., Lowry, L.D., 1978. Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans. Physiol. Behav. 20, 175 – 185. Evans, W.J., Kobal, G., Lorig, T.S., Prah, J.D., 1993. Suggestions for collection and reporting of chemosensory (olfactory) event-related potentials. Chem. Senses 18, 751 – 756. Frasnelli, J., Lotsch, J., Hummel, T., 2003. Event-related potentials to intranasal trigeminal stimuli change in relation to stimulus concentration and stimulus duration. J. Clin. Neurophysiol. 20, 80 – 86. Galizia, C.G., Kuttner, A., Joerges, J., Menzel, R., 2000. Odour representation in honeybee olfactory glomeruli shows slow temporal dynamics: an optical recording study using a voltage-sensitive dye. J. Insect Physiol. 46, 877 – 886. Gomez, G., Atema, J., 1996. Temporal resolution in olfaction: stimulus integration time of lobster chemoreceptor cells. J. Exp. Biol. 199, 1771 – 1779. Hummel, T., Kobal, G., 1999. Chemosensory event-related potentials to trigeminal stimuli change in relation to the interval between repetitive stimulation of the nasal mucosa. Eur. Arch. Otorhinolaryngol. 256, 16 – 21. Hummel, T., Kobal, G., 2002. Olfactory event related potentials. In: Simon, S., Nicolelis, M. (Eds.), Methods in Chemosensory Research. CRC press, Boca Raton. Hummel, T., Pietsch, H., Kobal, G., 1991. Kallmann’s syndrome and chemosensory evoked potentials. Eur. Arch. Otorhinolaryngol. 248, 311 – 312. Hummel, T., Barz, S., Pauli, E., Kobal, G., 1998. Chemosensory event-related potentials change with age. Electroencephalogr. Clin. Neurophysiol. 108, 208 – 217. Kobal, G., 1981. Elektrophysiologische Untersuchungen des Menschlichen Geruchssinns. Thieme Verlag, Stuttgart. Kobal, G., 1985. Gustatory evoked potentials in man. Electroencephalogr. Clin. Neurophysiol. 62, 449 – 454. Kobal, G., Hummel, C., 1988. Cerebral chemosensory evoked potentials elicited by chemical stimulation of the human olfactory and respiratory nasal mucosa. Electroencephalogr. Clin. Neurophysiol. 71, 241 – 250. Kobal, G., Hummel, T., Sekinger, B., Barz, S., Roscher, S., Wolf, S., 1996. ‘‘Sniffin’ sticks’’: screening of olfactory performance. Rhinology 34, 222 – 226. Kobal, G., Klimek, L., Wolfensberger, M., Gudziol, H., Temmel, A., Owen, C.M., Seeber, H., Pauli, E., Hummel, T., 2000. Multicenter investigation of 1036 subjects using a standardized method for the assessment of olfactory
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The influence of stimulus duration on odor perception Johannes Frasnelli *, Christiane Wohlgemuth, Thomas Hummel Smell and Taste Clinic, Department of Otorhinolaryngology, University of Dresden Medical School, Fetscherstr. 74, 01307 Dresden, Germany Received 29 September 2005; received in revised form 11 November 2005; accepted 15 November 2005 Available online 18 January 2006
Abstract Although different parameters are known to alter the shape of olfactory event related potentials (ERP), ERP parameters are generally thought to be independent from stimulus duration. Evidence from recent studies investigating trigeminal ERP indicates that this may not be true. Aim of the present study was to investigate the relationship of stimulus duration and ERP. A total of 20 young healthy subjects participated. Subjects were investigated on 5 occasions on 5 different days. ERP were recorded to olfactory stimuli of two different concentrations and 3 different durations (100 ms, 200 ms, 300 ms). In two sessions olfactory ERP to PEA were recorded, in another two sessions H2S was applied. During the same sessions, intensity ratings were recorded. In the fifth session, subjects were asked to rate the duration of H2S stimuli and PEA stimuli. Whereas at weak stimulus concentrations no effect of stimulus duration could be observed, there was a clear effect of ‘‘duration’’ in ERP amplitudes following stimuli with higher concentrations: the longer the stimulus duration the larger the ERP amplitudes. No effect was found on ERP latencies. With regard to intensity ratings, strong stimuli and longer lasting stimuli lead to higher ratings. Similarly, ratings of stimulus duration were dependent from stimulus concentration and stimulus duration. Results of the present study showed that similar to trigeminal ERP, information about stimulus duration is encoded in olfactory ERP, mainly in amplitudes. D 2005 Elsevier B.V. All rights reserved. Keywords: Olfaction; Duration; Event-related potentials
1. Introduction Chemosensory event-related potentials (CSERP) (Kobal and Hummel, 1988) are a means to investigate chemosensory activation on a central level. In contrast to gustatory ERP (Kobal, 1985), olfactory ERP (OERP) and trigeminal ERP (tERP) (Kobal and Hummel, 1988) are used routinely in both clinical investigations and chemosensory or pain research. CSERP have a typical shape. Following standardized procedures (Evans et al., 1993; Hummel and Kobal, 2002), the first positive peak of the chemosensory ERP is named P1. It typically occurs at latencies later than 200 ms. N1 is the following major negative peak, followed by the late positive complex, the major peak of which is named P2. The early components of ERP are thought to mainly depend on stimulus characteristics (exogenous components), whereas the later * Corresponding author. Tel.: +49 351 458 2268; fax: +49 351 458 4326. E-mail address: [email protected] (J. Frasnelli). 0167-8760/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2005.11.006
components are predominantly a reflection of the interaction between the subject and the stimulus (endogenous components) (Pause and Krauel, 2000). Different parameters are known to alter the shape of olfactory ERP. Increasing concentrations of H2S led to larger amplitudes and shorter latencies of olfactory ERP (Hummel et al., 1998). Similar observations were reported for vanillin, increasing concentrations of which led to shortened ERP latencies, increased ERP amplitudes, and increased ratings (Tateyama et al., 1998). Furthermore, while ERP amplitudes did not significantly increase in response to changes in concentrations of linalool, ERP latencies shortened with higher concentrations of this odor (Pause et al., 1997). In addition, a shortening of ERP latencies was found with higher H2S concentrations although ERP amplitudes did not seem to vary with stimulus concentration (Thiele and Kobal, 1984). Similar results have been found for trigeminal ERP when investigating the impact of stimulus concentration (Anton et al., 1992; Lo¨tsch et al., 1997; Pause et al., 1997; Frasnelli et al., 2003), or
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interstimulus interval (Hummel and Kobal, 1999). Stimulus duration, however, was thought not to affect chemosensory ERP. When stimulus durations from 100 to 700 ms were used (Kobal, 1981), ERP to the mixed trigeminal/ olfactory stimuli isoamylacetate and eucalyptol have been described to remain constant. Based on this observation in 5 subjects, it was hypothesized that olfactory ERP, similar to ERP in other sensory modalities (compare Hummel and Kobal, 2002), would contain mainly information about stimulus onset and stimulus concentration. On a psychophysical level, a number of studies showed a relationship between stimulus duration and perceived stimulus intensity. Longer lasting (up to 1 s) stimuli of isoamylacetate, eucalyptol (Kobal, 1981), linalool, H2S (Strecker, 1983) and amyl acetate (Wang et al., 2002) were perceived as more intense when compared to shorter lasting ones. In addition, with longer lasting stimuli lower perception thresholds were measured for n-butane when compared to stimuli of shorter duration (Schneider et al., 1966). Thus, stimulus duration and stimulus concentration can compensate and reinforce each other in their influence on perceived stimulus intensity. Compared to other sensory modalities, chemosensory ERP have a relatively long latency. Thus, it seems conceivable that – other than previously thought– stimulus duration could have an influence on parameters of chemosensory ERP. The intranasal trigeminal system, which also belongs to the chemosensory system, shares some properties with the olfactory system, e.g. the correlation between stimulus duration and intensity ratings (Anton et al., 1992; Frasnelli et al., 2003; Kobal, 1981). In fact, it was shown that trigeminal ERP also encode information about stimulus duration (Frasnelli et al., 2003). ERP amplitudes at position Cz were linearly related to duration (100 to 300 ms) of the stimulant CO2. Aim of the present study was the investigation of varying stimulus durations and concentrations on ERP parameters, intensity ratings, and duration ratings. It was hypothesized that increase of both stimulus parameters would lead to higher intensity ratings and larger ERP responses. 2. Material and methods A total of 20 subjects participated in the study, 10 of them were women, 10 were men. They were between 20 and 30 years of age. Health and normal olfactory function were ascertained with a detailed medical history, an ENT examination, and the ‘‘Sniffin’ Sticks’’ test (Kobal et al., 1996, 2000). The study was conducted according to the Declaration of Helsinki. Subjects gave written informed consent prior to the study. Using a bio-feedback device, subjects were trained to breathe through their mouth without concomitant nasal airflow (velopharyngeal closure (Kobal, 1981)), which avoided respiratory airflow in the nasal cavity during chemosensory stimulation. Subjects were investigated on 5 occasions. On 4 of these occasions olfactory event-related potentials (OERP) were recorded, using phenyl ethyl alcohol (PEA) and hydrogen
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sulfide (H2S) as stimulants which are known to be pure odorants (Doty et al., 1978; Hummel et al., 1991). In two sessions PEA was used as stimulant, in the other two occasions H2S was applied. Intensity ratings were also recorded during ERP measurements. The sequence of the sessions was pseudorandomized and counterbalanced. In the 5th session, subjects had to rate the duration of H2S stimuli and PEA stimuli. A single session lasted approximately 1 h. Subjects received white noise through headphones in order to mask switching clicks of the stimulation device. To stabilize vigilance, subjects performed a tracking task on a computer screen. Using a joystick, they had to keep a small square inside a larger one, which moved unpredictably (Hummel and Kobal, 2002). Following presentation of each odor stimulus, subjects rated stimulus intensity on a visual analogue scale (Aitken, 1969) displayed on the screen. The left-hand end of the scale was defined as ‘‘no stimulus perceived’’ (0%), the right-hand end as ‘‘extremely strong’’ (100%). Odor stimuli were applied by means of a computercontrolled air-dilution olfactometer (OM2S, Burghart, Wedel, Germany). This stimulator allows application of rectangularshaped chemical stimuli with controlled stimulus onset. Mechanical stimulation is avoided by embedding stimuli into a constant flow of odorless, humidified air of controlled temperature (80% relative humidity, total flow 8 L/min, 36 -C) (Kobal, 1981). Odor stimuli were applied in two different concentrations (weak and strong; H2S at 2 ppm and 8 ppm; PEA at 10% and 40% of saturated air) and 3 stimulus durations (100 ms, 200 ms, 300 ms) resulting in a 6 (2 * 3) conditions paradigm. Within the sessions, each stimulus condition was presented 15 times in a randomized order. The interstimulus interval was approximately 30 s (Hummel and Kobal, 1999; Kobal, 1981). Olfactory ERP were recorded at the position Pz of the 10/20 system (referenced against linked earlobes [A1 + A2]), where olfactory ERP are known to show largest amplitudes (Livermore et al., 1992). Eye blinks were monitored via the Fp2 lead. The sampling frequency was 250 Hz; the pre-trigger period (used for determination of baseline) was 500 ms with a recording time of 2048 ms per record (band pass 0.02– 30 Hz). Recordings were additionally filtered off-line (low-pass 15 Hz). ERP were averaged after records contaminated through motor artifacts or blinks had been discarded. As averages were based on a limited number of single recordings, peak-to-peak amplitude N1P2 was measured in order to obtain stable measures independent of the baseline. Analyses were performed by means of EPEvaluate software (Kobal, Erlangen, Germany). At stimulus duration of 200 ms of the strong H2S stimulus, N1 had a mean latency of 450 ms, and P2’s mean latency was 660 ms. On the fifth session, subjects received the two stimuli (H2S, PEA) at 2 different concentrations: (weak and strong; H2S: 2 ppm and 8 ppm; PEA: 10% and 40% of saturated air) at 4 different stimulus durations (100 ms, 200 ms, 300 ms, 600 ms). The subject’s task was to rate the perceived duration of the
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stimuli on a VAS. The left-hand end of the scale was defined as ‘‘extremely short stimulus’’ (0%), the right-hand end as ‘‘extremely long stimulus’’ (100%). Statistical analyses were performed through SPSS 12.0 for Windowsi (SPSS Inc., Chicago, IL, USA). For variables of interest (ERP parameters, intensity ratings, duration ratings) repeated measures ANOVA were computed (between-subject factor ‘‘sex’’; within-subject factors ‘‘duration’’ (100 ms, 200 ms, 300 ms for the first 4 sessions; 100 ms, 200 ms, 300 ms, 600 ms for the fifth session), ‘‘concentration’’ (weak, strong), ‘‘stimulus’’ (H2S, PEA); Greenhouse-Geisser correction of degrees of freedom; post hoc testing using paired t-tests). The a-level was set at 0.05. 3. Results 3.1. ERP data Grand means of ERP are depicted in Fig. 1. Amplitudes of olfactory ERP were found to change in relation to odor concentration. Strong stimuli evoked responses with larger amplitude (‘‘concentration’’: F[1,17] = 56.3; p < 0.001). The factor ‘‘duration’’ failed to reach significance ( p = 0.062). However, a significant interaction between ‘‘concentration’’ and ‘‘duration’’ was found indicating that varying durations affected ERP amplitudes differently with weak or strong concentrations of the stimulus ( F[2,34] = 6.5; p = 0.004). In fact, when ERP after weak and strong stimuli were analyzed separately, a differentiated picture emerged. Whereas at weak stimulus concentrations no effect of stimulus duration could be observed, there was a clear effect of ‘‘duration’’ in ERP amplitudes following stimuli of strong concentrations ( F[2,34] = 7.4; p = 0.003). Longer stimulus durations led to larger amplitudes (Fig. 2). Stimuli of higher concentrations evoked ERP with shorter latencies of the peaks N1 and P2 (‘‘concentration’’: F[1,17] > 5.84; p < 0.028). Neither an effect of stimulus duration was found on ERP latencies, nor could an interaction between
duration and concentration be detected. With regard to the latency of P2 there was an interaction between ‘‘odor’’ and ‘‘concentration’’ ( F[1,17] = 6.3; p = 0.023) indicating that the relationship between concentration and latency was dependent from the odor used. 3.2. Psychophysical data 3.2.1. Intensity ratings A significant effect of ‘‘concentration’’ was found on intensity ratings ( F[1,18] = 62.7; p = 0.001), with strong stimuli leading to higher ratings. The duration of the stimuli had also an effect on intensity ratings ( F[2,36] = 90.1; p < 0.001). Longer lasting stimuli led to higher intensity ratings (Fig. 3a). There was also an effect of the factor ‘‘sex’’ on intensity ratings ( F[1,18] = 14.3; p = 0.001). Women rated stimuli as more intense than men. In addition, the two odors were rated as differently intense ( F[1,18] = 5.7; p = 0.027), with PEA stimuli being rated as stronger than H2S stimuli. 3.2.2. Duration ratings With regard to ratings of stimulus duration there were significant effects of the factors ‘‘concentration’’ ( F[1,17] = 36.3; p < 0.001) and ‘‘duration’’ ( F[3,51] = 50.6; p < 0.001) on duration ratings of olfactory stimuli. Thus, longer lasting stimuli were rated as longer lasting, but stimuli of higher concentration were also rated as longer lasting (Fig. 3b). In contrast to intensity ratings, no effects of ‘‘sex’’ could be observed for ratings of stimulus duration. The results remained unchanged when only the responses to the stimuli with duration of 100 ms, 200 ms, and 300 ms were included in the statistical analysis. 4. Discussion CSERP have traditionally been thought to be mainly dependent from stimulus concentration and stimulus onset, but to be independent from stimulus duration. For example,
Fig. 1. Grand means of ERP. Results are shown separately for stimulation with weak (upper row) and strong (lower row) stimuli. Responses to H2S are depicted on the left side; responses to PEA are depicted on the right side. Responses to stimuli of 100 ms, 200 ms, 300 ms are shown in black, dark grey and light grey, respectively. Duration and onset of stimulation is represented by bars on the x-axis.
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Fig. 2. Mean (error bars: standard error of mean—SEM) ERP amplitude N1P2 following stimulation with 3 durations (from bright to dark: 100 ms, 200 ms, 300 ms) of 2 concentrations (weak, strong) of phenyl ethyl alcohol (PEA—p) and hydrogen sulfide (H2S—h).
ERP in response to the mixed olfactory/trigeminal stimuli isoamylacetate and eucalyptol appeared to be independent from stimulus duration (Kobal, 1981). However, a recent study showed different results. A positive correlation between stimulus duration and ERP amplitudes has been shown for trigeminal stimuli (Frasnelli et al., 2003). Results of the present study were obtained for ‘‘pure’’ olfactory stimuli. They indicate that olfactory ERP components are dependent from stimulus duration. Another recent study showed similar results. Wang et al. (2002), measured the influence of stimulus ‘‘strength’’ on olfactory ERP. In this
particular study the authors defined the strength of an olfactory stimulus as its width, i.e. its duration. Thus, although they discussed the stimulus concentration being the independent variable, in fact they changed the duration of their stimuli from 35 to 200 ms. They found an effect of stimulus duration on ERP amplitude, but not on latencies. This is in line with the present study, where ERP amplitudes, but not ERP latencies increased with increasing stimulus duration. The present study showed that stronger stimuli evoked ERP with larger amplitudes and shorter latencies. This is in line with previous studies where the relationship between concentration
Fig. 3. (a) Mean (error bars: SEM) intensity ratings following stimulation with 3 durations (from bright to dark: 100 ms, 200 ms, 300 ms) of 2 concentrations (weak, strong) of phenyl ethyl alcohol (PEA—p) and hydrogen sulfide (H2S—h). (b) Mean (error bars: SEM) duration ratings following stimulation with 4 durations (from bright to dark: 100 ms, 200 ms, 300 ms, 600 ms) of 2 concentrations (weak, strong) of phenyl ethyl alcohol (PEA—p) and hydrogen sulfide (H2S—h). Note that stimuli of 400 and 500 ms were not applied.
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of chemosensory stimuli and parameters of ERP components was investigated. In some studies pure olfactory stimuli, e.g. H2S (Hummel et al., 1998; Thiele and Kobal, 1984), vanillin (Tateyama et al., 1998), or linalool (Pause et al., 1997) were applied. In these studies a negative correlation between stimulus concentration and latencies of ERP components could be detected (Pause et al., 1997; Tateyama et al., 1998; Thiele and Kobal, 1984; Hummel et al., 1998). The two studies which investigated a larger number of subjects, in addition, found a positive relationship between stimulus concentration and ERP amplitudes (Hummel et al., 1998; Tateyama et al., 1998). Accordingly, the effect of stimulus concentration is more pronounced on ERP latencies than on ERP amplitudes. The results of the present and prior studies underline the importance of distinguishing between stimulus duration and stimulus concentration. In the literature there is some confusion about these terms (compare Wang et al., 2002). Here, we use the term ‘‘concentration’’, defined as amount per volume, whereas ‘‘duration’’ is defined as the time between beginning and ending of a stimulus. We suggest not to use terms like ‘‘stimulus strength’’, ‘‘stimulus intensity’’ (which are parameters related to perception), and ‘‘stimulus width’’ when describing physical characteristics of chemosensory stimuli. The studies investigating the influence of pure olfactory stimulus parameters on ERP components can be divided into two groups. In a first group of studies the influence of stimulus duration was examined, which was found to exclusively affect ERP amplitudes (Wang et al., 2002, present study). In the second group, the effect of stimulus concentration on ERP components was studied which was found to mainly affect ERP latencies, and, to a lesser degree, also ERP amplitudes (Tateyama et al., 1998; Thiele and Kobal, 1984; Pause et al., 1997; Hummel et al., 1998, present study). The picture is again different when mixed olfactory/trigeminal stimuli are investigated. When applying such stimuli, e.g. toluene (Prah and Benignus, 1992), butanol (Lorig et al., 1993), menthol (Pause et al., 1997), eucalyptol (Kobal, 1981), and citral (Pause et al., 1996), only the latter study showed shorter ERP latencies with stimuli of higher concentrations. However, all authors found a positive correlation between stimulus concentration and ERP amplitudes. Similarly, using the (putatively) pure trigeminal stimulant CO2, ERP amplitudes appeared to be larger in response to stronger stimuli (Frasnelli et al., 2003; Mu¨ller, 1988). Again, as only the latter showed a correlation, an effect on ERP latency was not consistently found. Thus, it seems as in the olfactory system higher stimulus concentrations affect mainly ERP latencies and to a smaller degree ERP amplitudes. In the trigeminal system higher stimulus concentrations have mainly an effect on ERP amplitudes and to a smaller degree on ERP latencies. On the other hand, with regard to stimulus durations the two sensory systems behave similarly. Longer stimulus durations exclusively lead to larger ERP amplitudes, ERP latencies seem to be unaffected. The effect of stimulus duration and stimulus concentration has been studied on a cellular level in both vertebrates and invertebrates. Measuring extracellularly recorded responses from lobster chemoreceptor cells, Gomez and Atema (1996)
found higher odor concentrations, but not longer stimulus duration to lead to shorter first spike latency. With regard to stimulus duration, pheromone-sensitive olfactory neurons have been shown to encode the duration of pheromone pulses with great accuracy in moths (Christensen and Hildebrand, 1997). On the level of the antennal lobe of honeybees, which is the functional analogue of the olfactory bulb, the representation of a particular odor has been shown to change over time. Thus, it is different at the beginning of stimulation when compared to the end of stimulation (Galizia et al., 2000). Finally, also in mammals, activity patterns have been found to change over time in rodents’ olfactory bulb. Higher odor concentrations have been found to lead to shorter response latencies. Longer stimulus durations, on the other hand, were found to have an enlarging effect on the activity of single glomeruli (Spors and Grinvald, 2002). Although both stimulus characteristics lead to higher overall activity, these studies indicate on a cellular level, that stimulus concentration and stimulus duration primarily have differential effects on the olfactory system. Both the olfactory and the trigeminal system seem to integrate information over a longer period of time on a subcortical level (Frasnelli et al., 2003). In a review comparing the perception of odors and language, Lorig stated that ‘‘in order to interpret both olfactory and verbal signals, the nervous system must accumulate the neural code over an epoch, parse the phased but temporally smeared signal and assign the event to some representation’’ (Lorig, 1999). The temporal integration is reflected in the relatively long latencies of chemosensory ERP compared to other sensory modalities. Given this long latency it is conceivable that increasing stimulus duration – leading to a higher total amount of odorous molecules at the olfactory epithelium –leads to a higher degree of activation. This is confirmed by the results of the intensity ratings: not only stimuli with higher concentrations but also longer lasting stimuli lead to higher intensity. This suggests that, similar to the trigeminal system (Cometto-Muniz and Cain, 1984; Frasnelli et al., 2003; Wise et al., 2004), there is a durationconcentration trading in the olfactory system. Longer stimuli are perceived as more intense than shorter ones, although the stimulus concentration is the same; thus, stimuli with lower concentrations are perceived as equally intense as a shorter stimulus with a higher concentration. Therefore, the trigeminal system has been described as a ‘‘mass detector rather than a concentration detector’’ (Cometto-Muniz and Cain, 1984). However, if the olfactory system would be a perfect and pure mass detector, it would be difficult to correctly rate the duration of olfactory stimuli. This was not the case; as subjects could clearly distinguish between different durations of chemosensory stimuli. References Aitken, R.C., 1969. Measurements of feelings using visual analogue scale. Proc. R. Soc. Med. 62, 989 – 996. Anton, F., Euchner, I., Handwerker, H.O., 1992. Psychophysical examination of pain induced by defined CO2 pulses applied to the nasal mucosa. Pain 49, 53 – 60.
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