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Background: Fatigue is a common symptom in both sick and healthy people. We examined autonomic nervous alterations associated with fatigue to clarify the mechanisms underlying fatigue. Methods: The study group consisted of 19 healthy participants who performed a 2-back test for 30 min as a fatigue-inducing mental task session. Before and after the session, they completed the advanced trail making test (ATMT) for 30 min for mental fatigue evaluation, subjective scales to measure fatigue sensation, and underwent electrocardiography to allow assessment of autonomic nerve activities. Results: After the fatigue-inducing task, the total error counts on the ATMT tended to increase (P = 0.076); the ATMT for total trial counts (P = 0.001), the subjective level of fatigue (P < 0.001), and the % low-frequency power (%LF) (P = 0.035) increased significantly; and the % high-frequency power (%HF) decreased compared with before the fatigue-inducing task although this did not reach the statistical significance (P = 0.170). Although LF measured in absolute units did not change significantly before and after the fatigue-inducing task (P = 0.771), and HF measured in absolute units decreased after the task (P = 0.020). The %LF and LF/HF ratio were positively associated with the daily level of fatigue evaluated using Chalder’s fatigue scale. In addition, %HF was negatively associated with the fatigue score. Conclusions: Increased sympathetic activity and decreased parasympathetic activity may be characteristic features of both acute and daily levels of fatigue. Our findings provide new perspectives on the mechanisms underlying fatigue. Keywords: Advanced trail making test, 2-back Test, Parasympathetic nerve function, Selective attention, Sympa- thetic nerve function Background fatigue are not effective . Therefore, it is important to Many people experience fatigue after or during a pro- clarify the mechanisms underlying fatigue, and in parti- longed period of activity . Large community surveys cular, long-term fatigue. have reported that up to half of the general adult popu- Fatigue-related alterations of autonomic nerve activ- lation complains of fatigue [2,3]. In Japan, more than ities have been reported in patients with chronic fatigue half of the general adult population complains of fatigue, syndrome (CFS) [6-11], multiple sclerosis [12-14], and and more than one third of the population suffers from primary biliary cirrhosis [9,15]. These reports suggest that changes in autonomic nerve activity are related to chronic fatigue . Acute fatigue is a normal phenom- enon that disappears after a period of rest; in contrast, the mechanisms underlying fatigue. However, this rela- chronic fatigue is sometimes irreversible and the com- tionship has been demonstrated only in patients with pensation mechanisms that are useful in reducing acute specific diseases and not in healthy subjects. Recently, we demonstrated that decreased parasympa- thetic activity and increased sympathetic activity were * Correspondence: email@example.com 1 induced in healthy volunteers following a 30-min fati- Department of Physiology, Osaka City University Graduate School of Medicine, 1-4-3 Asahimachi, Abeno-ku, Osaka 545-8585, Japan gue-inducing mental task session . As chronic or Full list of author information is available at the end of the article © 2011 Tanaka et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Tanaka et al. Behavioral and Brain Functions 2011, 7:46 Page 2 of 6 http://www.behavioralandbrainfunctions.com/content/7/1/46 daily levels of fatigue can be evaluated using a paper- participants . The reliability and validity of the Japa- and-pencil questionnaire , the relationships between nese version of Chalder’s fatigue scale to evaluate the daily levels of fatigue and alterations of autonomic nerve severity of daily fatigue have been previously confirmed activities may be identified. In addition, we can evaluate .The fatiguescaleconsistsof11questions usinga acute and daily levels of fatigue simultaneously in the 4-point (0-3) Likert scale that allows the following same participants by using previously performed fatigue- responses: 0 = less than usual; 1 = no more than usual; inducing and fatigue-evaluating experiments . The 2 = more than usual; 3 = much more than usual during aim of the present study was to determine alterations in the past several weeks. The total score for the 11-item autonomic nerve activities associated with daily levels of fatigue scale ranges from 0 to 33, with higher scores fatigue as well as acute fatigue. indicating a greater degree of daily fatigue. Methods Fatigue-inducing mental task Participants As a fatigue-inducing mental task, participants per- Nineteen healthy volunteers (mean age, 43.6 ± 10.1 formed the 2-back test for 30 min . During this task, years; 15 women and 4 men) were enrolled. None of the oneof fourletters waspresented on adisplay of aper- participants had a history of medical illness. Participants sonal computer every 3 sec, and they had to judge with a history of health problems, taking chronic medi- whether the target letter presented at the center of the cation or supplemental vitamins, and those who weighed screen was the same as the one that had appeared 2 < 40 kg [18-22] were excluded. Good health was presentations before. If it was, they were to press the assessed by physical examination, blood pressure, and right mouse button with their right middle finger; if it heart rate. The protocol was approved by the Ethics wasnot,theyweretopress theleftmousebuttonwith Committee of Osaka City University, and all participants their right index finger. They were instructed to perform provided written informed consent. the task trials as quickly and as correctly as possible. The results of each 2-back trial, that is, a correct Experimental design response or error, were continuously presented on the The day before the experiment, participants finished display of the personal computer. dinner by 9:00 pm and then fasted overnight. The fol- lowing morning, they had breakfast before the visit. At Fatigue-evaluating mental task 10:00 a.m., after the visit, they started the experiment. As a fatigue-evaluating mental task, participants per- Before the start of the experiment, a paper-and-pencil formed the ATMT for 30 min . In this test, circles questionnaire was distributed to participants to evaluate numbered from 1 to 25 were randomly placed on the their daily level of fatigue. As a fatigue-inducing mental display of a personal computer, and participants were task session, participants performed 2-back test  required to use a computer mouse to touch these circles trials for 30 min , and as a fatigue-evaluating mental in sequence, starting with number 1. Tasks A, B, and C task, they performed the advanced trail making test all ended when they touched the 25th target. They con- (ATMT; ) for 30 min  before and after the fati- tinued directly with the next Tasks B, C, and A, in that gue-inducing task session. Just before and after the fati- order, on and on for 30 min. The number of hits gue-inducing session, they recorded their subjective counted and the time were counted. In task A of the sensation of fatigue on a visual analogue scale (VAS) ATMT, when they touched a target circle, it remained from 0 (no fatigue) to 100 (complete exhaustion)  in the same position, but the color changed from black and underwent electrocardiography (ECG) with their to yellow. The positions of the other circles remained eyes closed for 1 min while sitting on a chair. VAS and the same. In task B of the ATMT, when they touched ECG recordings were performed before the ATMT the first target circle, it disappeared, and circle number trials. This study was conducted in a quiet, temperature- 26 appeared in a different position on the screen. The and humidity-controlled environment. For 1 day before positions of the other circles remained the same. For the visit, participants refrained from intense mental and example, touching circles 2, 3, and 4 resulted in their physical activities and caffeinated beverages, consumed a disappearance and the addition of circles 27, 28, and 29 normal diet, and maintained normal sleeping hours. on the screen, so that there were always 25 circles on the screen. In task C of the ATMT, when they touched Questionnaire the first target circle, it disappeared and circle number A paper-and-pencil questionnaire was distributed to 26 appeared in a different position on the screen and participants. The severity of daily level of fatigue was the position of all other circles changed at random. As measured using Chalder’s fatigue scale (Chalder et al. in task B, there were always 25 circles on the screen. Participants performed tasks A, B, and C consecutively. 1993), which has been previously used in Japanese Tanaka et al. Behavioral and Brain Functions 2011, 7:46 Page 3 of 6 http://www.behavioralandbrainfunctions.com/content/7/1/46 They were instructed to perform all task trials as quickly Table 1 Effect of acute mental fatigue on various parameters and as correctly as possible. Before After P value Electrocardiographic analyses ATMT for total error counts 16 ± 19 20 ± 26 0.076 ECG was recorded using active tracer AC301 (Global ATMT for total trial counts 305 ± 53 325 ± 45 0.001 Medical Solution Inc., Tokyo, Japan), and the ECG was VAS for fatigue 21 ± 13 47 ± 20 < 0.001 analyzed using MemCalc for Windows (Global Medical ECG variables Solution Inc.). Data were analyzed offline after analogue- %LF 38 ± 16 48 ± 18 0.035 to-digital conversion at 250 Hz. R-R wave. Irregularities in %HF 40 ± 20 33 ± 17 0.170 the ECG recordings were excluded from the analyses. LF/HF 3.4 ± 7.1 3.0 ± 3.8 0.396 Variability was measured as an indicator of autonomic Data are mean ± SD. nerve activity. For frequency domain analyses of the R-R ATMT, advanced trail making test; VAS, visual analogue scale; ECG, electrocardiography; %LF, % low-frequency power; %HF, % high-frequency wave intervals, the percent of low-frequency power (LF) power. was calculated as the power within the frequency range of 0.04 to 0.15 Hz, and the percent of high-frequency power (HF) was calculated as that within the frequency range of after the task (P = 0.020). The LF/HF ratio did not 0.15 to 0.4 Hz. LF and HF were measured in absolute and change significantly before and after the fatigue-inducing normalized units; normalization was performed by divid- task (P = 0.805). ing the absolute power by the total variance and then mul- Relationships between Chalder’s fatigue scale score tiplying by 100. The %HF is vagally mediated [28-30], but and task performances on the ATMT before the fatigue- the %LF originates from a variety of sympathetic and vagal inducing mental task are shown in Figure 1. The total mechanisms [28,31]. The LF/HF ratio represents the sym- error and trial counts were not associated with the pathetic to parasympathetic balance . Chalder’s fatigue scale score. Relationships between Chalder’s fatigue scale score Statistical analysis and ECG variables before the fatigue-inducing mental Values are shown as mean ± SD unless otherwise noted. task are shown in Figure 2. %LF and LF/HF ratio were Paired t-tests were used to evaluate the differences before positively associated with the Chalder’s fatigue scale and after the mental fatigue-inducing task as for the score, and %HF was negatively associated with the fati- ATMT performances and VAS scores and Wilcoxon’s gue score. signed rank tests as for the indices of the heart rate varia- bility. Pearson’s correlation analyses were conducted to Discussion evaluate relationships between two variables. All P values The present study showed that, after an acute fatigue- were 2-tailed, and P values less than 0.05 were considered inducing mental task, subjective levels of fatigue, %LF, statistically significant. Statistical analyses were performed and total error counts on the ATMT (tendency) using SPSS 17.0 software package (SPSS Inc., Chicago, IL). increased and %HF decreased (although this did not reach statistical signigicance) compared with before the Results fatigue-inducing task. In addition, %LF and LF/HF ratio Task performances, subjective level of fatigue, and ECG were positively, and %HF was negatively associated with variables before and after the fatigue-inducing mental the Chalder’s fatigue scale score. task areshown in Table1.After thefatigue-inducing task, the total error counts of the ATMT during the fatigue-evaluating mental task tended to increase com- pared with before the fatigue-inducing task, although differences did not reach statistical significance (P = 0.076). In addition, after the fatigue-inducing task, the total trial counts (sum of the counts to touch the circles in sequence) of the ATMT (P = 0.001) indicating that they became faster after the fatigue-inducing task, sub- jective level of fatigue (P < 0.001), and %LF (P = 0.035) increased significantly, whereas %HF decreased although Figure 1 Relationships between Chalder’sfatigue scalescore this did not reach statistical significance (P = 0.170). and task performances. The task performances were assessed using total error counts (a) and total trial counts (b) of the fatigue- Although LF measured in absolute units did not change evaluating mental task. Linear regression lines, Pearson’s correlation significantly before and after the fatigue-inducing task coefficients (R), and P values are shown. (P = 0.771), HF measured in absolute units decreased Tanaka et al. Behavioral and Brain Functions 2011, 7:46 Page 4 of 6 http://www.behavioralandbrainfunctions.com/content/7/1/46 Limitations The present study has several limitations. First, the study included a small number of participants. In addition, we did not obtain the information as for such as smoking habit or lifestyles, and a great majority of women was included maybe because we recruited the participants via advertisement. Studies involving a larger number of par- ticipants and more detailed information regarding the participants are needed to allow for generalization of these results. Second, conclusions about cause-and-effect relationshipscannotbemadedue to thecross-sectional nature of the data. Third, heart variability indices are measures of autonomic modulation of the sinus node-not autonomic tone. Heart rate variability indices must be Figure 2 Relationships between Chalder’sfatigue scalescore interpreted in light of the heart rate itself. Finally, the and autonomic nerve activities. Autonomic nerve activities were daily level of fatigue was evaluated using self-reports, and evaluated using the % low-frequency power (%LF; a), % high- frequency power (%HF; b), and LF/HF ratio (c) obtained on R-R as such, was subjective. An objective biomarker for daily wave interval analyses using electrocardiography. Linear regression level of fatigue has been developed . The number of lines, Pearson’s correlation coefficients (R), and P values are shown. saliva human herpesvirus (HHV)-6 DNA copies was decreased after holidays for approximately 1 week . These findings are consistent with the results of our The reliability and validity of the results of this study previous report , in which decreased parasympa- should be confirmed using this biomarker. thetic and increased sympathetic activities were caused after a 30-min fatigue-inducing mental task. The brain Conclusions network, including the prefrontal cortex (PFC) and ante- The present results provide evidence that increased rior cingulate cortex (ACC), has been shown to play an sympathetic activity and decreased parasympathetic important role in the regulation of autonomic nervous activity are associated with both the acute and daily activities . Decreased parasympathetic activity and level of fatigue. Because increased sympathetic activity increased sympathetic activity are interpreted as a state and decreased parasympathetic activity have been of autonomic hypervigilance [34,35], and sympathoexci- reported in patients with CFS [10,11,43], these altera- tatory subcortical circuits are normally under the inhibi- tions of the autonomic nerve activities may be common tory control of the PFC [34-36]. In addition, the ACC is characteristics of fatigue. Based on these findings, transi- related to the regulation of parasympathetic activity tional mechanisms from acute fatigue to chronic fatigue [37,38]. Because impaired selective attention assessed by and chronic fatigue to chronic fatigue-associated disease increased error counts of the ATMT  was observed might be clarified. Our findings provide new perspec- after the fatigue-inducing task, and the selective atten- tives on the mechanisms underlying fatigue. tion process activates the PFC and ACC [39-42], acute mental load might introduce temporary dysfunctions in List of abbreviations the PFC and ACC to cause decreased parasympathetic ACC: Anterior cingulate cortex; ATMT: Advanced trail making test; CFS: and increased sympathetic activities. chronic fatigue syndrome; ECG: Electrocardiography; HF: High-frequency power; HHV: Human herpesvirus; LF: Low-frequency power; PFC: Prefrontal Decreased parasympathetic nerve activity and cortex; VAS: Visual analogue scale. increased sympathetic activity have also been observed in patients with CFS [10,11,43]. Because bilateral reduc- Acknowledgements We thank Dr. Laini Dubach for editorial assistance with the manuscript. This tion of grey-matter volume in the PFC  and work was supported in part by the Ministry of Health, Labour and Welfare of decreased cerebral blood flow  and reduction of ser- the Japan and by the Grant-in-Aid for Scientific Research B (KAKENHI: otonin transporters  in the ACC were reported in 23300241) from Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan. The funder had no role in study design, data the patients with CFS, decreased parasympathetic and collection and analysis, decision to publish, or preparation of the manuscript. increased sympathetic activities may be induced by the chronic anatomical and/or functional alterations in the Author details Department of Physiology, Osaka City University Graduate School of PFC and ACC in these patients. Hence, chronic fatigue Medicine, 1-4-3 Asahimachi, Abeno-ku, Osaka 545-8585, Japan. Molecular is characterized as decreased parasympathetic and Probe Dynamics Laboratory, RIKEN Center for Molecular Imaging Science, 6- increased sympathetic activities, and the pathophysiolo- 7-3 Minatojima-minamimachi, Chuo-ku, Hyogo 650-0047, Japan. Department of Health Science, Faculty of Health Science for Welfare, Kansai University of gical background may be explained by chronic altera- Welfare Sciences, 3-11-1 Asahigaoka, Osaka 582-0026, Japan. Health tions in the PFC and ACC. Tanaka et al. Behavioral and Brain Functions 2011, 7:46 Page 5 of 6 http://www.behavioralandbrainfunctions.com/content/7/1/46 Chemical Co., Ltd., 179 Ikeda, Kume, Tokoname City, Aichi 479-0002, Japan. 18. Ataka S, Tanaka M, Nozaki S, Mizuma H, Mizuno K, Tahara T, Sugino T, Osaka Urban Industry Promotion Center, 1-4-5 Honmachi, Chuo-ku, Osaka Shirai T, Kajimoto Y, Kuratsune H, Kajimoto O, Watanabe Y: Effects of City, Osaka 541-0053, Japan. Applephenon and ascorbic acid on physical fatigue. Nutrition 2007, 23(5):419-423. Authors’ contributions 19. Ataka S, Tanaka M, Nozaki S, Mizuma H, Mizuno K, Tahara T, Sugino T, MT took part in planning and designing the experiment and cognitive tests, Shirai T, Kajimoto Y, Kuratsune H, Kajimoto O, Watanabe Y: Effects of oral collected the data, performed the data analyses and drafted the manuscript. administration of caffeine and D-ribose on mental fatigue. Nutrition 2008, KM, KY, and HK contributed to the design, planning of experiment and 24(3):233-238. cognitive tests, and helped performing the data analyses. AF, HB, AN, and TT 20. Mizuno K, Tanaka M, Nozaki S, Mizuma H, Ataka S, Tahara T, Sugino T, contributed to the design, planning of experiment, and collected the data. Shirai T, Kajimoto Y, Kuratsune H, Kajimoto O, Watanabe Y: Antifatigue YW took part in the planning and designing the experiment and cognitive effects of coenzyme Q10 during physical fatigue. Nutrition 2008, tests and helped drafting the manuscript. All authors read and approved the 24(4):293-299. final manuscript. 21. Mizuma H, Tanaka M, Nozaki S, Mizuno K, Tahara T, Ataka S, Sugino T, Shirai T, Kajimoto Y, Kuratsune H, Kajimoto O, Watanabe Y: Daily oral Competing interests administration of crocetin attenuates physical fatigue in human The authors declare that they have no competing interests. subjects. Nutr Res 2009, 29(3):145-150. 22. Nozaki S, Tanaka M, Mizuno K, Ataka S, Mizuma H, Tahara T, Sugino T, Received: 17 July 2011 Accepted: 27 October 2011 Shirai T, Eguchi A, Okuyama K, Yoshida K, Kajimoto Y, Kuratsune H, Published: 27 October 2011 Kajimoto O, Watanabe Y: Mental and physical fatigue-related biochemical alterations. Nutrition 2009, 25(1):51-57. 23. Braver TS, Cohen JD, Nystrom LE, Jonides J, Smith EE, Noll DC: A References parametric study of prefrontal cortex involvement in human working 1. Boksem MA, Tops M: Mental fatigue: costs and benefits. Brain Res Rev memory. 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Kondo K: Human herpesvirus latency and fatigue. Uirusu 2005, 55:9-17, (In Japanese). doi:10.1186/1744-9081-7-46 Cite this article as: Tanaka et al.: Autonomic nervous alterations associated with daily level of fatigue. Behavioral and Brain Functions 2011 7:46. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color ﬁgure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit
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