Research reportActivation of the serotonergic system by pedaling exercise changes anterior cingulate cortex activity and improves negative emotion
Introduction
Pedaling exercise (PE) of moderate intensity has been shown to ease anxiety and discomfort; however, the relationship of the changes that occur in brain activities and in the serotonergic (5-HT) system after PE remain unclear. It is well known that exercise is connected to changes in brain activity and psychological function. Acute exercise affects frontal asymmetry of the alpha wave in electroencephalography (EEG) [1], [2]. A model suggested by Davidson takes into account a possible function of the frontal asymmetry [3], [4], [5]. In particular, this model postulates that frontal asymmetrical activation, i.e., the relative imbalance of EEG activity in the alpha frequency band, influences an affective response and motivational biases of individuals. Namely, relative left frontal activation should reflect positive emotional states and relative right frontal activation should reflect negative emotional states. Furthermore, there is a report that subjective affect evaluation of the subjects who were trained to be in a condition of frontal asymmetry changed with repeated identical affect stimulation (with a photograph) as a result of training using biofeedback in frontal EEG [6]. It is suggested that frontal asymmetry possibly causes the emotional reaction. Although many studies have examined the effects of exercise on EEG frontal asymmetry, the mechanisms underlying the changes in EEG frontal asymmetry and psychological functions have yet to be elucidated.
Fumoto et al. [7] conducted a study in order to examine the changes in neurotransmitters and EEG in response to changes induced by PE. The results revealed an increase in the high-frequency alpha band (10–13 Hz), an increase in blood 5-HT levels, and improvements in negative mood after PE. They suggested that the activation of 5-HT system influenced the cortical EEG activity and that these changes might improve the affect. Nonetheless, the study employed 2-electrode EEG as the only method of measurement and therefore, it did not examine the association with frontal asymmetry (which has been examined in the previous study) and did not identify the EEG development source. Therefore, the purpose of the present study was to examine the relationship of changes in the psychological function with physical exercise, the frontal asymmetry (that has been described in past studies), and the activity of the 5-HT system.
Unlike animal experiments, analyzing cerebrospinal fluid in humans to assess the activity of 5-HT in nervous system is difficult; however, blood and urinary 5-HT concentration can be measured. For a long time, it was thought that 5-HT, a cranial nerve transmitter, and many proteins did not pass through the blood–brain barrier. However, in the last ten years, it has been shown that transportation systems pump out excessive protein and 5-HT across blood–brain barrier into the blood [8], [9]. Also, Audhya et al. [10] reported that urinary 5-HT concentration has an association with the 5-HT level in cerebrospinal fluid. Therefore, we estimated the activity of 5-HT neurons by measuring urine 5-HT levels because this technique is easier to use and more convenient than other assays used to measure brain 5-HT activity.
Section snippets
Subjects
Sixteen subjects volunteered for this study. Oral and written informed consents were obtained from all subjects. They were randomly divided into the following two groups: the PE group with a mean ± standard deviation (SD) age of 23.5 ± 1.9 years (four men and four women) and the control group with a mean ± standard deviation age of 23.1 ± 1.9 years (four men and four women). All procedures were conducted in accordance with the ethical standards of the Committee at Kio University and the Helsinki
Mood assessment
Pretest comparison of the two groups did not show any significant difference in any items of POMS (tension–anxiety: z = −1.19, p > 0.05; depression: z = −0.95, p > 0.05; anger–hostility: z = −0.11, p > 0.05; vigor: z = −1.10, p > 0.05; fatigue: z = −1.63, p > 0.05; and confusion: z = −1.83, p > 0.05).
We found a significant decrease in tension–anxiety (z = 2.37, p < 0.05) and a significant increase in vigor (z = 2.11, p < 0.05) after PE in the exercise group. For the other low-rank standards, significant differences were not
EEG frontal asymmetry
After PE, we observed a significant increase in the asymmetry score compared with that before PE. This increase reflects an increase in the relative right alpha-1 activity after PE compared with that before PE. The increased activity in the relative right frontal alpha-1 indicates a decrease of the relative left frontal activity because the frontal EEG activation of the alpha band is reportedly inversely proportional to the activation of the brain. We believe that these results indicate an
Limitation
In this study, only transient changes of subjective affect and EEG were found, and the changes over longer periods were not analyzed. In the future, we need to examine these factors along with temporal as well as the transient changes. Furthermore, the assessors knew who was in the exercise and in the control group. Therefore, it was necessary to consider the effects of the observer bias. We will blind assessors in future experiments.
EEG has low spatial resolution due to potential dampening by
Acknowledgements
We would like to thank the students of Kio University and the physical therapist and occupational therapists of Murata Hospital for their participation in this study.
In addition, we would like to thank Susumu Sakata (professor, graduate school of health science, Kio University) and Yasue Nishii (assistant, a physical therapy subject, department of health science, Kio University) for guidance with ELISA measurements.
We would also like to thank Enago (www.enago.jp) for the English language review.
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