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Influences of neck position and visual afferents on cardiac autonomic activity during diagonal shoulder resistance exercise 1 2 Fang-Chuan Kuo , Jung-Charg Lin 1 Institute of Physical Therapy, Hung Kung University, Taiwan email@example.com 2 Institute of Physical Education, National Taiwan Normal University, Taiwan Introduction Diagonal shoulder resistance exercise (DSRE) is commonly used to improve functional activities in neural lesion patients. To provide more sensory inputs, it usually combines with neck movement and visual afferents during DSRE. However, there are conflicting data concerning the influences of neck position and visual inputs on cardiovascular system. The aim of this study was to evaluate the effects of neck position and visual following on the cardiac autonomic activities during DSRE. Methods Heart rate (HR) and mean artery pressure (MAP) were continually measured through electrocardiography and indirect blood pressure monitor. Power spectrum was used to analysis the fluctuations of heart rate variability（HRV）, a marker of cardiac autonomic activities, in 13 healthy male subjects (mean age 21.3±1.5 yr). DSRE protocols were 30% of 1 RM, 30 repetitions per minute for four minutes. Subjects were assessed for HRV during the following four experimental conditions in balance order. The four trails were (1) neck in midline with eye closed (NMEC), (2) neck in hyperextension with eye closed (NEEC) to activate otoliths and neck muscle afferents, (3) neck in midline with visual following with hand (NMVF) to activate visual afferents, or (4) neck in hyperextension with visual following with hand (NEVF) to activate otoliths, neck muscle and visual afferents. Results There are no significance influences of neck position or visual following on the HR and MAP in four trails. The normalized high-frequency power (HFnu) of HRV had 6.5 and 11.1% respectively increased during NEEC and NEVF than NMEC (P<0.05) and the normalized low-frequency power (LFnu) was decreased by 6.7, 2.6 and 6.4% respectively during NEEC, NMVF, and NEVF than NMEC in recovery stage (P<0.05) Table 1. Discussion/Conclusion Our results indicate that the cardiac sympathetic nerve activity is significantly altered by NEEC and NEVF in recovery stage, suggesting the influences of the otolith organs, neck and visual afferents on autonomic modulation of the heart. For neuroanatomical pathways exist between the vestibular, visual and cardiovascular systems of animals, we speculate these reflexes also are powerful activator of cardiac autonomic nerve regulation during dynamic exercise in human. References Ray CA et al (2002). Clin Exp Pharm & Physio 29: 98-102 Jian BJ et al (1999). J Appl Physio 86: 152-6 Diagonal shoulder resistance exercise (DSRE) commonly used to improve the function of neural lesion patients. To provide more sensory inputs, it usually combines with neck movement and visual afferents during DSRE. However, there are conflicting data concerning the influences of neck position and visual afferents on cardiovascular system. Previous studies reported that the passive head-up tilt and head down neck flexion position, caused specific changes of both otoliths and neck muscle afferents, result in HR, BP, heart rate variability (HRV) and muscle sympathetic nerve activity (MSNA) changes.1-7 On the other hand, a repeated maneuver like a serious of rhythmical rotation of the eyes is know to temporarily reduce the gain of the horizontal vestibulocollic reflex 10-15% in health human.8In an attempt to gain a greater understanding of cardiac autonomic reflex during resistance exercise, we examined the influence of neck, otolith organs and visual inputs on HRV during shoulder exercise. Exercise-induced increase in HRV is primarily mediated by the activation of skeletal muscle afferents, 1, 9-12 however, during exercise, a number of neural reflexes can modulate muscle-related increases in HRV, HR, and mean artery pressure (MAP). The vestibular system, visual, and skeletal muscles play important roles in exercise and can regulate sympathetic outflow. It is reasonable to suspect that the vestibular and visual input may modulate sympathetic outflow during activation of the skeletal muscle afferents. Ray et al. found isometric handgrip and head down neck flexion in prone performed together elicited MSNA and arterial pressure responses that were equal to the sum of each stimulus when performed individually.2, 5 Thus, the further increase in MSNA via otolith stimulation during isometric handgrip when arterial pressure is markedly change indicates vestibulosympathetic reflexes is a powerful activator of blood pressure and flow regulation during dynamic exercise. 10, 13 Ray et al. also found that MSNA fail to increase when head-down neck extension in supine.2 Whereas other evidence from Hume reported MAP and HR both decreased during head down neck extension for 3-min and 30- min resting trials, showed that the lack of an increase in sympathetic outflow during head extension.3 We speculate these otolith stimulation are opposite during neck flexion and extension, it might be expected that sympathetic out flow of HRV would different between supine neck extension and prone flexion. Thus it needs more studies to clarify. Furthermore there are no studies illuminating the sympathetic adjustments to diagonal shoulder resistance exercise. An understanding of the sympathetic and cardiovascular adjustment to shoulder exercise is important because the diagonal shoulder resistance exercise is commonly used to facilitate normal upper extremity movement pattern and improve activity of daily living function. Therefore the aim of this study was to evaluate the effects of neck hyperextension and/or visual following during diagonal shoulder resistance exercise on the cardiac autonomic control. We hypothesized the cardiovascular activity would be apparent during head hyperextension but not head midline position. Similarly, we hypothesized that measures of HRV would be consistent with heightened sympathovagal balance during head hyperextension but not during head midline position. Methods: Subjects Thirteen health males (age 21.3±1.5 yr, height, 169.5±3.89 cm, weight 64.33± 6.85kg) normotensive, not on medication, and free of any known vestibular and cardiovascular disorder were studied. After a medical history and verbal explanation of the testing procedures, the written, informed consent was obtained from all subjects. The subjects were restricted to eat or drink coffee for at least 2 hours before testing. Experimental design To determine the interaction of the vestibulosympathetic and visual to cardiovascular reflexes, subjects performed four experimental trails in the supine position. The fist trail examined responses to head hyperextension 30°with eye covered. (ie., vestibular activation of otolith organs). The second trial examined the responses to head in midline with visual covered. The third trial examined responses during simultaneous performance of head hyperextension and visual following. The fourth trial examined responses to visual following with head in neutral (visual activation). The order of the four trails was randomized with one-day rest period interspersed between trials. The experiments were performed in the afternoon in a laboratory at ambient temperature 21 to 23oC. Each trail began with the head in the midline position for 3 min. The exercise protocol consisted of 120 repetition at 30 % of maximum voluntary contraction was performed with the arm extended on the right shoulder. This work intensity was chosen to elicit heart rate variability and presser response kept for 4-5 minutes. The electrical pulley system was used to display the force output on the screen to monitor the rhythmic and force output. Hemodynamic measurements and HRV evaluation Continuous measurements of arterial blood pressure were made throughout the entire experimental protocol by a Colin 7000 (San Antonio, TX) noninvasive arterial tonometry device. This device consisted of a sensor positioned over the left radial artery at the wrist and an occlusion cuff positioned around the upper left arm. The Colin 7000 was interfaced with a Biopac MP100 data-acquisition system (Santa Barbara, CA) using the AcqKnowledge ACK100 software program (Santa Barbara, CA) and was calibrated before each experiment. HRV was evaluated in accordance with the guidelines of the Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (18). The Biopac MP100 data-acquisition system and AcqKnowledge ACK100 software program were used to collect a continuous electrocardiogram (ECG) at a sampling rate of 1000 Hz during each of the four trails. The ECG was visually inspected for nonsinus beats and plotted as a tachogram of the heart period. The spectral power density of the waveform was derived via a 1024-point linear fast Fourier transformation using a Hamming window. The resultant power density spectra were then analyzed for total power (TP) (0.00-0.40 Hz), LF (0.04-0.15 Hz), and HF (0.15-0.40 Hz). To estimate the relative contribution of these power bands to TP, HF and LF were be normalized (Lfnu and Hfnu, where nu is normalized unit) by dividing each by TP minus very-low-frequency power (VLF) (0.00-0.04 Hz) and multiplying this value by 100. (18) The formula is HFnu = [HF÷(TP-VLF)]．100 LFnu = [LF÷(TP-VLF)]．100 Furthermore, the ratio of LF to HF (LF/HF) is reported as a measure of autonomic balance. The normalization procedure is particularly helpful in allowing comparisons between subjects or experimental conditions characterized by large differences in total power or DC noise. Data analysis Responses during each trial and the significance of head position and visual on the dependent variables in four trails were evaluated by using repeated-measures ANOVA. A significance level of P＜0.05 was used for all statistical tests. All values are means ±SE. Results: The HR, MAP and HRV responses during exercise phase of the four experimental trails are presented in Table l. There are no significance of head position and visual following on the dependent variables in four trails during exercise phase. Table 2 showed the responses during recovery, neither MAP nor heart rate was affected significantly by changing head position and visual following in recovery stage. However, the results showed there are 6.5, 6.1, and 11.1 % increase in the HFnu during HEVC, HMVF, and HEVF than HMVC in recovery stage (P<0.05 Tab2, fig2). 6.7, 2.6 and 6.5% decreased the LFnu during HEVC, HMVF, and HEVF than HMVC in recovery stage (P<0.05 Tab2, fig2). The change in MAP for the four trails is show in Tab3.During exercise stage MAP increased from baseline level by the same magnitude during all the experimental trial (from 10.43±6.10 , 12.75±2.17, 13.35± 3.03, 9.57±3.45, mmHg , HMVC, HEVC, HMVF and HEVF, respectively; P＞ 0.05).Also, the recovery in MAP from exercise level by the same magnitude during the recovery stage (from 10.08±5.43,14.91±4.60, 9.07±2.80, and 14.89±2.88 mmHg, HMVC, HEVC, HMVF and HEVF, respectively, P＞0.05).HR responses to exercise for the four trails are show in Tab 3 .HR increased from baseline level by the same magnitude during all the experimental trial (from 39.70±8.2 , 38.10.6±10.6, 29.63± 5.49, 37.675±4.89 beats/min, HMVC, HEVC, HMVF and HEVF, respectively; P＞ 0.05).Also, the recovery in HR from exercise level by the same magnitude during the recovery stage (from34.21±8.1,22.03±4.16, 30.86±6.89, and 31.53±4.52 beats/min, HMVC, HEVC, HMVF and HEVF, respectively, P＞0.05). Discussion Neuron anatomical pathways exist between the vestibular and cardiovascular systems of animals. Electrical stimulation or natural vestibular stimulation of the vestibular nerves in animals results in changes in sympathetic activity to different vascular beds. 15-19The major finding from this study is that neural interaction among the skeletal muscle, vestibular and visual reflexes for sympathetic and cardiovascular parameter is additive. This finding suggests that central modulation exists between these reflexes and the sympathetic output from these reflexes is dependent of each other in humans. Heart rate variability (HRV) has gained recent popularity as a noninvasive tool to estimate autonomic control spectral analysis of beat-to-beat variations in the R-R interval provides some information about sympathovagal balance regarding the neural control of the cardiovascular system. Within the power spectra of the R-R interval, the majority of the oscillations occur as peaks within the range of 0.04-0.4Hz. The high-frequency power (HF) (0.15-0.4 Hz) seems to reflect vagal activity to the heart; whereas the low-frequency power (LF) (0.04-0.15 Hz) represents vasomotor activity and reflects both sympathetic and parasympathetic modulation. 16. Our data indicate the NE and combine visual following results in an increased ANS balance during recovery stage, identified by increases in HFnu and decreases in LF/HF and HFnu. These findings are consistent with the hypothesis that NE and VF elicit increases in vagal nervous system activity. Furthermore, the LF and LF/HF power are especially sensitive to sympathetic modulation of the heart; So we provide evidence that HE and VF may further elicit a sympathetic withdrawal during recovery stage. One evidence for a vestibular-mediated regulation in sympathetic outflow is that MSNA fails to increase when head down neck extension is performed in the supine position2 Lee’s study reported the effect of prone head flexion on HRV indicated that HDNF resulted in lower high-frequency and higher low frequency power, along with higher lower-frequency-to-high-frequency ratio.1 Otolith stimulation is opposite during neck flexion and extension, it might be expected that sympathetic out flow of HRV would decrease during supine neck extension. We propose the central integration of otolith afferent input is different between head flexion and extension. Hume reported both MAP and HR decreased during head down neck extension for 3-min and 30- min resting trials. Their results showed that the lack of an increase in sympathetic outflow during head extension.3 The present study adds strength to the concept that the vestibular apparatus during head hyperextension mediates the reduction decrease in HR and MAP that contrast to that skeletal muscle increase sympathetic afferents and thereby possible contribute to the cardiovascular response to exercise. Neither MAP nor heart rate was affected significantly by changing head position. With a significant change in spectral parameters, that indicates HRV parameters are sensitivity to detect tinu changes in autonomic balance. There is no strong indication that visual following modulating cardiac autonomic activity may have been attributable to the lack of sufficient vestibule-ocular stimulus. The results are consistent with Shortt and Ray’s report that blindfolding subjects resulted in no noticeable differences in the autonomic response to HDNF. 4, 5 Except otolitic organs inputs and visual following there are several other potential afferents possible influences the HRV modulation. These include the central command, muscular afferent, respiratory pattern, and nonspecific pressure receptors in the head on autonomic activity during exercise. Normand and Bolton ‘s6, 7 study measured blood flower, mean arterial pressure, and heart rate in two body position (prone and sidling) and three head positions (midline, flexion, extension). Their results suggested that otolithic and neck mechanoreceptors exert significant influences over the cardiovascular system. These means the neck afferents, particularly muscle spindles, are well located and suited to provide information about changes in body position with respect to the head and vestibular signals. In our study HR and MAP were not significantly different during any of the trails, these factors appear to rule out the role of the arterial baroreflex, but the time course or exercise intensity of our measures may not have been rapid or strong enough to alter the baroreceptor activity. By the ways, the investigator paced the exercise speed at 30 repetitions per min to minimize the effect of central command and muscle afferent on afferent autonomic outflow, so the rang of motion and force output were at similar level. Although it has been documented that respiratory factors influence HRV, 20 neither O2 consumption nor respiratory rate was altered significantly in each trail. Therefore, our data suggest that respiration did not play a role in mediating the changes in HRV in this study. One limitation of this study is that we were unable to account for the possible influence of nonspecific pressure receptors in the head, However, Hume and Ray provided evidence against the role of such receptors in mediating autonomic alternations during HDNF, and we propose the central integration of nonspecific pressure receptors in the head is similar between HDNF and HEVC. In conclusion, we found that HE, VF significantly alters HRV that a parasympathetic activation accompanies the sympathetic withdrawal elicited by HE and VF during recovering stage. These findings suggest that the otolith organs, neck and visual afferents play a significant role in mediating autonomic outflow to the heart. References 1. Lee CM. Wood RH, Welsch MA. Influence of head down and lateral decubitus neck flexion on heart rate variability. J Appl physiol 2001; 90(1): 127-32. 2. Ray CA. Interaction between vestibulosympathetic and skeletal muscle reflexes on sympathetic activity in humans. J. Appl. Physiol 2001; 90: 242-7. 3. Hume KM, Ray CA. Sympathetic responses to head-down rotations in humans. J Appl. Physiol. 1999; 86: 1971-6. 4. Shortt TL, Ray CA. sympathetic and vascular responses to head-down neck flexion in humans. Am J Physio. 1997; 23:1780-6. 5. Ray CA, Monahan KD. The vestibulosympathetic reflex in humans: Neural interactions between cardiovascular reflexes. Clin Exp Phorm & Physio 2002; 29, 98-102. 6. Normad Herve, Etard Olivier, Denise P. Otolithic and tonic neck receptors control of limb blood flow in humans. J. Appl. Physiol. 1997; 82:1734-8. ． 7. Bolton PS, Ray CA Neck afferent involvement in cardiovascular control during movement. Brain Research Bulletin. 2000; 53:45-49. 8. Paquet N, Watt DG, Lefebvre L. Rhythmical eye-hand-torso rotation alters fore-after head stabilization during treadmill locomotion in humans. J Vestib Res 2000; 10:41-5. 9. O’Sullivan SE, Bell Christopher. The effects of exercise and testing on human cardiovascular reflex control. J. Autonomic Nervous system. 2000; 81:16-21. 10. Samuel L, Stelle JR, Ray Chester. Comparison of sympathetic nerve responses to neck and forearm isometric exercise. Med & Sci Sports & Exerc 2000 32:1109-13. 11. Fukushiman K. Cortico vestibular interactions: anatomy, electrophysiology, and functional considerations. Exp Brain Res. 1997; 117:1-16. 12. Gonzalez-Camarena R, S. Carrasco-Sosa, Roman-RAMOS, M.J GAitan- Gonzalez, V. Medina-Banuelos, J. Azpiroz-Leehan. Effect of static and dynamic exercise on heart rate and blood pressure variabilities. Med Sci Sports Exerc 2000; 32:1719-28. 13. Ray CA. Interaction of the vestibular system and baroreflexes on sympathetic nerve activity in humans. Am J Physiol Heart Circ Physiol. 2000; 279: H2399-404. 14. Task force of the European society of cardiology and the North American society of pacing and electrophysiology. Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 1996; P3: 1043~1065. 15. Jian BJ, Cotter LA, Emanuel BA, Cass BP, Yates BT. Effects of bilateral vestibular lesions on orthostatic tolerance in awake cats, J Appl Physio 1999; 86(5): 152-6. 16. Steinbacher Jr BC, Yates BJ. Brainstem interneurons necessary for vestibular influences on sympathetic outflow. Brain Res. 1996; 720:204-10. 17. Yamagata Y, Bolton PS. The ventrolateral medulla of the cat mediates vestibulosympathetic reflexes. Brain Res 1991; 552: 265-72. 18. Yates BJ, Miller AD. Properties of sympathetic reflexes elicited by natural vestibular stimulation: Implications for cardiovascular control J. Neurophysiol. 1994; 71: 2087-92. 19. Iwamoto GA, Wappel SM, Fox GM et al. Identification of diencephalic and brainstem cardiorespiratory areas activated during exercise. Brain Res. 1996; 726: 109-22. 20. Discoll D, Dicicco GT. The effects of metronome breathing on the variability of autonomic activity measurements. Manipulative Physiol Ther 2000; 23(9): 610 -4. Table 1.Heart rate variability and mean artery blood pressure during the exercise stage NMVC NEVC NMVF NEVF P Value HR beat/min 108.61±7.68 109.15±10.97 100.25±5.31 104.77±6.20 p≧0.05 MPA mmHg 93.177±4.71 98.78±3.46 96.11±2.373 94.61±3.68 p≧0.05 Mean R-R, ms 633.4±31.5 670.1±24.7 650.1±17.3 634.2±20.1 p≧0.05 59.85±3.3 53.08±3.6 56.0±3.9 60.46±3.6 Hfnu ﹪ p≧0.05 39.2±0.033 45.9±3.6 43.1±3.9 39.8±3.8 Lfnu ﹪ p≧0.05 LF/HF 0.814±0.137 1.058±0.147 1.014±0.174 0.752±0.134 p≧0.05 Values are means± SE. HR, heart rate; MAP, mean arterial pressure; R-R, R-wave to R-wave; HF, high-frequency power; LF, lower frequency power; nu, normalized units; LF/HF, ratio of LF to HF; NMVC, head midline with visual cover; NEVC, head hyperextension with visual cover; NMVF, head midline with visual follow; NEVF, head hyperextension with visual follow.＊P≦0.05 vs. NMVC. Tab 2.Heart rate variability and mean artery blood pressure during the recovery stage NMVC NEVC NEVC NEVF P Value HR beat/min 74.40±2.90 87.11±12.89 69.39±6.06 73.23±3.39 p≧0.05 MPA mmHg 83.09±1.822 83.872±2.878 87.037±2.611 79.726±3.94 p≧0.05 Mean R-R,ms 825.6±46.8 831.1±29 823.5±28.4 812.5±25.4 p≧0.05 46.4±1.7 52.5±3.3 p＜0.05 Hfnu ﹪ 52.9±2.3＊ 57.5±3.3＊ 52.9±1.7 46.5±2.7 p＜0.05 Lfnu ﹪ 46.2±2.3＊ 50.3±2.1＊ LF/HF 1.170±0.078 0.920±0.089 1.066±0.088 0.96±0.126 p≧0.05 Values are means± SE. HR, heart rate; MAP, mean arterial pressure; R-R, R-wave to R-wave; HF, high-frequency power; LF, lower frequency power; nu, normalized units; LF/HF, ratio of LF to HF; NMVC, head midline with visual cover; NEVC, head hyperextension with visual cover; NMVF, head midline with visual follow; NEVF, head hyperextension with visual follow.＊P≦0.05 vs. NMVC. 140 HF LF LF/HF 120 100 80 NU 60 40 20 0 HMVC HEVC HMVF HEVF Fig.1.Effect of the HMVC,HEVC,HMVF,and HEVF on normalized unit high frequency(HF),low frequency(LF) power and the ratio of two frequency in exercise stage.*significant difference vs.nomalized HF HMVC, p<0.05.Q significant difference vs. normalized LF HMVC,p<0.05. 140 HFnu LFnu LF/HF 120 100 80 NU Q Q , 60 , , 40 20 0 HMVC HEVC HMVF HEVF Fig.2.Effect of the HMVC,HEVC,HMVF,and HEVF on normalized unit high frequency, lower frequency power and the ratio of the two frequency in recovery stage.Q significant difference vs. normalized HF HMVC,p<0.05. , significant difference in normalized LF HMVC,p<0.05. Tab3 The change in MAP and HR during exercise NMVC NEVC NMVF NEVF Exercise stage HR 39.70±8.22 38.13±10.61 29.63±5.49 37.67±4.89 beats/min MPA mmHg 10.43±6.10 12.75±2.17 13.35±3.03 9.57±3.45 Recovery stage HR 34.21±8.11 22.03±4.16 30.86±6.89 31.53±4.52 beats/min MPA mmHg 10.08±5.43 14.91±4.60 9.07±2.80 14.89±2.88 ＊ P≦0.05 vs. NMVC.
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