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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   kfc@sunrise.hk.edu.tw
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:
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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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