How Do Horticultural Activities Affect Brain Activation and Emotion? Scientific Evidence Based on Functional Connectivity

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Pei-Hsuan Lai Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei, Taiwan

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Chia-Wei Li Department of Radiology, Wan Fang Hospital, Taipei Medical University, Taipei, Taiwan

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Shih-Han Hung Department of Landscape Architecture, Tunghai University, Taichung, Taiwan

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A-Young Lee Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei, Taiwan

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Chun-Yen Chang Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei, Taiwan

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Hsing-Feng Tang Department of Leisure Industry and Health Promotion, National Taipei University of Nursing and Health Sciences, Taipei, Taiwan

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Abstract

Research has confirmed that there are physical and mental benefits associated with performing horticultural activities, such as being in contact with soil and viewing plants. In addition, due to the rapidly increasing volume of affective neuroscience research, it is now possible to understand emotional processing in the brain through neuroimaging. The present study was conducted to explore subjects’ emotional responses after participating in horticultural activities, with functional magnetic resonance imaging (fMRI) and the Profile of Mood States used for physiological and psychological measurements, respectively. First, the subjects’ baseline brain activation levels were determined before any engagement in horticultural activities. A week later, the subjects participated in a 5-week horticultural activity. fMRI was used to detect physiological changes during the different stages of the activity—namely, preparation and sowing, fertilizing and weeding, and harvesting. The findings show that the functional connectivity of the brain regions was activated, including the emotional prosody network. Hence, this study provides evidence that gardening can stimulate functional connectivity, activation of positive emotions, and mindfulness in the brain. The findings provide a neuroscientific understanding of the types of horticultural activities that increase positive emotions, meditation, creativity, attention, and relaxation and reduce depression.

Overload and arousal are consistently experienced in modern life, which can lead to an increase in uncomfortable levels of psychological and physiological responses (Ulrich and Parsons 1992). In contrast, plant-based environments are less complex and reduce arousal and stress. This may be related to the long-term evolution of the human experience with nature (Balling and Falk 1982; Heerwagen and Orians 1995; Wilson 1984) and the deep connection that humans have to nature, feeling either biophilia (i.e., a love of life or life-like elements) or biophobia (i.e., a fear for nature) (Wilson 1984).

Horticultural activities use plants as a medium for contact with nature. Activities such as planting, caring for plants, and harvesting have been shown to generate positive emotions (Hayashi et al. 2008), relieve stress, increase social interactions, have environmental benefits (McFarland et al. 2018), and enhance overall life satisfaction (Waliczek et al. 2005) in terms of mental health and well-being (Waliczek et al. 1996) for people of different ages and genders. In terms of public health, many clinical studies have reported that horticultural activities can result in health benefits for a range of people, including physical, psychological, cognitive, social, and behavioral benefits (Park et al. 2016; Soga et al. 2017).

Lewis (1994) stated that the connection between horticultural therapy/activities and health was supported by theories related to natural experience, including attention restoration theory (ART) (Kaplan and Kaplan 1989) and stress recovery theory (SRT) (Ulrich et al. 1991). These theories formed the foundation of our research on the individual health benefits observed in people who engage in horticultural activities. According to ART (Kaplan and Kaplan 1989), the natural environment has restorative features that can help reestablish an individual’s direct attention, including feelings of being away, fascination, extent, and compatibility. Furthermore, Ulrich et al. (1991) proposed SRT, a psychoevolutionary theory that states that a healing garden reduces stress and restores health. In addition, Marcus and Barnes (1999) stated that a therapeutic place with natural distractions increases one’s sense of control in the horticultural activity taking place and also one’s sense of support from others. Evidence-based studies have provided empirical support for these theories, confirming that gardening activities reduce stress and foster attention restoration and positive emotions, including feelings of happiness and satisfaction (Cerwen et al. 2016; Chalmin-Pui et al. 2021; Oh et al. 2019).

It has been found that natural, green environments stimulate the parasympathetic system to reduce stress (Ewert and Chang 2018; Ulrich et al. 1991; van den Berg et al. 2015; Yao et al. 2021), while urban environments have no such effect. Park and Mattson (2009) found that an individual’s contact with plants has an impact on their physiological psychology; specifically, the psychological reactions associated with transplanting real flowering plants and handling artificial flowers differ. Furthermore, the participants in the experiment of Park et al. (2017) experienced a more relaxed state and had decreased blood oxygen concentrations in their frontal lobes upon exposure to potted plants. Due to the positive outcomes of horticultural activities, nursing homes (Rodiek 2002) and community gardens (Hayashi et al. 2008) offer horticultural activities to middle-aged and elderly residents, office workers, and the general public to reduce stress and boost positive emotions (Sahlin et al. 2014; van den Berg and Custers 2011). In addition, horticultural activities have been shown to benefit those with depression and anxiety disorders (Song et al. 2010; Vujcic et al. 2017). In terms of frequency and duration, short-term horticultural activities (i.e., those typically fewer than 10 sessions of 30–60 min each) tend to be the most popular, and these are suitable for all age groups (e.g., preschoolers, adolescents, adults, and the elderly) (Park et al. 2016).

Functional brain communication plays a crucial role in complex cognitive processes, as it facilitates the continuous integration of information from different brain regions (van den Heuvel and Hulshoff Pol 2010). Functional connectivity (FC) refers to the temporal dependency of neurophysiological events in different spaces (Friston et al. 1993) and is a concept that is used to study how neural activation of different brain regions is correlated. For example, Perrone-Bertolotti et al. (2016) examined the relationship between viewing pleasant and unpleasant images and emotion-related brain regions. The results showed that there was a greater involvement of the medial prefrontal cortex (mPFC) and right late positive complex when viewing pleasant images compared with when viewing unpleasant images (Perrone-Bertolotti et al. 2016).

The limbic system comprises the emotion-related brain regions and includes the cingulate gyrus, parahippocampal gyrus, hippocampus, amygdala, thalamus, hypothalamus, and mammillary bodies (Dalgleish 2004). Kim et al. (2010) found that the anterior cingulate cortex (ACC) is more highly activated when viewing natural landscapes (mountains, natural parks, forests, etc.) than when viewing urban landscapes. The amygdala is related to negative emotions, such as anxiety, fear, and unhappiness (Lane et al. 1997; Schwartz and Davidson 1997), and plays an essential role in detecting environmental threats (Scott et al. 1997). The hypothalamus has a wide range of complex functions that affect the human body’s response to the environment, turning sensations into emotions (Carter 2019). Vytal and Hamann (2010) reviewed emotion-related brain activation and found the following: happiness is related to the right superior temporal gyrus (R-STG) and left anterior cingulate cortex (L-ACC); sadness is correlated with the left middle frontal gyrus (L-MFG), left and right inferior frontal gyrus (L-IFG and R-IFG, respectively), and left and right caudate head; anger is related to the L-IGF and R-IFG and right parahippocampal gyrus (R-PHG); fear stems from the left and right amygdala, right cerebellum, and right insula; and disgust is related to the R-IFG.

Regarding the effect of the environment on the brain, Roth (2013) reported that the environment influences the human brain and sensory systems. Bratman et al. (2015a) tested the effects of nature experiences on brain region responses and found that subjects who walked around in a natural environment had reduced responses to subgenual prefrontal cortex (sgPFC) neural activity; in contrast, subjects who walked around in an urban environment did not experience neurological changes. Furthermore, sgPFC activity has been found to increase in response to sadness and negative self-reflection (Kross et al. 2009). Other studies have examined people’s states before and after participating in horticultural activities (Lai et al. 2021). The present study took a further step and focused on the different brain activities and emotions that arise during horticultural activities, considering the established inference that the human brain and sensory systems are stimulated by the environment.

Given that other studies have not explored the immediate neurological effects of different horticultural activities, a knowledge gap exists. Therefore, this study was designed to generate information about the connection between brain activity and horticultural activities and to examine the link between the impact of horticultural experiences and psychological responses. The present study explored the relationship between immediate functional connections and emotional activation after different horticultural activities, namely site preparation and sowing, fertilizing and weeding, and harvesting.

Materials and Methods

Participants.

The Social and Behavioral Research Ethics Committee of National Taiwan University approved this study (approval number 201807HM005). Online questionnaires were posted on social media platforms to recruit participants. The questionnaires were mainly posted on the sites of National Taiwan University student groups to reduce the impact of individual differences among participants. Applicants who had previously participated in horticultural activities, were from the department of horticulture, and did not meet the fMRI safety criteria were excluded. All recruited subjects were required to sign an informed consent form before participating in the study.

In addition to meeting the fMRI safety criteria and the needs of the research, participants were required to be 20 to 30 years old; be of good physical and mental health; have routine vision and hearing; exhibit right-handedness; have no previous history of brain damage, neurological diseases, or cardiovascular diseases; and to have no permanent metal implants (e.g., nails and artificial joints) or tattoos. The final sample consisted of 23 student subjects—12 male and 11 female—with an average age of 23 years.

Experimental site.

The Experimental Farm of the College of Bioresources and Agriculture, Horticulture Branch, at National Taiwan University was the experimental site for conducting the horticultural activities. The participants had their brain activity recorded at The Imaging Center for Integrated Body, Mind, and Culture Research’s 3T MRI Prisma Laboratory immediately after completing the horticultural activities. It was a 3-minute walk from the experimental site to the recording site (Fig. 1).

Fig. 1.
Fig. 1.

An aerial photo showing the location of the experimental farm where the horticultural activities were conducted and the location where the functional magnetic resonance imaging was performed.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

Functional magnetic resonance imaging.

Images were recorded using a Siemens Magnetom Prisma MRI with a magnetic field strength of 3 Tesla equipped with a head-sized coil and goggles display (VisuaStim XGA; Resonance Technology Inc., Northridge, CA, USA) that provided experimental visual stimulation. The fMRI structural acquisitions included a T1-weighted 3D Magnetization-Prepared Rapid Acquisition Gradient Echo (MPRAGE) Generalized Autocalibrating Partially Parallel Acquisition (GRAPPA) sequence acquired sagittally, with echo time (TE)/repetition time (TR) = 2.3/2000 ms, an 8° flip, a 256 × 256 acquisition matrix, a 240 × 240 mm2 field of view (FOV), 192 slices, and a 0.93-mm slice thickness, and T2 with TE/TR = 103/9530 ms, a 150° flip, a 288 × 384 acquisition matrix, a 192 × 192 mm2 FOV, 45 slices, and a 3-mm slice thickness. The functional scan settings included TE/TR = 30/3000 ms, a 90° flip, a 64 × 64 matrix, a 192 ×192 mm2 FOV, 45 slices, and a 3-mm slice thickness.

Profile of Mood States.

The study used a self-reported questionnaire to understand the participants’ psychological emotions during the different horticultural activities. The short version of the Chinese Profile of Mood States (POMS) questionnaire developed by Chang and Lu (2001) was used, which refers to the original literature (McNair et al. 1971). This instrument contains 37 questions that are classified into the following seven emotional states: vigor (7 items, e.g., full of vitality), esteem (4 items, e.g., dignity), confusion (7 items, e.g., unsure), fatigue (6 items, e.g., tired), anger (6 items, e.g., furious), tension (4 items, e.g., nervous), and depression (3 items, e.g., hopeless). Responses to each item were recorded using a Likert scale ranging from 0 (not at all) to 4 (totally agree). The total mood disturbance (TMD) was computed by calculating the total score for negative mood (tension, anger, fatigue, and depression) and then subtracting the total score for positive mood (vigor and esteem) and using a constant of 100 (Chang and Lu 2001). A lower TMD score indicates a more positive emotional state (Chang and Lu 2001). The reliability score was between 0.71 and 0.93, and the Cronbach α coefficient was 0.87, indicating good reliability and validity (Chang and Lu 2001).

Procedures for engaging in horticultural activities.

The study process is presented in Table 1 and Fig. 2A and B. fMRI and POMS pre-tests were performed in the first week, and experimental tests were subsequently performed 50 min after each horticultural activity in the second, fourth, and sixth weeks. During the fMRI, subjects were asked to stay awake in the resting state with their eyes open and to try to let thoughts pass through their minds without focusing on any particular mental activity. Each subject completed a 10-min scan in this resting state. Due to the limited availability of the fMRI equipment, the maximum number of participants for each stage of the horticultural activity was restricted to six. Therefore, four groups of students were recruited.

Fig. 2.
Fig. 2.

(A) A flow diagram of the experimental process with the details of the activities conducted in week 1 shown. (B) A flow diagram of the experimental process with the details of the activities conducted in week 2 is shown. fMRI = functional magnetic resonance imaging.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

Table 1.

The experimental details of the horticultural activities and the time taken for each activity.

Table 1.

There were two experimental periods: from 1 Oct 2018 to 6 Jan 2019, and 15 Apr to 26 May 2019. The average air temperature during the experimental periods ranged from 19.57 °C to 25.07 °C, and the amount of rainfall ranged from 1.45 mm to 7.98 mm. The experimental process lasted for 6 weeks, and included three stages of horticultural activities (site preparation and sowing, fertilizing and weeding, and harvesting) and brain scans (Table 1). The site for the horticultural activities was an experimental garden plot located in an urban area. The site preparation and sowing stage, which included weed removal, soil turning, leveling, planting, transplanting vegetable seedlings, and wetting the ground, took place at the garden plot. Lettuce (Lactuca sativa L.), arugula (Eruca sativa), and chicory (Cichorium intybus) were selected as the experimental plants due to their relatively short harvest times and the fact that they are easy to grow. Gardening tools, such as shovels, trowels, watering cans, and plastic cloth, were used for the horticultural activities (Table 1). All participants completed this stage between 1300 and 1700 HR, and they performed the activities alone for 30 to 50 min in each session. They were provided with an individual garden plot (3 m × 1.5 m). The participants received instructions from one researcher about the method and process before participating in each activity. In addition, there were restrictions placed on the use of electronic devices (e.g., mobile phones) during the activities so that the participants could focus entirely on their horticultural activities.

Data analysis.

SPM12 software was used to analyze the fMRI images and the Resting-State fMRI Data Analysis Toolkit (REST) running MATLAB (MathWorks, Natick, MA, USA). All of the raw experimental data were in the DICOM file format. The fMRI data were converted to the NIFTI format and preprocessed. This consisted of six steps: slice timing, realigning, detrending and filtering, normalizing, smoothing, and covariate extraction for further analysis. The following two steps were performed as part of the image statistical analysis:

  1. Individual analysis (first level): After preprocessing, analysis was performed at the individual seed-based level.

    1. Seed time course extraction: the coordinates of the regions of interest (ROIs) were used, and the time course of the ROIs was extracted for use in subsequent calculations.

    2. FC: The General Linear Model (GLM) and a t-test were used to calculate the connectivity of the brain regions. Fisher’s Z-value transformation with the r-maps was normalized to Z-maps, and all Fisher’s Z-maps were inputted into a two-sided one-sample t-test to detect regions with FC to the ROI.

  2. Group analysis (second level): A full factorial design was used to perform statistical calculations to determine the degree of activation between voxels in each stage of the horticultural activities.

This study aimed to understand the differences in the FC between brain regions among participants of a horticultural activity; data were gathered during the resting state. A t-test was used to analyze the contrast between the following activity stages: site preparation and sowing (SS) > nonparticipating (NP): [NP:SS] = [−1:1]; fertilizing and weeding (FW) > NP: [NP:FW] = [−1:1]; and harvesting (H) > NP: [NP:H] = [−1:1]. In accordance with previous research (Touroutoglou et al. 2015; Vytal and Hamann 2010), five emotion categories (anger, sadness, fear, disgust, and happiness) were selected and related to five ROIs for further analysis as follows: R-STG Montreal Neurological Institute and Hospital (MNI) coordinates [x, y, z] = 48, −55, −4; L-ACC MNI coordinates [x, y, z] = −2, 43, 7; L-IFG MNI coordinates [x, y, z] = −45, 23, −3; left amygdala MNI coordinates [x, y, z] = −23, −6, −11; and right amygdala MNI coordinates [x, y, z] = 23, −10, −14. In addition, the beta value was used to verify the degree of FC in the brain regions. The GLM formula was as follows: y = beta value * seed-fluctuation + constant.

To determine the effect of the horticultural activities on the psychological-emotional responses, we analyzed the participants’ POMS data using the IBM Social Science Statistics Package 20.0. A one-way repeated analysis of variance was used to analyze the subjects’ emotional states after each of the stages of the horticultural activities.

Results

Head motion analysis.

A head motion analysis was performed, which involved four fMRI tests with movement <1.8 mm and rotation < ±1°. This analysis revealed that each test subject met the standard, resulting in 23 valid samples.

Effects of the different horticultural activities on the functional connections between the R-STG and the ROIs.

First, the results that were obtained when the ROI was set to the R-STG MNI coordinates [x, y, z] = 48, −55, −4 are presented. Values were considered statistically significant at an uncorrected P < 0.001 with a minimum cluster size of 50 voxels and an extent threshold of P < 0.05. In the subjects who participated in site preparation and sowing, the right middle frontal gyrus (R-MFG) and the R-IFG were the brain regions found to be connected to the R-STG. However, these brain regions were not significantly connected to the R-STG in the fertilizing and weeding activity participants. In the subjects who participated in harvesting, the left medial superior frontal cortex (L-mSFC), right posterior cingulate cortex (R-PCC), and right and left precuneus were the brain regions associated with the R-STG. The results are shown in Table 2.

Table 2.

Different stages of the horticultural activity and differences in the right superior temporal gyrus (R-STG) functional connectivity.

Table 2.

The ROI was set to the L-ACC MNI coordinates [x, y, z] = 48, −55, −4 to further analyze the effects of the horticultural activities on brain connections. Values were considered statistically significant at an uncorrected P < 0.001 with a minimum cluster size of 50 voxels and an extent threshold of P < 0.05. Table 3 shows the results. In the subjects who participated in site preparation and sowing, the L-ACC was related to the right anterior cingulate cortex (R-ACC), right thalamus, left posterior cingulate cortex (L-PCC), L-MFG, and R-MFG. In the subjects who participated in the fertilizing and weeding stage, the left and right insula, left superior temporal gyrus (L-STG), R-STG, left cuneus, and left cingulate gyrus were the brain regions connected with the L-ACC. In subjects who participated in the harvesting, the brain regions connected with the L-ACC were the L-STG, R-STG, left cuneus, left parahippocampal gyrus, L-MFG, R-MFG, right thalamus, and right insula.

Table 3.

Different stages of the horticultural activity and differences in the left anterior cingulate cortex (L-ACC) functional connectivity.

Table 3.

The ROI was then set to the L-IFG MNI coordinates [x, y, z] = 48, −55, −4. Values were considered statistically significant at an uncorrected P < 0.001 with a minimum cluster size of 50 voxels and an extent threshold of P < 0.05. The results are shown in Table 4. In those who participated in site preparation and sowing, the brain regions connected with the L-IFG were the left middle occipital gyrus (L-MOG), right fusiform gyrus, R-PCC, R-STG, and left precuneus. In the subjects who participated in fertilizing and weeding, no brain regions were significantly connected to the L-IFG. In those who participated in harvesting, the left parahippocampal gyrus, L-STG, R-STG, L-PCC, R-PCC, left and right middle cingulate cortex (L-MCC and R-MCC, respectively), left insula, right cuneus, and L-MOG were the brain regions associated with the L-IFG.

Table 4.

Different stages of the horticultural activity and differences in the left inferior frontal gyrus (L-IFG) functional connectivity.

Table 4.

There were no significant differences observed in the left and right amygdala MNI coordinates ([x, y, z] = −23, −6, −11 and [x, y, z] = 23, −10, −14, respectively) after the different activity stages. Table 5 provides a summary of the results.

Table 5.

Summary of functional connectivity activation in different brain regions after different horticultural activities.

Table 5.

FC trends of brain regions during the different stages.

The baseline beta values in those who did not participate in the horticultural activities were significantly different from the values in those who exhibited FC in more than two stages. First, the FC between the L-ACC and the R-STG and L-STG increased with each stage of horticultural activity; the FC associated with the fertilizing and weeding and harvesting stages was significantly different from NP (Figs. 3 and 4). The underlying mechanism remains undetermined, although FC increased. Generally, the participants reported high levels of satisfaction due to the sense of accomplishment they acquired during harvesting (Han et al. 2018), which may be related to the high levels of FC observed during this stage. The findings suggest that the FC between the L-ACC and the R-STG and L-STG was related to participation in horticultural activities.

Fig. 3.
Fig. 3.

The functional connectivity of the left anterior cingulate cortex (L-ACC) and the right superior temporal gyrus (R-STG) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

Fig. 4.
Fig. 4.

The functional connectivity of the left anterior cingulate cortex (L-ACC) and the left superior temporal gyrus (L-STG) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

Second, as the fertilizing and weeding and harvesting stages induced significant differences compared with the baseline (nonparticipation in horticultural activities), the FC of the L-ACC and R-insula also increased with horticultural activity participation (Fig. 5). The upon-brain activations were found to be similar to the brain region responses to mindfulness meditation (Kamitsis and Simmonds 2017) and were related to the emotional processing brain network. Therefore, the possibility of FC between the L-ACC and the R-insula is related to the extent of participation in horticultural activities.

Fig. 5.
Fig. 5.

The functional connectivity of the left anterior cingulate cortex (L-ACC) and the right insula after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

Third, the FC between the L-IFG and R-STG was significantly different after the site preparation and sowing and harvesting stages (Fig. 6). Although research has demonstrated that this FC is related to the emotional prosody network (Bernard et al. 2018), no studies have investigated the FC during the horticultural activities of site preparation, sowing, and harvesting. The present study’s results indicate that there was low FC between the L-IFG and the R-STG in those who did not participate in the horticultural activities. It can, therefore, be surmised that the connectivity observed between the L-IFG and the R-STG was related to participation in horticultural activities.

Fig. 6.
Fig. 6.

The functional connectivity of the left inferior frontal gyrus (L-IFG) and the right superior temporal gyrus (R-STG) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

In addition, the FC between the L-IFG and R-PCC was found to be significantly different after the site preparation and sowing and harvesting stages (Fig. 7), and the highest connectivity was associated with the site preparation and sowing stage. This phenomenon relates to divergent creative thinking: the site preparation, sowing, and harvesting activities increased the FC of the brain regions responsible for innovative ideas.

Fig. 7.
Fig. 7.

The functional connectivity of the left inferior frontal gyrus (L-IFG) and the right posterior cingulate cortex (R-PCC) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

The effects of horticultural activities on psychological emotions.

When the POMS instrument is used, the higher the score, the more negative the subject’s emotional state. In this study, a least significant difference post hoc comparison showed that the scores of the nonparticipating subjects (M = 119.30, SD = 21.6, Table 6) were significantly higher than those of the subjects who participated in site preparation and sowing (M = 103.07, SD = 18.18) (P < 0.001), fertilizing and weeding (M = 96.30, SD = 19.30) (P < 0.001), and harvesting (M = 95, SD = 23.72) (P < 0.001). Moreover, the scores of those who participated in site preparation and sowing were significantly higher than the scores of those who participated in fertilizing and weeding (P = 0.008) and in harvesting (P = 0.002), meaning that participants experienced more positive emotions during the fertilizing and weeding and harvesting stages than the site preparation and sowing stage.

Table 6.

Differences in emotional state at different stages of the horticultural activity.

Table 6.

Discussion

This study focused on the differences in the functional connections of selected brain regions after each stage of a horticultural activity. It related the active brain regions to different ROI functional connections during various activities.

Site preparation and sowing and FC.

A significant connection between the R-STG and R-IFG was found in those who participated in site preparation and sowing compared with nonparticipants (Fig. 8, Table 7). The functional relationships between the R-STG and the R-IFG and L-IFG are related to emotional processing (Frühholz et al. 2011), and active connections between the R-STG and the IFG are involved in emotional prosody and the dorsal pathway (Bernard et al. 2018). Emotional prosody is an emotional processing network that involves sounds, such as those produced during voice-based communication, that convey information about the emotional state of the speaker (Bernard et al. 2018). However, the exact mechanism and relationship between the brain regions in the emotional prosody network after horticultural site preparation and sowing remain unclear.

Fig. 8.
Fig. 8.

Site preparation and sowing > nonparticipating connected brain regions. L-IFG = left inferior frontal gyrus; R-PCC = right posterior cingulate cortex; R-STG = right superior temporal gyrus; L-ACC = left anterior cingulate cortex; R-IFG = right inferior frontal gyrus; R-ACC = right anterior cingulate cortex.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

Table 7.

The connected brain regions and their functions in response to each horticultural activity.

Table 7.

The L-ACC and R-ACC were also found to have significant FC (Fig. 8, Table 6). The ACC is related to emotional regulation and emotional perception in cognitive processes (Bush et al. 2000). The results of the present study are specific to the emotion-processing region of the brain. Kamitsis and Simmonds (2017) conducted a study on the effects of mindfulness meditation and reported increased ACC activation and improved emotional regulation and self-control among the participants. Specifically, the researchers used horticultural activities to facilitate a nature-guided mindfulness meditation activity, allowing the participants to focus on experiencing nature and thus reduce stress and anxiety. In the present study, during the site preparation and sowing stage, the participants focused on repeatedly turning and leveling the soil, which made it easy for them to enter a state of focused awareness. Therefore, it is speculated that site preparation and sowing induce outcomes similar to those of mindfulness meditation. However, some have argued that the ACC is related to nonpositive emotions. For example, Carter (2019) demonstrated that sad emotions can cause ACC activation. There are reports, however, of horticultural activities causing sadness.

There was significant FC between the L-IFG and R-PCC during the site preparation and sowing stage (Fig. 8, Table 7). Consistent with the findings of previous studies, the present study’s findings demonstrate that contact with the natural environment enhances creativity among the general public (see Atchley et al. 2012). Furthermore, Plambech and van den Bosch (2015) found significant FC between the L-IFG and R-STG (Fig. 8, Table 7) and that multisensory stimuli in the natural environment (e.g., visual stimuli, birdsong, water sounds, smells in the air) can foster creativity. The results of the present study indicate that the novelty of experiencing horticultural activities elicits creativity, which is related to the FC of the R-STG and R-IFG, and belongs to the emotional processing and prosody networks.

Fertilizing and weeding and FC.

The L-ACC and L-STG and R-STG exhibited significant FC in this study (Fig. 9, Table 7). Harada et al. (2018) reported stronger functional connections between the ACC and STG in people with less depression. Therefore, it is reasonable to conclude that in our study, the fertilizing and weeding activities influenced the level of depression and emotional stability of the participants. A previous study also reported that participation in horticultural activities, such as weeding and fruit harvesting, enables natural environment recovery and thus reduces depression and anxiety symptoms (Vujcic et al. 2017).

Fig. 9.
Fig. 9.

Fertilizing and weeding > nonparticipating connected brain regions. L-ACC = left anterior cingulate cortex; L, R-STG = left, right superior temporal gyrus.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

The FC activities of the L-ACC and the L-insula and R-insula in subjects who participated in fertilizing and weeding were significantly different from those in nonparticipants (Fig. 9, Table 7). Given that the fertilizing and weeding stage involved caring for germinated seedlings, the participants may have developed an emotional connection with the plants they cared for, which has been shown to yield psychological benefits (Lewis 1994). Also, Lewis (1994) stated that participation in planting activities increases positive emotions. In addition, engaging activities in the natural environment improves positive emotions and attention (Barton and Pretty, 2010; Bratman et al. 2019). An active connection between the ACC and insula affects perceptual information and emotion in the body (Taylor et al. 2009).

Harvesting and FC.

Consistent with previous studies, this study demonstrated that contact with the natural environment can enhance creativity among professionals (Plambech and van den Bosch 2015) and the general public (Atchley et al. 2012). The L-IFG and R-STG were found to have significant FC in this study (Fig. 10, Table 6); this is similar to the FC of the R-IFG and R-STG, which is associated with emotional processing and emotional prosody. In addition, the L-IFG and L-insula were found to have significant FC (Fig. 10, Table 7). Notably, the connectivity between the IFG and the insula is part of the mirror neuron system (Uddin et al. 2007), which enables individuals to respond to specific actions in a relative way and is also related to self–other discriminations (Zhao et al. 2013).

Fig. 10.
Fig. 10.

Harvest > nonparticipating connected brain regions. L-ACC = left anterior cingulate cortex; L, R-STG = left, right superior temporal gyrus; L-IFG = left inferior frontal gyrus; L, R-PCC = left, right posterior cingulate cortex.

Citation: HortScience 58, 1; 10.21273/HORTSCI16788-22

Psychological-emotional state and horticultural activities.

The questionnaire results indicated that, relative to the nonparticipation baseline, participation in all of the horticultural activities led to positive emotions. These findings are consistent with the literature on the emotional benefits of horticultural activity (Bratman et al. 2015b; Chalmin-Pui et al. 2021; Ikei et al. 2014; Lowry et al. 2007; Oh et al. 2019). The fertilizing and weeding and harvesting stages induced more positive emotions than the site preparation and sowing stage, which is an important finding, as studies have rarely compared different types of horticultural activities and their benefits. We concluded that this result was due to differences in the intensity of the different horticultural activities. For example, Lee et al. (2021) reported that, compared with other horticultural tasks, activities associated with preparing garden plots (e.g., digging and raking) resulted in high levels of negative emotions, such as fatigue and anxiety, as measured using the POMS. During the fertilizing and weeding stage, most participants took photos to record the growth of the plants. This successful nurturing of the plants (i.e., the germination and growth) resulted in positive emotions among the participants, such as a sense of accomplishment. This result regarding the psychological benefits of horticultural activity is consistent with the reports of Lewis (1994) and Han et al. (2018).

Limitations and future research.

This study explored the benefits of horticultural activities for young, healthy individuals only; hence, the sample population was different from those used in other studies. Each subject fully participated in each of the different stages, which involved different types of activities, so the benefits associated with each subsequent stage might have been affected by the previous stage. Therefore, the results may represent a cumulative effect of different horticultural activities on brain connectivity and emotion.

Another limitation that must be taken into account is that horticultural activities are numerous and diverse. This study focused on outdoor planting and used easy-to-care-for crops with a high survival rate, namely Eruca sativa, Cichorium intybus, and Lactuca sativa L. The different growth requirements and cultivation times of horticultural crops could affect the practice and participation time. Subsequent research could involve longer growth periods and/or seasonal change crops to test the effect of horticultural activities on emotional experience and the FC of brain regions. Moreover, the experimental aspects of the study were conducted from October to January and April to May during afternoons and at similar temperatures. During the experimental period, the weather was not the main factor that affected our results. In contrast, future research would need to consider the seasonal changes that might affect the experimental results. Our study used a combined quantitative and qualitative approach to provide a scientific report on the horticultural benefits and brain activation. The qualitative data with descriptions of participants’ emotional experiences and horticultural activities might support the findings from the quantitative results. In future studies, it is necessary to continue to use mixed research methods with neurosciences (e.g., fMRI) and psychological responses associated with each type of horticultural activity in various age groups and client groups to widen the applicability of the research. In addition, further research should also include broad qualitative methods to verify the results we found; for example, interviews and case studies can be used to elucidate the factors responsible for the relationships between different horticultural activities and functional brain connections.

Conclusions

This research involved an initial exploration of the effects of on-site horticultural activities on the FC of selected brain areas. The physiological benefits of undertaking horticultural activities can be quantified using neuroscience, and the psychological benefits can be verified. Notably, the self-reported data obtained in this study confirmed the participants’ positive emotional states upon participating in the horticultural activities.

Concerning the study’s practical implications, it is first necessary to note that horticultural activity is gradually being valued as an alternative therapy due to the associated brain activations and physical and psychological benefits (Son et al. 2016). Our findings show that the site preparation and sowing stage involved brain regions related to mindfulness meditation, emotional regulation, self-control, and creative thinking. Participating in this stage produced more positive emotions and significant functional connections in the creative brain area than not participating. Like mindfulness meditation, the fertilizing and weeding stage involved brain regions associated with emotional processing and actions. After participating in this stage, the participants seemed to exhibit more positive emotions than after participating in the site preparation and sowing stage. Finally, participation in the harvesting stage mainly resulted in emotional processing and creative thinking and actions similar to mindfulness meditation. In other words, all stages of the horticultural activity positively influenced mood compared with not being involved in the horticultural activity.

When a crop has a high survival rate, participants can experience and enjoy the various phases of the growth process. In fact, the harvesting stage might elicit more positive experiences and health benefits than other stages. Our findings not only prove that gardening activities have health benefits, but also provide support for implementing horticultural activities into teaching systems and long-term care centers. This would allow children, students, the elderly, and others to get in touch with nature and to experience the joy of the entire planting process, which could support healing and improve physical and mental health.

Furthermore, the scientific and objective indicators derived from this study can serve as reference data for experts and practitioners designing horticultural activities and therapies. Based on the findings of this study, it can be concluded that different horticultural activities stimulate different functional connections between brain areas. For example, our results show that brain areas related to creativity (the L-ACC and R-insula) are activated in dynamic activities, such as making garden plots and sowing seeds, and that brain areas related to psychophysiological stability (the L-IFG and R-STG) are activated in static activities, such as fertilizing, weeding, and harvesting. Practitioners and experts can use such information to focus the attention of participants with particular needs on specific types of horticultural activities.

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  • Fig. 1.

    An aerial photo showing the location of the experimental farm where the horticultural activities were conducted and the location where the functional magnetic resonance imaging was performed.

  • Fig. 2.

    (A) A flow diagram of the experimental process with the details of the activities conducted in week 1 shown. (B) A flow diagram of the experimental process with the details of the activities conducted in week 2 is shown. fMRI = functional magnetic resonance imaging.

  • Fig. 3.

    The functional connectivity of the left anterior cingulate cortex (L-ACC) and the right superior temporal gyrus (R-STG) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 4.

    The functional connectivity of the left anterior cingulate cortex (L-ACC) and the left superior temporal gyrus (L-STG) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 5.

    The functional connectivity of the left anterior cingulate cortex (L-ACC) and the right insula after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 6.

    The functional connectivity of the left inferior frontal gyrus (L-IFG) and the right superior temporal gyrus (R-STG) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 7.

    The functional connectivity of the left inferior frontal gyrus (L-IFG) and the right posterior cingulate cortex (R-PCC) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 8.

    Site preparation and sowing > nonparticipating connected brain regions. L-IFG = left inferior frontal gyrus; R-PCC = right posterior cingulate cortex; R-STG = right superior temporal gyrus; L-ACC = left anterior cingulate cortex; R-IFG = right inferior frontal gyrus; R-ACC = right anterior cingulate cortex.

  • Fig. 9.

    Fertilizing and weeding > nonparticipating connected brain regions. L-ACC = left anterior cingulate cortex; L, R-STG = left, right superior temporal gyrus.

  • Fig. 10.

    Harvest > nonparticipating connected brain regions. L-ACC = left anterior cingulate cortex; L, R-STG = left, right superior temporal gyrus; L-IFG = left inferior frontal gyrus; L, R-PCC = left, right posterior cingulate cortex.

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    • Search Google Scholar
    • Export Citation
  • Balling, J.D. & Falk, J.H. 1982 Development of visual preference for natural environments Environ. Behav. 14 5 28 https://doi.org/10.1177/0013916582141001

    • Search Google Scholar
    • Export Citation
  • Barton, J. & Pretty, J. 2010 What is the best dose of nature and green exercise for improving mental health? A multi-study analysis Environ. Sci. Technol. 44 3947 3955 https://doi.org/10.1021/es903183r

    • Search Google Scholar
    • Export Citation
  • Bernard, F., Lemée, J.M., Ter Minassian, A. & Menei, P. 2018 Right hemisphere cognitive functions: From clinical and anatomic bases to brain mapping during awake craniotomy part I: Clinical and functional anatomy World Neurosurg. 118 348 359 https://doi.org/10.1016/j.wneu.2018.05.024

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Pei-Hsuan Lai Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei, Taiwan

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Chia-Wei Li Department of Radiology, Wan Fang Hospital, Taipei Medical University, Taipei, Taiwan

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Shih-Han Hung Department of Landscape Architecture, Tunghai University, Taichung, Taiwan

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A-Young Lee Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei, Taiwan

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Chun-Yen Chang Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei, Taiwan

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Hsing-Feng Tang Department of Leisure Industry and Health Promotion, National Taipei University of Nursing and Health Sciences, Taipei, Taiwan

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Contributor Notes

This article is based on Pei-Hsuan Lai’s (2020) unpublished master’s thesis titled “Effects of Horticultural Activities on Emotion and Brain Functional Connectivity.” The corresponding authors of this study received funding support from the Ministry of Science and Technology (Grant Number: MOST106-2410-H-002-173-MY3, https://www.most.gov.tw/). The funder played no role in the study design, data collection, analysis, decision to publish, or preparation of the manuscript.

C.Y.C. and H.F.T. are the corresponding authors. E-mail: cycmail@ntu.edu.tw or hsingfen@ntunhs.edu.tw.

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  • Fig. 1.

    An aerial photo showing the location of the experimental farm where the horticultural activities were conducted and the location where the functional magnetic resonance imaging was performed.

  • Fig. 2.

    (A) A flow diagram of the experimental process with the details of the activities conducted in week 1 shown. (B) A flow diagram of the experimental process with the details of the activities conducted in week 2 is shown. fMRI = functional magnetic resonance imaging.

  • Fig. 3.

    The functional connectivity of the left anterior cingulate cortex (L-ACC) and the right superior temporal gyrus (R-STG) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 4.

    The functional connectivity of the left anterior cingulate cortex (L-ACC) and the left superior temporal gyrus (L-STG) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 5.

    The functional connectivity of the left anterior cingulate cortex (L-ACC) and the right insula after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 6.

    The functional connectivity of the left inferior frontal gyrus (L-IFG) and the right superior temporal gyrus (R-STG) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 7.

    The functional connectivity of the left inferior frontal gyrus (L-IFG) and the right posterior cingulate cortex (R-PCC) after each stage of horticultural activity. NP = nonparticipating, SS = site preparation and sowing, FW = fertilizing and weeding, H = harvest. * Significant at P < 0.05 using one-way repeated analysis.

  • Fig. 8.

    Site preparation and sowing > nonparticipating connected brain regions. L-IFG = left inferior frontal gyrus; R-PCC = right posterior cingulate cortex; R-STG = right superior temporal gyrus; L-ACC = left anterior cingulate cortex; R-IFG = right inferior frontal gyrus; R-ACC = right anterior cingulate cortex.

  • Fig. 9.

    Fertilizing and weeding > nonparticipating connected brain regions. L-ACC = left anterior cingulate cortex; L, R-STG = left, right superior temporal gyrus.

  • Fig. 10.

    Harvest > nonparticipating connected brain regions. L-ACC = left anterior cingulate cortex; L, R-STG = left, right superior temporal gyrus; L-IFG = left inferior frontal gyrus; L, R-PCC = left, right posterior cingulate cortex.

 

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