Neuroscience Letters 594 (2015) 93–98
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Research article
Postural control during transient floor translation while standing with the leg and trunk fixed Katsuo Fujiwara a,∗ , Naoe Kiyota b , Maki Maekawa a , Semen V. Prokopenko c , Abroskina M. Vasilyevna c a
Department of Human Movement and Health, Graduate School of Medical Science, Kanazawa University, 13-1 Takara-machi, Kanazawa 920-8640, Japan Department of Rehabilitation Science, Osaka Health Science University, 1-9-27 Temma, Kita-ku, Osaka 530-0043, Japan c Neurology Department, Krasnoyarsk State Medical Academy, Partizana Zheleznyaka d.1, Krasnoyarsk 660022, Russia b
h i g h l i g h t s • • • • •
We investigated CNV and postural muscle activity before floor translation with joint fixation. Postural adaptation to the disturbance with fixation occurred rapidly. CNV peak amplitude was increased with the adaptation. A high correlation was found between CNV peak and start times of triceps surae activity. Attention would be focused on the sensory information related to the triceps surae activity.
a r t i c l e
i n f o
Article history: Received 5 December 2014 Received in revised form 21 February 2015 Accepted 18 March 2015 Available online 19 March 2015 Keywords: Postural control Contingent negative variation Transient floor translation Postural muscle activity Joint fixation
a b s t r a c t Postural movement was restricted above the ankle, and contingent negative variation (CNV) and postural muscle activity were investigated during a transient floor translation (S2) 2 s after an auditory warning signal (S1). For 13 healthy young adults, the joints of the knee, hip, and trunk were fixed using a cast brace. Under no-fixation and fixation, a set of 10 translations was repeated at least 4 times, and center of pressure in the anteroposterior direction (CoPap), posterior postural muscle activity of the body (elector spinae (ES), biceps femoris (BF), gastrocnemius (GcM) and soleus (Sol)), and late CNV at Cz were analyzed in the initial two sets (initial set) and last two sets (late set). In the no-fixation, CoPap forward displacement after S2 gradually decreased. In the first trial of the fixation, it had significantly increased, and then rapidly decreased across subsequent trials. CNV peak amplitude was largest in the late set of the fixation. The activity of postural muscles increased just before S2 and in the late set the start time showed high correlations with CNV peak time in all muscles (ES (r = 0.88), BF (0.92), GcM (0.80), and Sol (0.89)) under the no-fixation, but exclusively in the GcM (0.84) and Sol (0.88) under the fixation. When postural control was restricted mainly to the ankle, attention would have been focused mainly on processing sensory information from the triceps surae just before the floor translation. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction To investigate dynamic postural control during standing, many researchers have used a transient floor translation task [1]. Anticipation of the disturbance and postural preparation for floor translation is an important factor in this task [2]. The frontal lobe, including the prefrontal cortex, supplementary motor area, premotor area, and primary motor area, is closely involved in these
∗ Corresponding author. Tel.: +81 76 265 2225; fax: +81 76 234 4219. E-mail address: [email protected] (K. Fujiwara). http://dx.doi.org/10.1016/j.neulet.2015.03.033 0304-3940/© 2015 Elsevier Ireland Ltd. All rights reserved.
functions [3], but the contribution of these regions to dynamic postural control remains incompletely understood. Therefore, we investigated the activation of these brain regions, measuring contingent negative variation (CNV) from a warning signal (S1) to a transient floor translation (S2) [4,5]. CNV is the negative slow potential obtained by averaging the electroencephalogram (EEG) recorded between S1 and S2 [6]. The late component of CNV reflects the motor preparation process and anticipatory attention directed to S2 [7,8]. Late CNV shows a peak just before S2, and it has been suggested that this CNV peak corresponds to a peak of anticipatory attention and/or onset of attentional shift to objects other than S2 [4,9].
94
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
Fig. 1. Experimental setup and waveforms.
The triceps surae (TS) is activated in response to a backward floor translation [1]. We have demonstrated that there is a continuous (about 400 ms duration) increase in TS activity from around the CNV peak to S2 or a transient (50–100 ms duration) increase around the time of the CNV peak followed by backward displacement of the center of pressure in the anteroposterior direction (CoPap) [4]. After adaptation to such floor translation, the onset time of the muscle activity increase changed to have a significant correlation with the CNV peak time, suggesting that the peak related to the attentional allocation to the sensory information from TS just before the disturbance [5,10]. However, there were inter-individual differences in postural muscle activity after the floor translation. For some subjects, activation was observed in the thigh and/or trunk muscles [1]. Also, just before S2, some subjects showed no increase in TS activity around the CNV peak. These findings suggest that sensory information from the trunk and thigh muscles might contribute to the preparation for the postural disturbance. Thus, we created a task condition in which postural control must be focused on TS, by the joint fixation above the ankle. After sufficient adaptation with the fixation, attention will be focused to TS, and thus, we will be able to demonstrate a close relation between the CNV peak time and the onset time of the preparatory activation of TS. Such joint fixation also allows many researchers to apply the inverted pendulum model with a single axis at the ankle [11]. In this study, a cast brace that immobilized the joints in the leg and trunk except the ankle joint was made for each subject, and the relation between CNV and postural muscle activity before postural disturbance was investigated. The following working hypotheses were tested: After sufficient adaptation to the postural disturbance with joint fixation; (1) postural control would be focused on TS, and (2) a high correlation would exist between the CNV peak time, and the onset time of the preparatory activation of TS.
2. Methods 2.1. Subjects Subjects were 13 healthy adults (7 men, 6 women). Mean (standard deviation (SD)) age, height, weight, and foot length (FL) were 22.4 (3.5) years, 164.3 (7.4) cm, 56.8 (6.6) kg, and 24.3 (1.1) cm, respectively. No subject had any history of neurological or orthopedic impairment. Informed consent was obtained from all subjects following an explanation of the experimental protocols, which were approved by our institutional ethics committee. 2.2. Apparatus and data recording A force platform (FPA34; Electro Design, Japan) was used to measure CoPap. The CoPap signals were sent simultaneously to one computer (PC9801BX2; NEC, Japan) to determine CoPap position online and to another computer for analysis offline. The former received CoPap data via an A/D converter (PIO9045; I/O-Data, Japan) at 20 Hz with 12 bit resolution and could generate a buzzer sound when CoPap was within ±1 cm of the required position. CoPap position was calculated as the percentage distance from the heel in relation to FL (%FL). The platform was fixed to a handmade table that was movable horizontally in an anteroposterior direction by a linear motion guide actuator (SKR4610A-0290-1-1001; THK, Japan) with a computer-controlled electric motor (SANMOTION MODEL No. PB PBBR604; SANYO DENKI, Japan). Direction, velocity, and amplitude of the platform movement were adjusted by the motor. S1 was an auditory stimulus delivered via earphones with a 2000 Hz frequency, 35 dB intensity above the threshold and 50 ms duration. S2 was a backward floor translation. Ag–AgCl cup electrodes (8 mm diameter) for recording EEG were placed on the scalp at Fz, Cz, and Pz in accordance with the international 10–20 system, and referenced to linked ear lobes.
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
A ground electrode was placed at Fpz. Electrooculography (EOG) was recorded from a pair of electrodes placed above and below the left eye. To fix eye position, subjects were instructed to gaze at a fixation point presented on an Eye-trek face-mounted display (FMD011F; Olympus, Japan). To record surface electromyography (EMG), electrodes (P-00-S; Ambu, Denmark) used in bipolar derivation were affixed along the long axis of the following muscles on the left side with an inter-electrode distance of about 3 cm: erector spinae (ES), biceps femoris (BF), medial head of gastrocnemius (GcM), and soleus (Sol). Electrode input impedance was 50 ms. When a CoPap backward shift was observed, the start of the transient increase in EMG activity just before the start of the CoPap shift was identified as same manner as the start of the continuous increase. The time difference between the start of the increase in EMG and S2 was defined as EMG start time before S2. The EMG waveforms after S2 were analyzed in the trials adopted for averaging. In each trial, the envelope line of the EMG burst that continued for at least 50 ms was identified. The time point at which the EMG burst deviated more than the mean +2 SD from the background activity measured in the standing posture before S1 was
96
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
defined as the burst onset of EMG, and the onset time was measured relative to S2. To analyze the burst activity level, the EMG waveform from 500 ms before to 1000 ms after burst onset was averaged over all trials within each condition. The mean amplitude in the 300 ms period before S1 was used as the baseline. The averaged waveforms were smoothed using a 40 Hz low-pass filter and then the peak was identified. The peak amplitude relative to the baseline was measured. 2.6. Statistical analysis Shapiro–Wilks and Levene’s tests confirmed that, all data satisfied the assumptions of normality and equal variance, respectively. To assess the change in CoPap displacement with repetition of trials, one-way repeated-measures analysis of variance (ANOVA) of trial was performed for each set. When a significant main effect of trial was shown, the difference between the first trial and each subsequent trial was evaluated by Dunnett’s one-to-many posthoc test. For the mean CoPap displacement, and variables related to CNV peak and EMG after S2, one-way ANOVA was used to assess the differences among 4 sets (initial and late sets under the nofixation and fixation). Post-hoc Tukey HSD test was performed in the case of a significant main effect of set. In addition, to assess the effect of joint fixation, a paired t-test was used to compare variables between the late set under the no-fixation and the initial set under the fixation, and between the final trial in the late set under the no-fixation and the first trial in the initial set under the fixation. Pearson’s correlation was used to assess the relation between CNV peak time and EMG start time before S2. The alpha level for all tests was set at P < 0.05. All statistical analyses were performed using SPSS 14.0J software (SPSS Japan, Japan). 3. Results In the initial set under both conditions, CoPap displacement decreased with trial repetitions (no-fixation: F12,228 = 1.81, fixation: F12,228 = 2.23, P < 0.05). Compared with the first trial, CoPap displacement was significantly decreased after the 9th trial and the 3rd trial under the no-fixation (P < 0.05) and the fixation (P < 0.05), respectively. In the late set under both conditions, no significant changes in CoPap displacement were found across trials. The CoPap displacement in the first trial under the fixation was significantly larger than that in the final trial under the no-fixation (t12 = 2.89, P < 0.05). Mean CoPap displacement in the initial set under the nofixation (38.9 (4.1) %FL) was significantly larger than in the late set under the no-fixation (35.7 (5.4) %FL) and both sets under the fixation (initial: 35.9 (5.9) %FL, late: 33.8 (6.6) %FL; F3,36 = 10.80, P < 0.001). Burst activity of postural muscles after S2 (Fig. 2) occurred in the following order: Sol, GcM, BF, ES. The burst onset time of ES and BF was significantly shorter in the fixation than in the no-fixation, regardless of set (P < 0.01), and that in GcM was significantly shorter in the initial set under the fixation than the late set under the nofixation (P < 0.05). In every condition, GcM showed the largest peak of burst activity among the muscles. ES peak amplitude was significantly lower in the late set under the fixation than in either set under the no-fixation (P < 0.01). CNV peak amplitude was significantly larger in the late set under the fixation (15.7 (6.0) V) than in each of the other 3 sets (nofixation: initial 10.3 (5.3) V; late 11.7 (4.7) V, fixation: initial 12.0 (6.9) V, F3,36 = 8.88, P < 0.001; Fig. 1C). CNV peak time was similar across all 4 sets (mean across all sets: −243.2 (170.3) ms). Around the CNV peak point, the following EMG activations were found: a continuous (about 400 ms duration) increase from around the CNV peak to S2 in the following subjects (no-fixation: initial 8; late 9,
Fig. 2. EMG burst activity after S2. * P < 0.05, ** P < 0.01, *** P < 0.001.
fixation: initial 9; late 12) or a transient (50–100 ms duration) increase followed by a backward displacement of CoPap (nofixation: initial 0; late 4, fixation: initial 1; late 1). The EMG start time before S2 was similar across all 4 sets (mean −302.2 (161.9) ms). The EMG increase slightly preceded the CNV peak (mean 70 ms), with no significant differences between them. In the late set under the no-fixation, a significant correlation between CNV peak time and EMG start time was found in the ES (r = 0.88), BF (0.92), GcM (0.80), and Sol (0.89) (all P < 0.05), and in the late set under the fixation, it was found in the GcM (0.84) and Sol (0.88) (both P < 0.05) (Fig. 3). There was no significant correlation between CNV peak time and EMG start time of any muscle in the initial set under either condition. 4. Discussion In the no-fixation, CoPap displacement gradually decreased with the repetition of backward floor translations, reached a plateau within the initial 20 translations, supporting a previous study of forward translation [5]. The CoPap displacement did not change in the late set. Next, the joints above the ankle were fixed by a cast brace. CoPap displacement increased just after the fixation, then rapidly decreased until the 3rd trial and plateaued. With regard to the postural muscle activity after the floor translation, GcM showed the largest peak of burst activity in both fixation conditions. Sol activation was the earliest and its burst peak did not change with fixation. The fixation had a remarkable effect on the activity of other muscles than TS. In ES, the burst peak amplitude
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
97
Fig. 3. Correlations between CNV peak time and EMG start time before S2.
was markedly decreased with the fixation and the onset time was shortened significantly. BF burst activity was the smallest out of all measured muscles, regardless of the fixation condition, which is possibly related to a locking mechanism of the knee. The onset time of the BF burst was significantly shortened by the fixation. With the joint fixation above the ankle, postural control would be more focused on TS. In all sets, both with and without fixation, late CNV negatively peaked before S2, then started to decline. The CNV peak amplitude significantly increased with adaptation to the fixation. It has been suggested that the late CNV peak corresponds to a peak of anticipatory attention or motor preparation and/or the onset of
attentional shift to objects other than S2 [9]. The late CNV was reportedly increased in a task where attention had to be directed to S2 [14] or with sufficient adaptation to the disturbance [5]. Especially in late sets, there was either a continuous increase of EMG activity from around the CNV peak to S2 or a transient increase of EMG activity around the CNV peak followed by backward displacement of the CoPap. In the no-fixation, these EMG increases were found in either TS, ES or BF, while in the fixation, those were mainly observed only in TS. The continuous and transient EMG activities would relate to the increase of muscle stiffness against the disturbance (the passive torque in the inverted pendulum model) and the control of standing position to moderate the influence of
98
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
disturbance (the active torque), respectively [11]. A significant correlation between the CNV peak time and the EMG start time was observed in all muscles with the no-fixation, but exclusively in TS with the fixation. The EMG increase slightly preceded the CNV peak by about 70 ms. Quant et al. reported that a negative peak of EEG approximately 100 ms after transient floor translation related to the processing of sensory information associated with the perturbation [15]. The present study demonstrates that without the fixation, attention was partially dispersed to processing the sensory information related to different joints and postural muscles, but with the fixation, attention could be focused on those related to the activation of TS. 5. Conclusion Postural adaptation to the backward floor translation with fixation of the knee, hip and trunk occurred rapidly. After the adaptation, the onset time of the increase in TS activity just before S2 showed a high correlation with CNV peak time. We propose that, attention was strongly directed to processing sensory information related to the activation of TS just before the postural disturbance. Acknowledgement This work was supported by Grant-in-Aid for Scientific Research (B) (23300238). References [1] F.B. Horak, L.M. Nashner, Central programming of postural movements: adaptation to altered support-surface configurations, J. Neurophysiol. 55 (1986) 1369–1381.
[2] F.B. Horak, H.C. Diener, L.M. Nashner, Influence of central set on human postural responses, J. Neurophysiol. 62 (1989) 841–853. [3] M. Mihara, I. Miyai, M. Hatakenaka, K. Kubota, S. Sakoda, Role of the prefrontal cortex in human balance control, Neuroimage 43 (2008) 329–336. [4] K. Fujiwara, N. Kiyota, K. Maeda, Contingent negative variation and activation of postural preparation before postural perturbation by backward floor translation at different initial standing positions, Neurosci. Lett. 490 (2011) 135–139. [5] K. Fujiwara, M. Maekawa, N. Kiyota, C. Yaguchi, Adaptation changes in dynamic postural control and contingent negative variation during backward disturbance by transient floor translation in the elderly, J. Physiol. Anthropol. 31 (2012) 12. [6] W.G. Walter, R. Cooper, V.J. Aldridge, W.C. Mccallum, A.L. Winter, Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain, Nature 25 (1964) 380–384. [7] J.W. Rohrbaugh, K. Syndulko, D.B. Lindsley, Brain wave components of the contingent negative variation in humans, Science 191 (1976) 1055–1057. [8] C.H. Brunia, G.J. van Boxtel, Wait and see, Int. J. Psychophysiol. 43 (2001) 59–75. [9] F. Macar, F. Vidal, Time processing reflected by EEG surface Laplacians, Exp. Brain Res. 145 (2002) 403–406. [10] M. Maekawa, K. Fujiwara, N. Kiyota, C. Yaguchi, Adaptation changes in dynamic postural control and contingent negative variation during repeated transient forward translation in the elderly, J. Physiol. Anthropol. 32 (2013) 24. [11] P.G. Morasso, M. Schieppati, Can muscle stiffness alone stabilize upright standing? J. Neurophysiol. 82 (1999) 1622–1626. [12] T. Kiyota, K. Fujiwara, H. Toyama, N. Kiyota, K. Kunita, K. Maeda, M. Katayama, Determination of disturbance parameters of forward floor translation for balance training to prevent falling, Health Behav. Sci. 8 (2009) 9–16. [13] J.J. Tecce, Contingent negative variation (CNV) and psychological processes in man, Psychol. Bull. 77 (1972) 73–108. [14] M.J. Wright, G.M. Geffen, L.B. Geffen, Event related potentials during covert orientation of visual attention: effects of cue validity and directionality, Biol. Psychol. 41 (1995) 183–202. [15] S. Quant, A.L. Adkin, W.R. Staines, B.E. Maki, W.E. McIlroy, The effect of a concurrent cognitive task on cortical potentials evoked by unpredictable balance perturbations, BMC Neurosci. 17 (2004) 5–18.
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Research article
Postural control during transient floor translation while standing with the leg and trunk fixed Katsuo Fujiwara a,∗ , Naoe Kiyota b , Maki Maekawa a , Semen V. Prokopenko c , Abroskina M. Vasilyevna c a
Department of Human Movement and Health, Graduate School of Medical Science, Kanazawa University, 13-1 Takara-machi, Kanazawa 920-8640, Japan Department of Rehabilitation Science, Osaka Health Science University, 1-9-27 Temma, Kita-ku, Osaka 530-0043, Japan c Neurology Department, Krasnoyarsk State Medical Academy, Partizana Zheleznyaka d.1, Krasnoyarsk 660022, Russia b
h i g h l i g h t s • • • • •
We investigated CNV and postural muscle activity before floor translation with joint fixation. Postural adaptation to the disturbance with fixation occurred rapidly. CNV peak amplitude was increased with the adaptation. A high correlation was found between CNV peak and start times of triceps surae activity. Attention would be focused on the sensory information related to the triceps surae activity.
a r t i c l e
i n f o
Article history: Received 5 December 2014 Received in revised form 21 February 2015 Accepted 18 March 2015 Available online 19 March 2015 Keywords: Postural control Contingent negative variation Transient floor translation Postural muscle activity Joint fixation
a b s t r a c t Postural movement was restricted above the ankle, and contingent negative variation (CNV) and postural muscle activity were investigated during a transient floor translation (S2) 2 s after an auditory warning signal (S1). For 13 healthy young adults, the joints of the knee, hip, and trunk were fixed using a cast brace. Under no-fixation and fixation, a set of 10 translations was repeated at least 4 times, and center of pressure in the anteroposterior direction (CoPap), posterior postural muscle activity of the body (elector spinae (ES), biceps femoris (BF), gastrocnemius (GcM) and soleus (Sol)), and late CNV at Cz were analyzed in the initial two sets (initial set) and last two sets (late set). In the no-fixation, CoPap forward displacement after S2 gradually decreased. In the first trial of the fixation, it had significantly increased, and then rapidly decreased across subsequent trials. CNV peak amplitude was largest in the late set of the fixation. The activity of postural muscles increased just before S2 and in the late set the start time showed high correlations with CNV peak time in all muscles (ES (r = 0.88), BF (0.92), GcM (0.80), and Sol (0.89)) under the no-fixation, but exclusively in the GcM (0.84) and Sol (0.88) under the fixation. When postural control was restricted mainly to the ankle, attention would have been focused mainly on processing sensory information from the triceps surae just before the floor translation. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction To investigate dynamic postural control during standing, many researchers have used a transient floor translation task [1]. Anticipation of the disturbance and postural preparation for floor translation is an important factor in this task [2]. The frontal lobe, including the prefrontal cortex, supplementary motor area, premotor area, and primary motor area, is closely involved in these
∗ Corresponding author. Tel.: +81 76 265 2225; fax: +81 76 234 4219. E-mail address: [email protected] (K. Fujiwara). http://dx.doi.org/10.1016/j.neulet.2015.03.033 0304-3940/© 2015 Elsevier Ireland Ltd. All rights reserved.
functions [3], but the contribution of these regions to dynamic postural control remains incompletely understood. Therefore, we investigated the activation of these brain regions, measuring contingent negative variation (CNV) from a warning signal (S1) to a transient floor translation (S2) [4,5]. CNV is the negative slow potential obtained by averaging the electroencephalogram (EEG) recorded between S1 and S2 [6]. The late component of CNV reflects the motor preparation process and anticipatory attention directed to S2 [7,8]. Late CNV shows a peak just before S2, and it has been suggested that this CNV peak corresponds to a peak of anticipatory attention and/or onset of attentional shift to objects other than S2 [4,9].
94
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
Fig. 1. Experimental setup and waveforms.
The triceps surae (TS) is activated in response to a backward floor translation [1]. We have demonstrated that there is a continuous (about 400 ms duration) increase in TS activity from around the CNV peak to S2 or a transient (50–100 ms duration) increase around the time of the CNV peak followed by backward displacement of the center of pressure in the anteroposterior direction (CoPap) [4]. After adaptation to such floor translation, the onset time of the muscle activity increase changed to have a significant correlation with the CNV peak time, suggesting that the peak related to the attentional allocation to the sensory information from TS just before the disturbance [5,10]. However, there were inter-individual differences in postural muscle activity after the floor translation. For some subjects, activation was observed in the thigh and/or trunk muscles [1]. Also, just before S2, some subjects showed no increase in TS activity around the CNV peak. These findings suggest that sensory information from the trunk and thigh muscles might contribute to the preparation for the postural disturbance. Thus, we created a task condition in which postural control must be focused on TS, by the joint fixation above the ankle. After sufficient adaptation with the fixation, attention will be focused to TS, and thus, we will be able to demonstrate a close relation between the CNV peak time and the onset time of the preparatory activation of TS. Such joint fixation also allows many researchers to apply the inverted pendulum model with a single axis at the ankle [11]. In this study, a cast brace that immobilized the joints in the leg and trunk except the ankle joint was made for each subject, and the relation between CNV and postural muscle activity before postural disturbance was investigated. The following working hypotheses were tested: After sufficient adaptation to the postural disturbance with joint fixation; (1) postural control would be focused on TS, and (2) a high correlation would exist between the CNV peak time, and the onset time of the preparatory activation of TS.
2. Methods 2.1. Subjects Subjects were 13 healthy adults (7 men, 6 women). Mean (standard deviation (SD)) age, height, weight, and foot length (FL) were 22.4 (3.5) years, 164.3 (7.4) cm, 56.8 (6.6) kg, and 24.3 (1.1) cm, respectively. No subject had any history of neurological or orthopedic impairment. Informed consent was obtained from all subjects following an explanation of the experimental protocols, which were approved by our institutional ethics committee. 2.2. Apparatus and data recording A force platform (FPA34; Electro Design, Japan) was used to measure CoPap. The CoPap signals were sent simultaneously to one computer (PC9801BX2; NEC, Japan) to determine CoPap position online and to another computer for analysis offline. The former received CoPap data via an A/D converter (PIO9045; I/O-Data, Japan) at 20 Hz with 12 bit resolution and could generate a buzzer sound when CoPap was within ±1 cm of the required position. CoPap position was calculated as the percentage distance from the heel in relation to FL (%FL). The platform was fixed to a handmade table that was movable horizontally in an anteroposterior direction by a linear motion guide actuator (SKR4610A-0290-1-1001; THK, Japan) with a computer-controlled electric motor (SANMOTION MODEL No. PB PBBR604; SANYO DENKI, Japan). Direction, velocity, and amplitude of the platform movement were adjusted by the motor. S1 was an auditory stimulus delivered via earphones with a 2000 Hz frequency, 35 dB intensity above the threshold and 50 ms duration. S2 was a backward floor translation. Ag–AgCl cup electrodes (8 mm diameter) for recording EEG were placed on the scalp at Fz, Cz, and Pz in accordance with the international 10–20 system, and referenced to linked ear lobes.
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
A ground electrode was placed at Fpz. Electrooculography (EOG) was recorded from a pair of electrodes placed above and below the left eye. To fix eye position, subjects were instructed to gaze at a fixation point presented on an Eye-trek face-mounted display (FMD011F; Olympus, Japan). To record surface electromyography (EMG), electrodes (P-00-S; Ambu, Denmark) used in bipolar derivation were affixed along the long axis of the following muscles on the left side with an inter-electrode distance of about 3 cm: erector spinae (ES), biceps femoris (BF), medial head of gastrocnemius (GcM), and soleus (Sol). Electrode input impedance was 50 ms. When a CoPap backward shift was observed, the start of the transient increase in EMG activity just before the start of the CoPap shift was identified as same manner as the start of the continuous increase. The time difference between the start of the increase in EMG and S2 was defined as EMG start time before S2. The EMG waveforms after S2 were analyzed in the trials adopted for averaging. In each trial, the envelope line of the EMG burst that continued for at least 50 ms was identified. The time point at which the EMG burst deviated more than the mean +2 SD from the background activity measured in the standing posture before S1 was
96
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
defined as the burst onset of EMG, and the onset time was measured relative to S2. To analyze the burst activity level, the EMG waveform from 500 ms before to 1000 ms after burst onset was averaged over all trials within each condition. The mean amplitude in the 300 ms period before S1 was used as the baseline. The averaged waveforms were smoothed using a 40 Hz low-pass filter and then the peak was identified. The peak amplitude relative to the baseline was measured. 2.6. Statistical analysis Shapiro–Wilks and Levene’s tests confirmed that, all data satisfied the assumptions of normality and equal variance, respectively. To assess the change in CoPap displacement with repetition of trials, one-way repeated-measures analysis of variance (ANOVA) of trial was performed for each set. When a significant main effect of trial was shown, the difference between the first trial and each subsequent trial was evaluated by Dunnett’s one-to-many posthoc test. For the mean CoPap displacement, and variables related to CNV peak and EMG after S2, one-way ANOVA was used to assess the differences among 4 sets (initial and late sets under the nofixation and fixation). Post-hoc Tukey HSD test was performed in the case of a significant main effect of set. In addition, to assess the effect of joint fixation, a paired t-test was used to compare variables between the late set under the no-fixation and the initial set under the fixation, and between the final trial in the late set under the no-fixation and the first trial in the initial set under the fixation. Pearson’s correlation was used to assess the relation between CNV peak time and EMG start time before S2. The alpha level for all tests was set at P < 0.05. All statistical analyses were performed using SPSS 14.0J software (SPSS Japan, Japan). 3. Results In the initial set under both conditions, CoPap displacement decreased with trial repetitions (no-fixation: F12,228 = 1.81, fixation: F12,228 = 2.23, P < 0.05). Compared with the first trial, CoPap displacement was significantly decreased after the 9th trial and the 3rd trial under the no-fixation (P < 0.05) and the fixation (P < 0.05), respectively. In the late set under both conditions, no significant changes in CoPap displacement were found across trials. The CoPap displacement in the first trial under the fixation was significantly larger than that in the final trial under the no-fixation (t12 = 2.89, P < 0.05). Mean CoPap displacement in the initial set under the nofixation (38.9 (4.1) %FL) was significantly larger than in the late set under the no-fixation (35.7 (5.4) %FL) and both sets under the fixation (initial: 35.9 (5.9) %FL, late: 33.8 (6.6) %FL; F3,36 = 10.80, P < 0.001). Burst activity of postural muscles after S2 (Fig. 2) occurred in the following order: Sol, GcM, BF, ES. The burst onset time of ES and BF was significantly shorter in the fixation than in the no-fixation, regardless of set (P < 0.01), and that in GcM was significantly shorter in the initial set under the fixation than the late set under the nofixation (P < 0.05). In every condition, GcM showed the largest peak of burst activity among the muscles. ES peak amplitude was significantly lower in the late set under the fixation than in either set under the no-fixation (P < 0.01). CNV peak amplitude was significantly larger in the late set under the fixation (15.7 (6.0) V) than in each of the other 3 sets (nofixation: initial 10.3 (5.3) V; late 11.7 (4.7) V, fixation: initial 12.0 (6.9) V, F3,36 = 8.88, P < 0.001; Fig. 1C). CNV peak time was similar across all 4 sets (mean across all sets: −243.2 (170.3) ms). Around the CNV peak point, the following EMG activations were found: a continuous (about 400 ms duration) increase from around the CNV peak to S2 in the following subjects (no-fixation: initial 8; late 9,
Fig. 2. EMG burst activity after S2. * P < 0.05, ** P < 0.01, *** P < 0.001.
fixation: initial 9; late 12) or a transient (50–100 ms duration) increase followed by a backward displacement of CoPap (nofixation: initial 0; late 4, fixation: initial 1; late 1). The EMG start time before S2 was similar across all 4 sets (mean −302.2 (161.9) ms). The EMG increase slightly preceded the CNV peak (mean 70 ms), with no significant differences between them. In the late set under the no-fixation, a significant correlation between CNV peak time and EMG start time was found in the ES (r = 0.88), BF (0.92), GcM (0.80), and Sol (0.89) (all P < 0.05), and in the late set under the fixation, it was found in the GcM (0.84) and Sol (0.88) (both P < 0.05) (Fig. 3). There was no significant correlation between CNV peak time and EMG start time of any muscle in the initial set under either condition. 4. Discussion In the no-fixation, CoPap displacement gradually decreased with the repetition of backward floor translations, reached a plateau within the initial 20 translations, supporting a previous study of forward translation [5]. The CoPap displacement did not change in the late set. Next, the joints above the ankle were fixed by a cast brace. CoPap displacement increased just after the fixation, then rapidly decreased until the 3rd trial and plateaued. With regard to the postural muscle activity after the floor translation, GcM showed the largest peak of burst activity in both fixation conditions. Sol activation was the earliest and its burst peak did not change with fixation. The fixation had a remarkable effect on the activity of other muscles than TS. In ES, the burst peak amplitude
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
97
Fig. 3. Correlations between CNV peak time and EMG start time before S2.
was markedly decreased with the fixation and the onset time was shortened significantly. BF burst activity was the smallest out of all measured muscles, regardless of the fixation condition, which is possibly related to a locking mechanism of the knee. The onset time of the BF burst was significantly shortened by the fixation. With the joint fixation above the ankle, postural control would be more focused on TS. In all sets, both with and without fixation, late CNV negatively peaked before S2, then started to decline. The CNV peak amplitude significantly increased with adaptation to the fixation. It has been suggested that the late CNV peak corresponds to a peak of anticipatory attention or motor preparation and/or the onset of
attentional shift to objects other than S2 [9]. The late CNV was reportedly increased in a task where attention had to be directed to S2 [14] or with sufficient adaptation to the disturbance [5]. Especially in late sets, there was either a continuous increase of EMG activity from around the CNV peak to S2 or a transient increase of EMG activity around the CNV peak followed by backward displacement of the CoPap. In the no-fixation, these EMG increases were found in either TS, ES or BF, while in the fixation, those were mainly observed only in TS. The continuous and transient EMG activities would relate to the increase of muscle stiffness against the disturbance (the passive torque in the inverted pendulum model) and the control of standing position to moderate the influence of
98
K. Fujiwara et al. / Neuroscience Letters 594 (2015) 93–98
disturbance (the active torque), respectively [11]. A significant correlation between the CNV peak time and the EMG start time was observed in all muscles with the no-fixation, but exclusively in TS with the fixation. The EMG increase slightly preceded the CNV peak by about 70 ms. Quant et al. reported that a negative peak of EEG approximately 100 ms after transient floor translation related to the processing of sensory information associated with the perturbation [15]. The present study demonstrates that without the fixation, attention was partially dispersed to processing the sensory information related to different joints and postural muscles, but with the fixation, attention could be focused on those related to the activation of TS. 5. Conclusion Postural adaptation to the backward floor translation with fixation of the knee, hip and trunk occurred rapidly. After the adaptation, the onset time of the increase in TS activity just before S2 showed a high correlation with CNV peak time. We propose that, attention was strongly directed to processing sensory information related to the activation of TS just before the postural disturbance. Acknowledgement This work was supported by Grant-in-Aid for Scientific Research (B) (23300238). References [1] F.B. Horak, L.M. Nashner, Central programming of postural movements: adaptation to altered support-surface configurations, J. Neurophysiol. 55 (1986) 1369–1381.
[2] F.B. Horak, H.C. Diener, L.M. Nashner, Influence of central set on human postural responses, J. Neurophysiol. 62 (1989) 841–853. [3] M. Mihara, I. Miyai, M. Hatakenaka, K. Kubota, S. Sakoda, Role of the prefrontal cortex in human balance control, Neuroimage 43 (2008) 329–336. [4] K. Fujiwara, N. Kiyota, K. Maeda, Contingent negative variation and activation of postural preparation before postural perturbation by backward floor translation at different initial standing positions, Neurosci. Lett. 490 (2011) 135–139. [5] K. Fujiwara, M. Maekawa, N. Kiyota, C. Yaguchi, Adaptation changes in dynamic postural control and contingent negative variation during backward disturbance by transient floor translation in the elderly, J. Physiol. Anthropol. 31 (2012) 12. [6] W.G. Walter, R. Cooper, V.J. Aldridge, W.C. Mccallum, A.L. Winter, Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain, Nature 25 (1964) 380–384. [7] J.W. Rohrbaugh, K. Syndulko, D.B. Lindsley, Brain wave components of the contingent negative variation in humans, Science 191 (1976) 1055–1057. [8] C.H. Brunia, G.J. van Boxtel, Wait and see, Int. J. Psychophysiol. 43 (2001) 59–75. [9] F. Macar, F. Vidal, Time processing reflected by EEG surface Laplacians, Exp. Brain Res. 145 (2002) 403–406. [10] M. Maekawa, K. Fujiwara, N. Kiyota, C. Yaguchi, Adaptation changes in dynamic postural control and contingent negative variation during repeated transient forward translation in the elderly, J. Physiol. Anthropol. 32 (2013) 24. [11] P.G. Morasso, M. Schieppati, Can muscle stiffness alone stabilize upright standing? J. Neurophysiol. 82 (1999) 1622–1626. [12] T. Kiyota, K. Fujiwara, H. Toyama, N. Kiyota, K. Kunita, K. Maeda, M. Katayama, Determination of disturbance parameters of forward floor translation for balance training to prevent falling, Health Behav. Sci. 8 (2009) 9–16. [13] J.J. Tecce, Contingent negative variation (CNV) and psychological processes in man, Psychol. Bull. 77 (1972) 73–108. [14] M.J. Wright, G.M. Geffen, L.B. Geffen, Event related potentials during covert orientation of visual attention: effects of cue validity and directionality, Biol. Psychol. 41 (1995) 183–202. [15] S. Quant, A.L. Adkin, W.R. Staines, B.E. Maki, W.E. McIlroy, The effect of a concurrent cognitive task on cortical potentials evoked by unpredictable balance perturbations, BMC Neurosci. 17 (2004) 5–18.
