Quality of odor and olfactory lateralization processes in humans

Neuroscience Letters 316 (2001) 91–94 www.elsevier.com/locate/neulet

Quality of odor and olfactory lateralization processes in humans Ge´rard Brand*, Laurence Jacquot Laboratoire de Neurosciences, Faculte des Sciences, Place Leclerc, 25000 Besanc¸on, France Received 2 February 2001; received in revised form 10 October 2001; accepted 10 October 2001

Abstract The study of olfactory lateralization processes in humans has given rise to many publications, but the resulting data have not been homogeneous. Sensorial cerebral asymmetry depends on several factors (nature of task, characteristics of subjects, etc.) and could also depend on the quality of the stimulus, especially in olfaction. This field appears to be widely unexplored and the quality of odor is a complex property. The aim of this study was to investigate variations in psychophysiological measurements (bilateral electrodermal recordings) related to the quality of odors. Electrodermal asymmetries were used as a function of differential hemispheric activation. Two major characteristics of odor were explored, the hedonic valence (pleasant/unpleasant) and the trigeminal component (irritant/non-irritant). The results obtained in a sample of 30 right-handed subjects (15 males and 15 females) showed a predominance of the right hemisphere in the treatment of olfactory information not depending on the quality of odor, except the trigeminalnerve activation. q 2001 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Odor; Olfaction; Trigeminal stimuli; Lateralization; Hemispheric asymmetry; Electrodermal activity

In the field of human perception, the chemical senses (taste and smell) have received little attention from research when compared with the auditory, visual and tactile senses. In the case of olfaction, it would appear that the publications over the last few years have been trying to overcome this lack of research. Many investigations have been carried out with different methods (physiological, psychological, behavioral, etc.) and have described several aspects and characteristics of olfactory perception. Among them, one question which remains without a definitive response is whether olfactory processes are lateralized or not [2,11], as this lateralization has been established for visual, auditory and tactile senses. Current data suggest that the nature of the olfactory stimulus influences the lateralization processes. The quality of odor is a complex property, but the two most important characteristics could be the hedonic valence (i.e. pleasant/ unpleasant character) [12,15,18,23] and the trigeminal component (irritant/ non-irritant character) [17,22]. Firstly, the perception of smell is dominated by the hedonic valence because olfaction is an exteroceptive sensory modality processing with direct projections between the amygdala and primary sensory cortex. Thus, the anatomy presents a high level of functional connectivity between the olfactory * Corresponding author. Tel.: 133-3-8166-5752; fax.: 133-38166-5746. E-mail address: [email protected] (G. Brand).

and limbic systems, with ipsilateral projections. Secondly, the olfactory system coexists in the nasal cavity with other sensorial systems, especially the trigeminal system which projects contralaterally. In so far as some odorants stimulate both olfactory and trigeminal systems, the irritant component can be considered to be a quality of odor and must be investigated in the olfactory lateralization processes. The aim of the present study is to contribute to the question of olfactory lateralization processes in relation to the quality of odor with a psychophysiological measurement. From a methodological point of view, electrodermal activity (EDA) is a response frequently used in olfaction. Furthermore, monitoring bilateral activity in the electrodermal system may provide further information on brain mechanisms modulating peripheral responses. Several studies reported EDA asymmetries as a function of differential hemispheric activation [16,21], even though few bilateral EDA studies have used olfactory stimulations. In previous experiments using bilateral electrodermal recordings, it has been shown that bilateral asymmetry is not linked to the side of the nose [4], and is not linked to monorhinal or birhinal stimulations [5]. Four specific odorants were used in this study: one pleasant odorant, isoamyl acetate (C7H14O2; molecular weight, 130.2); one unpleasant odorant, triethylamine (C6H15N; molecular weight, 101.2); one odorant with minimal intra-

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G. Brand, L. Jacquot / Neuroscience Letters 316 (2001) 91–94

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Fig. 1. Mean SCR bilateral amplitudes (left hand 2 right hand) recorded during monorhinal and birhinal stimulations and related to the quality of odor (e.g. hedonic valence and trigeminal component). For significant differences: **P , 0.01 and *P , 0.05.

nasal trigeminal stimulative properties [9,10], phenyl ethyl alcohol (C8H10O; molecular weight, 122.2); and one odorant with great trigeminal properties [14], allyl isothiocyanate (C4H5NS; molecular weight, 99.15). The concentrations in suprathreshold were prepared in a previous experiment carried out with a sample of 15 subjects with a scale of intensity scored from 1 to 10 in order that the perceived intensity be similar for the four odorant stimuli. The odorant stimulus in liquid form was presented in a bottle (7.5 cm high, 1 cm in diameter at the opening) filled with 4 ml of liquid. The bottle was presented to the subject for a period of 3 s at a distance of 1 cm from the nostrils using a holder to avoid any olfactory or thermic interference with the experimenter’s hand. The olfactory stimuli were delivered in three ways: bilaterally; and unilaterally (right or left). When the stimulation was unilateral, the unstimulated nostril was blocked with a nose plug. The order of the tests was randomized. The session began with a rest period of 5 min and the average inter-trial interval was around 3 min.

Only right-handed subjects (15 males and 15 females) took part in this study because handedness is a readily available behavioral correlate of individual differences for the degree of sensorial lateralization [8] and bilateral EDA differences [19,20]. Here, the EDA parameter used was the skin conductance response (SCR) amplitude expressed in microsiemens (mS). The SCR was recorded from each hand with a MacLab System (GRS Amp. ADInstruments) interfaced to a compatible computer. The dry, bright-plated bipolar electrodes were attached with a Velcro attachment strap to the palmar surfaces of the middle phalanges of the first and the second fingers of both hands. Student’s t-tests (paired and independent) were used for the statistical analyses and non-significant results were noted as NS. The results are reported in Fig. 1. The statistical analyses showed that whatever the odor, the SCRs were not significantly different between the two nostrils (Table 1). Whereas the perceived intensities were similar for the four odorant stimuli, the amplitudes of the SCRs were

Table 1 Comparisons between the two nostrils

Right hand Left hand

Isoamyl acetate

Triethylamine

Phenyl ethyl alcohol

Allyl isothiocyanate

t ¼ 0.408; NS t ¼ 0.725; NS

t ¼ 0.897; NS t ¼ 0.561; NS

t ¼ 0.346; NS t ¼ 0.282; NS

t ¼ 0.366; NS t ¼ 0.904; NS

G. Brand, L. Jacquot / Neuroscience Letters 316 (2001) 91–94 Table 2 Comparison between isoamyl acetate and triethylamine

Right hand Left hand

Right nostril

Left nostril

Both nostrils

t ¼ 3.922; P , 0.001 t ¼ 3.887; P , 0.001

t ¼ 4.254; P , 0.001 t ¼ 4.619; P , 0.001

t ¼ 2.332; P , 0.01 t ¼ 1.940; P , 0.05

different for each odor. The SCR amplitudes obtained with isoamyl acetate appeared significantly lower than those obtained with triethylamine (Table 2). The SCR amplitudes obtained with phenyl ethyl alcohol appeared lower than those obtained with allyl isothiocyanate, a more significant result on the right hand than on the left hand recordings (Table 3). In the comparison between the pleasant odor (isoamyl acetate) and the unpleasant odor (triethylamine), the SCR amplitudes recorded on the left hand were always greater than those on the right hand (Table 4). On the contrary, the direction of SCR bilateral differences varied between the odor stimulus without the trigeminal component (phenyl ethyl alcohol) and the odor stimulus with great trigeminal properties (allyl isothiocyanate). In this case, the SCR amplitudes recorded on the left hand were greater than those on the right hand for phenyl ethyl alcohol, and the SC amplitudes recorded on the right hand were greater than those on the left hand for allyl isothiocyanate (Table 5). Finally, a comparative analysis of the male and female subjects showed that the SCRs were never significantly different whatever the stimulation (right nostril, left nostril, both nostrils), whatever the nasal stimulus, and whatever the hand recorded. The present study supports our previous studies reporting that the EDA in response to an olfactory stimulation did not differ according to the nostril involved and revealed the same findings for the trigeminal stimulation. Thus, bilateral EDA differences in olfaction could not have resulted from peripheral factors as the results were the same whatever the side of the nose. The results showed that the SCR amplitudes were significantly greater on the left hand than the right hand whatever the stimulation (right nostril, left nostril, both nostrils) during olfactory nasal inputs, and whatever the hedonic valence. As the EDA is contralaterally

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Table 4 Pleasant versus unpleasant odor stimulus a

Isoamyl acetate Triethylamine

Right nostril

Left nostril

Both nostrils

md ¼ 10.207 md ¼ 10.326 t ¼ 0.672; NS

md ¼ 10.261 md ¼ 10.292 t ¼ 0.033; NS

md ¼ 10.345 md ¼ 10.438 t ¼ 0.128; NS

a Mean bilateral differences (md) between the left hand and the right hand recordings (left hand 2 right hand).

governed, the results suggest a right hemispheric dominance. In the same way, the results could still indicate a left lateral dominance for the treatment of trigeminal information, in so far as the direction of EDA asymmetries during irritant odor stimulus was the opposite of the direction of EDA asymmetries during non-irritant odor. The assumption of a differential hemispheric asymmetry in relation to the trigeminal component of nasal input, whereas the hedonic valence could not play a clear role in olfactory lateralization processes, is in agreement with the findings of recent research using new techniques of functional imaging [6,22,24]. This could be worthy of investigation in so far as few studies of lateralization have explicitly characterized odorants in terms of these properties. Even though the psychophysical tests indicated the same perception level of intensity for the four odorant stimuli, the EDA amplitudes appeared very different according to each odorant. It is well known that the higher activation of the autonomic nervous system during trigeminal nasal input can be related to a protective role, especially in relation to the respiratory tract [13]. The higher activation of the autonomic nervous system in response to unpleasant versus pleasant nasal input is in agreement with the findings of Brauchli et al. [7] and Alaoui-Ismaı¨li et al. [1], but any explanation (such as that it could be related to a role in food intake) is good to establish today. There are sex differences in olfactory abilities along all of the pathways of perception, from smelling behavior to the complex processes of cognitive treatment [3]. In general, women tend to outperform men on many tasks, such as identification, discrimination or memory. However, in the same way, as was found in the present study, there is no

Table 5 Irritant versus non-irritant odor stimulus a Table 3 Comparison between phenyl ethyl alcohol and allyl isothiocyanate

Right hand Left hand

Right nostril

Left nostril

Both nostrils

t ¼ 3.296; P , 0.001 t ¼ 2.012; P , 0.05

t ¼ 4.338; P , 0.001 t ¼ 1.145; NS

t ¼ 2.549; P , 0.01 t ¼ 0.965; NS

Phenyl ethyl alcohol Allyl isothiocyanate

Right nostril

Left nostril

Both nostrils

md ¼ 10.246

md ¼ 10.165

md ¼ 10.170

md ¼ 20.182

md ¼ 20.316

md ¼ 20.087

t ¼ 2.143; P , 0.05

t ¼ 2.204; P , 0.05

t ¼ 1.523; NS

a Mean bilateral differences (md) between the left hand and the right hand recordings (left hand 2 right hand).

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