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Effect of mental fatigue on the central nervous system: an electroencephalography study

Effect of mental fatigue on the central nervous system: an electroencephalography study Background: Fatigue can be classified as mental and physical depending on its cause, and each type of fatigue has a multi-factorial nature. We examined the effect of mental fatigue on the central nervous system using electroencephalography (EEG) in eighteen healthy male volunteers. Methods: After enrollment, subjects were randomly assigned to two groups in a single-blinded, crossover fashion to perform two types of mental fatigue-inducing experiments. Each experiment consisted of four 30-min fatigue-inducing 0- or 2-back test sessions and two evaluation sessions performed just before and after the fatigue-inducing sessions. During the evaluation session, the participants were assessed using EEG. Eleven electrodes were attached to the head skin, from positions F3, Fz, F4, C3, Cz, C4, P3, Pz, P4, O1, and O2. Results: In the 2-back test, the beta power density on the Pz electrode and the alpha power densities on the P3 and O2 electrodes were decreased, and the theta power density on the Cz electrode was increased after the fatigue-inducing mental task sessions. In the 0-back test, no electrodes were altered after the fatigue-inducing sessions. Conclusions: Different types of mental fatigue produced different kinds of alterations of the spontaneous EEG variables. Our findings provide new perspectives on the neural mechanisms underlying mental fatigue. Keywords: Central nervous system, Electroencephalography, Mental fatigue, N-back Test Background mental fatigue have been proposed [6]. In a mental- Fatigue is a common symptom. In Japan, more than half fatigue-inducing task session, participants performed of the general adult population suffers from fatigue [1]. 0- or 2-back test trials [7]. The 0-back test was used to Fatigue decreases efficiency in the performance of daily represent a lower mental-load task, which could activities. In addition, fatigue is one of contributing be performed without use of working memory, while the factors for various medical conditions such as cardiovas- 2-back test was used to represent a higher mental-load cular diseases [2], epileptic seizures [3], and Karoshi task, which could not be performed without using work- (death from overwork) [4]. It would thus be of great ing memory [8]. The advantage of using these tasks is in interest to clarify the mechanisms underlying fatigue their ability to cause different types of mental fatigue. and to develop efficient methods for overcoming it. Since mental fatigue is a multi-faceted problem [5], it is However, the neural mechanisms of fatigue are not well of great importance to cause mental fatigue using differ- understood. ent types of tasks. As a fatigue evaluation mental task Fatigue is classified as physical or mental. Physical session, participants performed cognitive tasks, which fatigue is a bodily weakness that can occur because of are computer-based mental function tasks and the parti- repetitive muscle activity. In contrast, mental fatigue is cipants were required to use simple and conflict- observed as a reduced efficiency for mental tasks [5]. controlling selective attention. After the 0- or 2-back test Recently, new methods of induction and evaluation of sessions, error rates of the evaluation tasks were increased, thus demonstrating a deterioration of the task performance. Task performances were used to assess * Correspondence: masa-t@msic.med.osaka-cu.ac.jp mental fatigue, and the reliability and validity of the Department of Physiology, Osaka City University Graduate School of Medicine, 1-4-3 Asahimachi, Abeno-ku, Osaka 545-8585, Japan evaluation tasks were satisfactory. Full list of author information is available at the end of the article © 2012 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 2012, 8:48 Page 2 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 Although a variety of psychophysiological parameters evaluated using EEG and electrocardiography (ECG) have been used in previous research dealing with fatigue, with their eyes closed for 1 min sitting quietly. Sub- spontaneous electroencephalography (EEG) has been jects performed cognitive task trials for 9 min, and proposed as the most promising indicator of fatigue [9]. were then asked to rate their subjective level of fatigue The electrical activity of the brain is classified according on a Visual analogue scale (VAS) from 0 (minimum) to to rhythms, which are defined according to frequency 100 (maximum) [16]. Saliva samples were collected. This bands, including beta, alpha, theta, and delta, and each study was conducted in a room at Osaka City University frequency band is associated with specific internal infor- Graduate School of Medicine under quiet, temperature- mation processing in the central nervous system [10]. and humidity-controlled conditions. For 1 day before Therefore, alterations of resting-state EEG power each session, subjects refrained from intense mental and induced by mental fatigue may provide valuable clues to physical activities, consumed a normal diet and beverages identify its neural mechanisms. The aim of our study (excluding caffeinated beverages), and maintained nor- was thus to clarify the neural underpinnings of mental mal sleeping hours. They had breakfast just before the fatigue using EEG. session. Methods Participants Fatigue-inducing mental task sessions Eighteen healthy male volunteers [30.1 ± 10.8 years of Participants performed a 0-back or 2-back test for age (mean ± SD)] were enrolled in this study. Current 30 min four times as fatigue-inducing mental task ses- smokers, participants having a history of medical illness, sions [7]. During this task, one of four letters was pre- taking chronic medications or supplemental vitamins, or sented for 1 s on a display of a personal computer every with a body weight less than 40 kg were excluded from 3 s. In the 0-back test trial, participants were asked to the study based on our previous studies [11-15]. The press the right button with their right middle finger if study protocol was approved by the Ethics Committee of the target letter (shown beside the personal computer) Osaka City University, and all the participants provided was presented at the center of the screen. If any other written, informed consent. letters appeared, they were to press the left button with their right index finger. In the 2-back test trial, they had Experimental design to judge whether the target letter presented at the center After enrollment, the participants were randomly of the screen was the same as the one that had appeared assigned to two groups in a single-blinded, crossover two presentations before. If it was the same, they were fashion to perform two types of fatigue-inducing experi- to press the right button with their right middle finger. ments on separate days (Figure 1A). The time interval If it was not the same, they were to press the left button between each experiment was approximately 1 week. with their right index finger. They were instructed to Each experiment consisted of four 30-min mental-fatigue- perform the task trials as quickly and as correctly as inducing task sessions and two evaluation sessions per- possible. The result of each n-back trial, that is, a correct formed just before and after the fatigue-inducing sessions response or error, was continuously presented on the (Figure 1B). During the evaluation session, subjects were display of the personal computer. Figure 1 Experimental design (A) and procedures during experimental sessions (B). Participants were randomly assigned to two groups in a crossover fashion to perform two types of fatigue-inducing n-back test experiments on separate days. The time interval between each experiment was 1 week. Each experiment consisted of four 30-min fatigue-inducing mental task sessions and two evaluation sessions performed just before and after the four fatigue-inducing sessions. Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 3 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 Cognitive tasks theta (4–8 Hz), and delta (1–4 Hz), for each participant, The cognitive task presentation consisted of traffic lights electrode, and epoch. The average power densities in (placed on a letter corresponding to blue or red in Japa- these frequency bands were log-transformed (ln) for nese) and traffic signs for walkers (right or left) and normalization [17]. turns (right or left) shown on a personal computer screen. Participants performed Task 1 for 3 min and Electrocardiography Task 2 for 6 min. In Task 1, participants were told to ECG was recorded using active tracer AC301 (Global press the right button with their right middle finger if Medical Solution Inc., Tokyo, Japan), and the ECG was the blue traffic light was presented (placed on a letter analyzed using MemCalc for Windows (Global Medical corresponding to blue in Japanese) regardless of traffic Solution Inc.). Data were analyzed offline after analogue- signs for walkers or turns. If the red traffic light was pre- to-digital conversion at 250 Hz. R-R wave variability was sented, participants were told to press the left button measured as an indicator of autonomic nerve activity. with their right index finger. In Task 2, subjects had to For frequency domain analyses of the R-R wave inter- judge whether the target letter presented at the center of vals, low-frequency power (LF) was calculated as the a traffic light was blue or red. If the letter meant blue in power within the frequency range of 0.04 to 0.15 Hz, Japanese, regardless of the color of the traffic light or high-frequency power (HF) was calculated as that within traffic signs for walkers or turns, they were to press the the frequency range of 0.15 to 0.4 Hz. LF and HF were right button with their right middle finger; otherwise, measured in normalized units. Normalization was per- they were to press the left button with their right index formed by dividing the absolute power by the total vari- finger. The Stroop trial (mismatching the color of the ance then multiplying by 100. The %HF is vagally traffic light with the letter) and the non-Stroop trial mediated [18-20], but the %LF originates from a variety (matching the color of the traffic light with the letter) of sympathetic and vagal mechanisms [19,21]. The LF/ occurred equally. In these tasks, each trial was presented HF ratio is considered an index of sympathetic nervous 100 ms after pressing either of the buttons. During the system activity [22]. task period, blue or red trials and traffic signs for walk- ers (right or left) and turns (right or left) were given ran- Saliva sample analyses domly, and the occurrence of each color and type of We measured saliva cortisol level in order to examine sign was equal. Subjects were instructed to perform the whether the n-back test sessions cause stress response. task trials as quickly and as correctly as possible. The re- Saliva samples for the analysis of cortisol were collected sult of each cognitive task trial, that is, a correct re- in a tube (Salivette; Sarstedt, Rommelsdorf, Germany) sponse or error, was continuously presented on the and kept on ice until centrifuged at 1700 g for 5 min at display of the personal computer. 4°C. These supernatants were stored at −80°C until ana- lyzed. The assay for cortisol level was performed by Spe- Electroencephalography cial Reference Laboratories (SRL; Tokyo, Japan). EEG was performed using an EEG system (Neurofax μ EEG-9100; Nihon Kohden Corporation, Tokyo, Japan). Statistical analyses Eleven electrodes (Ag/AgCl) were attached to the head The paired t-test was used to evaluate the significance of skin, from positions F3, Fz, F4, C3, Cz, C4, P3, Pz, P4, differences between the two conditions. All P values O1, and O2; and electrooculography (EOG) was also were two-tailed, and values less than 0.05 were consid- measured to evaluate ocular artifacts. All the electrodes ered to be statistically significant. Statistical analyses were referenced to linked earlobes. Electrode impedance were performed using the SPSS 17.0 software package was maintained below 5 kΩ during the experiment. The (SPSS, Chicago, IL). EEG was amplified with a 0.3-s time constant and a 120- Hz low-pass filter, and sampled at 500 Hz. Prior to fre- Results quency analysis, all EEG data were divided into each Subjective levels of fatigue, cognitive task performances, epoch, with a duration of 1 s. The recorded data were ECG parameters and saliva cortisol levels for the fatigue- visually inspected and data segments containing possible inducing n-back test sessions are summarized in Table 1. residual artifacts were eliminated. EEG larger than VAS scores of general and mental fatigue were signifi- +50 μV were rejected as artifact. EOG artifact was also cantly increased after the 0- and 2-back test sessions. As removed by using EOG signals as predictors of the for the cognitive task performances, error rates of Task 2 artifact voltages at each EEG electrode. After artifact de- were significantly increased after the 0- and 2-back test tection, the data were subjected to a fast Fourier trans- sessions. As for the ECG variables, the LF/HF ratio was form, and after averaging, the power was determined in increased after the 2-back test sessions although this four frequency bands, beta (13–25 Hz), alpha (8–13 Hz), ratio was not altered after the 0-back test sessions. Saliva Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 4 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 Table 1 Measurements before and after the fatigue- after the fatigue-inducing mental task sessions. In the 0- inducing mental task sessions back test, the beta power densities were not altered on 0-back test 2-back test any of the electrodes after the fatigue-inducing task sessions. Before After Before After The EEG alpha power densities before and after the VAS for fatigue a a fatigue-inducing mental task sessions are shown in General fatigue 15.8 ± 11.2 53.2 ± 24.2 14.5 ± 10.4 47.8 ± 23.0 Figure 3. In the 2-back test, the alpha power densities a a Mental fatigue 15.2 ± 9.9 50.9 ± 27.5 13.2 ± 10.0 47.0 ± 26.0 on the P3 and O2 electrodes were significantly decreased Cognitive tasks after the fatigue-inducing mental task sessions. Error rate of Task 1 2.4 ± 1.9 3.4 ± 3.3 2.6 ± 2.1 3.7 ± 3.7 The EEG theta power densities before and after the a a Error rate of Task 2 4.4 ± 3.3 6.8 ± 4.9 5.1 ± 4.0 7.1 ± 5.2 fatigue-inducing mental task sessions are shown in Figure 4. In the 2-back test, the theta power density ECG b on the Fz electrode was significantly increased after the LF/HF 2.8 ± 5.2 3.7 ± 2.4 1.7 ± 1.0 4.2 ± 3.8 fatigue-inducing mental task sessions. In the 0-back test, %LF (%) 32.3 ± 16.7 43.2 ± 17.8 34.8 ± 14.9 40.0 ± 23.2 the theta power densities were not altered on any of the %HF (%) 32.0 ± 25.0 18.3 ± 13.6 26.2 ± 14.1 18.2 ± 17.2 electrodes after the fatigue-inducing task sessions. Saliva cortisol 9.4 ± 4.5 9.4 ± 4.5 8.7 ± 3.3 7.2 ± 3.3 The theta/beta and theta/alpha ratios before and after (nmol/l) the fatigue-inducing mental task sessions are also evalu- Data are presented as mean ± SD. ated. In the 2-back test, the theta/beta ratios on the Fz VAS, visual analogue scale; LF, low-frequency power; HF high-frequency (before, 1.89 ± 0.55, after, 2.26 ± 1.11; P = 0.044), Pz (be- power. a b P < 0.01, P < 0.05, significantly different from the corresponding values before fore, 1.62 ± 0.46, after, 1.97 ± 0.95; P = 0.047), and O1 (be- the fatigue-inducing mental task sessions (paired t-test). fore, 1.47 ± 0.49, after, 1.75 ± 0.82; P = 0.011) electrodes were significantly increased after the fatigue-inducing cortisol levels were not altered after the 0- or 2-back test mental task sessions, although the theta/alpha ratio did sessions. not show any alterations. In the 0-back test, the theta/ The spontaneous EEG beta power densities before and beta and theta/alpha ratios were not altered on any of after the fatigue-inducing mental task sessions are the electrodes after the fatigue-inducing task sessions. shown in Figure 2. In the 2-back test, the beta power Finally, the EEG delta power densities before and after density on the Pz electrode was significantly decreased the fatigue-inducing mental task sessions are shown in Figure 2 Electroencephalographic beta power densities before (open columns) and after (closed columns) 2- (A) and 0-back (B) test sessions and Gaussian distributions of the power densities on the Pz electrode before (solid line) and after (dotted line) 2-back test session (C). Data are presented as mean and SD. P < 0.05, significantly different from the corresponding values before the fatigue-inducing sessions (paired t-test). Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 5 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 Figure 3 Electroencephalographic alpha power densities before (open columns) and after (closed columns) 2- (A) and 0-back (B) test sessions and Gaussian distributions of the power densities on the P3 (C) and O2 (D) electrodes before (solid lines) and after (dotted lines) 2-back test session. Data are presented as mean and SD. P < 0.05, significantly different from the corresponding values before the fatigue-inducing sessions (paired t-test). Figure 4 Electroencephalographic theta power densities before (open columns) and after (closed columns) 2- (A) and 0-back (B) test sessions and Gaussian distributions of the power densities on the Fz electrode before (solid line) and after (dotted line) 2-back test session (C). Data are presented as mean and SD. P < 0.05, significantly different from the corresponding values before the fatigue-inducing sessions (paired t-test). Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 6 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 without or minimum influence of stress or stress response. The theta power density on the Fz electrode was increased after 2-back task sessions. This finding is con- sistent with the results of the previous studies, in which fatigue was caused by performing a monotonous simula- tion driving task [24] or Stroop neuropsychological test [25] for 90 min without any break: In these studies, the theta power density on the frontal EEG electrode site was increased after the mental fatigue-inducing task trials. It has been reported that the theta power density is positively related to sleepiness [26,27]. Thus, alteration of the theta power density in our study may be caused by sleepiness. In fact, the subjective level of sleepiness was increased after the fatigue-inducing mental task ses- sions (data not shown). Since sleep is one of the most ef- ficient strategies to recover from fatigue, the sleepiness caused by mental fatigue may reflect internal processes designed to meet the demand to recover from mental fa- tigue. Alternatively, since theta oscillations arising from predominantly fronto-central sources are increased by working memory load [10,28], alteration of the theta power density may be caused just by working memory Figure 5 Electroencephalographic delta power densities before load caused by performing 30-min 2-back test trials. (open columns) and after (closed columns) 2- (A) and 0-back In the 2-back test, the beta power density on the Pz (B) test sessions. Data are presented as mean and SD. electrode and the alpha power densities on the P3 and O2 electrodes were decreased after the fatigue-inducing Figure 5. In the 0- and 2-back tests, the delta power mental task sessions. Our results of the decreased beta densities were not altered on any of the electrodes after and alpha power densities are consistent with the results the fatigue-inducing task sessions. of previous studies: The beta power density was decreased by performing a monotonous simulation driv- ing task for 90 min without break [24]; while the alpha Discussion power density was decreased by keeping awake and ac- We found that in the 2-back test, the beta power density tive overnight [29]. While local synchronization in the on the Pz electrode and the alpha power densities on the brain during information processing evolved in the P3 and O2 electrodes were decreased, and the theta gamma frequency range, synchronization between neigh- power density on the Cz electrode was increased after boring cortices during multi-modal information proces- the fatigue-inducing mental task sessions, while in the 0- sing evolved in the beta frequency range, and long range back test, no electrodes were altered after the fatigue- interactions during high-level information processing inducing sessions. such as visuospatial attention evolved in the alpha fre- To confirm that the participants were actually fatigued quency range [30]. Since multi-modal and high-level in- as a result of performing n-back test trials, they per- formation processing are associated with the beta and alpha power densities, respectively, decreased beta and formed cognitive task trials and rated their subjective level of fatigue just before and after the n-back test ses- alpha power densities under conditions of mental fatigue sions. After the n-back test sessions, error rates of Tasks indicate deterioration of multi-modal and high-level in- formation processing in the central nervous system. Our 2 were increased (Table 1). These findings are consistent with those of our previous studies [6,23]. In addition, the results for the cognitive tasks (Table 1) support this VAS scores for general and mental fatigue were speculation. Different types of mental fatigue produced different increased after the sessions (Table 1). These findings demonstrate that the participants were markedly fati- styles of the alterations of the EEG variables: in the 2- gued after the n-back test sessions, and also demonstrate back test, the beta power density on the Pz electrode and the alpha power densities on the P3 and O2 electro- the validity of using the n-back test sessions as fatigue- inducing. No alterations of the saliva cortisol levels dem- des were decreased, and the theta power density on the onstrate that the n-back test sessions induced fatigue Fz electrode was increased. In the 0-back test,no Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 7 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 electrodes were altered after the fatigue-inducing ses- Conclusions sions. The 0-back test was used to represent a lower We identified mental fatigue-related changes in spontan- mental-load task, which could be performed without eous EEG variables. In the 2-back test, the beta power working memory use, while the 2-back test was used to density on the Pz electrode and the alpha power dens- represent a higher mental-load task, which could not be ities on the P3 and O2 electrodes were decreased, and performed without working memory use [7]. Most of the theta power density on the Cz electrode was the locations that showed changes of beta and alpha increased after the fatigue-inducing mental task sessions, power densities are located close to the visual areas (P3, while in the 0-back test, no electrodes were altered after Pz, and O2) in the 2-back test. Higher mental load to the fatigue-inducing sessions. Our findings provide new perform 2-back test may need more visual memory and perspectives on the neural mechanisms underlying men- implies more visual work in different visual areas to de- tal fatigue. velop the fatigue-related alterations of EEG power dens- Abbreviations ities in the posterior areas related to visual processing. ACC: Anterior cingulate cortex; ECG: Electrocardiography; Higher mental load thus may trigger processes designed EEG: Electroencephalography; HF: High-frequency power LF, low-frequency power; PFC: Prefrontal cortex; VAS: Visual analogue scale. to bring about deterioration of multi-modal and high- level information processing, while lower mental load Competing interests may induce fewer alterations. The authors declare that they have no competing interests. In addition to EEG, different types of mental fatigue produced different styles of the alterations of the ECG Authors’ contributions MT took part in planning and designing the experiment, collected the data, variables. The LF/HF ratio was increased after the 2- performed the data analyses and drafted the manuscript. YS, AI, MF, and EK back test sessions although this ratio was not altered took part in planning and designing the experiment, collected the data, and after the 0-back test sessions. Since increased LF/HF performed the data analyses. YW took part in the planning and designing the experiment and helped drafting the manuscript. All authors read and ratio during mental fatigue-inducing task session was approved the final manuscript. reported to be associated with the mental effort or mo- tivation [23], the different results of the LF/HF ratio be- Acknowledgements tween the 0- and 2-back test sessions might result from We thank Forte Science Communications for editorial help with the manuscript. This work was supported in part by the Ministry of Health, the difference of the mental effort or motivation between Labour and Welfare of the Japan and by the Grant-in-Aid for Scientific the sessions. The brain network, including the prefrontal Research B (KAKENHI: 23300241) from Ministry of Education, Culture, Sports, cortex (PFC) and anterior cingulate cortex (ACC), has Science and Technology (MEXT) of Japan and by the grant from Ministry of Health, Labor and Welfare of Japan. The funders had no roles in study been shown to play an important role in the regulation design, data collection and analysis, decision to publish, or preparation of of autonomic nervous activities [31]. Abnormalities in the manuscript. these brain regions have been shown to be associated Author details with fatigue [32,33]. Because impaired selective attention Department of Physiology, Osaka City University Graduate School of assessed by increased error rates in cognitive task trials 2 Medicine, 1-4-3 Asahimachi, Abeno-ku, Osaka 545-8585, Japan. Degital & were observed after the fatigue-inducing mental task Network Technology Development Center, Panasonic Corporation, 1006 Kadoma, Osaka 571-8501, Japan. RIKEN, Center for Molecular Imaging sessions, and the selective attention process activates the Science, 6-7-3 Minatojima-minamimachi, Chuo-ku, Hyogo 650-0047, Japan. PFC and ACC [34-37], the higher mental load required for the 2-back test sessions might introduce temporary Received: 19 March 2012 Accepted: 16 August 2012 Published: 6 September 2012 dysfunctions in the PFC and ACC to cause decreased parasympathetic and increased sympathetic activities, References while lower mental load necessary for performing the 0- 1. Watanabe Y: Preface and mini-review: fatigue science for human health. New back test sessions might induce fewer alterations of the York: In: Fatigue Science for Human Health. Edited by Watanabe Y, Evengård B, Natelson BH, Jason LA, Kuratsune H; 2008:5–11. ECG variables. 2. 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Effect of mental fatigue on the central nervous system: an electroencephalography study

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Copyright © 2012 by Tanaka et al.; licensee BioMed Central Ltd.
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Biomedicine; Neurosciences; Neurology; Behavioral Therapy; Psychiatry
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Abstract

Background: Fatigue can be classified as mental and physical depending on its cause, and each type of fatigue has a multi-factorial nature. We examined the effect of mental fatigue on the central nervous system using electroencephalography (EEG) in eighteen healthy male volunteers. Methods: After enrollment, subjects were randomly assigned to two groups in a single-blinded, crossover fashion to perform two types of mental fatigue-inducing experiments. Each experiment consisted of four 30-min fatigue-inducing 0- or 2-back test sessions and two evaluation sessions performed just before and after the fatigue-inducing sessions. During the evaluation session, the participants were assessed using EEG. Eleven electrodes were attached to the head skin, from positions F3, Fz, F4, C3, Cz, C4, P3, Pz, P4, O1, and O2. Results: In the 2-back test, the beta power density on the Pz electrode and the alpha power densities on the P3 and O2 electrodes were decreased, and the theta power density on the Cz electrode was increased after the fatigue-inducing mental task sessions. In the 0-back test, no electrodes were altered after the fatigue-inducing sessions. Conclusions: Different types of mental fatigue produced different kinds of alterations of the spontaneous EEG variables. Our findings provide new perspectives on the neural mechanisms underlying mental fatigue. Keywords: Central nervous system, Electroencephalography, Mental fatigue, N-back Test Background mental fatigue have been proposed [6]. In a mental- Fatigue is a common symptom. In Japan, more than half fatigue-inducing task session, participants performed of the general adult population suffers from fatigue [1]. 0- or 2-back test trials [7]. The 0-back test was used to Fatigue decreases efficiency in the performance of daily represent a lower mental-load task, which could activities. In addition, fatigue is one of contributing be performed without use of working memory, while the factors for various medical conditions such as cardiovas- 2-back test was used to represent a higher mental-load cular diseases [2], epileptic seizures [3], and Karoshi task, which could not be performed without using work- (death from overwork) [4]. It would thus be of great ing memory [8]. The advantage of using these tasks is in interest to clarify the mechanisms underlying fatigue their ability to cause different types of mental fatigue. and to develop efficient methods for overcoming it. Since mental fatigue is a multi-faceted problem [5], it is However, the neural mechanisms of fatigue are not well of great importance to cause mental fatigue using differ- understood. ent types of tasks. As a fatigue evaluation mental task Fatigue is classified as physical or mental. Physical session, participants performed cognitive tasks, which fatigue is a bodily weakness that can occur because of are computer-based mental function tasks and the parti- repetitive muscle activity. In contrast, mental fatigue is cipants were required to use simple and conflict- observed as a reduced efficiency for mental tasks [5]. controlling selective attention. After the 0- or 2-back test Recently, new methods of induction and evaluation of sessions, error rates of the evaluation tasks were increased, thus demonstrating a deterioration of the task performance. Task performances were used to assess * Correspondence: masa-t@msic.med.osaka-cu.ac.jp mental fatigue, and the reliability and validity of the Department of Physiology, Osaka City University Graduate School of Medicine, 1-4-3 Asahimachi, Abeno-ku, Osaka 545-8585, Japan evaluation tasks were satisfactory. Full list of author information is available at the end of the article © 2012 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 2012, 8:48 Page 2 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 Although a variety of psychophysiological parameters evaluated using EEG and electrocardiography (ECG) have been used in previous research dealing with fatigue, with their eyes closed for 1 min sitting quietly. Sub- spontaneous electroencephalography (EEG) has been jects performed cognitive task trials for 9 min, and proposed as the most promising indicator of fatigue [9]. were then asked to rate their subjective level of fatigue The electrical activity of the brain is classified according on a Visual analogue scale (VAS) from 0 (minimum) to to rhythms, which are defined according to frequency 100 (maximum) [16]. Saliva samples were collected. This bands, including beta, alpha, theta, and delta, and each study was conducted in a room at Osaka City University frequency band is associated with specific internal infor- Graduate School of Medicine under quiet, temperature- mation processing in the central nervous system [10]. and humidity-controlled conditions. For 1 day before Therefore, alterations of resting-state EEG power each session, subjects refrained from intense mental and induced by mental fatigue may provide valuable clues to physical activities, consumed a normal diet and beverages identify its neural mechanisms. The aim of our study (excluding caffeinated beverages), and maintained nor- was thus to clarify the neural underpinnings of mental mal sleeping hours. They had breakfast just before the fatigue using EEG. session. Methods Participants Fatigue-inducing mental task sessions Eighteen healthy male volunteers [30.1 ± 10.8 years of Participants performed a 0-back or 2-back test for age (mean ± SD)] were enrolled in this study. Current 30 min four times as fatigue-inducing mental task ses- smokers, participants having a history of medical illness, sions [7]. During this task, one of four letters was pre- taking chronic medications or supplemental vitamins, or sented for 1 s on a display of a personal computer every with a body weight less than 40 kg were excluded from 3 s. In the 0-back test trial, participants were asked to the study based on our previous studies [11-15]. The press the right button with their right middle finger if study protocol was approved by the Ethics Committee of the target letter (shown beside the personal computer) Osaka City University, and all the participants provided was presented at the center of the screen. If any other written, informed consent. letters appeared, they were to press the left button with their right index finger. In the 2-back test trial, they had Experimental design to judge whether the target letter presented at the center After enrollment, the participants were randomly of the screen was the same as the one that had appeared assigned to two groups in a single-blinded, crossover two presentations before. If it was the same, they were fashion to perform two types of fatigue-inducing experi- to press the right button with their right middle finger. ments on separate days (Figure 1A). The time interval If it was not the same, they were to press the left button between each experiment was approximately 1 week. with their right index finger. They were instructed to Each experiment consisted of four 30-min mental-fatigue- perform the task trials as quickly and as correctly as inducing task sessions and two evaluation sessions per- possible. The result of each n-back trial, that is, a correct formed just before and after the fatigue-inducing sessions response or error, was continuously presented on the (Figure 1B). During the evaluation session, subjects were display of the personal computer. Figure 1 Experimental design (A) and procedures during experimental sessions (B). Participants were randomly assigned to two groups in a crossover fashion to perform two types of fatigue-inducing n-back test experiments on separate days. The time interval between each experiment was 1 week. Each experiment consisted of four 30-min fatigue-inducing mental task sessions and two evaluation sessions performed just before and after the four fatigue-inducing sessions. Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 3 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 Cognitive tasks theta (4–8 Hz), and delta (1–4 Hz), for each participant, The cognitive task presentation consisted of traffic lights electrode, and epoch. The average power densities in (placed on a letter corresponding to blue or red in Japa- these frequency bands were log-transformed (ln) for nese) and traffic signs for walkers (right or left) and normalization [17]. turns (right or left) shown on a personal computer screen. Participants performed Task 1 for 3 min and Electrocardiography Task 2 for 6 min. In Task 1, participants were told to ECG was recorded using active tracer AC301 (Global press the right button with their right middle finger if Medical Solution Inc., Tokyo, Japan), and the ECG was the blue traffic light was presented (placed on a letter analyzed using MemCalc for Windows (Global Medical corresponding to blue in Japanese) regardless of traffic Solution Inc.). Data were analyzed offline after analogue- signs for walkers or turns. If the red traffic light was pre- to-digital conversion at 250 Hz. R-R wave variability was sented, participants were told to press the left button measured as an indicator of autonomic nerve activity. with their right index finger. In Task 2, subjects had to For frequency domain analyses of the R-R wave inter- judge whether the target letter presented at the center of vals, low-frequency power (LF) was calculated as the a traffic light was blue or red. If the letter meant blue in power within the frequency range of 0.04 to 0.15 Hz, Japanese, regardless of the color of the traffic light or high-frequency power (HF) was calculated as that within traffic signs for walkers or turns, they were to press the the frequency range of 0.15 to 0.4 Hz. LF and HF were right button with their right middle finger; otherwise, measured in normalized units. Normalization was per- they were to press the left button with their right index formed by dividing the absolute power by the total vari- finger. The Stroop trial (mismatching the color of the ance then multiplying by 100. The %HF is vagally traffic light with the letter) and the non-Stroop trial mediated [18-20], but the %LF originates from a variety (matching the color of the traffic light with the letter) of sympathetic and vagal mechanisms [19,21]. The LF/ occurred equally. In these tasks, each trial was presented HF ratio is considered an index of sympathetic nervous 100 ms after pressing either of the buttons. During the system activity [22]. task period, blue or red trials and traffic signs for walk- ers (right or left) and turns (right or left) were given ran- Saliva sample analyses domly, and the occurrence of each color and type of We measured saliva cortisol level in order to examine sign was equal. Subjects were instructed to perform the whether the n-back test sessions cause stress response. task trials as quickly and as correctly as possible. The re- Saliva samples for the analysis of cortisol were collected sult of each cognitive task trial, that is, a correct re- in a tube (Salivette; Sarstedt, Rommelsdorf, Germany) sponse or error, was continuously presented on the and kept on ice until centrifuged at 1700 g for 5 min at display of the personal computer. 4°C. These supernatants were stored at −80°C until ana- lyzed. The assay for cortisol level was performed by Spe- Electroencephalography cial Reference Laboratories (SRL; Tokyo, Japan). EEG was performed using an EEG system (Neurofax μ EEG-9100; Nihon Kohden Corporation, Tokyo, Japan). Statistical analyses Eleven electrodes (Ag/AgCl) were attached to the head The paired t-test was used to evaluate the significance of skin, from positions F3, Fz, F4, C3, Cz, C4, P3, Pz, P4, differences between the two conditions. All P values O1, and O2; and electrooculography (EOG) was also were two-tailed, and values less than 0.05 were consid- measured to evaluate ocular artifacts. All the electrodes ered to be statistically significant. Statistical analyses were referenced to linked earlobes. Electrode impedance were performed using the SPSS 17.0 software package was maintained below 5 kΩ during the experiment. The (SPSS, Chicago, IL). EEG was amplified with a 0.3-s time constant and a 120- Hz low-pass filter, and sampled at 500 Hz. Prior to fre- Results quency analysis, all EEG data were divided into each Subjective levels of fatigue, cognitive task performances, epoch, with a duration of 1 s. The recorded data were ECG parameters and saliva cortisol levels for the fatigue- visually inspected and data segments containing possible inducing n-back test sessions are summarized in Table 1. residual artifacts were eliminated. EEG larger than VAS scores of general and mental fatigue were signifi- +50 μV were rejected as artifact. EOG artifact was also cantly increased after the 0- and 2-back test sessions. As removed by using EOG signals as predictors of the for the cognitive task performances, error rates of Task 2 artifact voltages at each EEG electrode. After artifact de- were significantly increased after the 0- and 2-back test tection, the data were subjected to a fast Fourier trans- sessions. As for the ECG variables, the LF/HF ratio was form, and after averaging, the power was determined in increased after the 2-back test sessions although this four frequency bands, beta (13–25 Hz), alpha (8–13 Hz), ratio was not altered after the 0-back test sessions. Saliva Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 4 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 Table 1 Measurements before and after the fatigue- after the fatigue-inducing mental task sessions. In the 0- inducing mental task sessions back test, the beta power densities were not altered on 0-back test 2-back test any of the electrodes after the fatigue-inducing task sessions. Before After Before After The EEG alpha power densities before and after the VAS for fatigue a a fatigue-inducing mental task sessions are shown in General fatigue 15.8 ± 11.2 53.2 ± 24.2 14.5 ± 10.4 47.8 ± 23.0 Figure 3. In the 2-back test, the alpha power densities a a Mental fatigue 15.2 ± 9.9 50.9 ± 27.5 13.2 ± 10.0 47.0 ± 26.0 on the P3 and O2 electrodes were significantly decreased Cognitive tasks after the fatigue-inducing mental task sessions. Error rate of Task 1 2.4 ± 1.9 3.4 ± 3.3 2.6 ± 2.1 3.7 ± 3.7 The EEG theta power densities before and after the a a Error rate of Task 2 4.4 ± 3.3 6.8 ± 4.9 5.1 ± 4.0 7.1 ± 5.2 fatigue-inducing mental task sessions are shown in Figure 4. In the 2-back test, the theta power density ECG b on the Fz electrode was significantly increased after the LF/HF 2.8 ± 5.2 3.7 ± 2.4 1.7 ± 1.0 4.2 ± 3.8 fatigue-inducing mental task sessions. In the 0-back test, %LF (%) 32.3 ± 16.7 43.2 ± 17.8 34.8 ± 14.9 40.0 ± 23.2 the theta power densities were not altered on any of the %HF (%) 32.0 ± 25.0 18.3 ± 13.6 26.2 ± 14.1 18.2 ± 17.2 electrodes after the fatigue-inducing task sessions. Saliva cortisol 9.4 ± 4.5 9.4 ± 4.5 8.7 ± 3.3 7.2 ± 3.3 The theta/beta and theta/alpha ratios before and after (nmol/l) the fatigue-inducing mental task sessions are also evalu- Data are presented as mean ± SD. ated. In the 2-back test, the theta/beta ratios on the Fz VAS, visual analogue scale; LF, low-frequency power; HF high-frequency (before, 1.89 ± 0.55, after, 2.26 ± 1.11; P = 0.044), Pz (be- power. a b P < 0.01, P < 0.05, significantly different from the corresponding values before fore, 1.62 ± 0.46, after, 1.97 ± 0.95; P = 0.047), and O1 (be- the fatigue-inducing mental task sessions (paired t-test). fore, 1.47 ± 0.49, after, 1.75 ± 0.82; P = 0.011) electrodes were significantly increased after the fatigue-inducing cortisol levels were not altered after the 0- or 2-back test mental task sessions, although the theta/alpha ratio did sessions. not show any alterations. In the 0-back test, the theta/ The spontaneous EEG beta power densities before and beta and theta/alpha ratios were not altered on any of after the fatigue-inducing mental task sessions are the electrodes after the fatigue-inducing task sessions. shown in Figure 2. In the 2-back test, the beta power Finally, the EEG delta power densities before and after density on the Pz electrode was significantly decreased the fatigue-inducing mental task sessions are shown in Figure 2 Electroencephalographic beta power densities before (open columns) and after (closed columns) 2- (A) and 0-back (B) test sessions and Gaussian distributions of the power densities on the Pz electrode before (solid line) and after (dotted line) 2-back test session (C). Data are presented as mean and SD. P < 0.05, significantly different from the corresponding values before the fatigue-inducing sessions (paired t-test). Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 5 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 Figure 3 Electroencephalographic alpha power densities before (open columns) and after (closed columns) 2- (A) and 0-back (B) test sessions and Gaussian distributions of the power densities on the P3 (C) and O2 (D) electrodes before (solid lines) and after (dotted lines) 2-back test session. Data are presented as mean and SD. P < 0.05, significantly different from the corresponding values before the fatigue-inducing sessions (paired t-test). Figure 4 Electroencephalographic theta power densities before (open columns) and after (closed columns) 2- (A) and 0-back (B) test sessions and Gaussian distributions of the power densities on the Fz electrode before (solid line) and after (dotted line) 2-back test session (C). Data are presented as mean and SD. P < 0.05, significantly different from the corresponding values before the fatigue-inducing sessions (paired t-test). Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 6 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 without or minimum influence of stress or stress response. The theta power density on the Fz electrode was increased after 2-back task sessions. This finding is con- sistent with the results of the previous studies, in which fatigue was caused by performing a monotonous simula- tion driving task [24] or Stroop neuropsychological test [25] for 90 min without any break: In these studies, the theta power density on the frontal EEG electrode site was increased after the mental fatigue-inducing task trials. It has been reported that the theta power density is positively related to sleepiness [26,27]. Thus, alteration of the theta power density in our study may be caused by sleepiness. In fact, the subjective level of sleepiness was increased after the fatigue-inducing mental task ses- sions (data not shown). Since sleep is one of the most ef- ficient strategies to recover from fatigue, the sleepiness caused by mental fatigue may reflect internal processes designed to meet the demand to recover from mental fa- tigue. Alternatively, since theta oscillations arising from predominantly fronto-central sources are increased by working memory load [10,28], alteration of the theta power density may be caused just by working memory Figure 5 Electroencephalographic delta power densities before load caused by performing 30-min 2-back test trials. (open columns) and after (closed columns) 2- (A) and 0-back In the 2-back test, the beta power density on the Pz (B) test sessions. Data are presented as mean and SD. electrode and the alpha power densities on the P3 and O2 electrodes were decreased after the fatigue-inducing Figure 5. In the 0- and 2-back tests, the delta power mental task sessions. Our results of the decreased beta densities were not altered on any of the electrodes after and alpha power densities are consistent with the results the fatigue-inducing task sessions. of previous studies: The beta power density was decreased by performing a monotonous simulation driv- ing task for 90 min without break [24]; while the alpha Discussion power density was decreased by keeping awake and ac- We found that in the 2-back test, the beta power density tive overnight [29]. While local synchronization in the on the Pz electrode and the alpha power densities on the brain during information processing evolved in the P3 and O2 electrodes were decreased, and the theta gamma frequency range, synchronization between neigh- power density on the Cz electrode was increased after boring cortices during multi-modal information proces- the fatigue-inducing mental task sessions, while in the 0- sing evolved in the beta frequency range, and long range back test, no electrodes were altered after the fatigue- interactions during high-level information processing inducing sessions. such as visuospatial attention evolved in the alpha fre- To confirm that the participants were actually fatigued quency range [30]. Since multi-modal and high-level in- as a result of performing n-back test trials, they per- formation processing are associated with the beta and alpha power densities, respectively, decreased beta and formed cognitive task trials and rated their subjective level of fatigue just before and after the n-back test ses- alpha power densities under conditions of mental fatigue sions. After the n-back test sessions, error rates of Tasks indicate deterioration of multi-modal and high-level in- formation processing in the central nervous system. Our 2 were increased (Table 1). These findings are consistent with those of our previous studies [6,23]. In addition, the results for the cognitive tasks (Table 1) support this VAS scores for general and mental fatigue were speculation. Different types of mental fatigue produced different increased after the sessions (Table 1). These findings demonstrate that the participants were markedly fati- styles of the alterations of the EEG variables: in the 2- gued after the n-back test sessions, and also demonstrate back test, the beta power density on the Pz electrode and the alpha power densities on the P3 and O2 electro- the validity of using the n-back test sessions as fatigue- inducing. No alterations of the saliva cortisol levels dem- des were decreased, and the theta power density on the onstrate that the n-back test sessions induced fatigue Fz electrode was increased. In the 0-back test,no Tanaka et al. Behavioral and Brain Functions 2012, 8:48 Page 7 of 8 http://www.behavioralandbrainfunctions.com/content/8/1/48 electrodes were altered after the fatigue-inducing ses- Conclusions sions. The 0-back test was used to represent a lower We identified mental fatigue-related changes in spontan- mental-load task, which could be performed without eous EEG variables. In the 2-back test, the beta power working memory use, while the 2-back test was used to density on the Pz electrode and the alpha power dens- represent a higher mental-load task, which could not be ities on the P3 and O2 electrodes were decreased, and performed without working memory use [7]. Most of the theta power density on the Cz electrode was the locations that showed changes of beta and alpha increased after the fatigue-inducing mental task sessions, power densities are located close to the visual areas (P3, while in the 0-back test, no electrodes were altered after Pz, and O2) in the 2-back test. Higher mental load to the fatigue-inducing sessions. Our findings provide new perform 2-back test may need more visual memory and perspectives on the neural mechanisms underlying men- implies more visual work in different visual areas to de- tal fatigue. velop the fatigue-related alterations of EEG power dens- Abbreviations ities in the posterior areas related to visual processing. ACC: Anterior cingulate cortex; ECG: Electrocardiography; Higher mental load thus may trigger processes designed EEG: Electroencephalography; HF: High-frequency power LF, low-frequency power; PFC: Prefrontal cortex; VAS: Visual analogue scale. to bring about deterioration of multi-modal and high- level information processing, while lower mental load Competing interests may induce fewer alterations. The authors declare that they have no competing interests. In addition to EEG, different types of mental fatigue produced different styles of the alterations of the ECG Authors’ contributions MT took part in planning and designing the experiment, collected the data, variables. The LF/HF ratio was increased after the 2- performed the data analyses and drafted the manuscript. YS, AI, MF, and EK back test sessions although this ratio was not altered took part in planning and designing the experiment, collected the data, and after the 0-back test sessions. Since increased LF/HF performed the data analyses. YW took part in the planning and designing the experiment and helped drafting the manuscript. All authors read and ratio during mental fatigue-inducing task session was approved the final manuscript. reported to be associated with the mental effort or mo- tivation [23], the different results of the LF/HF ratio be- Acknowledgements tween the 0- and 2-back test sessions might result from We thank Forte Science Communications for editorial help with the manuscript. This work was supported in part by the Ministry of Health, the difference of the mental effort or motivation between Labour and Welfare of the Japan and by the Grant-in-Aid for Scientific the sessions. The brain network, including the prefrontal Research B (KAKENHI: 23300241) from Ministry of Education, Culture, Sports, cortex (PFC) and anterior cingulate cortex (ACC), has Science and Technology (MEXT) of Japan and by the grant from Ministry of Health, Labor and Welfare of Japan. The funders had no roles in study been shown to play an important role in the regulation design, data collection and analysis, decision to publish, or preparation of of autonomic nervous activities [31]. Abnormalities in the manuscript. these brain regions have been shown to be associated Author details with fatigue [32,33]. Because impaired selective attention Department of Physiology, Osaka City University Graduate School of assessed by increased error rates in cognitive task trials 2 Medicine, 1-4-3 Asahimachi, Abeno-ku, Osaka 545-8585, Japan. Degital & were observed after the fatigue-inducing mental task Network Technology Development Center, Panasonic Corporation, 1006 Kadoma, Osaka 571-8501, Japan. RIKEN, Center for Molecular Imaging sessions, and the selective attention process activates the Science, 6-7-3 Minatojima-minamimachi, Chuo-ku, Hyogo 650-0047, Japan. PFC and ACC [34-37], the higher mental load required for the 2-back test sessions might introduce temporary Received: 19 March 2012 Accepted: 16 August 2012 Published: 6 September 2012 dysfunctions in the PFC and ACC to cause decreased parasympathetic and increased sympathetic activities, References while lower mental load necessary for performing the 0- 1. Watanabe Y: Preface and mini-review: fatigue science for human health. New back test sessions might induce fewer alterations of the York: In: Fatigue Science for Human Health. Edited by Watanabe Y, Evengård B, Natelson BH, Jason LA, Kuratsune H; 2008:5–11. ECG variables. 2. 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Published: Sep 6, 2012

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