Introduction
The smell in terms of odor, aroma, fragrance or scent plays a remarkable role in the behavior, emotions, and cognitive functions of humans. In general, people encounter various odors in day-to-day life that influence their mood, stress, and work ability (Sowndhararajan and Kim, 2016). In aromatherapy, fragrances, especially those obtained from essential oils (EOs) have been used to maintain human homeostasis via inhalation, skin absorption, or ingestion (Kim et al., 2009, Choi and Hong, 2009). In this treatment, inhalation of fragrances has been employed to reduce depression, stress, anxiety and stress as well as improve relaxation and alertness states (Kako et al., 2008; Kiecolt-Glaser et al., 2008; Djilani and Dicko, 2012; Kubeczka, 2020). Hence, interest in stress management by aromatherapy-based treatment has increased.
There are two major mechanisms behind the actions of fragrances on human autonomic functioning and behavior. The first mechanism is a direct interaction between odor molecules and the second is receptor or nerve endings (Lahlou, 2004). It is well described that odor molecules in fragrances are transmitted to the brain via the olfactory sensory neurons in the olfactory system. During the olfactory process, chemical signals are transferred into electrical signals in the brain and then travel all over the central nervous system, including the limbic system and hypothalamus, thereby controlling human emotions (Kutlu et al., 2008, Touhara and Vosshall, 2009). Recently, numerous studies have confirmed that fragrance-associated olfactory stimulation exhibited various spontaneous psychophysiological changes in humans (Matsubara and Ohira, 2018; Liu et al., 2019; Jiang et al., 2021; Hong et al., 2022). Further, olfactory stimulation affects physiological parameters, including blood pressure, skin temperature, pulse rate, brain activity, etc (Angelucci et al., 2014; Hoferl et al., 2016; Choi et al., 2022). Therefore, it is important to study the psychophysiological effects of fragrance molecules to improve the mental health of humans.
Different electrophysiological techniques have been employed to investigate the effect of fragrances on brain function. In these, electroencephalography (EEG) is a frequently used method to determine the brain’s electrical activity (Angelucci et al., 2014; Sowndhararajan et al., 2016). EEG is one of the safest methods to study the neuronal electrical activity in healthy as well as diseased states (Lorig and Schwartz, 1988). Previous studies reported that the EEG can be used to determine the relationship between brain activity via olfactory stimulation and human central nervous system activity. Based on the stimulus condition, EEG recordings exhibit neuronal oscillations in terms of alpha, beta, theta, and delta waves at different brain regions. The changes in brain waves are highly correlated with different brain functions (Lin et al., 2022; Sun et al., 2022; Ueda et al., 2023).
Previously, Sowndhararajan and Kim (2016) presented an extensive review of the psychological and physiological influences of fragrances on human brain functions. Hence, the present review aimed to discuss the available literature from October 2016 and afterwards.
Psychological studies
Previous studies documented that pleasant fragrances can improve the physical and mental health of humans. Aromatherapy effectively improved the physical and mental health and attenuated stress states of middle-aged and old-aged persons (Ke et al., 2022). A recent study found that odors from the EOs of Japanese citrus fruits, Citrus iyo and C. junos significantly reduced fatigue feelings and improved refreshment feelings. Further, the authors observed that Yuzu EO improved task performance by increasing the concentration of oxyhemoglobin in the prefrontal cortex (Ohata et al., 2022). Fir EO improved the relaxation state by lowering the ratio of low and high frequencies compared to control conditions (Kim and Song, 2022).
Santalum album and S. spicatum EOs markedly decreased systolic blood pressure, particularly during the recreation phase. An endocrine stress indicator, the salivary level was significantly reduced during recreation in the S. spicatum EO. Based on the findings, the author suggested that EOs can improve psychological stress conditions (Hoferl et al., 2016). Another study reported that volatile organic compounds emitted from Japanese cedar timber effectively suppressed the activation of sympathetic nervous activity. Whereas, non-volatile organic compounds of Japanese cedar increased the level of cortisol in female participants (Matsubara and Kawai, 2018). In women, the EO of Japanese cedar (Cryptomeria japonica) wood modulated mood states by transiently decreasing sympathetic nervous activity (Matsubara and Ohira, 2018).
Sriraksa et al. (2018) demonstrated that the inhalation of lemongrass (Cymbopogon citratus) EO enhanced the cognitive function and regulated mood of healthy women. However, this EO did not produce any effect on the physiological status. Effects of EOs of Mentha spicata (spearmint) and Mentha piperita (peppermint) on human cognition and mood were investigated by Kennedy et al. (2018). The results revealed that M. piperita EO beneficially modulated cognitive task performance in healthy adults.
In children, sleep disorder is a major problem, thereby poor sleep quality resulting in various harmful effects on their growth and development. In aromatherapy, EOs from different aromatic plants have been used to improve sleep. Keyhanmehr et al. (2018) found that the inhalation of Rosa damascena EO during the night effectively improved sleep quality in children. Tomi et al. (2017) studied the psychophysiological effects of fresh flowers of rose and their hydrosols on humans. The authors reported that rose flower fragrance showed a sedative effect.
The subjective feelings of happiness and content were enhanced during exposure to fragrances of pine needles EO, cedar wood EO, α-pinene, and thymoquinone (Schreiner et al., 2020). Joussain et al. (2017) reported that physiological responses to odors facilitated healthier food selection with better nutritional status.
Electrophysiological studies
It is well described that women experienced neurological and physical transitions during their mid-life, thereby suffering various menopausal symptoms. The data showed that fragrances of Lavandula angustifolia, Boswellia carterii, and Cymbopogon martini EOs increased alpha activity and decreased β/α ratio based on the severity of menopausal symptoms (Moon et al., 2020). Sleep quality is essential for healthy life and it is crucial to brain metabolism. During sleep, delta wave often indicates good sleep quality whereas alpha wave normally shows poor sleep quality. A study indicated that lavender (Lavendula angustifolia) aroma enhanced sleep quality with more daytime vigorous by decreasing the alpha wave in the wake stage and increasing the delta wave in slowwave sleep (Ko et al., 2021).
Air with the fragrance of common rush (Juncus effusus L. var. decipiens) enhanced the relaxation state by increasing alpha wave activity and parasympathetic nervous activity. In addition, a lower concentration of common rush resulted in a greater enhancement of relaxation (Sun et al., 2022). Park et al. (2019) reported that lavender aroma showed stabilizing effect by increasing alpha wave and peppermint (Mentha x piperita) and coffee aromas exhibited arousal effects by decreasing alpha wave activity. A study indicated that fragrant and non-fragrant Primula plants significantly decreased blood pressure and pulse rate. Further, Primula improved relaxation and comfort states by activating high alpha and high beta waves (Jiang et al., 2021). The inhalation of lavender and peppermint fragrances exhibited EEG abnormalities, mainly affecting the right hemisphere and temporal region. When compared with peppermint, lavender fragrance showed a more relaxed state of the brain (Ojha et al., 2017).
The floral fragrance of Rosa hybrida improved the concentration state and Cymbidium faberi fragrance enhanced the relaxation state (Kim et al., 2016). In women, olfactory stimulation with ten EOs such as lavender, rosemary (Salvia rosmarinus), rose (Rosa sp.), eucalyptus, jasmine, geranium (Geranium sanguineum), chamomile (Chamaemelum nobile), clary sage (Salvia sclarea), thyme (Thymus vulgaris), and peppermint exhibited a stabilizing effect by modulating brain activity and decreasing systolic blood pressure (Choi et al., 2022). Songsamoe et al. (2021) stated that cooked brown rice with the fragrance of Michelia alba EO increased alpha and beta waves, resulting in anti-stress effects with a relaxation state. Saengwong-Ngam et al. (2022) found that consumption of tangerine EO-treated bananas increased brain alertness by activating the beta wave activity.
Seo et al. (2016) revealed the influence of binasal and uninasal inhalations on the EEG activity of the EO of Abies koreana twigs. The results indicated that significant increases in the absolute alpha and fast alpha activity were observed during the inhalation of A. koreana EO via binasal. However, absolute beta and theta waves were significantly decreased via uninasal inhalation. These EEG changes may enhance relaxation (binasal inhalation) and alertness (right uninasal inhalation) states of the brain.
The inhalation of Litsea cubeba EO had a sedative effect by decreasing alpha and beta wave activity. In the case of Garlic EO, lower concentration produced changes in the fast alpha activity. Further, Litsea cubeba and turmeric EO showed higher positive effects when compared with garlic EO (Sattayakhom et al., 2021). The inhalation of the EO of Chrysanthemum indicum showed a relaxation effect by activating theta and alpha waves and showed excessive attention by decreasing beta and gamma waves (Kim et al., 2018a). Peppermint EO exhibited various effects on the brain based on different visual stimuli. In the white-sniffing group, Peppermint EO increased alpha waves in the prefrontal area, which improved learning and thinking (Lin et al., 2022).
Sowndhararajan et al. (2017) reported that the inhalation of EO and supercritical carbon dioxide extract (SC-CO2) of Angelica gigas root produced significantly different EEG activity. However, no significant change was observed in absolute waves during the inhalation of SC-CO2. The authors suggested that the EO of A. gigas root may enhance language learning abilities by altering the absolute low beta activity. Recently, Ueda et al. (2023) studied the effects of the inhalation of lemon, sandalwood, and kusunoki EOs on the psychophysiological activity of humans. The authors reported that lemon EO inhalation significantly improved task performance by activating delta and theta bands in the prefrontal cortex. Further, the inhalation of sandalwood EO activated beta and gamma bands in the prefrontal cortex. Liu et al. (2019) suggested that blended EO improved human selective attention by significantly changing brain activity and functional connections.
Gender variation plays a critical role in the EEG activity of various fragrances. Interestingly, geosmin and 2-methylisoborneol have similar smell characteristics of soil but they exhibited different EEG activity based on gender difference (Kim et al., 2017). Kim et al. (2019) reported that Cambodian black pepper EO produced markedly different EEG activity in men and women. A significant increase of ASEF was noticed during the inhalation of black pepper EO in women. Whereas significant increases in relative gamma, ratio of sensorimotor rhythm (SMR) to theta (RST), spectral edge frequency 50% (SEF50), spectral edge frequency 90% (SEF90), and Spectral dege frequency 50% of alpha (ASEF) were observed in men.
Pinene compounds are major monoterpene components in a variety of EOs. Among them, (+)-α-Pinene and (+)-β-pinene isomers have different fragrance qualities and these isomers produced markedly different EEG activity. Further, the EEG activity of these components varied according to gender difference. When compared with men, women were highly sensitive to these isomeric compounds. Exposure to (+)-α-pinene significantly increased absolute alpha, beta, and high beta waves in women. Whereas exposure to (+)-β-pinene significantly increased absolute fast alpha and high beta waves in women. On the other hand, absolute theta, beta, low beta, and high beta waves significantly increased during the inhalation of (+)-α-pinene in men but no significant change in EEG activity was observed during exposure to (+)-β-pinene (Kim et al., 2018b).
The olfactory stimulation of EO of Inula helenium root markedly reduced absolute theta, beta, and mid beta and relative theta waves. On the other hand, significant increases in the ratio of SMR to theta, SMR~mid beta to theta, and spectral edge frequency 50% of alpha (ASEF) were noticed during exposure to I. helenium EO (Sowndhararajan et al., 2016). In a recent study, Agastache rugosa (Korean mint) EO with a pleasant fragrance significantly decreased absolute theta and relative theta waves. Further, significant increases in relative alpha, relative slow alpha, SEF50, and ASEF activity were observed during A. rugosa EO exposure. These changes in EEG activity may enhance the freshness and alertness states of the brain functions (Hong et al., 2022).
In perfumery products, aldehydes are commonly used for different fragrance notes. In these, nonanal (C9) and decanal (C10) are used to enrich floral and citrus notes in various perfumery products. A study indicated that olfactory stimulation with C10 odor showed different EEG changes according to uninasal and binasal inhalations. In particular, a significant decrease in absolute alpha and beta waves was observed during the inhalation of C10 odor. However, C9 odor produced significant changes in EEG power spectra only via binasal inhalation (Kim et al., 2019a). Further, Sowndhararajan et al. (2023) and Kim et al. (2019c) demonstrated that exposure to aldehydes C9 and C10 odor produced a highly unstable EEG activity. Hence, EEG recording and analysis time play a critical role in the EEG response to olfactory stimulation of different odors.
Conclusions
Previous studies clearly demonstrated that olfactory stimulation with fragrances affected spontaneous brain wave activity and these changes may contribute to various psychophysiological functions of humans. Further, EEG is a good technique to measure brain wave changes during exposure to different fragrances. It can be understood that different brain waves (delta, theta, alpha, beta, and gamma) are representative of particular functions of the brain. The published literature technically confirmed the beneficial effect of fragrances in aromatherapy. Among different fragrances, the fragrance of lavender EO exhibited an exceptional role in producing various positive psychophysiological effects. Moreover, gender and nostril variations, age of the participants, the concentration of fragrant molecules, the nature of fragrances, EEG recording time, statistical analysis method, and fragrant administration techniques play a crucial role in the psychophysiological activity of fragrances in humans.
Acknowledgments
This study was carried out with the support of the “Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ01669705)”, Rural Development Administration, Republic of Korea.