Physiology & Behavior 142 (2015) 146–151
Contents lists available at ScienceDirect
Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Time-of-day effects on postural control and attentional capacities in children Rym Baccouch a,d,⁎, Nidhal Zarrouk b, Hamdi Chtourou c, Haithem Rebai a, Sonia Sahli a a
Research Unit: Education, Motricity, Sports and Health, High Institute of Sport and Physical Education, Sfax, Sfax University, Tunisia Research Laboratory: "Medical Imaging Technologies" (LR 12ES06, LTIM), Faculty of Medicine of Monastir, University of Monastir, Tunisia Research Laboratory: "Sports Performance Optimization", National Center of Medicine and Science in Sports (CNMSS), Tunis, Tunisia d Faculty of Sciences of Bizerte, University of Carthage, Tunisia b c
H I G H L I G H T S • Children's postural control is better in the middle morning and the late afternoon. • The diurnal rhythm of postural control is close to that of body temperature. • The diurnal rhythm of postural control is close to that of attentional capacities.
a r t i c l e
i n f o
Article history: Received 20 April 2014 Received in revised form 5 October 2014 Accepted 22 January 2015 Available online 23 January 2015 Keywords: Time-of-day Posture Children Temperature Attention
a b s t r a c t The present study aimed to examine the effect of time-of-day on postural control, body temperature, and attentional capacities in 5–6 year old children. Twelve male children (5–6-year-old) were asked to maintain an upright bipedal stance on a force platform with eyes open (EO) and eyes closed (EC) at 07:00, 10:00, 14:00, and 18:00 h. Postural control was evaluated by center of pressure (CoP) surface area (CoPArea), CoP mean velocity (CoPVm), length of the CoP displacement as a function of the surface (LFS) ratio and Romberg's index (RI). Oral temperature and the simple reaction time were also recorded at the beginning of each test session. The one way ANOVA (4 time-of-day) showed significant time-of-day effects on CoPArea (p b 0.001), CoPVm (p b 0.01), LFS ratio (p b 0.001) and RI (p b 0.01). Children's postural control was lower at 07:00 h and at 14:00 h in comparison with 10:00 h and 18:00 h. Likewise, the reaction time was significantly (p b 0.001) better at 10:00 h and 18:00 h in comparison with 07:00 h and 14:00 h. Oral temperature was higher at 14:00 h and 18:00 h than 08:00 h and 10:00 h (p b 0.001). In conclusion, the children's postural control fluctuates during the daytime (i.e., better postural control at 10:00 h and at 18:00 h) with a diurnal rhythm close to that of body temperature and attentional capacities. Therefore, the evaluation of changes in postural control of 5–6-year-old children using force plate measures is recommended in the middle morning or the late afternoon to avoid the post-awakening and the post-prandial phases. © 2015 Published by Elsevier Inc.
1. Introduction Chronobiology refers to the branch of science concerned with timekeeping functions in biological-systems [1]. A multitude of biological rhythms in the human body can be attributed to (i) a mixture of influences from the external environment (e.g., daylight, temperature, social interactions, and timing of meals) [2], (ii) the individual's sleep–wake cycle and (iii) the internal body clock [1]. The term “circadian rhythms” refers to the systematic fluctuations in physiological functions that recur ⁎ Corresponding author at: High Institute of Sport and Physical Education, Sfax, Sfax University, BP 1068 Route de l’Aérodrôme, Km 3.5, 3000 Sfax, Tunisia. Tel.: + 216 28315014. E-mail address: [email protected] (R. Baccouch).
http://dx.doi.org/10.1016/j.physbeh.2015.01.029 0031-9384/© 2015 Published by Elsevier Inc.
over a 24-hour period [1]. These rhythms induce fluctuations in physiological functions in the human organism that affect our ability to perform various types of motor tasks [3]. Previous studies concerning circadian rhythms and their desynchronizations had practical applications in the postural control field [4–6]. Postural control results from the integration of visual, somatosensory and vestibular information [4] by the central nervous system [5] to contract muscles adequately in order to maintain balance [6]. Furthermore, it has been shown that postural control requires attentional resources [7]. In fact, this sensory integration needs a high level of vigilance, particularly when one of the sensory inputs is no longer effective [8]. Recently, it has been found that attentional capacities in trained adults are time-of-day dependent, with the best values observed in the afternoon for reaction time [9,10].
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151
Several studies have reported that postural control is influenced by the time-of-day [6,11–15]. It has been reported that the postural control is low between 05:00 and 08:00 h [11,16] corresponding to the bathyphase of the body temperature rhythm [17] and around 13:00 h [18] corresponding to the post-lunch dip observed in the vigilance level [19]. In this context, it has been established that the postural control of young adults fluctuates according to a rhythm [6] which is close to that of body temperature and/or vigilance [11,18]. However, it has been reported that older adults were less stable in the late afternoon [20]. These authors suggested that this impaired postural control observed during the later parts of the day could be related to sleepiness, fatigue accumulating throughout the day or hormone levels. Thus, previous studies have proposed that the time-of-day influence on postural control may exist in young [6] and old adults [20] and this effect varied depending on the age factor. To the best of our knowledge, this aspect has not been examined in young children. It has been showed that young children exhibit a greater magnitude of postural sway than adults during a quiet standing position [21]. Moreover, the age range between 5- and 6-year olds has been identified as one of the critical stages of postural development [22]. During this age range, children seem to be learning how to integrate sensory information and how to calibrate sensory feedback for use in postural control [23]. In fact, they have been shown to use higher rate of postural corrections [24] indicating the predominance of feedback responses. Indeed, the impaired postural control observed in children at this age may increase the fall risk [24]. Clinicians and scientists were interested in evaluating and developing the balance control in children at this critical age. They seek to protect them from injuries and to develop their ability in completing the required movements [25,26]. Since it has been established that the postural control fluctuates according to time-of-day in young and older adults as mentioned above, we hypothesized that children's postural control could be affected by time-of-day. Moreover, we think that we need to know the diurnal rhythm of children's postural control at this age to take it into account when evaluating children's postural control in order to ovoid disparate findings. To date, despite the broad use of postural force plate analysis in both scientific and clinical settings, a lack of consensus exists on when and how the technique should be used. Therefore, the aim of the present study was to examine the effect of time-of-day on postural control, on the attentional capacities and on the body temperature in 5–6-year-old children.
147
and their guardians, and they all gave their written informed consent before testing. In order to guarantee sample homogeneity, the subjects were selected according to their chronotype with reference to their parents' answers to the Morningness–Eveningness questionnaire (MEQ: version for infants) [29], modified for students [30]. This questionnaire consisted of seven questions: three pertaining to sleep onset, three to sleep offset, and once to the peak timing of activity. Each question allows for choice (scored from 1 to 4) and the M–E score was the sum of the seven answers. Scores ranged from 7 to 28, with lower scores representing evening-types and higher scores representing morningtypes. All of the subjects were morning-types. 2.2. Experimental design Each subject was evaluated during four test sessions. As postural control may develop concomitantly with body temperature and/or vigilance rhythm, it seemed necessary to carry out recordings at the bathyphase and acrophase of these rhythms. Thus, four test sessions had to be set-up in a randomized order: in the early morning (at 07:00 h just after the habitual awakening time of our subjects), in the middle morning (10:00 h), in the early afternoon (14:00 h) and in the late afternoon (18:00 h) (Fig. 1). Subjects perform one test session per day. All test sessions are randomized and separated by a period of rest (more than 36 h) in order to eliminate the learning effect. In this study, the control of a number of factors recommended for diurnal fluctuation studies was taken into account (i.e., chronotype). Masking effects such as the consumption of stimulant drinks (coffee), meals or even physical activity [31] were also controlled [18]. Throughout the experimental protocol, the mean ambient temperature of the laboratory was kept stable (21.2 ± 1.0 °C). Parents were asked to keep the usual sleeping habits of their children. Children were requested to avoid tiring activities during the 24 h before each test session in order to eliminate the fatigue effect which may affect the postural control. It was easy to control compliance with these instructions, because the subjects had exactly the same daily schedules in the pre-school. 2.3. Temperature measurements
2. Methods
Oral temperature was recorded during the four test sessions with a calibrated digital clinical thermometer (Omron®, Paris, France; accuracy: 0.1 °C) inserted sublingually for at least 3 min with the subjects in a seated resting position for at least 15-min.
2.1. Subjects
2.4. Posturographic assessments
Twelve male children (age: 5.6 ± 0.4 years; height: 115.2 ± 2 cm; weight: 20.6 ± 2.3 kg; foot length: 27 ± 2 cm) were recruited from a private pre-school in Sousse (Tunisia), to participate in the present experiment. They have the same criteria in terms of socio-economic status and ethnic origin. Moreover, they are sedentary without previous experience in any type of sport (i.e., they practice only recreational activities irregularly). We have taken into account the level of fitness of the subjects because it could influence the results. In previous studies, it has been reported that physical training may improve the postural control in children [26,27]. In fact, practitioners of specific sports acquired new specific balance and sensory organization abilities compared to sedentary subjects [26,27]. Besides, in the chronobiology field, it has been shown that the amplitude of the diurnal rhythm is higher in trained compared to untrained subjects [28]. The exclusion criteria were the presence of vestibular or visual disorder, musculoskeletal or neurological disease and history of injury in the past 12 months requiring medical attention. The study was conducted in accordance with the Declaration of Helsinki and was approved by the Clinical Research Ethics Committee of the National Centre of Medicine and Science of Sports of Tunis (CNMSS). The procedures were fully explained to the participants
Postural control was evaluated using a force platform (PostureWin©, Techno Concept ®, Cereste, France; 40 Hz frequency, 12-bits A/D conversion) which records the displacements of the center of pressure (CoP) with three strain gauges. The platform was level with the surrounding floor. The subjects were asked to stand as still as possible on a force platform with their arms comfortably placed downward at either side of the body, their bare feet were separated by an angle of 30° and their heels placed 5 cm apart. To maintain the same foot positions for all the measurements, a plastic device provided with the platform was used. The subjects were first requested to maintain balance with the eyes open (EO) and then with the eyes closed (EC). In the EO condition, participants were instructed to look straight ahead at a white cross placed onto the wall 2 m away at eye level. In the EC conditions, they were asked to keep their gaze horizontal in a straight-ahead direction. Following French Posturology Association norms, each trial lasts 25.6 s. CoP excursions were computed from the ground reaction forces and their associated torques. As subjects oscillate during the upright standing postures with their body relatively rigid, the reaction force applied to the body is relatively constant and so the variations of the
148
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151
Fig. 1. Experimental procedure.
associated torque depend mainly on the CoP excursions [32]. The CoP excursions represent the muscular torque that controls the body oscillations [32,33]. The COP area (CoPArea) (90% confidence ellipse) evaluated the subject's postural performance. The LFS ratio corresponding to the length of the CoP displacement as a function of the surface (index of energy expenditure) [34]. The mean CoP velocity (CoPVm) corresponding to the sum of the CoP displacement scalars divided by the sampling time and the Romberg's index (RI) [(surface EC / surface EO) × 100] evaluating the contribution of vision to maintaining posture [35] were also measured. The smaller the area and/or the lower the velocity, the better the performance [36].
3. Results 3.1. Temperature The time-of-day effect was significant (F(3.11) = 63.05; p b 0.001; Table 1) with post-hoc tests showing that the temperature improved significantly (p b 0.001) from 07:00 to 10:00 h and from 10.00 to 14.00 h. The temperature was significantly higher (p b 0.001) at 14:00 and 18:00 h compared to 07:00 and 10:00 h.
3.2. Posturographic assessments 2.5. Attentional capacities Attentional capacities were evaluated by a simple reaction time test. This test was measured using a “Superlab 4.5” program (Cedrus, San Pedro, USA). It measures the reaction time to visual stimuli. The subject sat 0.4 to 0.5 m in front of the computer screen. After 10 familiarization trials, each subject performed randomly and double-blinded 20 simple reaction time tests. The stimulus was a black square, presented for 50 ms at the center of the screen, preceded by a white square stimulus to direct the fixation. The interval between the appearances of two consecutive stimuli was randomized (average 1.5 s). After a training trial, the subject's task was to press a specific computer key as quickly as possible, using the favored hand, after the appearance of the black square. The score is established by evaluating the number of correct answers (correct response score) and the mean reaction time for the 20 trials (response time score). Reaction times of less than 150 ms and greater than 800 ms were excluded from analysis to avoid any effects from either anticipation or a temporary lapse of concentration. 2.6. Statistical analysis All statistical tests were processed using STATISTICA Software (StatSoft, France). The Shapiro–Wilk W-test of normality revealed that the data were normally distributed. The CoP data, the reaction time and the body temperature recorded during the four test sessions were analyzed by a one way repeated-measure analysis of variance (ANOVA) [4 time-of-day]. When significant differences were observed (p b 0.05), a post-hoc analysis was then performed with a Fisher–Snedecor least significant difference (LSD) test. Significance was set as p b 0.05.
The one-way ANOVA (4 time-of-day) showed a significant time-ofday effect (F(3.11) = 15.06, p b 0.001; Fig. 2) on the CoPArea. Post-hoc test revealed that the CoPArea decreased significantly (p b 0.001) from 07:00 to 10:00 h. The CoPArea increased significantly (p b 0.05) from 10:00 to 14:00 h. Then, it decreased significantly (p b 0.05) from 14:00 to 18:00 h. The CoPArea was significantly (p b 0.01) smaller at 14:00 compared to 07:00 h. However, no significant (p = 0.81) difference was observed between 10:00 and 18:00 h. The ANOVA indicated a significant time-of-day effect (F(3.11) = 5.99, p b 0.01; Fig. 3) on the CoPVm. Post-hoc analysis showed that the CoPVm decreased significantly (p b 0.001) from 07:00 to 10:00 h before increasing (p b 0.05) from 10:00 to 14:00 h. No significant differences were observed between 18:00 h and 10:00 h (p = 0.58) or 14:00 h (p = 0.11). However, the CoPVm was significantly (p b 0.01) lower at 18:00 compared to 07:00 h. For the LFS ratio, the ANOVA indicated a significant time-of-day effect (F(3.11) = 9.28, p b 0.001; Fig. 4). Post-hoc analysis revealed that the LFS ratio was significantly higher (p b 0.001) at 07:00 compared to 10:00 h. The LFS ratio increased significantly (p b 0.01) from 10:00 to 14:00 h, followed by a significant decrease (p b 0.01) at 18:00 h. No significant (p = 0.22) difference was observed between the LFS values recorded at 07:00 and those at 14:00 h. Similarly, the difference between the LFS values assessed at 10:00 and those at 18:00 h was not significant (p = 1.00). Concerning the RI, the ANOVA indicated a significant time-of-day effect (F(3.11) = 5.62, p b 0.01; Fig. 5). The post-hoc analysis showed that the contribution of vision to maintain posture was significantly more important at 10:00 h compared to 07:00 h (p b 0.01), 14:00 h (p b 0.01) and 18:00 h (p b 0.001).
Table 1 Mean values (±SD) of mean reaction time and oral temperature (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h.
Mean reaction time (S) M ± (SD) Oral temperature (°C) M ± (SD)
07:00 h
10:00 h
14:00 h
18:00 h
0.63 ± (0.036) 35.99 ± (0.19)
0.56 ± (0.046) 36.80 ± (0.21)
0.62 ± (0.052) 37.10 ± (0.27)
0.55 ± (0.047) 37.20 ± (0.26)
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151
Fig. 2. Mean values (±SD) of center of pressure area (CoPArea) (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h. *, **, ***: significant differences in comparison between test sessions at p b 0.05, p b 0.01 and p b 0.001, respectively. NS: non-significant difference between test sessions.
149
Fig. 4. Mean values (± SD) of LFS ratio (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h. **, ***: significant differences in comparison between test sessions at p b 0.01 and p b 0.001, respectively. NS: non-significant difference between test sessions.
The main purpose of the present study was (i) to explore the effect of time-of-day on postural control in 5–6-year-old children and (ii) to assess the diurnal fluctuations of the body temperature and of the attentional capacities to clarify the origins of any putative postural control fluctuations. Concerning postural control measurements, the results showed diurnal variations of the COPArea, the CoPVm, the LFS ratio and the RI. The oral temperature increases from morning to afternoon. Moreover, our results indicated that the reaction time was lower in the middle morning and in the late afternoon compared to the other times-of-day. Our results showed that the CoPArea and the CoPVm were high in the early morning (i.e., 07:00 h) in children. Similar findings were established in young adults [6,13,37]. In this context, it has been reported that the postural control was low between 05:00 and 08:00 h [11,16]. The LFS ratio in our children was high in the early morning indicating
high energy expenditure [34]. In contrast, in previous studies, adults spent less energy in the early morning [6]. At this time of day, our findings showed that the reaction time was high indicating low attentional capacities which corresponds to “the post-awakening phase” characterized by a transient hypovigilance, mood disorders and a momentary physical and mental performance degradation [38–40]. It was confirmed that the diurnal fluctuations of vigilance and intellectual performances resulted in the attention skill test variation [38,39]. Consequently, we suggested that the vigilance level in children was low at the early morning as reported for young adults [11–13]. Moreover, we found that the bathyphase of the body temperature rhythm in children was situated at the early morning, this result concurs with the findings of Reilly [17]. It has been established that the decrease of central body temperature may decrease nerve conduction velocity, joint suppleness, and muscle strength [41]. The postural control is a complex system consisting of a sensory part (vestibular-, somatosensory- and visual system), a processing part (central nervous system) and an effectuating part (spinal alpha-motor neurons and muscles) [20] which all possibly could be affected by either low attentional capacities and body temperature decrease in the early morning. At 10:00 h, the CoPArea, the CoPVm and the LFS ratio were lower compared to values assessed at 07:00 h. This result confirms that the postural control of children improves during the morning as reported in adults [11–13]. At this time of day, the reaction time decreased indicating better attentional capacities in the present study' participants. Similarly, an augmentation of vigilance level was reported after 9:00 h in young students with a maximum of intellectual capacities recorded in the middle morning [38,39]. Besides, our results confirm that the body temperature improves from 7:00 h to 10:00 h in children [17]. Around this time, a small peak for the muscular strength was previously highlighted
Fig. 3. Mean values (±SD) of center of pressure mean velocity (CoPVm) (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h. *, **, ***: significant differences in comparison between test sessions at p b 0.05, p b 0.01 and p b 0.001, respectively. NS: non-significant difference between test sessions.
Fig. 5. Mean values (±SD) of Romberg's index (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h. **, ***: significant differences in comparison between test sessions at p b 0.01 and p b 0.001, respectively. NS: non-significant difference between test sessions.
3.3. Attentional capacities The one way ANOVA (4 time-of-day) revealed a significant time-ofday effect (F(3.11) = 17.54, p b 0.001; Table 1) on the reaction time. Posthoc analysis showed that the reaction time decreased significantly (p b 0.001) from 07:00 to 10:00 h before increasing (p b 0.001) at 14:00 h. The reaction time decreased significantly (p b 0.001) from 14:00 to 18:00 h. No significant (p = 0.80) difference between the reaction time values recorded at 10:00 and those at 18:00 h was observed. Similarly, no significant (p = 0.46) difference was revealed between the reaction time values recorded at 07:00 and those at 14:00 h.
4. Discussion
150
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151
[42]. Furthermore, our findings showed that the RI was better at 10:00 compared to 18:00 h indicating that the contribution of vision to maintaining posture [35] was more pronounced in the middle morning compared to the other test sessions. However, the RI was not influenced by the time of day in adults [6]. These controversies could be explained by the specificity of the age range of our subjects. In fact, it has been reported that the children prefer to rely on visual inputs more than other sensory information in achieving postural equilibrium [43,44]. Moreover, at this critical age of 5–6 years old, children seem to be learning how to integrate sensory information and how to calibrate sensory feedback for use in postural control [23]. At 14:00 h, the CoPArea, the CoPVm and the LFS values were higher compared to 10:00 h indicating a low postural control at this time despite the fact that the body temperature of children continues to increase from the early morning. Similarly, postural control was low at 13:00 h [18] and at 14:00 h [6] in adults. It seems that, despite increased energy expenditure [34], children were unable to improve their stability at this time-of-day. Besides, the reaction time assessed in our subjects was high at 14:00 h indicating a low attention level as reported in young students [38,39]. It has been reported that this time period corresponds to the post-lunch dip observed in the vigilance level [19]. Besides, in previous studies, performances for muscular power decreased at the post-lunch dip period [42]. At 18:00 h, the CoPArea and the LFS ratio were lower compared to values assessed at 14:00 h and the CoPVm was lower than at 07:00 h. These findings indicated a better postural control observed in the late afternoon in young children as established in young adults [6,11–13]. In contrast, it was reported that the older adults were less stable around this time [20]. The reaction time decreased from 14:00 to 18:00 h indicating an improvement of children's attentional capacities in the late afternoon. At this time, our results showed an important peak of the body temperature. Similarly, the optimum of the reaction time was observed at the early evening near the peak of the body temperature [9,10,38,39]. It has been found that performances for strength and power in children improved significantly from morning to the afternoon [45]. It was generally accepted that the diurnal increase in central body temperature could act as a passive warm-up that may increase nerve conduction velocity, joint suppleness, and muscle strength [41]. Thus, increased core temperature due to circadian patterns would facilitate enhancement of the neuromuscular and metabolic systems [46] which may improve the efficiency of postural muscle activity to control children's balance. It has been established that the cause of the child's diurnal variations of muscle power and fatigue during a short-term maximal performance was related to peripheral mechanisms [47] through an improvement of the muscle contractile properties at the end of the day as reported in young adults [48–50]. In the present study, children showed a better postural control at 10:00 and 18:00 h with no significant difference observed between these two times of day. However, it was reported that the postural control of young adults reaches a most important peak at 18:00 h [6]. Thus, despite the fact that the temperature and the muscular power were reported to be better at the end of the day [45,17], 5–6-year-old children controlled their balance at the middle morning similarly to the late afternoon. This finding may be related to the important attentional capacities indicating probably better sensory integration ability and to the better contribution of vision to maintaining posture revealed at 10:00 h in the present study' participants. Many scientific and clinical studies used the force plate measures to assess changes in postural control especially for the critical ages as children or older adults [51,52]. To limit contrasting findings, it was recommended to verify many variables such as heterogeneity of the group, small sample size, the presence of vestibular or visual disorder, or musculoskeletal or neurological diseases, history of injury in the past or regular training in sports. Recently, in older adults, it was suggested to control the time-of-day when subjects were tested because they were less stable in the late afternoon [18]. If the time of testing was not
controlled this would probably influence the results. Thus, by the present findings, we suggested that it will be better if we evaluate children's postural control in the middle morning or in the late afternoon and to avoid the post-awakening and the post-lunch phases. Moreover, based on our findings, the time-of-day should be taken into account when evaluating the postural control improvement after balance training intervention in children as it has been suggested in older adults [20]. 5. Limitations There were some limitations in this study that need to be considered when interpreting the findings. In the present study we measured the static postural control with and without elimination of visual inputs. Our results might be stronger if dynamic postural control had been examined as it could be more reliable to the daily activities. Moreover, the current study focused on the diurnal variations of postural control in 5–6-year-old children which is one of the critical stages of postural development. In further study we should compare different age ranges during childhood because the balance systems are not fully matured in young people until the age of 14 [53]. 6. Conclusion Children's postural control was low in the early morning and in the early afternoon and improved during the middle morning and in the late afternoon. The children's postural control fluctuates according to a diurnal rhythm (i.e., better postural control at 10:00 and 18:00 h) which is close to that of body temperature and/or attentional capacities. Therefore, clinicians could rely on these findings and may take into account the time-of-day when evaluating the children's postural control to avoid disparate results. Moreover, if balance training is recommended for 5–6-year-old children in order to prevent them from falls and injuries, it should be programmed at 10:00 h or 18:00 h when the postural control is better. Declaration of interest There is no financial conflict with the subject matter or materials discussed in this manuscript at any of the authors' academic institutions or employers. Finally, authors did not receive any financial interest. Acknowledgments We would like to thank Professor Dogui Mohamed, the head of the Laboratory of Physiology, Faculty of Medicine, Monastir — Tunisia, for collaboration and help. We also thank all the participants and their guardians. References [1] T. Reilly, J. Waterhouse, Chronobiologie and exercise, Med. Sport. 13 (2009) 54–60. [2] D. Hoyer, J. Clairambault, Rhythms from seconds to days. Physiological importance and therapeutic implications, IEEE Eng. Med. Biol. Mag. 26 (2007) 12–13. [3] C.M. Winget, C.W. DeRoshia, D.C. Holley, Circadian rhythms and athletic performance, Med. Sci. Sports Exerc. 17 (1985) 498–516. [4] J. Massion, Postural control system, Curr. Opin. Neurobiol. 4 (1994) 877–887. [5] Y. Ouchi, H. Okada, E. Yoshikawa, S. Nobezawa, M. Futatsubashi, Brain activation during maintenance of standing postures in humans, Brain 122 (1999) 329–338. [6] C. Bougard, M.C. Lepelley, D. Davenne, The influences of time-of-day and sleep deprivation on postural control, Exp. Brain Res. 209 (2011) 109–115. [7] M. Woollacott, A. Shumway-Cook, Attention and the control of posture and gait: a review of an emerging area of research, Gait Posture 16 (2002) 1–14. [8] M.S. Redfern, L. Yardley, A.M. Bronstein, Visual influences on balance, J. Anxiety Disord. 15 (2001) 81–94. [9] S. Jarraya, M. Jarraya, H. Chtourou, N. Souissi, Diurnal variations on cognitive performances in handball goalkeepers, Biol. Rhythm. Res. 45 (2013) 93–101. [10] S. Jarraya, M. Jarraya, H. Chtourou, N. Souissi, Effect of time of day and partial sleep deprivation on the reaction time and the attentional capacities of the handball goalkeeper, Biol. Rhythm. Res. 45 (2014) 183–191.
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151 [11] N. Avni, I. Avni, E. Barenboim, B. Azaria, D. Zadok, R. Kohen-Raz, Y. Morad, Brief posturographic test as an indicator of fatigue, Psychiatry Clin. Neurosci. 60 (2006) 340–346. [12] P.A. Gribble, W.S. Tucker, P.A. White, Time-of-day influences on static and dynamic postural control, J. Athl. Train. 42 (2007) 35–41. [13] T. Nakano, K. Araki, A. Michimori, H. Inbe, H. Hagiwara, E. Koyama, Nineteen-hour variation of postural sway, alertness and rectal temperature during sleep deprivation, Psychiatry Clin. Neurosci. 55 (2001) 277–278. [14] N. Souissi, A. Zouita, H. Chtourou, H. Ferchichi, C. Dziri, S. Abedelmalek, N. Souissi, The effect of Ramadan intermittent fasting on dynamic postural control in judo athletes, Biol. Rhythm. Res. 45 (2013) 27–36. [15] N. Souissi, H. Chtourou, A. Zouita, C. Dziri, N. Souissi, Effects of Ramadan intermittent fasting on postural control in judo athletes, Biol. Rhythm. Res. 44 (2) (2013) 237–244. [16] Y. Morad, B. Azaria, I. Avni, Y. Barkana, D. Zadok, R. Kohen-Raz, E. Barenboim, Posturography as an indicator of fatigue due to sleep deprivation, Aviat. Space Environ. Med. 78 (2007) 859–863. [17] T. Reilly, Human circadian rhythms and exercise, Crit. Rev. Biomed. Eng. 18 (1990) 165–180. [18] P. Forsman, E. Haeggstrom, A. Wallin, E. Toppila, I. Pyykko, Daytime changes in postural stability and repeatability of posturographic measurements, J. Occup. Environ. Med. 49 (2007) 591–596. [19] M. Clodore, J. Foret, O. Benoit, Diurnal variation in subjective and objective measures of sleepiness: the effects of sleep reduction and circadian type, Chronobiol. Int. 3 (1986) 255–263. [20] M.G. Jorgensen, M.S. Rathleff, U. Laessoe, P. Caserotti, O.B.F. Nielsen, P. Aagaard, Timeof-day influences postural balance in older adults, Gait Posture 35 (2012) 653–657. [21] M.L. Peterson, E. Christou, K.S. Rosengren, Children achieve adult-like sensory integration during stance at 12-years-old, Gait Posture 23 (2006) 455–463. [22] A. Shumway-Cook, M. Woollacott, The growth of stability: postural control from a developmental perspective, J. Mot. Behav. 17 (1985) 131–147. [23] C. Riach, J. Starkes, Stability limits of quiet standing postural control in children and adults, Gait Posture 1 (1993) 105–111. [24] C. Riach, K. Hayes, Maturation of postural sway in young children, Dev. Med. Child Neurol. 29 (1987) 650–658. [25] C. Assaiante, S. Mallau, S. Viel, M. Jover, C. Schmitz, Development of postural control in healthy children: a functional approach, Neural Plast. 12 (2005) 109–118. [26] S. Sahli, S. Ghroubi, H. Rebai, M. Chaâbane, A. Yahia, D. Pérennou, M.H. Elleuch, The effect of circus activity training on postural control of 5–6-year-old children, Sci. Sports 28 (2013) 11–16. [27] C. Garcia, J. Barela, A. Viana, A. Barela, Influence of gymnastics training on the development of postural control, Neurosci. Lett. 492 (2011) 29–32. [28] G. Atkinson, A. Coldwells, T. Reilly, J.M. Waterhouse, A comparison of circadian rhythms in work performance between physically active and inactive subjects, Ergonomics 36 (1993) 273–281. [29] L. Torsvall, T. Åkerstedt, A diurnal type scale: construction, consistency and validation in shift work, Scand. J. Work Environ. Health 6 (1980) 283–290. [30] H. Takeuchi, M. Inoue, N. Watanabe, Y. Yamashita, M. Hamada, G. Kadota, T. Harada, Parental enforcement of bedtime during childhood results in Japanese junior high school students preferring morningness to eveningness, Chronobiol. Int. 18 (2001) 823–829. [31] T. Reilly, E. Bambaeichi, Methodological issues in studies of rhythms in human performance, Biol. Rhythm. Res. 34 (2003) 321–336.
151
[32] F. Asseman, O. Caron, J. Crémieux, Are there specific conditions for which expertise in gymnastics could have an effect on postural control and performance? Gait Posture 27 (2008) 76–81. [33] D.A. Winter, A.E. Patla, F. Prince, M. Ischac, F. Gielo-Perczak, Stiffness control of balance in quiet standing, J. Neurophysiol. 80 (1998) 1211–1221. [34] P.M. Gagey, B. Weber, Posturologie; Régulation et dérèglements de la station debout, Masson, Paris, 1999. [35] C.J. Njiokiktjien, J.A. van Parys, Romberg's sign expressed in a quotient. II. Pathology, Agressologie 17 (1976) 19–23. [36] O. Caron, T. Gelat, P. Rougier, J.P. Blanchi, A comparative analysis of the center of gravity of pressure trajectory path lengths in standing posture: an estimation of active stiffness, J. Appl. Biomech. 16 (2000) 234–247. [37] Y. Liu, S. Higuchi, Y. Motohashi, Changes in postural sway during a period of sustained wakefulness in male adults, Occup. Med. 51 (2001) 490–495. [38] F. Testu, Quelques constantes dans les fluctuations journalières et hebdomadaires de l'activité intellectuelle des élèves en Europe, Enfance (1994) 389–400. [39] F. Testu, Chronopsychologie et rythmes scolaires, Masson, Paris, 2000. [40] P.R. Jeanneret, W.B. Wilse, Strength of grip on arousal from a full night's sleep, Percept. Mot. Skills 17 (1963) 759–761. [41] L.D. Hayes, G.F. Bickerstaff, J.S. Baker, Interactions of cortisol, testosterone, and resistance training: influence of circadian rhythms, Chronobiol. Int. 27 (2010) 675–705. [42] G. Atkinson, T. Reilly, Circadian variation in sports performance, Sports Med. 21 (1996) 292–312. [43] V.L. Cumberworth, N.N. Patel, W. Rogers, The maturation of balance in children, J. Laryngol. Otol. 121 (2007) 449–454. [44] S. Hirabayashi, Y. Iwasaki, Developmental perspective of sensory organization on postural control, Brain Dev. 17 (1995) 111–113. [45] H. Souissi, A. Chaouachi, K. Chamari, M. Dogui, M. Amri, N. Souissi, Time-of-day effects on short-term exercise performances in 10–11-years-old boys, Pediatr. Exerc. Sci. 22 (2010) 613–623. [46] S. Racinais, Different effects of heat exposure upon exercise performance in the morning and afternoon, Scand. J. Med. Sci. Sports 20 (2010) 80–89. [47] H. Souissi, H. Chtourou, A. Chaouachi, K. Chamari, N. Souissi, M. Amri, Time-of-day effects on EMG parameters during the Wingate test in boys, J. Sports Sci. Med. 11 (2012) 380–386. [48] H. Chtourou, N. Zarrouk, A. Chaouachi, M. Dogui, D.G. Behm, K. Chamari, F. Hug, N. Souissi, Diurnal variation in Wingate-test performance and associated electromyographic parameters, Chronobiol. Int. 28 (2011) 706–713. [49] M. Guette, J. Gondin, A. Martin, Time-of-day effect on the torque and neuromuscular properties of dominant and nondominant quadriceps femoris, Chronobiol. Int. 22 (2005) 541–558. [50] A. Martin, A. Carpentier, N. Guissard, J. Van Hoecke, J. Duchateau, Effect of time of day on force variation in a human muscle, Muscle Nerve 22 (1999) 1380–1387. [51] L. Ajrezo, S. Wiener-Vacher, M.P. Bucci, Saccades improve postural control: a developmental study in normal children, PLoS ONE 8 (11) (2013) e81066. http:// dx.doi.org/10.1371/ journal.pone.0081066. [52] M. Moghadam, H. Ashayeri, M. Salavati, J. Sarafzadeh, K.D. Taghipoor, A. Saeedi, R. Salehi, Reliability of center of pressure measures of postural stability in healthy older adults: effects of postural task difficulty and cognitive load, Gait Posture 33 (2011) 651–655. [53] S.S. Fong, S.N. Fu, G.Y. Ng, Taekwondo training speeds up the development of balance and sensory functions in young adolescents, J. Sci. Med. Sport 15 (2012) 64–68.
Contents lists available at ScienceDirect
Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Time-of-day effects on postural control and attentional capacities in children Rym Baccouch a,d,⁎, Nidhal Zarrouk b, Hamdi Chtourou c, Haithem Rebai a, Sonia Sahli a a
Research Unit: Education, Motricity, Sports and Health, High Institute of Sport and Physical Education, Sfax, Sfax University, Tunisia Research Laboratory: "Medical Imaging Technologies" (LR 12ES06, LTIM), Faculty of Medicine of Monastir, University of Monastir, Tunisia Research Laboratory: "Sports Performance Optimization", National Center of Medicine and Science in Sports (CNMSS), Tunis, Tunisia d Faculty of Sciences of Bizerte, University of Carthage, Tunisia b c
H I G H L I G H T S • Children's postural control is better in the middle morning and the late afternoon. • The diurnal rhythm of postural control is close to that of body temperature. • The diurnal rhythm of postural control is close to that of attentional capacities.
a r t i c l e
i n f o
Article history: Received 20 April 2014 Received in revised form 5 October 2014 Accepted 22 January 2015 Available online 23 January 2015 Keywords: Time-of-day Posture Children Temperature Attention
a b s t r a c t The present study aimed to examine the effect of time-of-day on postural control, body temperature, and attentional capacities in 5–6 year old children. Twelve male children (5–6-year-old) were asked to maintain an upright bipedal stance on a force platform with eyes open (EO) and eyes closed (EC) at 07:00, 10:00, 14:00, and 18:00 h. Postural control was evaluated by center of pressure (CoP) surface area (CoPArea), CoP mean velocity (CoPVm), length of the CoP displacement as a function of the surface (LFS) ratio and Romberg's index (RI). Oral temperature and the simple reaction time were also recorded at the beginning of each test session. The one way ANOVA (4 time-of-day) showed significant time-of-day effects on CoPArea (p b 0.001), CoPVm (p b 0.01), LFS ratio (p b 0.001) and RI (p b 0.01). Children's postural control was lower at 07:00 h and at 14:00 h in comparison with 10:00 h and 18:00 h. Likewise, the reaction time was significantly (p b 0.001) better at 10:00 h and 18:00 h in comparison with 07:00 h and 14:00 h. Oral temperature was higher at 14:00 h and 18:00 h than 08:00 h and 10:00 h (p b 0.001). In conclusion, the children's postural control fluctuates during the daytime (i.e., better postural control at 10:00 h and at 18:00 h) with a diurnal rhythm close to that of body temperature and attentional capacities. Therefore, the evaluation of changes in postural control of 5–6-year-old children using force plate measures is recommended in the middle morning or the late afternoon to avoid the post-awakening and the post-prandial phases. © 2015 Published by Elsevier Inc.
1. Introduction Chronobiology refers to the branch of science concerned with timekeeping functions in biological-systems [1]. A multitude of biological rhythms in the human body can be attributed to (i) a mixture of influences from the external environment (e.g., daylight, temperature, social interactions, and timing of meals) [2], (ii) the individual's sleep–wake cycle and (iii) the internal body clock [1]. The term “circadian rhythms” refers to the systematic fluctuations in physiological functions that recur ⁎ Corresponding author at: High Institute of Sport and Physical Education, Sfax, Sfax University, BP 1068 Route de l’Aérodrôme, Km 3.5, 3000 Sfax, Tunisia. Tel.: + 216 28315014. E-mail address: [email protected] (R. Baccouch).
http://dx.doi.org/10.1016/j.physbeh.2015.01.029 0031-9384/© 2015 Published by Elsevier Inc.
over a 24-hour period [1]. These rhythms induce fluctuations in physiological functions in the human organism that affect our ability to perform various types of motor tasks [3]. Previous studies concerning circadian rhythms and their desynchronizations had practical applications in the postural control field [4–6]. Postural control results from the integration of visual, somatosensory and vestibular information [4] by the central nervous system [5] to contract muscles adequately in order to maintain balance [6]. Furthermore, it has been shown that postural control requires attentional resources [7]. In fact, this sensory integration needs a high level of vigilance, particularly when one of the sensory inputs is no longer effective [8]. Recently, it has been found that attentional capacities in trained adults are time-of-day dependent, with the best values observed in the afternoon for reaction time [9,10].
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151
Several studies have reported that postural control is influenced by the time-of-day [6,11–15]. It has been reported that the postural control is low between 05:00 and 08:00 h [11,16] corresponding to the bathyphase of the body temperature rhythm [17] and around 13:00 h [18] corresponding to the post-lunch dip observed in the vigilance level [19]. In this context, it has been established that the postural control of young adults fluctuates according to a rhythm [6] which is close to that of body temperature and/or vigilance [11,18]. However, it has been reported that older adults were less stable in the late afternoon [20]. These authors suggested that this impaired postural control observed during the later parts of the day could be related to sleepiness, fatigue accumulating throughout the day or hormone levels. Thus, previous studies have proposed that the time-of-day influence on postural control may exist in young [6] and old adults [20] and this effect varied depending on the age factor. To the best of our knowledge, this aspect has not been examined in young children. It has been showed that young children exhibit a greater magnitude of postural sway than adults during a quiet standing position [21]. Moreover, the age range between 5- and 6-year olds has been identified as one of the critical stages of postural development [22]. During this age range, children seem to be learning how to integrate sensory information and how to calibrate sensory feedback for use in postural control [23]. In fact, they have been shown to use higher rate of postural corrections [24] indicating the predominance of feedback responses. Indeed, the impaired postural control observed in children at this age may increase the fall risk [24]. Clinicians and scientists were interested in evaluating and developing the balance control in children at this critical age. They seek to protect them from injuries and to develop their ability in completing the required movements [25,26]. Since it has been established that the postural control fluctuates according to time-of-day in young and older adults as mentioned above, we hypothesized that children's postural control could be affected by time-of-day. Moreover, we think that we need to know the diurnal rhythm of children's postural control at this age to take it into account when evaluating children's postural control in order to ovoid disparate findings. To date, despite the broad use of postural force plate analysis in both scientific and clinical settings, a lack of consensus exists on when and how the technique should be used. Therefore, the aim of the present study was to examine the effect of time-of-day on postural control, on the attentional capacities and on the body temperature in 5–6-year-old children.
147
and their guardians, and they all gave their written informed consent before testing. In order to guarantee sample homogeneity, the subjects were selected according to their chronotype with reference to their parents' answers to the Morningness–Eveningness questionnaire (MEQ: version for infants) [29], modified for students [30]. This questionnaire consisted of seven questions: three pertaining to sleep onset, three to sleep offset, and once to the peak timing of activity. Each question allows for choice (scored from 1 to 4) and the M–E score was the sum of the seven answers. Scores ranged from 7 to 28, with lower scores representing evening-types and higher scores representing morningtypes. All of the subjects were morning-types. 2.2. Experimental design Each subject was evaluated during four test sessions. As postural control may develop concomitantly with body temperature and/or vigilance rhythm, it seemed necessary to carry out recordings at the bathyphase and acrophase of these rhythms. Thus, four test sessions had to be set-up in a randomized order: in the early morning (at 07:00 h just after the habitual awakening time of our subjects), in the middle morning (10:00 h), in the early afternoon (14:00 h) and in the late afternoon (18:00 h) (Fig. 1). Subjects perform one test session per day. All test sessions are randomized and separated by a period of rest (more than 36 h) in order to eliminate the learning effect. In this study, the control of a number of factors recommended for diurnal fluctuation studies was taken into account (i.e., chronotype). Masking effects such as the consumption of stimulant drinks (coffee), meals or even physical activity [31] were also controlled [18]. Throughout the experimental protocol, the mean ambient temperature of the laboratory was kept stable (21.2 ± 1.0 °C). Parents were asked to keep the usual sleeping habits of their children. Children were requested to avoid tiring activities during the 24 h before each test session in order to eliminate the fatigue effect which may affect the postural control. It was easy to control compliance with these instructions, because the subjects had exactly the same daily schedules in the pre-school. 2.3. Temperature measurements
2. Methods
Oral temperature was recorded during the four test sessions with a calibrated digital clinical thermometer (Omron®, Paris, France; accuracy: 0.1 °C) inserted sublingually for at least 3 min with the subjects in a seated resting position for at least 15-min.
2.1. Subjects
2.4. Posturographic assessments
Twelve male children (age: 5.6 ± 0.4 years; height: 115.2 ± 2 cm; weight: 20.6 ± 2.3 kg; foot length: 27 ± 2 cm) were recruited from a private pre-school in Sousse (Tunisia), to participate in the present experiment. They have the same criteria in terms of socio-economic status and ethnic origin. Moreover, they are sedentary without previous experience in any type of sport (i.e., they practice only recreational activities irregularly). We have taken into account the level of fitness of the subjects because it could influence the results. In previous studies, it has been reported that physical training may improve the postural control in children [26,27]. In fact, practitioners of specific sports acquired new specific balance and sensory organization abilities compared to sedentary subjects [26,27]. Besides, in the chronobiology field, it has been shown that the amplitude of the diurnal rhythm is higher in trained compared to untrained subjects [28]. The exclusion criteria were the presence of vestibular or visual disorder, musculoskeletal or neurological disease and history of injury in the past 12 months requiring medical attention. The study was conducted in accordance with the Declaration of Helsinki and was approved by the Clinical Research Ethics Committee of the National Centre of Medicine and Science of Sports of Tunis (CNMSS). The procedures were fully explained to the participants
Postural control was evaluated using a force platform (PostureWin©, Techno Concept ®, Cereste, France; 40 Hz frequency, 12-bits A/D conversion) which records the displacements of the center of pressure (CoP) with three strain gauges. The platform was level with the surrounding floor. The subjects were asked to stand as still as possible on a force platform with their arms comfortably placed downward at either side of the body, their bare feet were separated by an angle of 30° and their heels placed 5 cm apart. To maintain the same foot positions for all the measurements, a plastic device provided with the platform was used. The subjects were first requested to maintain balance with the eyes open (EO) and then with the eyes closed (EC). In the EO condition, participants were instructed to look straight ahead at a white cross placed onto the wall 2 m away at eye level. In the EC conditions, they were asked to keep their gaze horizontal in a straight-ahead direction. Following French Posturology Association norms, each trial lasts 25.6 s. CoP excursions were computed from the ground reaction forces and their associated torques. As subjects oscillate during the upright standing postures with their body relatively rigid, the reaction force applied to the body is relatively constant and so the variations of the
148
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151
Fig. 1. Experimental procedure.
associated torque depend mainly on the CoP excursions [32]. The CoP excursions represent the muscular torque that controls the body oscillations [32,33]. The COP area (CoPArea) (90% confidence ellipse) evaluated the subject's postural performance. The LFS ratio corresponding to the length of the CoP displacement as a function of the surface (index of energy expenditure) [34]. The mean CoP velocity (CoPVm) corresponding to the sum of the CoP displacement scalars divided by the sampling time and the Romberg's index (RI) [(surface EC / surface EO) × 100] evaluating the contribution of vision to maintaining posture [35] were also measured. The smaller the area and/or the lower the velocity, the better the performance [36].
3. Results 3.1. Temperature The time-of-day effect was significant (F(3.11) = 63.05; p b 0.001; Table 1) with post-hoc tests showing that the temperature improved significantly (p b 0.001) from 07:00 to 10:00 h and from 10.00 to 14.00 h. The temperature was significantly higher (p b 0.001) at 14:00 and 18:00 h compared to 07:00 and 10:00 h.
3.2. Posturographic assessments 2.5. Attentional capacities Attentional capacities were evaluated by a simple reaction time test. This test was measured using a “Superlab 4.5” program (Cedrus, San Pedro, USA). It measures the reaction time to visual stimuli. The subject sat 0.4 to 0.5 m in front of the computer screen. After 10 familiarization trials, each subject performed randomly and double-blinded 20 simple reaction time tests. The stimulus was a black square, presented for 50 ms at the center of the screen, preceded by a white square stimulus to direct the fixation. The interval between the appearances of two consecutive stimuli was randomized (average 1.5 s). After a training trial, the subject's task was to press a specific computer key as quickly as possible, using the favored hand, after the appearance of the black square. The score is established by evaluating the number of correct answers (correct response score) and the mean reaction time for the 20 trials (response time score). Reaction times of less than 150 ms and greater than 800 ms were excluded from analysis to avoid any effects from either anticipation or a temporary lapse of concentration. 2.6. Statistical analysis All statistical tests were processed using STATISTICA Software (StatSoft, France). The Shapiro–Wilk W-test of normality revealed that the data were normally distributed. The CoP data, the reaction time and the body temperature recorded during the four test sessions were analyzed by a one way repeated-measure analysis of variance (ANOVA) [4 time-of-day]. When significant differences were observed (p b 0.05), a post-hoc analysis was then performed with a Fisher–Snedecor least significant difference (LSD) test. Significance was set as p b 0.05.
The one-way ANOVA (4 time-of-day) showed a significant time-ofday effect (F(3.11) = 15.06, p b 0.001; Fig. 2) on the CoPArea. Post-hoc test revealed that the CoPArea decreased significantly (p b 0.001) from 07:00 to 10:00 h. The CoPArea increased significantly (p b 0.05) from 10:00 to 14:00 h. Then, it decreased significantly (p b 0.05) from 14:00 to 18:00 h. The CoPArea was significantly (p b 0.01) smaller at 14:00 compared to 07:00 h. However, no significant (p = 0.81) difference was observed between 10:00 and 18:00 h. The ANOVA indicated a significant time-of-day effect (F(3.11) = 5.99, p b 0.01; Fig. 3) on the CoPVm. Post-hoc analysis showed that the CoPVm decreased significantly (p b 0.001) from 07:00 to 10:00 h before increasing (p b 0.05) from 10:00 to 14:00 h. No significant differences were observed between 18:00 h and 10:00 h (p = 0.58) or 14:00 h (p = 0.11). However, the CoPVm was significantly (p b 0.01) lower at 18:00 compared to 07:00 h. For the LFS ratio, the ANOVA indicated a significant time-of-day effect (F(3.11) = 9.28, p b 0.001; Fig. 4). Post-hoc analysis revealed that the LFS ratio was significantly higher (p b 0.001) at 07:00 compared to 10:00 h. The LFS ratio increased significantly (p b 0.01) from 10:00 to 14:00 h, followed by a significant decrease (p b 0.01) at 18:00 h. No significant (p = 0.22) difference was observed between the LFS values recorded at 07:00 and those at 14:00 h. Similarly, the difference between the LFS values assessed at 10:00 and those at 18:00 h was not significant (p = 1.00). Concerning the RI, the ANOVA indicated a significant time-of-day effect (F(3.11) = 5.62, p b 0.01; Fig. 5). The post-hoc analysis showed that the contribution of vision to maintain posture was significantly more important at 10:00 h compared to 07:00 h (p b 0.01), 14:00 h (p b 0.01) and 18:00 h (p b 0.001).
Table 1 Mean values (±SD) of mean reaction time and oral temperature (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h.
Mean reaction time (S) M ± (SD) Oral temperature (°C) M ± (SD)
07:00 h
10:00 h
14:00 h
18:00 h
0.63 ± (0.036) 35.99 ± (0.19)
0.56 ± (0.046) 36.80 ± (0.21)
0.62 ± (0.052) 37.10 ± (0.27)
0.55 ± (0.047) 37.20 ± (0.26)
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151
Fig. 2. Mean values (±SD) of center of pressure area (CoPArea) (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h. *, **, ***: significant differences in comparison between test sessions at p b 0.05, p b 0.01 and p b 0.001, respectively. NS: non-significant difference between test sessions.
149
Fig. 4. Mean values (± SD) of LFS ratio (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h. **, ***: significant differences in comparison between test sessions at p b 0.01 and p b 0.001, respectively. NS: non-significant difference between test sessions.
The main purpose of the present study was (i) to explore the effect of time-of-day on postural control in 5–6-year-old children and (ii) to assess the diurnal fluctuations of the body temperature and of the attentional capacities to clarify the origins of any putative postural control fluctuations. Concerning postural control measurements, the results showed diurnal variations of the COPArea, the CoPVm, the LFS ratio and the RI. The oral temperature increases from morning to afternoon. Moreover, our results indicated that the reaction time was lower in the middle morning and in the late afternoon compared to the other times-of-day. Our results showed that the CoPArea and the CoPVm were high in the early morning (i.e., 07:00 h) in children. Similar findings were established in young adults [6,13,37]. In this context, it has been reported that the postural control was low between 05:00 and 08:00 h [11,16]. The LFS ratio in our children was high in the early morning indicating
high energy expenditure [34]. In contrast, in previous studies, adults spent less energy in the early morning [6]. At this time of day, our findings showed that the reaction time was high indicating low attentional capacities which corresponds to “the post-awakening phase” characterized by a transient hypovigilance, mood disorders and a momentary physical and mental performance degradation [38–40]. It was confirmed that the diurnal fluctuations of vigilance and intellectual performances resulted in the attention skill test variation [38,39]. Consequently, we suggested that the vigilance level in children was low at the early morning as reported for young adults [11–13]. Moreover, we found that the bathyphase of the body temperature rhythm in children was situated at the early morning, this result concurs with the findings of Reilly [17]. It has been established that the decrease of central body temperature may decrease nerve conduction velocity, joint suppleness, and muscle strength [41]. The postural control is a complex system consisting of a sensory part (vestibular-, somatosensory- and visual system), a processing part (central nervous system) and an effectuating part (spinal alpha-motor neurons and muscles) [20] which all possibly could be affected by either low attentional capacities and body temperature decrease in the early morning. At 10:00 h, the CoPArea, the CoPVm and the LFS ratio were lower compared to values assessed at 07:00 h. This result confirms that the postural control of children improves during the morning as reported in adults [11–13]. At this time of day, the reaction time decreased indicating better attentional capacities in the present study' participants. Similarly, an augmentation of vigilance level was reported after 9:00 h in young students with a maximum of intellectual capacities recorded in the middle morning [38,39]. Besides, our results confirm that the body temperature improves from 7:00 h to 10:00 h in children [17]. Around this time, a small peak for the muscular strength was previously highlighted
Fig. 3. Mean values (±SD) of center of pressure mean velocity (CoPVm) (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h. *, **, ***: significant differences in comparison between test sessions at p b 0.05, p b 0.01 and p b 0.001, respectively. NS: non-significant difference between test sessions.
Fig. 5. Mean values (±SD) of Romberg's index (n = 12) recorded at 07:00, 10:00, 14:00 and 18:00 h. **, ***: significant differences in comparison between test sessions at p b 0.01 and p b 0.001, respectively. NS: non-significant difference between test sessions.
3.3. Attentional capacities The one way ANOVA (4 time-of-day) revealed a significant time-ofday effect (F(3.11) = 17.54, p b 0.001; Table 1) on the reaction time. Posthoc analysis showed that the reaction time decreased significantly (p b 0.001) from 07:00 to 10:00 h before increasing (p b 0.001) at 14:00 h. The reaction time decreased significantly (p b 0.001) from 14:00 to 18:00 h. No significant (p = 0.80) difference between the reaction time values recorded at 10:00 and those at 18:00 h was observed. Similarly, no significant (p = 0.46) difference was revealed between the reaction time values recorded at 07:00 and those at 14:00 h.
4. Discussion
150
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151
[42]. Furthermore, our findings showed that the RI was better at 10:00 compared to 18:00 h indicating that the contribution of vision to maintaining posture [35] was more pronounced in the middle morning compared to the other test sessions. However, the RI was not influenced by the time of day in adults [6]. These controversies could be explained by the specificity of the age range of our subjects. In fact, it has been reported that the children prefer to rely on visual inputs more than other sensory information in achieving postural equilibrium [43,44]. Moreover, at this critical age of 5–6 years old, children seem to be learning how to integrate sensory information and how to calibrate sensory feedback for use in postural control [23]. At 14:00 h, the CoPArea, the CoPVm and the LFS values were higher compared to 10:00 h indicating a low postural control at this time despite the fact that the body temperature of children continues to increase from the early morning. Similarly, postural control was low at 13:00 h [18] and at 14:00 h [6] in adults. It seems that, despite increased energy expenditure [34], children were unable to improve their stability at this time-of-day. Besides, the reaction time assessed in our subjects was high at 14:00 h indicating a low attention level as reported in young students [38,39]. It has been reported that this time period corresponds to the post-lunch dip observed in the vigilance level [19]. Besides, in previous studies, performances for muscular power decreased at the post-lunch dip period [42]. At 18:00 h, the CoPArea and the LFS ratio were lower compared to values assessed at 14:00 h and the CoPVm was lower than at 07:00 h. These findings indicated a better postural control observed in the late afternoon in young children as established in young adults [6,11–13]. In contrast, it was reported that the older adults were less stable around this time [20]. The reaction time decreased from 14:00 to 18:00 h indicating an improvement of children's attentional capacities in the late afternoon. At this time, our results showed an important peak of the body temperature. Similarly, the optimum of the reaction time was observed at the early evening near the peak of the body temperature [9,10,38,39]. It has been found that performances for strength and power in children improved significantly from morning to the afternoon [45]. It was generally accepted that the diurnal increase in central body temperature could act as a passive warm-up that may increase nerve conduction velocity, joint suppleness, and muscle strength [41]. Thus, increased core temperature due to circadian patterns would facilitate enhancement of the neuromuscular and metabolic systems [46] which may improve the efficiency of postural muscle activity to control children's balance. It has been established that the cause of the child's diurnal variations of muscle power and fatigue during a short-term maximal performance was related to peripheral mechanisms [47] through an improvement of the muscle contractile properties at the end of the day as reported in young adults [48–50]. In the present study, children showed a better postural control at 10:00 and 18:00 h with no significant difference observed between these two times of day. However, it was reported that the postural control of young adults reaches a most important peak at 18:00 h [6]. Thus, despite the fact that the temperature and the muscular power were reported to be better at the end of the day [45,17], 5–6-year-old children controlled their balance at the middle morning similarly to the late afternoon. This finding may be related to the important attentional capacities indicating probably better sensory integration ability and to the better contribution of vision to maintaining posture revealed at 10:00 h in the present study' participants. Many scientific and clinical studies used the force plate measures to assess changes in postural control especially for the critical ages as children or older adults [51,52]. To limit contrasting findings, it was recommended to verify many variables such as heterogeneity of the group, small sample size, the presence of vestibular or visual disorder, or musculoskeletal or neurological diseases, history of injury in the past or regular training in sports. Recently, in older adults, it was suggested to control the time-of-day when subjects were tested because they were less stable in the late afternoon [18]. If the time of testing was not
controlled this would probably influence the results. Thus, by the present findings, we suggested that it will be better if we evaluate children's postural control in the middle morning or in the late afternoon and to avoid the post-awakening and the post-lunch phases. Moreover, based on our findings, the time-of-day should be taken into account when evaluating the postural control improvement after balance training intervention in children as it has been suggested in older adults [20]. 5. Limitations There were some limitations in this study that need to be considered when interpreting the findings. In the present study we measured the static postural control with and without elimination of visual inputs. Our results might be stronger if dynamic postural control had been examined as it could be more reliable to the daily activities. Moreover, the current study focused on the diurnal variations of postural control in 5–6-year-old children which is one of the critical stages of postural development. In further study we should compare different age ranges during childhood because the balance systems are not fully matured in young people until the age of 14 [53]. 6. Conclusion Children's postural control was low in the early morning and in the early afternoon and improved during the middle morning and in the late afternoon. The children's postural control fluctuates according to a diurnal rhythm (i.e., better postural control at 10:00 and 18:00 h) which is close to that of body temperature and/or attentional capacities. Therefore, clinicians could rely on these findings and may take into account the time-of-day when evaluating the children's postural control to avoid disparate results. Moreover, if balance training is recommended for 5–6-year-old children in order to prevent them from falls and injuries, it should be programmed at 10:00 h or 18:00 h when the postural control is better. Declaration of interest There is no financial conflict with the subject matter or materials discussed in this manuscript at any of the authors' academic institutions or employers. Finally, authors did not receive any financial interest. Acknowledgments We would like to thank Professor Dogui Mohamed, the head of the Laboratory of Physiology, Faculty of Medicine, Monastir — Tunisia, for collaboration and help. We also thank all the participants and their guardians. References [1] T. Reilly, J. Waterhouse, Chronobiologie and exercise, Med. Sport. 13 (2009) 54–60. [2] D. Hoyer, J. Clairambault, Rhythms from seconds to days. Physiological importance and therapeutic implications, IEEE Eng. Med. Biol. Mag. 26 (2007) 12–13. [3] C.M. Winget, C.W. DeRoshia, D.C. Holley, Circadian rhythms and athletic performance, Med. Sci. Sports Exerc. 17 (1985) 498–516. [4] J. Massion, Postural control system, Curr. Opin. Neurobiol. 4 (1994) 877–887. [5] Y. Ouchi, H. Okada, E. Yoshikawa, S. Nobezawa, M. Futatsubashi, Brain activation during maintenance of standing postures in humans, Brain 122 (1999) 329–338. [6] C. Bougard, M.C. Lepelley, D. Davenne, The influences of time-of-day and sleep deprivation on postural control, Exp. Brain Res. 209 (2011) 109–115. [7] M. Woollacott, A. Shumway-Cook, Attention and the control of posture and gait: a review of an emerging area of research, Gait Posture 16 (2002) 1–14. [8] M.S. Redfern, L. Yardley, A.M. Bronstein, Visual influences on balance, J. Anxiety Disord. 15 (2001) 81–94. [9] S. Jarraya, M. Jarraya, H. Chtourou, N. Souissi, Diurnal variations on cognitive performances in handball goalkeepers, Biol. Rhythm. Res. 45 (2013) 93–101. [10] S. Jarraya, M. Jarraya, H. Chtourou, N. Souissi, Effect of time of day and partial sleep deprivation on the reaction time and the attentional capacities of the handball goalkeeper, Biol. Rhythm. Res. 45 (2014) 183–191.
R. Baccouch et al. / Physiology & Behavior 142 (2015) 146–151 [11] N. Avni, I. Avni, E. Barenboim, B. Azaria, D. Zadok, R. Kohen-Raz, Y. Morad, Brief posturographic test as an indicator of fatigue, Psychiatry Clin. Neurosci. 60 (2006) 340–346. [12] P.A. Gribble, W.S. Tucker, P.A. White, Time-of-day influences on static and dynamic postural control, J. Athl. Train. 42 (2007) 35–41. [13] T. Nakano, K. Araki, A. Michimori, H. Inbe, H. Hagiwara, E. Koyama, Nineteen-hour variation of postural sway, alertness and rectal temperature during sleep deprivation, Psychiatry Clin. Neurosci. 55 (2001) 277–278. [14] N. Souissi, A. Zouita, H. Chtourou, H. Ferchichi, C. Dziri, S. Abedelmalek, N. Souissi, The effect of Ramadan intermittent fasting on dynamic postural control in judo athletes, Biol. Rhythm. Res. 45 (2013) 27–36. [15] N. Souissi, H. Chtourou, A. Zouita, C. Dziri, N. Souissi, Effects of Ramadan intermittent fasting on postural control in judo athletes, Biol. Rhythm. Res. 44 (2) (2013) 237–244. [16] Y. Morad, B. Azaria, I. Avni, Y. Barkana, D. Zadok, R. Kohen-Raz, E. Barenboim, Posturography as an indicator of fatigue due to sleep deprivation, Aviat. Space Environ. Med. 78 (2007) 859–863. [17] T. Reilly, Human circadian rhythms and exercise, Crit. Rev. Biomed. Eng. 18 (1990) 165–180. [18] P. Forsman, E. Haeggstrom, A. Wallin, E. Toppila, I. Pyykko, Daytime changes in postural stability and repeatability of posturographic measurements, J. Occup. Environ. Med. 49 (2007) 591–596. [19] M. Clodore, J. Foret, O. Benoit, Diurnal variation in subjective and objective measures of sleepiness: the effects of sleep reduction and circadian type, Chronobiol. Int. 3 (1986) 255–263. [20] M.G. Jorgensen, M.S. Rathleff, U. Laessoe, P. Caserotti, O.B.F. Nielsen, P. Aagaard, Timeof-day influences postural balance in older adults, Gait Posture 35 (2012) 653–657. [21] M.L. Peterson, E. Christou, K.S. Rosengren, Children achieve adult-like sensory integration during stance at 12-years-old, Gait Posture 23 (2006) 455–463. [22] A. Shumway-Cook, M. Woollacott, The growth of stability: postural control from a developmental perspective, J. Mot. Behav. 17 (1985) 131–147. [23] C. Riach, J. Starkes, Stability limits of quiet standing postural control in children and adults, Gait Posture 1 (1993) 105–111. [24] C. Riach, K. Hayes, Maturation of postural sway in young children, Dev. Med. Child Neurol. 29 (1987) 650–658. [25] C. Assaiante, S. Mallau, S. Viel, M. Jover, C. Schmitz, Development of postural control in healthy children: a functional approach, Neural Plast. 12 (2005) 109–118. [26] S. Sahli, S. Ghroubi, H. Rebai, M. Chaâbane, A. Yahia, D. Pérennou, M.H. Elleuch, The effect of circus activity training on postural control of 5–6-year-old children, Sci. Sports 28 (2013) 11–16. [27] C. Garcia, J. Barela, A. Viana, A. Barela, Influence of gymnastics training on the development of postural control, Neurosci. Lett. 492 (2011) 29–32. [28] G. Atkinson, A. Coldwells, T. Reilly, J.M. Waterhouse, A comparison of circadian rhythms in work performance between physically active and inactive subjects, Ergonomics 36 (1993) 273–281. [29] L. Torsvall, T. Åkerstedt, A diurnal type scale: construction, consistency and validation in shift work, Scand. J. Work Environ. Health 6 (1980) 283–290. [30] H. Takeuchi, M. Inoue, N. Watanabe, Y. Yamashita, M. Hamada, G. Kadota, T. Harada, Parental enforcement of bedtime during childhood results in Japanese junior high school students preferring morningness to eveningness, Chronobiol. Int. 18 (2001) 823–829. [31] T. Reilly, E. Bambaeichi, Methodological issues in studies of rhythms in human performance, Biol. Rhythm. Res. 34 (2003) 321–336.
151
[32] F. Asseman, O. Caron, J. Crémieux, Are there specific conditions for which expertise in gymnastics could have an effect on postural control and performance? Gait Posture 27 (2008) 76–81. [33] D.A. Winter, A.E. Patla, F. Prince, M. Ischac, F. Gielo-Perczak, Stiffness control of balance in quiet standing, J. Neurophysiol. 80 (1998) 1211–1221. [34] P.M. Gagey, B. Weber, Posturologie; Régulation et dérèglements de la station debout, Masson, Paris, 1999. [35] C.J. Njiokiktjien, J.A. van Parys, Romberg's sign expressed in a quotient. II. Pathology, Agressologie 17 (1976) 19–23. [36] O. Caron, T. Gelat, P. Rougier, J.P. Blanchi, A comparative analysis of the center of gravity of pressure trajectory path lengths in standing posture: an estimation of active stiffness, J. Appl. Biomech. 16 (2000) 234–247. [37] Y. Liu, S. Higuchi, Y. Motohashi, Changes in postural sway during a period of sustained wakefulness in male adults, Occup. Med. 51 (2001) 490–495. [38] F. Testu, Quelques constantes dans les fluctuations journalières et hebdomadaires de l'activité intellectuelle des élèves en Europe, Enfance (1994) 389–400. [39] F. Testu, Chronopsychologie et rythmes scolaires, Masson, Paris, 2000. [40] P.R. Jeanneret, W.B. Wilse, Strength of grip on arousal from a full night's sleep, Percept. Mot. Skills 17 (1963) 759–761. [41] L.D. Hayes, G.F. Bickerstaff, J.S. Baker, Interactions of cortisol, testosterone, and resistance training: influence of circadian rhythms, Chronobiol. Int. 27 (2010) 675–705. [42] G. Atkinson, T. Reilly, Circadian variation in sports performance, Sports Med. 21 (1996) 292–312. [43] V.L. Cumberworth, N.N. Patel, W. Rogers, The maturation of balance in children, J. Laryngol. Otol. 121 (2007) 449–454. [44] S. Hirabayashi, Y. Iwasaki, Developmental perspective of sensory organization on postural control, Brain Dev. 17 (1995) 111–113. [45] H. Souissi, A. Chaouachi, K. Chamari, M. Dogui, M. Amri, N. Souissi, Time-of-day effects on short-term exercise performances in 10–11-years-old boys, Pediatr. Exerc. Sci. 22 (2010) 613–623. [46] S. Racinais, Different effects of heat exposure upon exercise performance in the morning and afternoon, Scand. J. Med. Sci. Sports 20 (2010) 80–89. [47] H. Souissi, H. Chtourou, A. Chaouachi, K. Chamari, N. Souissi, M. Amri, Time-of-day effects on EMG parameters during the Wingate test in boys, J. Sports Sci. Med. 11 (2012) 380–386. [48] H. Chtourou, N. Zarrouk, A. Chaouachi, M. Dogui, D.G. Behm, K. Chamari, F. Hug, N. Souissi, Diurnal variation in Wingate-test performance and associated electromyographic parameters, Chronobiol. Int. 28 (2011) 706–713. [49] M. Guette, J. Gondin, A. Martin, Time-of-day effect on the torque and neuromuscular properties of dominant and nondominant quadriceps femoris, Chronobiol. Int. 22 (2005) 541–558. [50] A. Martin, A. Carpentier, N. Guissard, J. Van Hoecke, J. Duchateau, Effect of time of day on force variation in a human muscle, Muscle Nerve 22 (1999) 1380–1387. [51] L. Ajrezo, S. Wiener-Vacher, M.P. Bucci, Saccades improve postural control: a developmental study in normal children, PLoS ONE 8 (11) (2013) e81066. http:// dx.doi.org/10.1371/ journal.pone.0081066. [52] M. Moghadam, H. Ashayeri, M. Salavati, J. Sarafzadeh, K.D. Taghipoor, A. Saeedi, R. Salehi, Reliability of center of pressure measures of postural stability in healthy older adults: effects of postural task difficulty and cognitive load, Gait Posture 33 (2011) 651–655. [53] S.S. Fong, S.N. Fu, G.Y. Ng, Taekwondo training speeds up the development of balance and sensory functions in young adolescents, J. Sci. Med. Sport 15 (2012) 64–68.
