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Upper and lower extremity proprioceptive inputs modulate EMG activity of the trapezius
Journal of Electromyography and Kinesiology 21 (2011) 77–81
Contents lists available at ScienceDirect
Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Upper and lower extremity proprioceptive inputs modulate EMG activity of the trapezius Cengiz Tataroglu ⇑, Fatma Kursad Kuçuk, Ayca Ozkul Adnan Menderes University, Medical Faculty, Department of Neurology, 09020 Aydin, Turkey
a r t i c l e
i n f o
Article history: Received 28 June 2010 Received in revised form 13 September 2010 Accepted 28 September 2010
Keywords: Trapezius Long latency reflex Posture Axial muscles
s u m m a r y Axial muscles like the trapezius have different reflexive and functional properties. The aim of this study was to analyze the long latency reflexes obtained from the trapezius by the electrical stimulation of upper and lower extremity peripheral nerves. Thirty-one healthy volunteers were included in the study. Surface EMG activity of both trapezius muscles was recorded and averaged after electrical stimulation of the median and peroneal mixed nerves. The recordings were performed during supine and erect posture in nine subjects to evaluate of the effect of postural differences on reflex response. Reflex recordings were also performed in six subjects from some other muscles together with the trapezius by the stimulation of the peroneal nerve. Reflex responses including three components were recorded from the trapezius muscle (unilateral or bilateral) by electrical stimulation of the peroneal nerve. The most stable of them was the second component (23/31) which had a latency of 72.6 ± 7.9 ms for the ipsilateral, and 74.2 ± 8.5 ms for the contralateral trapezius (15/31). For median stimulation, the first component recorded at 32.0 ± 6.7 ms was the most stable (25/31). The second component was more frequently recorded on the contralateral side (14/ 31). Erect posture increased the amplitude of these components. Upper and lower extremity proprioceptive inputs modulate the EMG activity of the trapezius. This modulation probably related with postural adjustments. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Long latency reflexes (LLR) mostly recorded from upper limb distal muscles, and a cortical contribution in the generation of these reflex responses, have been generally accepted (Deuschl and Lücking, 1990; Cruccu and Deuschl, 2000). These reflexes have generally been recorded by rapid mechanical changes in the muscle length (Sinkjaer et al., 1988; Toft et al., 1991; Mrachacz-Kersting et al., 2006). Electrical stimulation of the peripheral nerve can also generate these reflexes from distal muscles (Deuschl and Lücking, 1990; Cruccu and Deuschl, 2000; Alexander and Harrison, 2003; Mrachacz-Kersting et al., 2006). LLRs recorded from proximal muscles of the upper and lower limbs have also been studied (Kavounoudias et al., 2001; Kagamihara et al., 2003; MrachaczKersting et al., 2006). Long latency reflexes obtained from proximal and distal muscles may include two or three components depending on target muscle (Mrachacz-Kersting et al., 2006). It was suggested that monosynaptic excitation of alpha motor neuron generates the first component; however, the origin of later components is not known exactly (Matthews, 1984). Some strong evi⇑ Corresponding author. Tel.: +90 256 4441256x114; fax: +90 256 2146495. E-mail addresses: [email protected], [email protected] (C. Tataroglu). 1050-6411/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2010.09.011
dences regarding a supraspinal and transcortical contributions to these late components have been reported (Kavounoudias et al., 2001; Kagamihara et al., 2003; Mrachacz-Kersting et al., 2006). Lower extremity inputs carry useful information for the preparation of posture. In addition, periscapular muscles may have an important role in postural adjustments (Bloem et al., 2000; Kavounoudias et al., 2001; Vuillerme et al., 2005). It has been demonstrated that some axial muscles and periscapular muscles have particular monosynaptic and polysynaptic reflexive properties, in the same way as some other axial muscles (Deuschl and Lücking, 1990; Alexander and Harrison, 2002; Ertekin et al., 2006). A reflex connection between some periscapular muscles and hand muscle afferents has recently been reported (Alexander and Harrison, 2003). In that paper, the authors concluded that scapular muscles help efficient use of hand muscles. On the other hand, Marsden et al. (1981) observed a reflex response from the pectoralis major by the mechanical stretch of thumb flexors, and this response is referred as a postural reflex. If this connection between upper extremity mixed nerve afferents and periscapular muscles helps postural adjustments, lower extremity proprioceptive afferents may also have a connection with these muscles. In this study, we investigated the reflex connection between upper and lower extremity mixed nerve afferents and bilateral tra-
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C. Tataroglu et al. / Journal of Electromyography and Kinesiology 21 (2011) 77–81
pezius muscle innervations. Demonstration of these reflex connections can be important for further studies designed to investigate central postural mechanisms.
2. Materials and methods Thirty-one healthy volunteers aged between 18–42 years (mean 26.9 ± 6.8) participated to the study. No history of systemic disorder or toxic exposure was recorded in any subject. All subjects gave informed written consent and the local ethics committee approved the study. Routine nerve conduction studies of median, ulnar, peroneal and sural nerves were normal in conventional electrophysiological testing. Reflex recording: A surface electromyogram was recorded with Ag/AgCl surface cup electrodes from both right and left trapezius muscles simultaneously. Active and reference surface electrodes were placed 3 cm apart on the upper fibers of the trapezius muscle. Active electrode was placed at the superior border of the shoulder just medial to the acromioclavicular joint and the reference was placed at inferomedial side to the active electrode. 20–40 traces were averaged. At least 2 averaged traces were recorded and superimposed. Amplifier filters were between 20 Hz and 3 kHz. Oscilloscope sweep time was 300 ms. Electrode impedance was kept below 20 kX. A standard bipolar surface stimulator was used for stimulation. Stimulus duration was 1 ms. Stimulus frequency was random; however electrical pulses were delivered every 3– 5 s. The median nerve was stimulated at the wrist level and the peroneal nerve was stimulated at the level of the capitulum fibula. The peripheral nerves on the right side were chosen for stimulation. These nerves were stimulated by 1 ms square-wave pulses. Stimulus intensity was chosen as twice the motor threshold (2XMT) because Kagamihara et al. observed that facilitation of H reflexes recorded from far away muscle after median nerve stimulation increased after the level of 1.6 MT (7). This stimulation intensity was not painful for subjects. Initially, recording was performed on both trapezius muscles in the resting state (trapezius muscle inactive) in order to eliminate any startle reflex. This recording was performed while the subject was sitting on a comfortable armchair. After this initial evaluation, electrophysiological recordings were made while the subject was in a standing position. Mild and stable muscle activity (shoulder girdle elevation) was requested from subjects. This muscle activity was about 20% of maximal voluntary muscle activity for each muscle and this muscle activity was easily provided during erect posture of the subject. Underlying muscle activity was monitored by auditory feedback and this muscle activity continued during the evaluation. Surface electromyographic signals were picked up from both sides simultaneously. A Medtronic-Keypoint EMG machine (version 5.06) was used for stimulation, recording and amplification of EMG activity. The experiment was repeated by cutaneous nerve stimulation. This procedure was performed by the electrical stimulation of the superficial radial nerve and sural nerve in ten subjects. Initially, sensory perception thresholds were determined for these cutaneous nerves. For cutaneous stimulation, stimulus intensity was accepted as three times the sensory perception threshold. The superficial radial nerve was stimulated at 10 cm proximal to the wrist by standard surface electrodes. The sural nerve was stimulated from just behind the lateral malleolus. Stimulus duration was 1 ms and frequency was random and interstimulus interval was not below than 3 s. The degree of voluntary muscle activity of trapezius was the same with mixed nerve stimulation. The other stimulation and recording conditions were the same as in the previous experiment.
An attempt was made to record reflex responses from some other muscles in addition to the trapezius by the stimulation of a unilateral peroneal nerve to exclude an interlimb reflex contribution to the responses when recording from the trapezius. These muscles were also tested on both sides. Simultaneous recording of bilateral cervical paraspinalis (C6–C7 level), deltoideus, biceps and masseter were performed on six subjects in a standing position. Bipolar surface recording were also performed from these muscles. A slight voluntary EMG activity (20% of maximal voluntary force) was maintained during the analysis in all muscles. Bipolar recording electrodes were placed on the cervical paraspinalis muscle. The active electrode was located 2 cm lateral to the spinous process of the C7 vertebra and the reference electrode was located 3 cm caudal to the active one. For the deltoideus and biceps muscles, the active electrode was located on the belly of the muscle and the reference electrode was located on the tendon. For the masseter, the active electrode was placed on the belly of the muscle and the reference electrode was placed on the zygomatic bone. The recording and stimulation conditions described above were the same for this experiment. In nine subjects, reflex recordings were performed during sitting and stance position. During sitting position subjects were requested to make a slight shoulder elevation. Same muscle activity of trapezius was continued during stance position. During neutral stance position of shoulder, a slight muscle activity of both trapezius are already continued. Other stimulating and recording parameters were same with previous experiments. For data analysis, the onset latencies and peak to peak amplitudes of each component reflex response were analyzed. The onset latency of the response was accepted as the first clear deflection from the baseline. All electrophysiological analysis was performed by the same investigator. Statistical analysis: descriptive statistics were performed. Additionally, amplitude differences of reflex responses between during supine and erect posture were analyzed by T test. Two tailed tests were used and p < 0.05 was considered as significant. 3. Results 3.1. Median nerve stimulation Trapezius long latency reflexes were recorded in all subjects by the stimulation of the median nerve. Reflex responses obtained from both ipsilateral and contralateral trapezius muscles by the stimulation of median nerve included three components (ipsilateral-M1, M2, M3; contralateral-cM1, cM2, cM3) (Fig. 1). Their latencies were 32.0 ± 6.7 and 52.1 ± 4.3 ms for ipsilateral, and 31.8 ± 7.7 and 51.3 ± 5.3 ms for contralateral. A last component (M3 and cM3) was recorded at 72.5 ± 5.6 and 96.5–127.5 ms from ipsilateral and contralateral trapezius, respectively, however its frequency was very low. The most stable component was the first component (M1) for ipsilateral (25/31subjects) and the second (cM2) for the contralateral response (18/31 subjects). No response was recorded by cutaneous stimulation. Tables 1 and 2 summarize electrophysiological data. 3.2. Peroneal nerve stimulation Latency reflexes of the trapezius of 28 out of 31 subjects were recorded. Reflex responses were recorded from both the ipsilateral and contralateral trapezius by electrical stimulation of the peroneal nerve. No response was obtained while the trapezius muscle was relaxed. An early component (ipsilateral-P1 and contralateral-cP1) was recorded at 44.2 ± 5.6 and 47.6 ± 8.4 ms from both trapezius muscles, respectively. A second component (ipsilateral-
C. Tataroglu et al. / Journal of Electromyography and Kinesiology 21 (2011) 77–81
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Fig. 1. Trapezius long latency reflexes obtained by the stimulation of median (A) and peroneal nerve (B). Upper traces were recorded from ipsilateral, bottom traces were recorded from contralateral trapezius. In this subject, amplitudes of reflex responses obtained from contralateral trapezius smaller than those obtained from ipsilateral trapezius.
Table 1 Latency values of trapezius long latency reflexes. Ipsilateral
M1–cM1 M2–cM2 M3 P1–cP1 P2–cP2 P3
Contralateral
Latency (ms)
Range
Latency (ms)
Range
32.0 ± 6.7 (n:25) 52.1 ± 4.3 (n:18) 72.5 ± 5.6 (n:5) 44.2 ± 5.6 (n:10) 72.6 ± 7.9 (n:23) 101.5 ± 5.7 (n:2)
21.7–40.6 47.2–62.8 66.0–80.5 32.5–51.3 60.0–88.0 97.5–105.5
31.8 ± 7.7 (n:7) 51.3 ± 5.3 (n:14)
23.3–40.8 41.3–56.6
47.6 ± 8.4 (n:6) 74.2 ± 8.5 (n:15)
36.8–58.8 41.3–56.6
M1, M2, M3: first, second and third components of median stimulated trapezius long latency reflexes. cM1, cM2: first and second components of contralateral median nerve stimulated trapezius long latency reflexes. P1, P2, P3: first, second and third components of peroneal stimulated trapezius long latency reflexes. cP1, cP2: first and second components of contralateral peroneal nerve stimulated trapezius long latency reflexes.
Table 2 Amplitude values of trapezius long latency reflexes. Amplitudes (lV)
M1–cM1 M2–cM2 M3 P1–cP1 P2–cP2 P3
Ipsilateral
Contralateral
120.4 ± 57.8 150.0 ± 50.0 178.6 ± 63.6 86.2 ± 52.8 112.7 ± 74.8 90.0 ± 61.8
82.2 ± 26.8 106.7 ± 74.2 141.7 ± 73.6 111.2 ± 74.0
P2 and contralateral-cP2) was recorded at 72.6 ± 7.9 and 74.2 ± 8.5 ms, respectively. The most stable component was P2 on both sides (23/31 for the ipsilateral side and 15/31 for the contralateral side) (Fig. 1). Occasionally, a third component was observed at the ipsilateral trapezius. No response was recorded by cutaneous stimulation, nor was any response recorded from other muscles by stimulation of the peroneal nerve. Tables 1 and 2 demonstrate the electrophysiological data regarding trapezius long latency responses evoked by stimulation of the peroneal nerve. Effect of Posture: Reflex responses were amplified during erect posture by the stimulation of both lower and upper extremities (Fig. 2). The amplitude of trapezius long latency reflex by the stim-
ulation of median nerve (M1) was increased during erect posture from 85.2 ± 33.2 lV to 118.7 ± 28,6 lV (p: 0.001). The amplitude of second component (P2) of trapezius long latency reflex by the stimulation of peroneal nerve was also increased during stance from 67.9 ± 32.8 lV to 110.7 ± 42.8 lV (p: 0.001). 4. Discussion In this study, long latency reflex responses were only recorded from both trapezius muscles by the non-nociceptive electrical stimulation of upper and lower extremity mixed nerves, and these reflex responses were only recorded during slight voluntary activity of the trapezius. Also, cutaneous stimulation of upper and lower extremities failed to generate any reflex response. Our results suggested that there was a reflex connection between upper and lower extremity muscle afferents and trapezius muscle innervations. Alexander and Harrison (2003) recently demonstrated a reflex connection between hand muscle afferents and shoulder girdle muscles. They described a reflex response of the trapezius obtained at about 35 ms by the electrical stimulation of upper extremity mixed nerves. The authors estimated that its central delay was about 18 ms and this lag was sufficient for a supraspinal route of reflex circuit. In the present study, we showed that late responses were also recorded from the contralateral trapezius. The delayed component (cM2) was more frequently recorded from the contralateral trapezius than the first one. However, a series of reflex responses to stimulation of the median nerve were observed in the present study, which included three components. The latency of the first component was similar to that of the previous study. The second component (cM2) was recorded more frequently from the contralateral trapezius. M3 was not a stable response. Reflex activity of the trapezius muscle in response to stimulation of lower extremity mixed nerves included three components. The first and second responses were mostly recorded from both ipsi- and contralateral trapezius muscles. The first response was obtained at about 40 ms, and had a short latency. This response cannot be attributed to a supraspinal generator because its latency does not permit a cortical generator. Therefore, a spinal generator, probably a propriospinal system, must be responsible in the generation of this response. However, the latency of the P2 component (about 70 ms) may include a supraspinal and even a transcortical pathway. A third component observed at about 100 ms was recorded mostly unilaterally and its frequency was very low.
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Fig. 2. Erect posture amplified trapezius long latency reflexes by stimulation of both median and peroneal nerves. Upper traces are from ipsilateral trapezius, bottom traces are from contralateral trapezius. By the erect posture both ipsilateral and contralateral responses were amplified.
Cutaneous stimulation failed to generate these reflex responses from stimulation of the upper and lower extremities. The same finding was observed by Alexander and Harrison for upper extremity stimulation and recording of the trapezius. In fact, some studies regarding long latency reflexes recorded from far-away muscles also gave similar results (Marque et al., 2001; Vuillerme et al., 2005; Lourenço et al., 2006). However, long latency reflexes obtained from distal hand muscles can also be evoked by the stimulation of pure cutaneous nerves (Deuschl and Lücking, 1990). Additionally, Zehr et al. (2001) found that excitation of cutaneous afferents can modulate EMG activity of far-away muscles. However, train stimulus was used to evoke late responses from faraway muscles in their study and these responses were accepted as interlimb reflexes. It is believed that these reflexes were generated by propriospinal interlimb connections located in spinal cord and have shorter latency than long latency reflexes (Kagamihara et al., 2003). On the other hand, Kavounoudias et al. (2001) showed that tactile stimulus can also affect postural responses like proprioceptive inputs; however stimulus frequency of tactile stimulation was different from the proprioceptive inputs for this aim. They concluded that tactile and proprioceptive inputs have complementary role in the maintenance of posture. According to this study tactile stimulation can influence the EMG activity of far-away muscles, however, long latency reflexes of trapezius could not obtained in our study by cutaneous stimulation. Startle reflex as a late response could be erroneously accepted as long latency reflexes of the trapezius obtained in the present study since both responses have similar latencies (Walls-Sole et al., 2008). Startle responses can be recorded during relaxed state of muscle and easily habituate. However, responses of the trapezius in the present study were obtained only in contracted muscle. Also, we did not observe any habituation in our experiment. Long latency reflexes have been recorded during voluntary activation of the muscle. These responses reflect a modulation of EMG activity of target muscle by a specific stimulation (electrical or mechanical) (Tarkka and Larsen, 1986). Additionally, these responses could also be conceived as an interlimb reflex, but these responses were not recorded from other far-away muscles and cutaneous stimulation failed to record any response in the present study. Since train stimulus was used in
the recording of interlimb reflexes, it is unlikely that responses recorded in the present study could be an interlimb reflex as mentioned above (Zehr et al., 2001). Our results also suggested that the reflex responses obtained from trapezius by the stimulation of both upper and lower extremity mixed nerves affected from postural changes. Supine posture enlarged these responses. We believe that electromyographic activity of the trapezius was the same during the recording of trapezius in the different postural conditions however any special equipment monitoring muscle force level was not used in the present study. This finding suggested that neural circuits responsible in the postural adjustments may have a role in the generation of these responses. In brief, lower extremity muscle afferents can modulate electromyographic activity of the trapezius in the same way as hand muscle afferents. This modulation may have a supraspinal contribution. Neural mechanisms responsible in postural control may have a role in the generation of these responses.
References Alexander CM, Harrison PJ. Bilateral reflex control of the trapezius muscle in humans. Exp Brain Res 2002;142:418–24. Alexander CM, Harrison PJ. Reflex connections from forearm and hand afferents to shoulder girdle muscles in humans. Exp Brain Res 2003;148:277–82. Bloem BR, Allum JHJ, Carpenter MG, Honegger F. Is lower leg proprioception essential for triggering human automatic postural responses? Exp Brain Res 2000;130:375–91. Cruccu G, Deuschl G. The clinical use of brainstem reflexes and hand muscle reflexes. Clin Neurophysiol 2000;111:371–87. Deuschl G, Lücking CH. Physiology and clinical applications of hand muscle reflexes. Electroencephalogr Clin Neurophysiol Suppl 1990;41:84–101. _ Karapınar N. Adductor T and H Ertekin C, Bademkıran F, Tataroglu C, Aydogdu I, reflexes in humans. Muscle Nerve 2006;34:640–5. Kagamihara Y, Hayashi A, Masakado Y, Kouno Y. Long loop reflex from arm afferents to remote muscles in normal man. Exp Brain Res 2003;151:136–44. Kavounoudias A, Roll R, Roll JP. Foot sole and ankle muscle inputs contribute jointly human erect posture regulation. J Physiol 2001;532:869–78. Lourenço G, Iglesias C, Cavallari P, Pierrot-Deseilligny E, Marchand-Pauvert V. Mediation of late excitation from human hand muscles via parallel group II spinal and group I transcortical pathways. J Physiol 2006;572:585–603. Marque P, Nicolas G, Marchand-Pauvert V, Gautier J, Simonetta-Moreau M, PierrotDeseilligny E. Group 1 projections from intrinsic foot muscles to motoneurons of leg and thigh muscles in humans. J Physiol 2001;536:313–27.
C. Tataroglu et al. / Journal of Electromyography and Kinesiology 21 (2011) 77–81 Marsden CD, Merton PA, Morton HB. Human postural responses. Brain 1981;104:513–34. Matthews PB. Evidence from the use of vibration that the human long latency stretch reflex depends upon spindle secondary afferents. J Physiol 1984;348:383–415. Mrachacz-Kersting N, Grey MJ, Sinkjaer T. Evidence for a supraspinal contribution to the human quadriceps long latency stretch reflex. Exp Brain Res 2006;168:529–40. Sinkjaer T, Toft E, Andreassen S, Hornemann BC. Muscle stiffness in human ankle dorsiflexors: intrinsic and reflex components. J Neurophysiol 1988;60:1110–21. Tarkka IM, Larsen TA. Short and long latency reflex responses elicited by electrical and mechanical stimulation in human hand muscle. Acta Physiol Scand 1986;128:71–6. Toft E, Sinkjaer T, Andreassen S, Larsen K. Mechanical and electromyographic responses to stretch of the human ankle extensors. J Neurophysiol 1991;65:1402–10. Vuillerme N, Pinsault N, Vaillant J. Postural control during quiet standing following cervical muscular fatigue: effects of changes in sensory inputs. Neurosci Lett 2005;378:135–9. Walls-Sole J, Kumru H, Kofler M. Interaction between startle and voluntary reactions in humans. Exp Brain Res 2008;187:497–507. Zehr EP, Collins DF, Chua R. Human interlimb reflexes evoked by electrical stimulation of cutaneous nerves innervating the hand and foot. Exp Brain Res 2001;140:495–504.
Cengiz Tataroglu graduated from Aegean Universıty _ Medical Faculty-Izmir at 1985. He completed his neurological residency at 9 Eylul University-Izmir between 1992-1997. He Works in Adnan Menderes University Medical Faculty as associated professor of neurology from 2004. His scientific interested areas are clinical neurophysiology and clinical neuromuscular disorders.
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Fatma Kursad Kucuk is graduated from Dokuz Eylul University Medical Faculty (Izmir) at 1997. She worked as a resident in Neurology Department of Dokuz Eylul University Medical Faculty, Department of Neurology between 1999-2004. She is working as an neurologist in the Mugla State Hospital since 2004. Her scientific interested areas are demyelinating disease and neurophysiology.
Ayca Ozkul is graduated from Eskisehir Osman Gazi University Medical Faculty at 1997. She worked as a resident in Neurology Department of Adnan Menderes University Medical Faculty between 1999-2004. She is working as an assisstant professor in the same department since 2006. Her scientific interested areas are neurological intensive care and neurophysiology.
Contents lists available at ScienceDirect
Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Upper and lower extremity proprioceptive inputs modulate EMG activity of the trapezius Cengiz Tataroglu ⇑, Fatma Kursad Kuçuk, Ayca Ozkul Adnan Menderes University, Medical Faculty, Department of Neurology, 09020 Aydin, Turkey
a r t i c l e
i n f o
Article history: Received 28 June 2010 Received in revised form 13 September 2010 Accepted 28 September 2010
Keywords: Trapezius Long latency reflex Posture Axial muscles
s u m m a r y Axial muscles like the trapezius have different reflexive and functional properties. The aim of this study was to analyze the long latency reflexes obtained from the trapezius by the electrical stimulation of upper and lower extremity peripheral nerves. Thirty-one healthy volunteers were included in the study. Surface EMG activity of both trapezius muscles was recorded and averaged after electrical stimulation of the median and peroneal mixed nerves. The recordings were performed during supine and erect posture in nine subjects to evaluate of the effect of postural differences on reflex response. Reflex recordings were also performed in six subjects from some other muscles together with the trapezius by the stimulation of the peroneal nerve. Reflex responses including three components were recorded from the trapezius muscle (unilateral or bilateral) by electrical stimulation of the peroneal nerve. The most stable of them was the second component (23/31) which had a latency of 72.6 ± 7.9 ms for the ipsilateral, and 74.2 ± 8.5 ms for the contralateral trapezius (15/31). For median stimulation, the first component recorded at 32.0 ± 6.7 ms was the most stable (25/31). The second component was more frequently recorded on the contralateral side (14/ 31). Erect posture increased the amplitude of these components. Upper and lower extremity proprioceptive inputs modulate the EMG activity of the trapezius. This modulation probably related with postural adjustments. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Long latency reflexes (LLR) mostly recorded from upper limb distal muscles, and a cortical contribution in the generation of these reflex responses, have been generally accepted (Deuschl and Lücking, 1990; Cruccu and Deuschl, 2000). These reflexes have generally been recorded by rapid mechanical changes in the muscle length (Sinkjaer et al., 1988; Toft et al., 1991; Mrachacz-Kersting et al., 2006). Electrical stimulation of the peripheral nerve can also generate these reflexes from distal muscles (Deuschl and Lücking, 1990; Cruccu and Deuschl, 2000; Alexander and Harrison, 2003; Mrachacz-Kersting et al., 2006). LLRs recorded from proximal muscles of the upper and lower limbs have also been studied (Kavounoudias et al., 2001; Kagamihara et al., 2003; MrachaczKersting et al., 2006). Long latency reflexes obtained from proximal and distal muscles may include two or three components depending on target muscle (Mrachacz-Kersting et al., 2006). It was suggested that monosynaptic excitation of alpha motor neuron generates the first component; however, the origin of later components is not known exactly (Matthews, 1984). Some strong evi⇑ Corresponding author. Tel.: +90 256 4441256x114; fax: +90 256 2146495. E-mail addresses: [email protected], [email protected] (C. Tataroglu). 1050-6411/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2010.09.011
dences regarding a supraspinal and transcortical contributions to these late components have been reported (Kavounoudias et al., 2001; Kagamihara et al., 2003; Mrachacz-Kersting et al., 2006). Lower extremity inputs carry useful information for the preparation of posture. In addition, periscapular muscles may have an important role in postural adjustments (Bloem et al., 2000; Kavounoudias et al., 2001; Vuillerme et al., 2005). It has been demonstrated that some axial muscles and periscapular muscles have particular monosynaptic and polysynaptic reflexive properties, in the same way as some other axial muscles (Deuschl and Lücking, 1990; Alexander and Harrison, 2002; Ertekin et al., 2006). A reflex connection between some periscapular muscles and hand muscle afferents has recently been reported (Alexander and Harrison, 2003). In that paper, the authors concluded that scapular muscles help efficient use of hand muscles. On the other hand, Marsden et al. (1981) observed a reflex response from the pectoralis major by the mechanical stretch of thumb flexors, and this response is referred as a postural reflex. If this connection between upper extremity mixed nerve afferents and periscapular muscles helps postural adjustments, lower extremity proprioceptive afferents may also have a connection with these muscles. In this study, we investigated the reflex connection between upper and lower extremity mixed nerve afferents and bilateral tra-
78
C. Tataroglu et al. / Journal of Electromyography and Kinesiology 21 (2011) 77–81
pezius muscle innervations. Demonstration of these reflex connections can be important for further studies designed to investigate central postural mechanisms.
2. Materials and methods Thirty-one healthy volunteers aged between 18–42 years (mean 26.9 ± 6.8) participated to the study. No history of systemic disorder or toxic exposure was recorded in any subject. All subjects gave informed written consent and the local ethics committee approved the study. Routine nerve conduction studies of median, ulnar, peroneal and sural nerves were normal in conventional electrophysiological testing. Reflex recording: A surface electromyogram was recorded with Ag/AgCl surface cup electrodes from both right and left trapezius muscles simultaneously. Active and reference surface electrodes were placed 3 cm apart on the upper fibers of the trapezius muscle. Active electrode was placed at the superior border of the shoulder just medial to the acromioclavicular joint and the reference was placed at inferomedial side to the active electrode. 20–40 traces were averaged. At least 2 averaged traces were recorded and superimposed. Amplifier filters were between 20 Hz and 3 kHz. Oscilloscope sweep time was 300 ms. Electrode impedance was kept below 20 kX. A standard bipolar surface stimulator was used for stimulation. Stimulus duration was 1 ms. Stimulus frequency was random; however electrical pulses were delivered every 3– 5 s. The median nerve was stimulated at the wrist level and the peroneal nerve was stimulated at the level of the capitulum fibula. The peripheral nerves on the right side were chosen for stimulation. These nerves were stimulated by 1 ms square-wave pulses. Stimulus intensity was chosen as twice the motor threshold (2XMT) because Kagamihara et al. observed that facilitation of H reflexes recorded from far away muscle after median nerve stimulation increased after the level of 1.6 MT (7). This stimulation intensity was not painful for subjects. Initially, recording was performed on both trapezius muscles in the resting state (trapezius muscle inactive) in order to eliminate any startle reflex. This recording was performed while the subject was sitting on a comfortable armchair. After this initial evaluation, electrophysiological recordings were made while the subject was in a standing position. Mild and stable muscle activity (shoulder girdle elevation) was requested from subjects. This muscle activity was about 20% of maximal voluntary muscle activity for each muscle and this muscle activity was easily provided during erect posture of the subject. Underlying muscle activity was monitored by auditory feedback and this muscle activity continued during the evaluation. Surface electromyographic signals were picked up from both sides simultaneously. A Medtronic-Keypoint EMG machine (version 5.06) was used for stimulation, recording and amplification of EMG activity. The experiment was repeated by cutaneous nerve stimulation. This procedure was performed by the electrical stimulation of the superficial radial nerve and sural nerve in ten subjects. Initially, sensory perception thresholds were determined for these cutaneous nerves. For cutaneous stimulation, stimulus intensity was accepted as three times the sensory perception threshold. The superficial radial nerve was stimulated at 10 cm proximal to the wrist by standard surface electrodes. The sural nerve was stimulated from just behind the lateral malleolus. Stimulus duration was 1 ms and frequency was random and interstimulus interval was not below than 3 s. The degree of voluntary muscle activity of trapezius was the same with mixed nerve stimulation. The other stimulation and recording conditions were the same as in the previous experiment.
An attempt was made to record reflex responses from some other muscles in addition to the trapezius by the stimulation of a unilateral peroneal nerve to exclude an interlimb reflex contribution to the responses when recording from the trapezius. These muscles were also tested on both sides. Simultaneous recording of bilateral cervical paraspinalis (C6–C7 level), deltoideus, biceps and masseter were performed on six subjects in a standing position. Bipolar surface recording were also performed from these muscles. A slight voluntary EMG activity (20% of maximal voluntary force) was maintained during the analysis in all muscles. Bipolar recording electrodes were placed on the cervical paraspinalis muscle. The active electrode was located 2 cm lateral to the spinous process of the C7 vertebra and the reference electrode was located 3 cm caudal to the active one. For the deltoideus and biceps muscles, the active electrode was located on the belly of the muscle and the reference electrode was located on the tendon. For the masseter, the active electrode was placed on the belly of the muscle and the reference electrode was placed on the zygomatic bone. The recording and stimulation conditions described above were the same for this experiment. In nine subjects, reflex recordings were performed during sitting and stance position. During sitting position subjects were requested to make a slight shoulder elevation. Same muscle activity of trapezius was continued during stance position. During neutral stance position of shoulder, a slight muscle activity of both trapezius are already continued. Other stimulating and recording parameters were same with previous experiments. For data analysis, the onset latencies and peak to peak amplitudes of each component reflex response were analyzed. The onset latency of the response was accepted as the first clear deflection from the baseline. All electrophysiological analysis was performed by the same investigator. Statistical analysis: descriptive statistics were performed. Additionally, amplitude differences of reflex responses between during supine and erect posture were analyzed by T test. Two tailed tests were used and p < 0.05 was considered as significant. 3. Results 3.1. Median nerve stimulation Trapezius long latency reflexes were recorded in all subjects by the stimulation of the median nerve. Reflex responses obtained from both ipsilateral and contralateral trapezius muscles by the stimulation of median nerve included three components (ipsilateral-M1, M2, M3; contralateral-cM1, cM2, cM3) (Fig. 1). Their latencies were 32.0 ± 6.7 and 52.1 ± 4.3 ms for ipsilateral, and 31.8 ± 7.7 and 51.3 ± 5.3 ms for contralateral. A last component (M3 and cM3) was recorded at 72.5 ± 5.6 and 96.5–127.5 ms from ipsilateral and contralateral trapezius, respectively, however its frequency was very low. The most stable component was the first component (M1) for ipsilateral (25/31subjects) and the second (cM2) for the contralateral response (18/31 subjects). No response was recorded by cutaneous stimulation. Tables 1 and 2 summarize electrophysiological data. 3.2. Peroneal nerve stimulation Latency reflexes of the trapezius of 28 out of 31 subjects were recorded. Reflex responses were recorded from both the ipsilateral and contralateral trapezius by electrical stimulation of the peroneal nerve. No response was obtained while the trapezius muscle was relaxed. An early component (ipsilateral-P1 and contralateral-cP1) was recorded at 44.2 ± 5.6 and 47.6 ± 8.4 ms from both trapezius muscles, respectively. A second component (ipsilateral-
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Fig. 1. Trapezius long latency reflexes obtained by the stimulation of median (A) and peroneal nerve (B). Upper traces were recorded from ipsilateral, bottom traces were recorded from contralateral trapezius. In this subject, amplitudes of reflex responses obtained from contralateral trapezius smaller than those obtained from ipsilateral trapezius.
Table 1 Latency values of trapezius long latency reflexes. Ipsilateral
M1–cM1 M2–cM2 M3 P1–cP1 P2–cP2 P3
Contralateral
Latency (ms)
Range
Latency (ms)
Range
32.0 ± 6.7 (n:25) 52.1 ± 4.3 (n:18) 72.5 ± 5.6 (n:5) 44.2 ± 5.6 (n:10) 72.6 ± 7.9 (n:23) 101.5 ± 5.7 (n:2)
21.7–40.6 47.2–62.8 66.0–80.5 32.5–51.3 60.0–88.0 97.5–105.5
31.8 ± 7.7 (n:7) 51.3 ± 5.3 (n:14)
23.3–40.8 41.3–56.6
47.6 ± 8.4 (n:6) 74.2 ± 8.5 (n:15)
36.8–58.8 41.3–56.6
M1, M2, M3: first, second and third components of median stimulated trapezius long latency reflexes. cM1, cM2: first and second components of contralateral median nerve stimulated trapezius long latency reflexes. P1, P2, P3: first, second and third components of peroneal stimulated trapezius long latency reflexes. cP1, cP2: first and second components of contralateral peroneal nerve stimulated trapezius long latency reflexes.
Table 2 Amplitude values of trapezius long latency reflexes. Amplitudes (lV)
M1–cM1 M2–cM2 M3 P1–cP1 P2–cP2 P3
Ipsilateral
Contralateral
120.4 ± 57.8 150.0 ± 50.0 178.6 ± 63.6 86.2 ± 52.8 112.7 ± 74.8 90.0 ± 61.8
82.2 ± 26.8 106.7 ± 74.2 141.7 ± 73.6 111.2 ± 74.0
P2 and contralateral-cP2) was recorded at 72.6 ± 7.9 and 74.2 ± 8.5 ms, respectively. The most stable component was P2 on both sides (23/31 for the ipsilateral side and 15/31 for the contralateral side) (Fig. 1). Occasionally, a third component was observed at the ipsilateral trapezius. No response was recorded by cutaneous stimulation, nor was any response recorded from other muscles by stimulation of the peroneal nerve. Tables 1 and 2 demonstrate the electrophysiological data regarding trapezius long latency responses evoked by stimulation of the peroneal nerve. Effect of Posture: Reflex responses were amplified during erect posture by the stimulation of both lower and upper extremities (Fig. 2). The amplitude of trapezius long latency reflex by the stim-
ulation of median nerve (M1) was increased during erect posture from 85.2 ± 33.2 lV to 118.7 ± 28,6 lV (p: 0.001). The amplitude of second component (P2) of trapezius long latency reflex by the stimulation of peroneal nerve was also increased during stance from 67.9 ± 32.8 lV to 110.7 ± 42.8 lV (p: 0.001). 4. Discussion In this study, long latency reflex responses were only recorded from both trapezius muscles by the non-nociceptive electrical stimulation of upper and lower extremity mixed nerves, and these reflex responses were only recorded during slight voluntary activity of the trapezius. Also, cutaneous stimulation of upper and lower extremities failed to generate any reflex response. Our results suggested that there was a reflex connection between upper and lower extremity muscle afferents and trapezius muscle innervations. Alexander and Harrison (2003) recently demonstrated a reflex connection between hand muscle afferents and shoulder girdle muscles. They described a reflex response of the trapezius obtained at about 35 ms by the electrical stimulation of upper extremity mixed nerves. The authors estimated that its central delay was about 18 ms and this lag was sufficient for a supraspinal route of reflex circuit. In the present study, we showed that late responses were also recorded from the contralateral trapezius. The delayed component (cM2) was more frequently recorded from the contralateral trapezius than the first one. However, a series of reflex responses to stimulation of the median nerve were observed in the present study, which included three components. The latency of the first component was similar to that of the previous study. The second component (cM2) was recorded more frequently from the contralateral trapezius. M3 was not a stable response. Reflex activity of the trapezius muscle in response to stimulation of lower extremity mixed nerves included three components. The first and second responses were mostly recorded from both ipsi- and contralateral trapezius muscles. The first response was obtained at about 40 ms, and had a short latency. This response cannot be attributed to a supraspinal generator because its latency does not permit a cortical generator. Therefore, a spinal generator, probably a propriospinal system, must be responsible in the generation of this response. However, the latency of the P2 component (about 70 ms) may include a supraspinal and even a transcortical pathway. A third component observed at about 100 ms was recorded mostly unilaterally and its frequency was very low.
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Fig. 2. Erect posture amplified trapezius long latency reflexes by stimulation of both median and peroneal nerves. Upper traces are from ipsilateral trapezius, bottom traces are from contralateral trapezius. By the erect posture both ipsilateral and contralateral responses were amplified.
Cutaneous stimulation failed to generate these reflex responses from stimulation of the upper and lower extremities. The same finding was observed by Alexander and Harrison for upper extremity stimulation and recording of the trapezius. In fact, some studies regarding long latency reflexes recorded from far-away muscles also gave similar results (Marque et al., 2001; Vuillerme et al., 2005; Lourenço et al., 2006). However, long latency reflexes obtained from distal hand muscles can also be evoked by the stimulation of pure cutaneous nerves (Deuschl and Lücking, 1990). Additionally, Zehr et al. (2001) found that excitation of cutaneous afferents can modulate EMG activity of far-away muscles. However, train stimulus was used to evoke late responses from faraway muscles in their study and these responses were accepted as interlimb reflexes. It is believed that these reflexes were generated by propriospinal interlimb connections located in spinal cord and have shorter latency than long latency reflexes (Kagamihara et al., 2003). On the other hand, Kavounoudias et al. (2001) showed that tactile stimulus can also affect postural responses like proprioceptive inputs; however stimulus frequency of tactile stimulation was different from the proprioceptive inputs for this aim. They concluded that tactile and proprioceptive inputs have complementary role in the maintenance of posture. According to this study tactile stimulation can influence the EMG activity of far-away muscles, however, long latency reflexes of trapezius could not obtained in our study by cutaneous stimulation. Startle reflex as a late response could be erroneously accepted as long latency reflexes of the trapezius obtained in the present study since both responses have similar latencies (Walls-Sole et al., 2008). Startle responses can be recorded during relaxed state of muscle and easily habituate. However, responses of the trapezius in the present study were obtained only in contracted muscle. Also, we did not observe any habituation in our experiment. Long latency reflexes have been recorded during voluntary activation of the muscle. These responses reflect a modulation of EMG activity of target muscle by a specific stimulation (electrical or mechanical) (Tarkka and Larsen, 1986). Additionally, these responses could also be conceived as an interlimb reflex, but these responses were not recorded from other far-away muscles and cutaneous stimulation failed to record any response in the present study. Since train stimulus was used in
the recording of interlimb reflexes, it is unlikely that responses recorded in the present study could be an interlimb reflex as mentioned above (Zehr et al., 2001). Our results also suggested that the reflex responses obtained from trapezius by the stimulation of both upper and lower extremity mixed nerves affected from postural changes. Supine posture enlarged these responses. We believe that electromyographic activity of the trapezius was the same during the recording of trapezius in the different postural conditions however any special equipment monitoring muscle force level was not used in the present study. This finding suggested that neural circuits responsible in the postural adjustments may have a role in the generation of these responses. In brief, lower extremity muscle afferents can modulate electromyographic activity of the trapezius in the same way as hand muscle afferents. This modulation may have a supraspinal contribution. Neural mechanisms responsible in postural control may have a role in the generation of these responses.
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Cengiz Tataroglu graduated from Aegean Universıty _ Medical Faculty-Izmir at 1985. He completed his neurological residency at 9 Eylul University-Izmir between 1992-1997. He Works in Adnan Menderes University Medical Faculty as associated professor of neurology from 2004. His scientific interested areas are clinical neurophysiology and clinical neuromuscular disorders.
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Fatma Kursad Kucuk is graduated from Dokuz Eylul University Medical Faculty (Izmir) at 1997. She worked as a resident in Neurology Department of Dokuz Eylul University Medical Faculty, Department of Neurology between 1999-2004. She is working as an neurologist in the Mugla State Hospital since 2004. Her scientific interested areas are demyelinating disease and neurophysiology.
Ayca Ozkul is graduated from Eskisehir Osman Gazi University Medical Faculty at 1997. She worked as a resident in Neurology Department of Adnan Menderes University Medical Faculty between 1999-2004. She is working as an assisstant professor in the same department since 2006. Her scientific interested areas are neurological intensive care and neurophysiology.