Motor Control, 2015, 19, 242 -249 http://dx.doi.org/10.1123/mc.2013-0104 © 2015 Human Kinetics, Inc.
research note
Spinal Reflexes During Postural Control Under Psychological Pressure Yoshifumi Tanaka Mukogawa Women’s University This study investigated the effect of psychological pressure on spinal reflex excitability. Thirteen participants performed a balancing task by standing on a balance disk with one foot. After six practice trials, they performed one nonpressure and one pressure trial involving a performance-contingent cash reward or punishment. Stress responses were successfully induced; state anxiety, mental effort, and heart rates all increased under pressure. Soleus Hoffmann reflex amplitude in the pressure trial was significantly smaller than in the nonpressure trial. This modification of spinal reflexes may be caused by presynaptic inhibition under the control of higher central nerve excitation under pressure. This change did not prevent 12 of the 13 participants from successfully completing the postural control task under pressure. These results suggest that Hoffmann reflex inhibition would contribute to optimal postural control under stressful situations. Keywords: balance, electromyography, Hoffmann reflex, stress
During sports competition, athletes have to demonstrate optimal performance under changing conditions that involve the impact of a number of psychological factors. Psychological pressure is a major factor that can impair performance, such that many athletes strive to overcome its negative effects. Recent studies have examined motor control functions and behavior under pressure to clarify mechanisms underlying such performance changes in psychological pressure situations. Neuronal excitability in the efferent pathways from the primary motor area to the innervated muscles has been examined by recording motor evoked potentials (MEPs) in the muscle, which are elicited by monophasic transcranial magnetic stimulation (TMS) of the primary motor area. In these studies, increased amplitude of MEP (i.e., higher corticospinal excitability) were observed during (Tanaka, Funase, Sekiya, & Murayama, 2012; Tanaka, Funase, Sekiya, Sasaki, & Takemoto, 2011) or after (Rollnik, Schubert, & Dengler, 2000) participants performed voluntary hand movements under pressure evoked using monetary incentives or competition. The central nervous system can be divided into higher (cortical, subcortical, and brainstem) and lower (spinal) levels. Previous studies have focused on the cortical level and little is known about how spinal mechanisms operate under pressure. It is The author is with the Department of Health and Sports Sciences, Mukogawa Women’s University, Hyogo, Japan. Address author correspondence to Yoshifumi Tanaka at [email protected]. 242
Spinal Reflexes During Postural Control 243
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therefore necessary to investigate motor neuron activity via the spinal cord under pressure. Given the aforementioned background, the current study examined the effect of psychological pressure on spinal reflex activity by evoking the Hoffmann reflex (H-reflex) from the soleus muscle during a postural task. It has been reported that reduced H-reflex amplitude occurs along with several cognitive demands, such as postural anxiety by being on a high place (Sibley, Carpenter, Perry, & Frank, 2007), high levels of task difficulty (Hoffman & Koceja, 1995), and demands for accurate task performance (McIlroy, Bishop, Staines, Nelson, Maki, & Brooke, 2003). It is therefore reasonable to expect that reduced H-reflex amplitude will be observed in association with the increased cognitive demand associated with attentional and affective changes under pressure in this study.
Methods Participants Thirteen healthy male university students (mean age = 20.5, standard deviation = 2.1) participated in this study. Only males were tested to avoid the potential complications that could arise if a male experimenter were to attach surface electrodes to a female participant. Dominant leg according to participant self-report was the right for all participants. Informed consent was obtained from all participants before their participation in the study. The local ethics committee approved the experiment.
Task Each participant performed a balancing task, standing on a balance disk (28 cm diameter, 11 cm height) with only their dominant leg. For each trial, participants were requested to stabilize their posture on the board for 20 s. If the left leg or another body part touched a wall or the floor, the trial was deemed to be a “failure” trial. I classified the trial as a “success” in cases of postural maintenance on the board for 20 s. The participants were asked to fixate on a dot (2.5 cm diameter) on 21-inch display while performing the balancing task, so that gaze behavior did not influence task performance. The center of the display was at a 110 cm height from the floor, and 90 cm away from the participant.
Induction and Recording of Physiological Indices EMGs for the right soleus (SOL) and tibialis anterior (TA) were amplified and extracted using Ag-AgCl bipolar surface electrodes. Recordings were made with a sampling frequency of 2000 Hz and a bandwidth of 10–2000 Hz (Power Laboratory 26T, Chart 7 for Windows, AD Instruments Pty. Ltd., Castle Hill, Australia). For electrical stimulation of the right tibial nerve, a circular cathodal stimulating electrode (6 mm diameter) was attached over a suitable spot at the right popliteal fossa. A rectangular anodal electrode (8 cm2 area) was placed over the skin of the right patella. M- and H-waves were obtained by applying a square wave of 1 ms duration at a rate of 1 Hz to the right tibial nerve (SS-104j, Nihon Kohden, Tokyo, Japan). Both anodal and cathodal electrodes were fixed using a rubber band to maintain stimulus stability during the trial. Heart rate (HR) was measured using MC Vol. 19, No. 3, 2015
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244 Tanaka
a transmitter attached to each participant’s chest (CE0537 N2965, Polar Electro, Finland) and wireless receiver placed in front of participant (MLAC35/ST, Polar Electro, Finland). The maximum amplitude of the SOL motor response (Mmax) and SOL H-reflex (Hmax) were measured keeping the knee angle at approximately 90 ° by sitting a comfortable chair before the beginning of the experimental trial. The mean electrical intensities for all participants to induce Mmax and Hmax were 89.15 V (range 67–131 V) and 61.9 V (range 35–84 V) respectively. Mean peak-to-peak Mmax and Hmax amplitudes for all participants were 15.53 mV (range 6.21–28.57 mV) and 6.19 mV (range 2.8–14.5 mV). Administered electrical intensities during the experimental trials were determined such that H-reflex amplitude reached approximately 50% of each participant’s Hmax (cf., Hoffman & Koceja, 1995; McIloy et al., 2003). Mean intensity across all participants was 56.0 V (range 32–75 V).
Procedure Participants performed six practice trials to familiarize themselves with the postural maintenance task. The electrical stimulus for the tibial nerve was administered during the latter four practice trials so that participants could familiarize themselves with the task of keeping their posture stable in the presence of perturbation by stimulus administrations. Following the practice trials, participants received two more experimental trials, one nonpressure and one pressure trial. Intertrial intervals were one minute for the practice trials and two minutes between the nonpressure and pressure trials. The order of the nonpressure and pressure trials was counterbalanced across participants to mitigate a possible order effect. In this study, a combination of psychological stressors in the form of rewards and punishments was used to induce relatively strong stress responses in participants. Similarly in the current study, participants received 1000 JPY (about 10 USD) before the pressure trial as a reward for participation in the experiment. The following instruction was given before the pressure trial: “I will give you an extra 1000 JPY if you succeed at postural maintenance during this trial. However, if you fail this trial, you will have to return the 1000 JPY.” During the nonpressure trial, participants were instructed to perform the task as well as possible, with no pressure induction provided. All participants were debriefed after the experiment and informed that the instruction about returning the cash reward was false. To determine the psychological effects of the pressure manipulation, subjective state anxiety and mental effort required to perform the task were measured using a Visual Analog Scale (VAS: Cella & Perry, 1986) before each nonpressure and pressure trial.
Data Analysis Eighteen electrical stimulations were administrated during each trial. In terms of M-wave and H-wave activity for each stimulus, peak-to-peak amplitudes were calculated and mean amplitudes for 18 stimuli in each trial were calculated for each participant. In addition, RMSs for background EMGs (bEMG) of both muscles were calculated for the 40 ms duration before the electrical stimulus was applied (Hoffman & Koceja, 1995). Paired t tests were used to analyze mean subjective state anxiety and mental effort scores, HR, and EMG variables for nonpressure MC Vol. 19, No. 3, 2015
Spinal Reflexes During Postural Control 245
and pressure trials. The significance level for all analyses was set at a p-value of less than 5% (two-tailed).
Results Pressure Manipulation Check
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Table 1 shows the means and standard errors for all dependent variables in the nonpressure and pressure trials. T test results indicated that there were significant increases in state anxiety (t (12) = 4.24, p = .001), mental effort (t (12) = 2.96, p = .012), and HR (t (12) = 4.57, p = .001) from the nonpressure to the pressure trials.
M- and H-waves Figure 1 illustrates arithmetic mean M and H waveforms for each trial recorded from one participant. A t-test showed that H-wave amplitude decreased significantly from the nonpressure to pressure trials (t (12) = 2.31, p = .040) although M-wave Table 1 Means and Standard Errors of All Dependent Variables in the Nonpressure Trial and the Pressure Trial
Nonpressure
Pressure
Subjective state anxiety (mm)
45.54 ± 7.80
76.62 ± 7.75**
Mental effort (mm)
68.39 ± 6.99
87.77 ± 5.15*
Heart rate (bpm)
88.90 ± 4.81
110.04 ± 8.14**
1.48 ± .56
1.70 ± .71
M-wave amplitude (mV) H-wave amplitude (mV)
3.73 ± .50
3.16 ± .44*
Soleus bEMG (μV)
81.6 5± 5.75
86.48 ± 6.82
Tibialis anterior bEMG (μV)
85.23 ±12.87
94.48 ±10.84
** p < .01, * p < .05
Figure 1 — Typical arithmetic waveforms during the nonpressure (dashed line) and pressure trial (solid line) recorded from one participant. His H-reflex amplitude of SOL decreased 23.68% from the nonpressure to the pressure trial. MC Vol. 19, No. 3, 2015
246 Tanaka
amplitude showed no significant changes (t (12) = .94, p = .364). There were no significant between trial differences for SOL bEMG (t (12) = .89, p = .391), and this also held true for TA (t (12) = .89, p = .392). All participants successfully maintained their balance for 20 s during the nonpressure trial. Twelve of the thirteen participants successfully completed the pressure trial.
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Discussion Psychological pressure was induced in the current study using rewards and punishments for performance of a postural maintenance balance task. Subjective state anxiety, mental effort, and HR were assessed to investigate the effects of added pressure on psychological and physiological domains. These variables all increased in the pressure trial relative to the nonpressure trial. These results indicate that the pressure manipulation used in this study induced both psychological and physiological stress responses in participants, and that the manipulation of added pressure was therefore effective. The prediction that spinal reflex excitability would be inhibited under pressure was also supported, as mean H-reflex amplitude for the SOL showed a 15.3% reduction from the nonpressure to the pressure trials. In the current study, the order of the nonpressure and pressure trials was counterbalanced across participants. Therefore, it might be possible that the final nonpressure trial of participants that performed the pressure trial first (n = 6) was affected by the prior exposure to stress. However, the H-reflex amplitudes of these participants from pressure (mean = 3.15, standard error = .62 mV) to nonpressure trials (mean = 3.99, standard error = .97 mV) had a trend similar to participants (n = 7) that performed the nonpressure trial first (mean = 3.51, standard error = .50 mV) followed by the pressure trial (mean = 3.16, standard error = .66 mV). This suggests that the preceding pressure exposure did not affect the H-reflex in the subsequent nonpressure condition. No significant difference was shown for M-wave amplitude, indicating that stimulus stability was maintained during the experiment and motor unit activation from the motor neuron pool of the SOL muscle was at same level for nonpressure and pressure trials. In addition, postsynaptic activation and reciprocal inhibition would not relate to the reduced H-reflex excitability in this study, given that there were no significant differences between trials for bEMG of the SOL and TA. Therefore, it would be reasonable to consider that another neural mechanism is related to changes in H-reflex excitability under pressure. Reduced H-reflex excitability under the pressure manipulation used in this study might have been caused by presynaptic inhibition. It has been reported that the presynaptic inhibition is related to the modulation mechanism of the H-reflex (Capaday & Stein, 1986). Because other mechanisms such as vestibular inputs (Knikou & Rymer, 2002) could modify the H-reflex, it remains possible that these functions might contribute to H-reflex changes under pressure. Furthermore, it has been found that tendon reflex excitability via muscle spindle activation increased association with postural threat (Horslen, Murnaghan, Inglis, Chua, & Carpenter, 2013) and unpleasant emotionality (Bonnet, Bradley, Lang, & Requin, 1995; Both, Everaerd, & Laan, 2003). Although H-reflex excitability is likely to be independent from tendon reflex (Horslen et al.), in future research it would be useful to evaluate spinal reflex mechanisms under pressure, including the tendon reflex. MC Vol. 19, No. 3, 2015
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Spinal Reflexes During Postural Control 247
Previous MEP recording studies that examined corticospinal excitability via the TMS technique have found increased corticospinal excitability under pressure (Rollnik et al., 2000; Tanaka et al., 2012). These results taken together with the present findings suggest that higher central nervous system (CNS) control, with a focus on the primary motor area, would be facilitated under pressure whereas lower-level motor neuron excitability in the spinal cord would be inhibited under pressure. McIlroy et al. (2003) found increased somatosensory evoked potential (SEP) in combination with H-reflex inhibition when people were asked to perform a motor task as accurately as possible. Weaver, Janzen, Adkin, and Tokuno (2012) showed that cognitive demand produced by a dual-task involving quickly responding to auditory cues inhibited H-reflex amplitude only when participants maintained a standing posture. Such H-reflex inhibition was not observed when they maintained a lying posture. Furthermore, it has been observed that some cognitive demands such as postural anxiety (Sibley et al., 2007) and task difficulty (Hoffman & Koceja, 1995) cause H-reflex inhibition. Cognitive demand should increase under the pressure manipulation used in this study because of the reward-punishment motivated drive to succeed, thereby shifting the motor control system to higher CNS control with consequent inhibition of spinal reflex excitability. In short, it would appear that higher CNS control by stress responses under pressure led to spinal reflex inhibition, although spinal reflex excitability would be more involved in maintaining postural control under nonstressful circumstances. Previous studies also show that the H-reflex of expert ballet dancers was smaller relative to athletes who practice other sports (Nielsen, Crone, & Hultborn, 1993) as well as nonathletes (Koceja, Burke, & Kamen, 1991). These previous results suggest that inhibited plastic changes of the spinal reflex function as profit modification for the ability of fine postural control of the lower limbs in ballet dancers. In addition, it is known that balance training leads to H-reflex inhibition through improvement in postural stability (Mynark & Koceja, 2002; Trimble & Koceja, 1994). Accordingly, it is possible that the reduced H-reflex excitability under pressure observed in the current study represent adaptive neural changes to aid postural control during task performance. This study is the first to provide evidence that reduced H-reflex response during a postural maintenance task performed under psychological pressure. Finally, some points concerning the limitations of this study and some implications for future research should be mentioned. The first limitation is that motor neuron activity in higher central nervous system was not measured in the current study. Future studies should investigate both higher and lower central nervous systems in an intraexperiment by recording MEP inducted by TMS on the primary motor area, in combination with measuring spinal reflex excitability. The second limitation is that different types of stressors (i.e., reward and punishment) were used simultaneously during the pressure trial to induce greater stress responses for participants. It therefore remains unclear whether reward and/or punishment caused H-reflex inhibition during the pressure trial. For both human and animal behavior, it has been reported that reward and punishment function on the basis of different higher central nervous system mechanisms (e.g., Kobayashi, Nomoto, Watanabe, Hikosaka, Schultz, & Sakagami, 2006; Schultz, 2000). Reward and punishment should be separated in future investigations of motor control and behavior under pressure. Third, there might be the possibility of fatigue from standing on the disk with one MC Vol. 19, No. 3, 2015
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foot, receiving electrical stimulations at a rate of per one second. Furthermore, there might be a habituation effect of the electrical stimulus over the course of six practice and two test trials (i.e., one nonpressure trial and one pressure trial). Future research needs to consider the possibility of fatigue or habituation effects of the task and electrical stimuli to obtain more elaborate physiological data. Furthermore, it is necessary to evaluate postural control performance in detail, given that the performance index measured in this study was relatively crude, within the context of recording only task success or failure. The possibility that changes in postural control under pressure can influence spinal reflex activity cannot be denied. For example, self-reports of perceived changes in movements during a postural task could be coupled with recordings of other behavioral indices of postural control, such as center of pressure and kinematics. To exclude the effects of such postural control modifications on spinal reflex excitability, H-reflex could be measured via another muscle not involved in postural control (i.e., the flexor carpi radialis), with consideration of interlimb neural communication (Domingo, Klimstra, Nakajima, Lam, & Hundza, 2014). Acknowledgments This work was supported by a Grant-in-Aid for Young Scientists (b) from Japan Society for the Promotion of Science (JSPS) KAKENHI (No. 23700761) and a Research Grants from the University of Fukui.
References Bonnet, M., Bradley, M.M., Lang, P.J., & Requin, J. (1995). Modulation of spinal reflexes: Arousal, pleasure, action. Psychophysiology, 32, 367–372. PubMed doi:10.1111/j.1469-8986.1995.tb01219.x Both, S., Everaerd, W., & Laan, E. (2003). Modulation of spinal reflexes by aversive and sexually appetitive stimuli. Psychophysiology, 40, 174–183. PubMed doi:10.1111/14698986.00019 Capaday, C., & Stein, R.B. (1986). Amplitude modulation of the soleus H-reflex in the human during walking and standing. The Journal of Neuroscience, 6, 1308–1313. PubMed Cella, D.F., & Perry, S.W. (1986). Reliability and concurrent validity of three visualanalogue mood scale. Psychological Reports, 59, 827–833. PubMed doi:10.2466/ pr0.1986.59.2.827 Domingo, A., Klimstra, M., Nakajima, T., Lam, T., & Hundza, S.R. (2014). Walking phase modulates H-reflex amplitude in flexor carpi radialis. Journal of Motor Behavior, 46, 49–57. PubMed doi:10.1080/00222895.2013.854731 Hoffman, M.A., & Koceja, D.M. (1995). The effects of vision and task complexity on Hoffmann reflex gain. Brain Research, 700, 303–307. PubMed doi:10.1016/00068993(95)01082-7 Horslen, B.C., Murnaghan, C.D., Inglis, J.T., Chua, R., & Carpenter, M.G. (2013). Effects of postural threat on spinal stretch reflexes: evidence for increased muscle spindle sensitivity. Journal of Neurophysiology, 110, 899–906. PubMed doi:10.1152/jn.00065.2013 Knikou, M., & Rymer, W.Z. (2002). Effects of changes in hip joint angle on H-reflex excitability in humans. Experimental Brain Research, 143, 149–159. PubMed doi:10.1007/ s00221-001-0978-4 Kobayashi, S., Nomoto, K., Watanabe, M., Hikosaka, O., Schultz, W., & Sakagami, M. (2006). Influences of rewarding and aversive outcomes on activity in macaque latMC Vol. 19, No. 3, 2015
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eral prefrontal cortex. Neuron, 51, 861–870. PubMed doi:10.1016/j.neuron.2006. 08.031 Koceja, D.M., Burke, J.R., & Kamen, G. (1991). Organization of segmental reflexes in trained dancers. International Journal of Sports Medicine, 12, 285–289. PubMed doi:10.1055/s-2007-1024682 McIlroy, W.E., Bishop, D.C., Staines, W.R., Nelson, A.J., Maki, B.E., & Brooke, J.D. (2003). Modulation of afferent inflow during the control of balancing tasks using the lower limbs. Brain Research, 961, 73–80. PubMed doi:10.1016/S0006-8993(02)03845-3 Mynark, R.G., & Koceja, D.M. (2002). Down training of the elderly soleus H reflex with the use of a spinally induced balance perturbation. Journal of Applied Physiology, 93, 127–133. PubMed doi:10.1152/japplphysiol.00007.2001 Nielsen, J., Crone, C., & Hultborn, H. (1993). H-reflexes are smaller in dancers from The Royal Danish Ballet than in well-trained athletes. European Journal of Applied Physiology and Occupational Physiology, 66, 116–121. PubMed doi:10.1007/BF01427051 Rollnik, J.D., Schubert, M., & Dengler, R. (2000). Effects of a competitive stressor on motor cortex excitability: a pilot study. Stress Medicine, 16, 49–54. doi:10.1002/(SICI)10991700(200001)16:13.0.CO;2-E Schultz, W. (2000). Multiple reward signals in the brain. Nature Reviews. Neuroscience, 1, 199–207. PubMed doi:10.1038/35044563 Sibley, K.M., Carpenter, M.G., Perry, J.C., & Frank, J.S. (2007). Effects of postural anxiety on the soleus H-reflex. Human Movement Science, 26, 103–112. PubMed doi:10.1016/j. humov.2006.09.004 Tanaka, Y., Funase, K., Sekiya, H., & Murayama, T. (2012). Modulation of corticospinal motor tract excitability during a fine finger movement under psychological pressure: A TMS study. International Journal of Sport and Health Science, 10, 39–49. doi:10.5432/ ijshs.201131 Tanaka, Y., Funase, K., Sekiya, H., Sasaki, J., & Takemoto, T. (2011). Multiple EMG activity and intracortical inhibition and facilitation during a fine finger movement under pressure. Journal of Motor Behavior, 43, 73–81. PubMed doi:10.1080/00222895.2010.542508 Trimble, M.H., & Koceja, D.M. (1994). Modulation of the triceps surae H-reflex with training. The International Journal of Neuroscience, 76, 293–303. PubMed doi:10.3109/00207459408986011 Weaver, T.B., Janzen, M.R., Adkin, A.L., & Tokuno, C.D. (2012). Changes in spinal excitability during dual task performance. Journal of Motor Behavior, 44, 289–294. PubMed doi:10.1080/00222895.2012.702142
MC Vol. 19, No. 3, 2015
research note
Spinal Reflexes During Postural Control Under Psychological Pressure Yoshifumi Tanaka Mukogawa Women’s University This study investigated the effect of psychological pressure on spinal reflex excitability. Thirteen participants performed a balancing task by standing on a balance disk with one foot. After six practice trials, they performed one nonpressure and one pressure trial involving a performance-contingent cash reward or punishment. Stress responses were successfully induced; state anxiety, mental effort, and heart rates all increased under pressure. Soleus Hoffmann reflex amplitude in the pressure trial was significantly smaller than in the nonpressure trial. This modification of spinal reflexes may be caused by presynaptic inhibition under the control of higher central nerve excitation under pressure. This change did not prevent 12 of the 13 participants from successfully completing the postural control task under pressure. These results suggest that Hoffmann reflex inhibition would contribute to optimal postural control under stressful situations. Keywords: balance, electromyography, Hoffmann reflex, stress
During sports competition, athletes have to demonstrate optimal performance under changing conditions that involve the impact of a number of psychological factors. Psychological pressure is a major factor that can impair performance, such that many athletes strive to overcome its negative effects. Recent studies have examined motor control functions and behavior under pressure to clarify mechanisms underlying such performance changes in psychological pressure situations. Neuronal excitability in the efferent pathways from the primary motor area to the innervated muscles has been examined by recording motor evoked potentials (MEPs) in the muscle, which are elicited by monophasic transcranial magnetic stimulation (TMS) of the primary motor area. In these studies, increased amplitude of MEP (i.e., higher corticospinal excitability) were observed during (Tanaka, Funase, Sekiya, & Murayama, 2012; Tanaka, Funase, Sekiya, Sasaki, & Takemoto, 2011) or after (Rollnik, Schubert, & Dengler, 2000) participants performed voluntary hand movements under pressure evoked using monetary incentives or competition. The central nervous system can be divided into higher (cortical, subcortical, and brainstem) and lower (spinal) levels. Previous studies have focused on the cortical level and little is known about how spinal mechanisms operate under pressure. It is The author is with the Department of Health and Sports Sciences, Mukogawa Women’s University, Hyogo, Japan. Address author correspondence to Yoshifumi Tanaka at [email protected]. 242
Spinal Reflexes During Postural Control 243
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therefore necessary to investigate motor neuron activity via the spinal cord under pressure. Given the aforementioned background, the current study examined the effect of psychological pressure on spinal reflex activity by evoking the Hoffmann reflex (H-reflex) from the soleus muscle during a postural task. It has been reported that reduced H-reflex amplitude occurs along with several cognitive demands, such as postural anxiety by being on a high place (Sibley, Carpenter, Perry, & Frank, 2007), high levels of task difficulty (Hoffman & Koceja, 1995), and demands for accurate task performance (McIlroy, Bishop, Staines, Nelson, Maki, & Brooke, 2003). It is therefore reasonable to expect that reduced H-reflex amplitude will be observed in association with the increased cognitive demand associated with attentional and affective changes under pressure in this study.
Methods Participants Thirteen healthy male university students (mean age = 20.5, standard deviation = 2.1) participated in this study. Only males were tested to avoid the potential complications that could arise if a male experimenter were to attach surface electrodes to a female participant. Dominant leg according to participant self-report was the right for all participants. Informed consent was obtained from all participants before their participation in the study. The local ethics committee approved the experiment.
Task Each participant performed a balancing task, standing on a balance disk (28 cm diameter, 11 cm height) with only their dominant leg. For each trial, participants were requested to stabilize their posture on the board for 20 s. If the left leg or another body part touched a wall or the floor, the trial was deemed to be a “failure” trial. I classified the trial as a “success” in cases of postural maintenance on the board for 20 s. The participants were asked to fixate on a dot (2.5 cm diameter) on 21-inch display while performing the balancing task, so that gaze behavior did not influence task performance. The center of the display was at a 110 cm height from the floor, and 90 cm away from the participant.
Induction and Recording of Physiological Indices EMGs for the right soleus (SOL) and tibialis anterior (TA) were amplified and extracted using Ag-AgCl bipolar surface electrodes. Recordings were made with a sampling frequency of 2000 Hz and a bandwidth of 10–2000 Hz (Power Laboratory 26T, Chart 7 for Windows, AD Instruments Pty. Ltd., Castle Hill, Australia). For electrical stimulation of the right tibial nerve, a circular cathodal stimulating electrode (6 mm diameter) was attached over a suitable spot at the right popliteal fossa. A rectangular anodal electrode (8 cm2 area) was placed over the skin of the right patella. M- and H-waves were obtained by applying a square wave of 1 ms duration at a rate of 1 Hz to the right tibial nerve (SS-104j, Nihon Kohden, Tokyo, Japan). Both anodal and cathodal electrodes were fixed using a rubber band to maintain stimulus stability during the trial. Heart rate (HR) was measured using MC Vol. 19, No. 3, 2015
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244 Tanaka
a transmitter attached to each participant’s chest (CE0537 N2965, Polar Electro, Finland) and wireless receiver placed in front of participant (MLAC35/ST, Polar Electro, Finland). The maximum amplitude of the SOL motor response (Mmax) and SOL H-reflex (Hmax) were measured keeping the knee angle at approximately 90 ° by sitting a comfortable chair before the beginning of the experimental trial. The mean electrical intensities for all participants to induce Mmax and Hmax were 89.15 V (range 67–131 V) and 61.9 V (range 35–84 V) respectively. Mean peak-to-peak Mmax and Hmax amplitudes for all participants were 15.53 mV (range 6.21–28.57 mV) and 6.19 mV (range 2.8–14.5 mV). Administered electrical intensities during the experimental trials were determined such that H-reflex amplitude reached approximately 50% of each participant’s Hmax (cf., Hoffman & Koceja, 1995; McIloy et al., 2003). Mean intensity across all participants was 56.0 V (range 32–75 V).
Procedure Participants performed six practice trials to familiarize themselves with the postural maintenance task. The electrical stimulus for the tibial nerve was administered during the latter four practice trials so that participants could familiarize themselves with the task of keeping their posture stable in the presence of perturbation by stimulus administrations. Following the practice trials, participants received two more experimental trials, one nonpressure and one pressure trial. Intertrial intervals were one minute for the practice trials and two minutes between the nonpressure and pressure trials. The order of the nonpressure and pressure trials was counterbalanced across participants to mitigate a possible order effect. In this study, a combination of psychological stressors in the form of rewards and punishments was used to induce relatively strong stress responses in participants. Similarly in the current study, participants received 1000 JPY (about 10 USD) before the pressure trial as a reward for participation in the experiment. The following instruction was given before the pressure trial: “I will give you an extra 1000 JPY if you succeed at postural maintenance during this trial. However, if you fail this trial, you will have to return the 1000 JPY.” During the nonpressure trial, participants were instructed to perform the task as well as possible, with no pressure induction provided. All participants were debriefed after the experiment and informed that the instruction about returning the cash reward was false. To determine the psychological effects of the pressure manipulation, subjective state anxiety and mental effort required to perform the task were measured using a Visual Analog Scale (VAS: Cella & Perry, 1986) before each nonpressure and pressure trial.
Data Analysis Eighteen electrical stimulations were administrated during each trial. In terms of M-wave and H-wave activity for each stimulus, peak-to-peak amplitudes were calculated and mean amplitudes for 18 stimuli in each trial were calculated for each participant. In addition, RMSs for background EMGs (bEMG) of both muscles were calculated for the 40 ms duration before the electrical stimulus was applied (Hoffman & Koceja, 1995). Paired t tests were used to analyze mean subjective state anxiety and mental effort scores, HR, and EMG variables for nonpressure MC Vol. 19, No. 3, 2015
Spinal Reflexes During Postural Control 245
and pressure trials. The significance level for all analyses was set at a p-value of less than 5% (two-tailed).
Results Pressure Manipulation Check
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Table 1 shows the means and standard errors for all dependent variables in the nonpressure and pressure trials. T test results indicated that there were significant increases in state anxiety (t (12) = 4.24, p = .001), mental effort (t (12) = 2.96, p = .012), and HR (t (12) = 4.57, p = .001) from the nonpressure to the pressure trials.
M- and H-waves Figure 1 illustrates arithmetic mean M and H waveforms for each trial recorded from one participant. A t-test showed that H-wave amplitude decreased significantly from the nonpressure to pressure trials (t (12) = 2.31, p = .040) although M-wave Table 1 Means and Standard Errors of All Dependent Variables in the Nonpressure Trial and the Pressure Trial
Nonpressure
Pressure
Subjective state anxiety (mm)
45.54 ± 7.80
76.62 ± 7.75**
Mental effort (mm)
68.39 ± 6.99
87.77 ± 5.15*
Heart rate (bpm)
88.90 ± 4.81
110.04 ± 8.14**
1.48 ± .56
1.70 ± .71
M-wave amplitude (mV) H-wave amplitude (mV)
3.73 ± .50
3.16 ± .44*
Soleus bEMG (μV)
81.6 5± 5.75
86.48 ± 6.82
Tibialis anterior bEMG (μV)
85.23 ±12.87
94.48 ±10.84
** p < .01, * p < .05
Figure 1 — Typical arithmetic waveforms during the nonpressure (dashed line) and pressure trial (solid line) recorded from one participant. His H-reflex amplitude of SOL decreased 23.68% from the nonpressure to the pressure trial. MC Vol. 19, No. 3, 2015
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amplitude showed no significant changes (t (12) = .94, p = .364). There were no significant between trial differences for SOL bEMG (t (12) = .89, p = .391), and this also held true for TA (t (12) = .89, p = .392). All participants successfully maintained their balance for 20 s during the nonpressure trial. Twelve of the thirteen participants successfully completed the pressure trial.
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Discussion Psychological pressure was induced in the current study using rewards and punishments for performance of a postural maintenance balance task. Subjective state anxiety, mental effort, and HR were assessed to investigate the effects of added pressure on psychological and physiological domains. These variables all increased in the pressure trial relative to the nonpressure trial. These results indicate that the pressure manipulation used in this study induced both psychological and physiological stress responses in participants, and that the manipulation of added pressure was therefore effective. The prediction that spinal reflex excitability would be inhibited under pressure was also supported, as mean H-reflex amplitude for the SOL showed a 15.3% reduction from the nonpressure to the pressure trials. In the current study, the order of the nonpressure and pressure trials was counterbalanced across participants. Therefore, it might be possible that the final nonpressure trial of participants that performed the pressure trial first (n = 6) was affected by the prior exposure to stress. However, the H-reflex amplitudes of these participants from pressure (mean = 3.15, standard error = .62 mV) to nonpressure trials (mean = 3.99, standard error = .97 mV) had a trend similar to participants (n = 7) that performed the nonpressure trial first (mean = 3.51, standard error = .50 mV) followed by the pressure trial (mean = 3.16, standard error = .66 mV). This suggests that the preceding pressure exposure did not affect the H-reflex in the subsequent nonpressure condition. No significant difference was shown for M-wave amplitude, indicating that stimulus stability was maintained during the experiment and motor unit activation from the motor neuron pool of the SOL muscle was at same level for nonpressure and pressure trials. In addition, postsynaptic activation and reciprocal inhibition would not relate to the reduced H-reflex excitability in this study, given that there were no significant differences between trials for bEMG of the SOL and TA. Therefore, it would be reasonable to consider that another neural mechanism is related to changes in H-reflex excitability under pressure. Reduced H-reflex excitability under the pressure manipulation used in this study might have been caused by presynaptic inhibition. It has been reported that the presynaptic inhibition is related to the modulation mechanism of the H-reflex (Capaday & Stein, 1986). Because other mechanisms such as vestibular inputs (Knikou & Rymer, 2002) could modify the H-reflex, it remains possible that these functions might contribute to H-reflex changes under pressure. Furthermore, it has been found that tendon reflex excitability via muscle spindle activation increased association with postural threat (Horslen, Murnaghan, Inglis, Chua, & Carpenter, 2013) and unpleasant emotionality (Bonnet, Bradley, Lang, & Requin, 1995; Both, Everaerd, & Laan, 2003). Although H-reflex excitability is likely to be independent from tendon reflex (Horslen et al.), in future research it would be useful to evaluate spinal reflex mechanisms under pressure, including the tendon reflex. MC Vol. 19, No. 3, 2015
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Previous MEP recording studies that examined corticospinal excitability via the TMS technique have found increased corticospinal excitability under pressure (Rollnik et al., 2000; Tanaka et al., 2012). These results taken together with the present findings suggest that higher central nervous system (CNS) control, with a focus on the primary motor area, would be facilitated under pressure whereas lower-level motor neuron excitability in the spinal cord would be inhibited under pressure. McIlroy et al. (2003) found increased somatosensory evoked potential (SEP) in combination with H-reflex inhibition when people were asked to perform a motor task as accurately as possible. Weaver, Janzen, Adkin, and Tokuno (2012) showed that cognitive demand produced by a dual-task involving quickly responding to auditory cues inhibited H-reflex amplitude only when participants maintained a standing posture. Such H-reflex inhibition was not observed when they maintained a lying posture. Furthermore, it has been observed that some cognitive demands such as postural anxiety (Sibley et al., 2007) and task difficulty (Hoffman & Koceja, 1995) cause H-reflex inhibition. Cognitive demand should increase under the pressure manipulation used in this study because of the reward-punishment motivated drive to succeed, thereby shifting the motor control system to higher CNS control with consequent inhibition of spinal reflex excitability. In short, it would appear that higher CNS control by stress responses under pressure led to spinal reflex inhibition, although spinal reflex excitability would be more involved in maintaining postural control under nonstressful circumstances. Previous studies also show that the H-reflex of expert ballet dancers was smaller relative to athletes who practice other sports (Nielsen, Crone, & Hultborn, 1993) as well as nonathletes (Koceja, Burke, & Kamen, 1991). These previous results suggest that inhibited plastic changes of the spinal reflex function as profit modification for the ability of fine postural control of the lower limbs in ballet dancers. In addition, it is known that balance training leads to H-reflex inhibition through improvement in postural stability (Mynark & Koceja, 2002; Trimble & Koceja, 1994). Accordingly, it is possible that the reduced H-reflex excitability under pressure observed in the current study represent adaptive neural changes to aid postural control during task performance. This study is the first to provide evidence that reduced H-reflex response during a postural maintenance task performed under psychological pressure. Finally, some points concerning the limitations of this study and some implications for future research should be mentioned. The first limitation is that motor neuron activity in higher central nervous system was not measured in the current study. Future studies should investigate both higher and lower central nervous systems in an intraexperiment by recording MEP inducted by TMS on the primary motor area, in combination with measuring spinal reflex excitability. The second limitation is that different types of stressors (i.e., reward and punishment) were used simultaneously during the pressure trial to induce greater stress responses for participants. It therefore remains unclear whether reward and/or punishment caused H-reflex inhibition during the pressure trial. For both human and animal behavior, it has been reported that reward and punishment function on the basis of different higher central nervous system mechanisms (e.g., Kobayashi, Nomoto, Watanabe, Hikosaka, Schultz, & Sakagami, 2006; Schultz, 2000). Reward and punishment should be separated in future investigations of motor control and behavior under pressure. Third, there might be the possibility of fatigue from standing on the disk with one MC Vol. 19, No. 3, 2015
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foot, receiving electrical stimulations at a rate of per one second. Furthermore, there might be a habituation effect of the electrical stimulus over the course of six practice and two test trials (i.e., one nonpressure trial and one pressure trial). Future research needs to consider the possibility of fatigue or habituation effects of the task and electrical stimuli to obtain more elaborate physiological data. Furthermore, it is necessary to evaluate postural control performance in detail, given that the performance index measured in this study was relatively crude, within the context of recording only task success or failure. The possibility that changes in postural control under pressure can influence spinal reflex activity cannot be denied. For example, self-reports of perceived changes in movements during a postural task could be coupled with recordings of other behavioral indices of postural control, such as center of pressure and kinematics. To exclude the effects of such postural control modifications on spinal reflex excitability, H-reflex could be measured via another muscle not involved in postural control (i.e., the flexor carpi radialis), with consideration of interlimb neural communication (Domingo, Klimstra, Nakajima, Lam, & Hundza, 2014). Acknowledgments This work was supported by a Grant-in-Aid for Young Scientists (b) from Japan Society for the Promotion of Science (JSPS) KAKENHI (No. 23700761) and a Research Grants from the University of Fukui.
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