111 1. Introduction Recent studies have focused on the physiological relax- ing effects of the natural environment (Park et al., 2009; 2012). It has been reported that staying in a forest environ- ment enhances parasympathetic nervous activity (Park et al., 2012; Tsunetsugu et al., 2013), suppresses sympathetic nervous activity (Park et al., 2012; Tsunetsugu et al., 2013; Lee et al., 2014), decreases blood pressure and pulse rate (Park and Mattson, 2009; Park et al., 2012), and decreases cortisol concentration (Park et al., 2012). Studies by Li et al. (2007, 2008 a, b) demonstrated that staying in a forest environment for three days and two nights improved the immune function of office workers (Li et al., 2007), and this effect was sustained for approximately one month (Li et al., 2008 a, b). Another study reported that walking in an urban park enhances parasympathetic nervous activity and decreases heart rate (Song et al., 2013). In addition, spend- ing time in rooftop gardens enhances parasympathetic ner- vous activity and suppresses sympathetic nervous activity in elderly people requiring care (Matsunaga et al., 2011). Evidence-based medicine has been attracting attention globally, with physiological data from field tests making a significant contribution. We expect that accumulating physiological data from field experiments will continue to demonstrate the preventive medical effects of nature ther- apy in the future (Lee et al., 2012). In modern society, many individuals spend the major- ity of their time in intensely stressful states, and they have no time to make contact with nature outside of their im- mediate surroundings. High school students, who spend most of their everyday life at school, are typical examples. Previous studies have evaluated the psychological stress levels in high school students (Anda et al., 2000; Takakura and Sakihara, 2001). Moreover, many high school students have stressful relationships with friends or teachers (Mi- ura and Kawada, 2008). In a document by the Japanese Ministry of Education, the percentage of students who progressed to universities or junior colleges in 2010 was 56.9%, which was 18.5% higher than the rate in 1975 (Sta- tistics Bureau, Ministry of Internal Affairs and Communi- cations, 2012), and the pressure from entrance examina- tions is extremely high among high school students (Equal Employment, Children and Families Bureau, Ministry of Health, Labour and Welfare, 2009). Physiological and psychological relaxing effects of visual stimulation with foliage plants in high school students H. Ikei*, C. Song*, M. Igarashi*, T. Namekawa**, Y. Miyazaki*(1) * Center for Environment, Health and Field Sciences, Chiba University, 6-2-1 Kashiwanoha, Kashiwa, Chiba 277-0882, Japan. ** Chiba Prefectural Kashiwanoha Senior High School, 6-1 Kashiwanoha, Kashiwa, Chiba 277-0882, Japan. Key words: heart rate variability, minors, house plant, stress reduction, visual stimuli. Abstract: With lifestyles in modern society becoming increasingly stressful, there is growing interest in the physiological relaxing effects of the natural environment. Particular interest has been paid to the physiological effects of indoor plants, however no studies have revealed the effects of such visual stimulation on minors. In this study 85 (41 male and 44 fe- male; 16.5±0.9 years; mean±SD) students were exposed, or not as control, to a typical foliage plant, dracaena (Dracaena deremensis; Lemon Lime), for 3 min. Physiological indices included heart rate variability (HRV) and pulse rate, using an accelerated plethysmography at the fingertip, were collected continuously during the experiments. The results indicated that the high frequency component (HF), a general index of parasympathetic nervous activity, was significantly higher; the low frequency component [LF/(LF+HF)], a general index of sympathetic nervous activity, was significantly lower; and the pulse rate was significantly lower. After exposure, or not, the subjects completed a questionnaire as psychological evaluation. A 13-point rating scale was used for following parameters: “comfortable-uncomfortable,” “relaxed-awaken- ing,” and “natural-artificial.” Results of the study showed that subjects felt more comfortable, relaxed and natural after visualizing the dracaena plants. Overall, the physiological and psychological relaxing effects of visual stimulation with foliage plants in high school students is confirmed. Adv. Hort. Sci., 2014 28(2): 111-116 (1) Corresponding author: ymiyazaki@faculty.chiba-u.jp Received for publication 31 March 2014 Accepted for publication 29 July 2014 112 Flowers and foliage plants are common natural sur- roundings that can be incorporated into the school and home. We previously conducted surveys to evaluate the physiological effects of visual stimulation with fresh rose flowers in high school students (Ikei et al., 2013), middle-aged and elderly medical staff (Komatsu et al., 2013), and office workers (Ikei et al., 2014). The results showed enhanced parasympathetic nervous activity (Ikei et al., 2013; Komatsu et al., 2013; Ikei et al., 2014), sup- pressed sympathetic nervous activity (Ikei et al., 2013), and decreased pulse rates (Komatsu et al., 2013) during visual stimulation. It was reported in a previous study that natural views from hospital windows or the presence of indoor plants hasten the recovery of patients after surgery and decrease systolic blood pressure (Park and Mattson, 2009). These effects have also been studied in a classroom, demonstrat- ing that the ambience of indoor space can be improved by including foliage plants (Doxey et al., 2009), as reflected by enhanced feelings of comfort among the students (Han, 2009). However, there have been no reports on the influ- ence of visual stimulation with foliage plants on heart rate variability (HRV) and subjective feelings in minors. Therefore, this study was conducted to examine the effects of exposure to the foliage plant dracaena (Ministry of Ag- riculture, Forestry and Fisheries, 2008) on physiological and psychological variables (HRV, pulse rate, and subjec- tive responses) in high school students. 2. Materials and Methods The experiments were conducted in a classroom of the Chiba Prefectural Kashiwanoha Senior High School in October 2012. The room temperature was approximately 25.9°C, relative humidity approximately 52.6%, and illumi- nation approximately 900  lux. Eighty-five high school stu- dents (41 male and 44 female; 16.5±0.9 years; mean±SD) participated in the experiment. The study was conducted with the approval of the Ethics Committee of the Center for Environment, Health and Field Sciences, Chiba University. All subjects provided written informed consent. Three dracaena plants (Dracaena deremensis, Lemon Lime), 55-60 cm high, were placed at intervals of 8 cm on a desk in front of each subject (test situation). The distance from the subject’s eyes to the plants was approximately 55 cm, and they were adjusted according to the height of the subjects. No exposure to foliage plants was used as the con- trol condition. Before visual stimulation, the plants and the control were covered by a corrugated cardboard box (rest condition). Figure 1 shows the study protocol, figure 2 the rest condition, and figure 3 the visual stimuli (the dracaena Fig. 1 - Study protocol for testing the physiological and psychological relaxing effects of visual stimulation with foliage plants in high school students. Fig. 2 - The rest condition. Fig. 3 -The visual stimulation condition. 113 plants or control). After viewing the cardboard box at rest in a sitting posture for 1 min (Fig. 2), the subject was exposed to the plants or control for 3 min (Fig. 3). After the experi- ments, each subject completed a questionnaire. The order of stimuli was counterbalanced among subjects. HRV and pulse rate were measured as physiological indices. HRV was calculated by spectral analysis of the coefficient of variation of the a-a interval on an accelerated plethysmograph (APG; ARTETT, U-Medica Inc., Osaka, Japan). Previous studies have reported that the a-a interval on an APG and R-R interval on an electrocardiogram are strongly correlated (Takada and Okino, 2004; Takada et al., 2008). The sampling frequency was set at 1000 Hz. The maximum entropy method was used for frequency analysis, and variance of the low frequency (LF; 0.04-0.15 Hz) and high frequency (HF; 0.15-0.40 Hz) components were calculated. The LF/(LF+HF) ratio for R-R interval variability was also assessed. The HF component was used as an index of parasympathetic nervous activity and the LF/(LF+HF) ratio was used as an index of sympathetic nervous activity (Weise and Heydenreich, 1989; Cacioppo et al., 1994; Sawada et al., 1997). Generally, parasympa- thetic nervous activity is enhanced during relaxation and sympathetic nervous activity is enhanced at the time of awakening and stress (Ackerknecht, 1974). Therefore, the pulse rate was converted by dividing 60 by the a-a inter- val on APG. The HRV and pulse rate data were collected continuously during the 3-min experiments and averaged. In addition, the subjects subjectively evaluated the emotional effects of the dracaena plants and control using the modified semantic differential (SD) method (Osgood et al., 1957), which uses three pairs of adjectives on 13 scales, including “comfortable-uncomfortable,” “relaxed- awakening,” and “natural-artificial.” The Statistical Package for Social Sciences software (v20.0, IBM Corp., Armonk, NY, USA) was used for all statistical analyses. A paired t-test was used to compare the physiological responses to visual stimulation with dra- caena plants or control, followed by Holm correction of the changes in each 1-min average, while the Wilcoxon signed rank test was used to compare the psychological responses to visual stimulation with dracaena plants or control. For both conditions, one-sided tests were used because of the hypothesis that humans are relaxed by visual stimulation with foliage plants. Statistical differences were considered significant at P<0.05. 3. Results Significant differences were found in the values of the HF component and the LF/(LF+HF) ratio of HRV between dracaena and the control. Figure 4 shows the HF component of HRV, an estimate of parasympathetic nervous activity. HF between 0 and 1 min was 1210.7±120.3 (mean±SE) ms2 during the test condition and 1032.9±95.2 ms2 during the control condition, showing a significant increase of 17.2% (P<0.05) (Fig. 4A) during the test condition. Similarly, HF between 1 and 2 min was 1052.0±109.3 ms2 during the test condition and 893.1±87.1 ms2 during the control condition, showing a significant in- crease of 17.8% (P<0.05) (Fig. 4A) during the test condi- tion. There was no significant difference in HF between 2 and 3 min. The overall HF during the 3-min experiment was 1083.9 ± 101.5 ms2 in the test condition and 954.8±83.5 ms2 in the control condition, showing a significant increase of 13.5% (P<0.01) (Fig. 4B) with the test condition, indicat- ing that parasympathetic nervous activity was significantly higher during dracaena plant exposure. The results of the LF/(LF+HF) ratio, a marker of sympathetic nervous activity, are shown in figure 5. For 1-min segment analysis, the LF/(LF+HF) ratio between 0 and 1 min was 0.47±0.02 during the test condition and 0.52±0.02 during the control condition, showing a signifi- cant decrease of 9.6% (P<0.05) (Fig. 5A) with the former. Fig. 4 - The 1-min averages and overall mean high frequency component (HF) of heart rate variability (HRV) during visual stimulation with dracaena plants and control. (A) Changes in each 1-min average HF value over 3 min. (B) Overall mean HF values. n=85. mean±SE. *P < 0.05, **P < 0.01 as determined by the paired t-test, Holm correction. Fig. 5 - The 1-min averages and the overall mean LF/(LF+HF) ratio of heart rate variability. (HRV) during visual stimulation with dracaena plants and control. (A) Changes in each 1-min average LF/(LF+HF) value over the 3 min. (B) Overall mean LF/(LF+HF) values. n=85. mean±SE. *P<0.05 as determined by the paired t-test, Holm correction. 114 Similarly, between 1 and 2 min, the ratio was 0.48±0.02 during the test condition and 0.54±0.02 during the con- trol condition, showing a significant decrease of 11.1% (P<0.05) (Fig. 5A) during the test. No significant differ- ence was observed between 2 and 3 min. For the entire 3-min duration, LF/(LF+HF) was 5.6% lower during the test condition than during the control condition (dracaena: 0.51±0.02, control: 0.54±0.02; P<0.05) (Fig. 5B), indi- cating that sympathetic nervous activity was significantly lower during dracaena plant exposure. Clear differences in pulse rate were observed between dracaena and control exposure. The pulse rate between 0 and 1 min was 71.9±1.2 beats/min during the test condi- tion and 72.7±1.2 beats/min during the control condition, showing a significant decrease of 1.1% (P<0.05) (Fig. 6A) during the test condition. Similarly, between 1 and 2 min, the pulse rate was 72.6±1.2 beats/min during the test con- dition and 73.3±1.2 beats/min during the control condition, showing a significant decrease of 1.0% (P<0.05) (Fig. 6A) during dracaena plant exposure. No significant difference was observed between 2 and 3 min. The mean pulse rate was 0.1% lower during the test condition than during the control condition (dracaena: 72.4±1.2 beats/min, control: 73.0±1.2 beats/min; P<0.05) (Fig. 6B). The subjective evaluation data clearly showed the ef- fect of the two different visual stimuli on the psychological states of participants. Participants felt significantly more comfortable (dracaena: “slightly comfortable”; control: “indifferent”; P<0.01) (Fig. 7, left), relaxed (dracaena: “slightly relaxed”; control: “indifferent”; P<0.01) (Fig. 7, center), and natural (dracaena: “slightly natural”; control: “indifferent”; P<0.01) (Fig. 7, right) in the dracaena con- dition than in the control condition after stimuli. 4. Discussion and Conclusions An improved ambience resulting from the placement of foliage plants in a classroom may significantly enhance physiological relaxation and mental health in high school students, as shown in the present investigation. Relatively brief (3 min) visualization of foliage plants resulted in significantly enhanced parasympathetic ner- vous activity (13.5%), suppressed sympathetic nervous activity (-5.6%), and decreased pulse rate (-0.8%), results which are consistent with previous studies involving the visualization of a forest scene (Park et al., 2010; Tsunetsu- gu et al., 2010; Park et al., 2011). Furthermore, our find- ings are consistent with those of our previous report on the calming effects of roses in high school students (Ikei et al., 2013), where similar physiological responses were found. Also in line with our findings, visual stimulation with fresh roses enhanced parasympathetic nervous activity and significantly decreased the heart rate in middle-aged and elderly medical staff (Komatsu et al., 2013), while it en- hanced parasympathetic nervous activity in office workers (Ikei et al., 2014). According to our analysis of the three questionnaires, the subjects in the present study felt more comfortable, relaxed, and natural after visualizing the dracaena plants. This result is consistent with that of our previous report on the calming effects of roses (Ikei et al., 2013; Komatsu et al., 2013; Ikei et al., 2014). The results of this study support the hypothesis that placement of foliage plants in classrooms can induce a re- laxing effect, improve physiological activity, and improve the psychological state in high school students. Because of the growing interest in mental health in modern times (Murray and Lopez, 1996), the psychological benefits of indoor plants are expected to play an important role in the promotion of mental health in the future. However this study had limitations. First, we only eval- uated HRV. Thus, the results cannot be interpreted in terms of a complete physiological evaluation. Other experimen- tal indices such as brain activity and stress hormone lev- els should be assessed to determine the effects of visual stimulation with natural objects, such as foliage plants on human response. Second, only dracaena plants were used. Fig. 6 - The 1-min averages and overall mean pulse rate during visual stimulation with dracaena plants and control. (A) Changes in each 1-min average pulse rate over the 3 min. (B) Overall mean pulse rates. n=85. mean±SE. *P < 0.05 as determined by the paired t-test, Holm correction. Fig. 7 - Changes in subjective evaluation for “comfortable–uncomfort- able,” “relaxed–awakening,” and “natural–artificial” with dra- caena plant exposure and control exposure. n=85. mean±SE. **P < 0.01 as determined by the Wilcoxon signed-rank test. 115 In future experiments, we will examine human responses to exposure to multiple types of foliage plants. We predict that the physiological data will support the physiological and psychological relaxing effects of foliage plants, which may subsequently lead to their increased use in educa- tional establishments in attempts to decrease stress among students. A brief visual stimulation of foliage plants shifted the sympathetic/parasympathetic balance and improved mood, suggesting a simple method to decrease stress and improve the health of high school students. Acknowledgements This work was supported by a grant from the Policy Research Institute, Ministry of Agriculture, Forestry and Fisheries (Extramural Research Program for Agricultural, Forestry and Fishery Policy Research). We would like to express our gratitude to Ms. Misako Komatsu and Ms. Mariko Aga for their valuable contributions to data col- lection. References ACKERKNECHT E.H., 1974 - The history of the discovery of the vegetative (autonomic) nervous system. - Med. Hist., 18: 1-8. ANDA D., BARONI S., BOSKIN L., BUCHWALD L., MOR- GAN J., OW J., GOLD J.S., WEISS R., 2000 - Stress, stress- ors and coping among high school students. - Child Youth Serv Rev., 22: 441-463. CACIOPPO J.T., BERNTSON G.G., BINKLEY P.F., QUIG- LEY K.S., UCHINO B.N., FIELDSTONE A., 1994 - Au- tonomic cardiac control. II. Noninvasive indices and basal response as revealed by autonomic blockades. - Psychophys- iology. 31: 586–598. DOXEY J.S., WALICZEK T.M., ZAJICEK J.M., 2009 - The impact of interior plants in university classrooms on student course performance and on student perceptions of the course and instructor. - HortScience, 44: 384-391. EQUAL EMPLOYMENT, CHILDREN AND FAMILIES BU- REAU, MINISTRY OF HEALTH, LABOUR AND WEL- FARE, 2009 - 2-6-1. Anxiety and worries of current. Nation- wide Survey on Families and Children 2009. - Japan Ministry of Health, Labour and Welfare, Tokyo, Japan. HAN K.T., 2009 - Influence of limitedly visible leafy indoor plants on the psychology, behavior, and health of students at a junior high school in Taiwan. - Environ. Behav., 41: 658- 692. IKEI H., KOMATSU M., SONG C., HIMORO E., MIYAZAKI Y., 2014 - The physiological and psychological relaxing ef- fects of viewing rose flowers in office workers. - J. Physiol. Anthropol., 33: 6. IKEI H., LEE J., SONG C., KOMATSU M., HIMORO E., MI- YAZAKI Y., 2013 - Physiological relaxation of viewing rose flowers in high school students. - Jpn. J. Physiol. Anthropol. (Japan), 18: 97-103. KOMATSU M., MATSUNAGA K., LEE J., IKEI H., SONG C., HIMORO E., MIYAZAKI Y., 2013 - The physiological and psychological relaxing effects of viewing rose flowers in medical staff. - Jpn. J. Physiol. Anthropol. (Japan), 18: 1-7. LEE J., LI Q., TYRVAINEN L., TSUNETSUGU Y., PARK B.J., KAGAWA T., MIYAZAKI Y., 2012 - Nature therapy and preventive medicine, pp. 325-350. - In: MADDOCK J. (ed.). Public Health-Social and Behavioral Health. InTech, pp. 582. LEE J., TSUNETSUGU Y., TAKAYAMA N., PARK B.J., LI Q., SONG C.R., KOMATSU M., IKEI H., TYRVÄINEN L., KAGAWA T., MIYAZAKI Y., 2014 - Influence of forest therapy on cardiovascular relaxation in young adults. - Evid. Based Complement. Alternat. Med., Vol. 2014, 834360, pp. 7. LI Q., MORIMOTO K., KOBAYASHI M., INAGAKI H., KAT- SUMATA M., HIRATA Y., HIRATA K., SHIMIZU T., LI Y.J., WAKAYAMA Y., KAWADA T., OHIRA T., TAKAYA- MA N., KAGAWA T., MIYAZAKI Y., 2008 b - A forest bathing trip increases human natural killer activity and ex- pression of anti-cancer proteins in female subjects. - J. Biol. Regul. Hoemeost. Agents, 22: 45-55. LI Q., MORIMOTO K., KOBAYASHI M., INAGAKI H., KAT- SUMATA M., HIRATA Y., HIRATA K., SUZUKI H., LI Y.J., OHIRA T., MATSUI N., KAGAWA T., MIYAZAKI Y., KREN- SKY A.M., 2008 a - Visiting forest, but not a city, increases human natural killer activity and expression of anti-cancer pro- teins. - Int. J. Immunopathol. Pharmacol., 21: 117-127. LI Q., MORIMOTO K., NAKADAI A., INAGAKI H., KATSU- MATA M., SHIMIZU T., HIRATA Y., HIRATA K., SUZUKI H., MIYAZAKI Y., KAGAWA T., KOYAMA Y., OHIRA T., TAKAYAMA N., KRENSKY A.M., KAWADA T., 2007 - Forest bathing enhances human natural killer activity and expression of anti-cancer proteins. - Int. J. Immunopathol. Pharmacol., 20(Suppl. 2): 3-8. MATSUNAGA K., PARK B.J., KOBAYASHI H., MIYAZAKI Y., 2011 - Physiologically relaxing effect of a hospital roof- top forest on elderly women requiring care. - J. Am. Geriatr. Soc., 59: 2162-2163. MINISTRY OF AGRICULTURE, FORESTRY AND FISHER- IES, 2008 - Report of the statistical survey on the distribu- tion of flowers in 2008. - Ministry of Internal Affairs and Communications Statistics Statistical Research and Training Institute, Tokyo, Japan. MIURA M., KAWADA F., 2008 - Development of a school stressor scale for high school students (SSS). - Jpn. J. Couns. Sci. (Japan), 41: 73-83. MURRAY C.J.L., LOPEZ A.D., 1996 - Evidence-based health policy-lessons from the Global Burden of Disease Study. - Science, 274: 740-743. OSGOOD C.E., SUCI G.J., TANNENBAUM P., 1957 - The measurement of meaning. - University of Illinois Press, Champaign, Urbana, Illinois, USA. PARK B.J., FURUYA K., KASETANI T., TAKAYAMA N., KAGAWA T., MIYAZAKI Y., 2011 - Relationship between psychological responses and physical environment in forest settings. - Landsc. Urban Plan, 102: 24-32. PARK B.J., TSUNETSUGU Y., KASETANI T., KAGAWA T., MIYAZAKI Y., 2010 - The physiological effects of Shinrin- yoku (taking in the forest atmosphere or forest bathing): evidence from field experiments in 24 forests across Japan. - Environ. Health Prev. Med., 15: 18-26. 116 PARK B.J., TSUNETSUGU Y., KASETANI T., MORIKAWA T., KAGAWA T., MIYAZAKI Y., 2009 - Physiological ef- fects of forest recreation in a young conifer forest in Hino- kage town, Japan. - Silva. Fenn., 43(2): 291-301. PARK B.J., TSUNETSUGU Y., LEE J., KAGAWA T., MI- YAZAKI Y., 2012 - Effect of the forest environment on physi- ological relaxation using the results of field tests at 35 sites throughout Japan, pp. 55-65. - In: LI Q (ed.) Forest medi- cine. Nova Science Publishers Press, New York. PARK S.H., MATTSON R.H., 2009 - Ornamental indoor plants in hospital rooms enhanced health outcomes of patients re- covering from surgery. - J. Altern. Complement. Med., 15: 975-980. SAWADA Y., OHTOMO N., TANAKA Y., TANAKA G., YA- MAKOSHI K., TERACHI S., SHIMAMOTO K., NAK- AGAWA M., SATOH S., KURODA S., IIMURA O., 1997 - New technique for time series analysis combining the maximum entropy method: its value in heart rate variability analysis. - Med. Biol. Eng. Comput., 35: 318-322. SONG C., JOUNG D., IKEI H., IGARASHI M., AGA M., PARK B.J., MIWA M., TAKAGAKI M., MIYAZAKI Y., 2013 - Physiological and psychological effects of walking on young males in urban parks in winter. - J. Physiol. An- thropol., 32: 18. STATISTICS BUREAU, MINISTRY OF INTERNAL AF- FAIRS AND COMMUNICATIONS, 2012 - 16–1. School- Based Education. - MINISTRY OF INTERNAL AFFAIRS AND COMMUNICATIONS STATISTICS STATISTICAL RESEARCH AND TRAINING INSTITUTE (ed.) Statisti- cal Handbook of Japan 2012. Japan Statistical Association, Tokyo, Japan. TAKADA H., OKINO K., 2004 - An evaluation method for heart rate variability by using acceleration plethysmogra- phy. - Health Eval. Promot., 3: 547-551. TAKADA M., EBARA T., SAKAI Y., 2008 - The acceleration plethysmography system as a new physiological technology for evaluating autonomic modulations. - Health Eval. Pro- mot., 35: 373-377. TAKAKURA M., SAKIHARA S., 2001 - Psychosocial corre- lates of depressive symptoms among Japanese high school students. - J. Adolesc Health., 28: 82-89. TSUNETSUGU Y., LEE J., PARK B.J., TYRVAINEN L., KAGAWA T., MIYAZAKI Y., 2013 - Physiological and psy- chological effects of viewing urban forest landscapes assessed by multiple measurements. - Landsc. Urban Plan, 113: 90-93. TSUNETSUGU Y., PARK B.J., MIYAZAKI Y., 2010 - Trends in research related to “Shinrin-yoku” (taking in the forest atmosphere or forest bathing). - Environ. Health Prev. Med., 15: 27-37. WEISE F., HEYDENREICH F., 1989 - Effects of modified respi- ratory rhythm on heart rate variability during active ortho- static load. Biomed. - Biochim. Acta, 48: 549-556.