Journal of Electromyography and Kinesiology

Transcription

1 Journal of Electromyography and Kinesiology 20 (2010) Contents lists available at ScienceDirect Journal of Electromyography and Kinesiology journal homepage: Role of vision and task complexity on soleus H-reflex gain Salih Pinar a,b, *, Koichi Kitano b, David M. Koceja b a Marmara University, School of Physical Education and Sports, Anadoluhisari, Istanbul, Turkey b Department of Kinesiology and Program in Neuroscience, Motor Control Laboratory, Indiana University, Bloomington-IN, USA article info abstract Article history: Received 23 July 2008 Received in revised form 5 March 2009 Accepted 5 March 2009 Keywords: Reflex Modulation Stance Vision There exists extensive evidence supporting the presence of reflex modulation in humans during a variety of motor tasks. The soleus H-reflex has been shown to be modulated during static and dynamic balance conditions as well as during various motor tasks. The purpose of this study was to examine the effects of two different stance positions and visual conditions on soleus H-reflex gain in 15 apparently healthy adults (mean age = ± 6.92 yrs). The soleus H-reflexes were examined in two experimental stance conditions: two-legged (stable) and one-leg (unstable), and two visual conditions: eyes open and eyes closed. To assess the reflex gain, subjects performed ten trials under each of the four conditions and a soleus H-reflex was elicited during the performance of each trial. For each condition the peak-to-peak amplitude of the H-reflex and the EMG activity 50 ms prior to the stimulus was recorded. Differences in the peak-to-peak amplitudes of the soleus H-reflex for the experimental conditions were compared with a 2 2 (Stance Vision) repeated measures ANOVA. The level of significance was p < Results demonstrated significant differences in reflex gain for both the vision (F l,15 = 4.87, p < 0.05) and the stance condition (F l,15 = 14.86, p < 0.05). Although both the stance condition and vision significantly affected the H-reflex gain, there was no interaction between these two variables (F l,15 = 0.17). From these results, we conclude that H-reflex gain was decreased both as stance complexity increased and as visual inputs were removed. Consistent with previous reports, it may be speculated that changes in presynaptic inhibition to the soleus Ia fibers regulate these gain changes. We propose that vision and stability of stance affect soleus H-reflex gain, but do so without any interactive effects. Ó 2009 Elsevier Ltd. All rights reserved. 1. Introduction * Corresponding author. Address: Marmara University, School of Physical Education and Sports, Anadoluhisari, Istanbul, Turkey. addresses: spinar@indiana.edu, salihpinar@superonline.com (S. Pinar). The Hoffmann reflex (H-reflex), a segmental monosynaptic reflex, serves as an effective tool for investigating task-specific changes occurring at the level of the Ia-motoneuron synapse. There exists extensive evidence supporting the presence of segmental reflex modulation in humans during a variety of motor tasks (Capaday and Stein, 1986, 1987; Llewellyn et al., 1990) as well as during the learning of novel tasks (Perez et al., 2007). For example, changes in the gain of the soleus H-reflex (D in H-reflex amplitude/d in background EMG) have been documented during different body orientations (Katz et al., 1988; Koceja et al., 1993) locomotion (Capaday and Stein, 1986, 1987) as well as during tasks of varying complexity (Llewellyn et al., 1990). Previous research has shown that H-reflex gain can be modulated in a functionally and environmentally appropriate manner, and that the regulation of soleus H-reflex gain may be important for behavioral tasks. For example, it is well-documented that when an individual is put in an unstable postural environment, the soleus H-reflex is suppressed, and it has been postulated that this reflex suppression may provide more cortical control over the task as well as to prevent unwanted oscillations in postural control (Koceja et al., 1995). In one of our earlier studies we found that young subjects, when moving from a position of lying prone (e.g., non weight-bearing) to standing (e.g., weight-bearing) showed a 14.5% depression in the amplitude of the soleus H-reflex. Thus, even in conditions in which muscle activation is increased, a depression of the soleus H-reflex is observed. The net result is a significant depression in the gain of the soleus H-reflex when standing (Koceja et al., 1995). This depression in reflex gain has also been documented for standing, walking and running: as the task complexity increases, the gain of the reflex is depressed (Zehr, 2002). It has also been shown in our laboratory that elderly subjects, as a group, demonstrate an inability to depress the reflex when standing (Koceja et al., 1995), although this is not the case for all elderly. Some elderly subjects are able to demonstrate this task-appropriate depression in the soleus H-reflex when standing, and those who do also demonstrate less postural sway during quiet standing, leading one to speculate on the importance of this modulation during postural control tasks. The notion that reflexes are adaptable to environmental conditions has since been determined in both /$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi: /j.jelekin

2 S. Pinar et al. / Journal of Electromyography and Kinesiology 20 (2010) animal and human models, and is a critical aspect of efficient movement (Wolpaw, 2007). Several neurological mechanisms have been proposed to mediate H-reflex changes during different environmental conditions: reciprocal inhibition, presynaptic inhibition, recurrent inhibition and vestibular influences. However, before a mediating spinal mechanism can be identified, a better understanding of the role of different sensory inputs to the motoneuron is warranted. For example, it is well known that visual, somatosensory and vestibular information all project to the cerebellum (Brodal, 1981) and due to this convergence of information, there exists opportunity for the integration of input from multiple sources to contribute to the H- reflex modulation. Previous studies have examined the soleus H-reflex gain during one-legged and two-legged stance (Chalmers and Knutzen, 2002; Huang et al., 2009), the effects of manipulating somatosensory information from the foot (Misiaszek et al., 1998) and the effects of vestibular activation (Kamiya et al., 2006), but to date few studies have investigated the effects of visual deprivation and task complexity on the H-reflex. The primary purpose of this study was to examine the effects of two different stance and visual conditions on the soleus H-reflex gain to elucidate the integrative process of the sensory system on the neuromuscular system. 2. Materials and methods 2.1. Subjects Fifteen male subjects were recruited for this study (Age: ± 6.92 yrs; Height: 1.74 ± 0.12 m; Weight: ± Kg; Body Mass Index: ± 2.39). These subjects were drawn from the healthy adult population at a university setting. All subjects gave informed consent to the procedures as approved by the University s Committee for the Protection of Human Subjects and indicated no apparent neurological, orthopedic or neuromuscular problems on a preliminary screening questionnaire. Each subject was tested for approximately 1.5 h on one day. Each subject was tested in two experimental balance conditions: two-legged stance and one-legged stance positions. Each of these stances was performed with eyes open and eyes closed. All testing was performed in the Motor Control Laboratory at Indiana University Experimental protocol Each subject was tested when performing two different tasks: quiet normal two-legged stance (Stable) and one-legged stance (Unstable). For the two-legged stance, each subject stood on a custom smooth surfaced platform with a normal two-legged stance position. The subject was barefooted with arms supported on the waist, and was instructed to stare straight ahead at a dot located at eye level two meters away. The feet were approximately 10 cm apart. Subjects performed 10 trials of the stable stance condition with eyes open (EO Stable Stance) and ten trials with eyes closed (EC Stable Stance). For the one-legged (Unstable) position, the subject stood on the dominant foot, barefooted, on the platform. The non-dominant foot was held so that it touched the inside of the supporting knee. The hands were placed on the waist and as soon as the proper position was established, the test was started. The subject was instructed to hold this position as long as possible, and was allowed to rest after each H-reflex was administered. When the dominant foot was moved away from the knee, the test was stopped. During the vision condition, the subjects were also instructed to stare straight ahead at a dot located at eye level two meters away during the test. Eyes open (EO Unstable Stance) and eyes closed (EC Unstable Stance) tests were applied in the same session H-reflex and EMG recording Surface electrodes were used both for muscle recording and for H-reflex nerve stimulation. For the EMG recording electrode (Therapeutics Unlimited, Iowa City, IA), Ag/Ag Cl electrodes with 2 cm intraelectrode distance were used. The electrodes consisted of an on-site preamplifier, thus minimizing movement artifact. One of two recording electrodes was positioned over the soleus muscle and the other was placed over the tibialis anterior muscle of subject s right leg. Specifically, the electrode on the soleus muscle was adhered parallel to the muscle fibers at the midpoint between the distal fibers of the gastrocnemius muscles and the proximal boarder of the Achilles tendon. The electrode for the tibialis anterior was placed lateral to the medial shaft of the tibia at one third the distance between the knee and the ankle. All electrodes were placed vertically along the presumed muscle fiber direction. For the H-reflex stimulating electrodes, a 0.8 cm-diameter cathode and a 4 cmdiameter anode were used. To elicit the soleus H-reflex, a cathode electrode was placed in the popliteal fossa and an anode electrode was placed just superior to the patella of the right leg (Schieppati, 1987). Soleus H-reflexes were evoked through tibial nerve stimulation with a 1 ms duration pulse. Prior to starting the balance task the maximum amplitudes of the unconditioned H-reflex (Hmax) and the M-wave (Mmax) were measured. The size of the test H-reflex was measured as the peak-to-peak amplitude. It has been demonstrated earlier that the susceptibility of the H-reflex to conditioning depends on the size of the control reflex (Crone et al., 1990). For the H-reflex during the different tasks, the intensity of the H-reflex stimulation was monitored by keeping constant the small M-wave preceding each H response (Schieppati, 1987), and throughout testing, special care was taken to ensure that the size of the small M-wave during each experimental trial was constant. The EMG signals were DC coupled from the electrodes to a high impedance DC amplifier with low bias current requirements. All EMG signals were sampled at 2 khz, amplified (gain = 1000), and band-pass filtered ( Hz). For H-reflex measurements, the peak-to-peak amplitude of the signal was used as the dependent variable. To quantify the amount of muscle activity present prior to the H-reflex stimulation, the background EMG (bemg) activity in the muscle prior to the H-reflex stimulation for each postural condition was calculated. After sampling, the bemg was bandpassed filtered from 20 to 450 Hz, full-wave rectified and smoothed with a 25 Hz low-pass filter for the 50 ms prior to H-reflex stimulation Statistical analysis Differences in the peak-to-peak amplitudes of the soleus H-reflex for the two stance and two visual conditions were compared with a 2 2 (Stance Vision) repeated measures ANOVA. The level of significance was p < Also, the Pearson correlation coefficient was estimated between the bemg and the H-reflex (p < 0.05). 3. Results (Fig. 1) depicts the raw data from a typical subject in each of the experimental conditions. It can be seen that as vision is removed and stance complexity increased, the H-reflex amplitude is depressed. Note also that the trial M-wave in each of the four experimental conditions remains constant, ensuring that stimulus intensity, a critical control variable in this study, was the same on all trials.

3 356 S. Pinar et al. / Journal of Electromyography and Kinesiology 20 (2010) Gain (%) Fig. 1. Raw EMG trace of the soleus H-reflex for one subjects in the four conditions: stable stance with eyes open; unstable stance with eyes closed; stable stance with eyes open; and unstable stance with eyes closed. Note the gradual depression in the peak-to-peak amplitude of the soleus H-reflex as task difficulty increases, with relatively little change in the trial M-wave. (Fig. 2) illustrates the average bemg activity in the soleus muscle in each of the four experimental conditions. It can be seen that the bemg activity in the soleus muscle increased across these four conditions, and was significantly greater, as expected in the unstable stance when compared to the stable stance. However, no significant correlation between EMG activity and H-reflex was found (p > 0.05). When the data from all subjects were grouped, and the H-reflex gain was calculated by dividing the changes in soleus H-reflex amplitude by bemg, there were significant differences in reflex gain for both the vision (F l,15 = 4.87, p < 0.05) and the balance condition (F l,15 = 14.86, p < 0.05). Although both stance complexity and vision significantly affected the H-reflex gain, there was no interaction between these two variables (F l,15 = 0.17). Specifically, there was a 24.4% reduction in the gain of the soleus H-reflex when vision was removed, and a 68.8% reduction in the gain of the soleus H-reflex when task complexity (stable versus unstable surface) was increased. These results are shown in Fig Discussion Background EMG (mv) EO-Stable EC-Stable EO-Unstable EC-Unstable Conditions Fig. 2. Background EMG activity (mv) of the soleus muscle 50 ms prior to the delivery of the H-reflex stimulus for the four experimental conditions. EO denotes eyes open and EC denotes eyes closed; Stable denotes two-legged stance and unstable denotes one-legged stance. Values are mean ± SE EO-Stable EC-Stable EO-Unstable EC-Unstable Conditions Fig. 3. Soleus H-reflex gain (H-reflex/background EMG activity) for the four experimental conditions. EO denotes eyes open and EC denotes eyes closed; Stable denotes two-legged stance and unstable denotes one-legged stance. Values are mean ± SE. The present study demonstrated that during tasks of increasing behavioral complexity induced by manipulating vision and the stability of stance, the background EMG activity of the soleus muscle was increased while at the same time the gain of the soleus H-reflex was significantly reduced. Interestingly as the present study was designed to test the interaction between vision and stability of stance, there was no interaction between these two factors. These stance results concur with the previous study reported by Huang et al. (2009) who reported that the soleus H-reflex in onelegged stance was depressed as compared to two-legged stance; however the interaction between vision and complexity has not been thoroughly examined in the literature. Support for the idea that reflex modulation is related to postural stability was demonstrated in elderly subjects (Koceja et al., 1995) and patients with cerebellar ataxia (Tokuda et al., 1991) and there are several neurophysiological mechanisms that may modulate monosynaptic connections in the spinal cord. One likely mechanism is an increase in presynaptic inhibition impinging on the Ia fibers which connect to the alpha motoneurons. Presynaptic inhibition could be influenced by feedback from a variety of sensory systems and/or numerous supraspinal sites responsible for motor control: motor cortex, cerebellum and basal ganglia. Past research has implicated presynaptic inhibition as an important spinal regulatory network for the transfer of sensory information to the motoneurons and it has also been shown to be increased during learning (Perez et al., 2007) and during periods of postural complexity (Zehr, 2002). Presynaptic inhibition is a likely candidate mediating the changes observed in this study since background EMG activity was increased during periods of postural instability but at the same time the H-reflex was depressed. Intuitively, any increases in background EMG should be accompanied by increases in H-reflex amplitude. Since we observed a decrease in the H-reflex amplitude with an identical stimulus during periods of postural instability, a reduction in communication between the Ia-sensory fiber and the alpha motoneurons seems plausible. Moreover, presynaptic inhibition has been identified as an important reflex gain control mechanism (Zehr, 2006) and has been suggested in a variety of studies to be influential during postural control tasks (Hultborn et al., 1987; Meunier and Perrot-Deseilligny, 1989; Misiaszek, 2003). However, it is important to keep in mind that other spinal mechanisms (e.g., reciprocal inhibition, recurrent inhibition, propriospinal connections) may also play a mediating role. Given that several experimental H-reflex protocols have been developed for use in humans that can indirectly assess presynaptic inhibition, reciprocal inhibition and recurrent inhibition (Pierrot-Deseilligny and Burke, 2005) perhaps future studies can address this question more formally. Regardless of the spinal mechanism(s) involved, we surmise that the soleus H-reflex gain is more acutely affected by stance stability rather than visual inputs. Whereas both conditions (vision and stance stability) led to decreased soleus H-reflex gain, the effect was consistently greater for the stance stability condition. Overall there was a 24.4% reduction in the gain of the soleus H-re-

4 S. Pinar et al. / Journal of Electromyography and Kinesiology 20 (2010) flex when vision was removed, and a 68.8% reduction in the gain of the soleus H-reflex when task complexity (stable versus unstable surface) was increased. Whereas the role of visual inputs in depressing the H-reflex gain found in this study is consistent with a previous report (Huang et al., 2009) and the observed change in reflex gain due to stance was also compatible with previous studies (Chalmers and Knutzen, 2002; Trimble and Koceja, 2001), the interaction of these two factors when studied in the same individuals is a new finding. This leads one to believe that perhaps the regulation of reflex gain is controlled by a central, rather than peripheral source, in which inputs from multiple sensory sources are combined. Support for this idea is found in the literature. A recent study (Laudani et al., 2009) demonstrated that repetitive stretches of the soleus tendons during balancing may cause an increase in spindle afferent discharge, which by itself would result in increased excitability of the H-reflex. Under this condition, excessive autogenic excitation of the muscle due to elevated Ia-activation was counterbalanced by an adaptive decline in gain of the reflex loop through presynaptic inhibition of the Ia afferent. We agree with this explanation that postural equilibrium during a one-legged stance task may in fact be regulated by central control as opposed to a reliance on a direct spinal adaptation (Winter et al., 2003). Keeping in mind that presynaptic spinal networks are also known to be under the influence of central commands (Hultborn et al., 1987), unraveling the complexities of reflex modulation may require creative experimental protocols. The decrease observed in the H-reflex gain during one-legged stance may be related to the demands associated with postural stability. This parallels similar findings by Capaday and Stein (1986) who demonstrated that soleus H-reflex gain is modulated throughout the gait cycle to accommodate for the biomechanical demands of the task (Klein et al., 1996). This downward modulation of the soleus H-reflex substantiates readjustment of reflexive control over medial lateral sway in the ankle joint, in place of a predominant reliance upon a hip strategy to control postural sway during one-legged stance (Gribble and Hertel, 2004; Hayashi et al., 1991). As presynaptic inhibition increases, the output of the motoneuron pool in response to Ia afferent input will be decreased, limiting the influence of the Ia afferents without changing their structural extent. A decrease in H-reflex gain would serve to attenuate the spinal stretch reflexes that would otherwise hinder attempts to balance. Therefore, using this strategy, the possibility of counterproductive spinal stretch reflexes for subjects is reduced during the one-legged stance, and this is consistent with the current findings. In conclusion, the results of this study demonstrated that the gain of the soleus H-reflex was depressed when subjects were asked to perform a static balance test without vision as opposed to doing the same with vision, as well as during one-legged stance when compared to a two-legged stance. Moreover, there was no interaction between the visual and stance conditions, lending support for the notion that a common mechanism controls changes in gain for the two conditions. Consistent with previous reports, it may be speculated that changes in presynaptic inhibition to the soleus Ia fibers (Hultborn et al., 1987; Meunier and Perrot-Deseilligny, 1989; Schieppati, 1987) regulate these gain changes. Conflict of interest statement Capaday C, Stein RB. Amplitude modulation of the soleus H reflex in the human during walking and standing. J Neurosci 1986;6: Capaday C, Stein RB. Difference in the amplitude of the human soleus H reflex during walking and running. J Physiol 1987;392: Chalmers GR, Knutzen KM. Soleus H-reflex gain in healthy elderly and young adults when lying, standing, and balancing. J Gerontol 2002;57(8):B Crone C, Hultborn H, Mazieres L, Morin C, Nielsen J, Pierrot-Deseilligny E. Sensitivity of monosynaptic test reflexes to facilitation and inhibition as a function of the test reflex size: a study in man and the cat. Exp Brain Res 1990;81: Gribble PA, Hertel J. Effect of lower-extremity muscle fatigue on postural control. Arch Phys Med Rehab 2004;85(4): Hayashi R, Tako K, Tokuda T, Yanagisawa N. Modification of the soleus H-reflex during sitting and standing in normal humans. In: Shimamura M, Grillner S, Edgerton VR, editors. Neurobiological basis of human locomotion. Tokyo: Japan Scientific Society Press; p Huang C, Cherng R, Yang Z, Chen Y, Hwang I. Modulation of soleus H reflex due to stance pattern and haptic stabilization of posture. J Electromyogr Kinesiol 2009;19(3): Hultborn H, Meunier S, Pierrot-Desseilligny E, Shindo M. Changes in presynaptic inhibition of Ia fibers at the onset of voluntary contractions in man. J Physiol 1987;389: Kamıya A, Tanabe S, Muraoka Y, Masakado Y. Modulation of the soleus H-reflex during static and dynamic imposed hip angle changes. Int J Neurosci 2006;116: Katz R, Meunier S, Pierrot-Deseilligny E. Changes in presynaptic inhibition of Ia fibres in man while standing. Brain 1988;11 I: Klein P, Mattys S, Rooze M. Moment arm length variations of selected muscles acting on talocrural and subtalar joints during movement: an in vitro study. J Biomech 1996;29(1): Koceja DM, Markus CA, Trimble MH. Postural modulation of the soleus H reflex in young and old subjects. Electroencephalogr clin Neurophysiol 1995;97: Koceja DM, Trimble MH, Earles DR. Inhibition of the soleus H-reflex in standing man. Brain Res 1993;629: Laudani L et al. Effects of repeated ankle plantar-flexions on H-reflex and body sway during standing. J Electromyogr Kinesiol 2009;19(1): Llewellyn M, Yang JF, Prochazka A. Human H-reflexes are smaller in difficult beam walking than in normal treadmill walking. Exp Brain Res 1990;83:22 8. Meunier S, Perrot-Deseilligny E. Gating of the afferent volley of the monosynaptic stretch reflex during movement in man. J Physiol 1989;419: Misiaszek JE, Cheng J, Brooke JD, Staines W. Movement-induced modulation of soleus H reflexes with altered length of biarticular muscles. Brain Res 1998;795: Misiaszek JE. The H-reflex as a tool in neurophysiology: Its limitations and uses in understanding nervous system function. Muscle Nerve 2003;28: Perez MA, Lundbye-Jensen J, Nielsen JB. Task-specific depression of the soleus H- reflex after cocontraction training of antagonist muscles. J Neurophysiol 2007;98: Pierrot-Deseilligny E, Burke D. The circuitry of the human spinal cord: its role in motor control and movement disorders. Cambridge: Cambridge University Press; Schieppati M. The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 1987;28: Tokuda T, Tako K, Hayashi R, Yanagisawa N. Disturbed modulation of the stretch reflex gain during standing in cerebellar ataxia. Electroencephalogr clin Neurophysiol 1991;81: Trimble MH, Koceja DM. Effect of a reduced base of support in standing and balance training on the soleus H-reflex. Int J Neurosci 2001;106(1 2):1 20. Winter DA, Patla AE, Ishac M, Gage WH. Motor mechanisms of balance during quiet standing. J Electromyogr Kinesiol 2003;13(1): Wolpaw JR. Spinal cord plasticity in acquisition and maintenance of motor skills. Acta Physiol 2007;189: Zehr EPC. Considerations for use of the Hoffman reflex in exercise studies. Eur J Appl Physiol 2002;86: Zehr EP. Training-induced adaptive plasticity in human somatosensory reflex pathways. J Appl Physiol 2006;101: Salih PINAR earned his Ph.D. in Sport and Sport Health Science from Marmara University in He is currently a Professor of Movement and Training Science. He is employed by the Department of Coaching Education at Marmara University. He serves as the department head and graduate programs coordinator of Movement and Training Science Program. His research interests include muscle physiology and neurology and their effects on exercise. None declared. References Brodal A. Neurological anatomy in relation to clinical medicine. 3rd ed. New York: Oxford University Press; 1981.

5 358 S. Pinar et al. / Journal of Electromyography and Kinesiology 20 (2010) David M. Koceja earned a Ph.D. in Motor Control from Indiana University in He is currently a Professor in the Department of Kinesiology at Indiana University as well as the Associate Dean for Research in the School of Health, Physical Education and Recreation. He is the Director of the Motor Control Laboratory and his research interests include the neuromuscular control of posture and balance in the elderly.