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3T functional magnetic resonance in healthy subjects: effects evaluation of MS6 scalp acupuncture

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3T functional magnetic resonance in healthy subjects: effects evaluation of MS6 scalp acupuncture
Methods and Materials
Results
Conclusion
References
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Authors: R. Zanardi, M. Maieron, C. M. Giovanardi, B. Tomasino; Udine/IT, San Lazzaro di Savena/IT, San Vito al Tagliamento/IT

Section: Purpose

Acupuncture is a therapy of inserting and manipulating fine filiform needles into specific body locations (acupuncture points) to treat diseases. Acupuncture is an ancient Chinese treatment that has been systematically used for over 2000 years (1). Currently, acupuncture is used widely all over the world, but its brain functional mechanism is not well understood.Scalp acupuncture (SA) has developed from traditional acupuncture since the Fifties. SA has combined the concept of cerebral cortex organization and its function with the principles of acupuncture, allowing treatment of diseases through needling of points on the scalp (2). Generally in SA the stimulation area corresponds with the functions represented in a section of the cerebral cortex. Scalp acupuncture is usually used to treat cerebrovascular diseases (stroke rehabilitation) and other central nervous system illnesses. SA indications are: paresis, asthenia, contralateral limb pain, contralateral central facial paralysis, disartria, afasia and face soreness. There is a SA standard system of 14 MS lines. (Micro-System Scalp-Point).The MS6 line, the anterior oblique parietal-temporal line, corresponds to the primary motor area, and goes from qianshenchong to GB6 (xuanli).

The MS6 line is divided into three segments:

  • the superior 1/5 which corresponds to the motor segment of the inferior limb and the trunk;
  • the middle 2/5 which correspond to the motor segment of the superior limb;
  • the inferior 2/5 which correspond to the motor segment of the face and language.

Whilst scientists have tried to clarify the underlying mechanisms of acupuncture since the 1950s, research involving the human central nervous system has been limited by the lack of non-invasive measurement methods. With the invention of functional magnetic resonance imaging (fMRI) in the early 1990s, a new tool became available that allowed non-invasive measurement of human brain activity with a temporal resolution of approximately 3s, and a spatial resolution of approximately 3mm. In the previous decade, an increasing number of studies applied fMRI to investigate acupuncture stimulation (3). The purpose of this study is to evaluate cortical activation after stimulation of the middle 2/5 of the MS6 scalp acupuncture line on the left side using fMRI.

 



 

Section: Methods and Materials

Fifteen healthy right-handed volunteers, one woman and fourteen men, aged 26-37 years, were recruited and consented to the study. Volunteer candidates suffering from neurological, mental or internal problems, drug abuse, alcohol abuse, or those with a history of cardiovascular or cerebrovascular disease and on medication that could affect cerebral blood flow were excluded. Caffeinated drinks such as coffee were restricted on the day of the examination (4). This study was approved by the Ethics Committee of our institute, and informed consent was obtained from the volunteers. They were acupuncture-naïve. 3 Tesla MRI was used; BOLD-EPI sequence 3D-TFE T1-weighted images on sagittal plane (echo time TE 3,7 ms, repetition time TR 8,1 ms, flip angle 8°, field of view FOV 240x240x170 mm, 170 slices, slice width 1.0 mm, matrix 240x240). and BOLD T2*-weighted gradient-echo EPI sequence (TE 35 ms, TR 1600 ms, flip angle 90°, FOV 230x230x116 mm, matrix 64x64) were acquired using 8 channel Sense coil. There were 29 slices, 5 mm width, the voxel size was 3.59x3.59x4 mm. Volunteers were positioned supine; the head was fixed by a sponge to minimize head movements; non-magnetic goggles were employed during fMRI tasks. Three explicit motor tasks were used in a blocked design fMRI paradigm:

  • (1) right and left alternating hand clenching movements (finger flexion-extension),
  • (2) tongue high-low movements and
  • (3) right and left foot flexion-extension movements (as control tasks).

In addition, one implicit motor imagery task: hand movement imagination was employed. Rotated hand images were presented; volunteers had to recognize whether the hand-stimulus corresponded to their own right or left hand by imagining their own hand movements. In addition, the hand-stimuli presented contained a red marker on one finger; in the control task volunteers had to decide whether the red marker was on the right or left side of the picture imagined upright. Participants were required to answer by using a custom made foot-response device.

A whole brain fMRI was performed before, and immediately after, two needle stimulation of the middle 2/5 of the MS6 line on the left side, corresponding to the motor segment of the superior limb (Fig. 1). Needle insertion was performed outside the magnet room by one experienced acupuncturist (R.Z.); needles were inserted 4-5 mm obliquely and retention was 30 minutes, with volunteers positioned supine. For acupuncture, disposable, stainless steel 0.30 mm x 25 mm (diameter x length) needles were used. After the needles were pulled out, fMRI was repeated in the same manner as before the acupuncture.

Fig. 1: FIG. 1:Stimulation (two needles 0.30 mm diameter, 25 mm length) of the middle 2/5 of the MS6 line on the left side. References: Neuroradiology Department, AOUSMM Udine/Italy
References: Neuroradiology Department, Azienda Ospedaliero Universitaria S.M.Della Misericordia di Udine - Udine/IT


Volunteers were presented with the Massachusetts General Hospital acupuncture sensation scales (MASS) to rate the sensations they experienced during acupuncture administration de qi (5), considering de qi does not refer to the sensation of the needle being inserted or withdrawn, but to the sensation felt when the needle is stationary. Prior to the procedure, the subject was told that the type and intensity of sensation would vary with different individuals and different acupoints, and that a range from nil to multiple sensations could be experienced. (Fig. 2).

Fig. 2: FIG. 2: The Massachusetts General Hospital acupuncture sensation scales (MASS). The scale includes 12 descriptors: soreness, aching, deep pressure, heaviness, fullness/distension, tingling, numbness, sharp pain, dull pain, warmth, cold, throbbing and a subject defined “other.”
References: Kong J, Gollub R, Huang T, et al.(2007) Acupucture de qi, from qualitative history to quantitative measurement. J Altern Complemen Med;13:1059-1070.

he fMRI data was processed using SPM5 Statistical Parametric Mapping software; Welcome Department of Imaging Neuroscience, London, UK http://www.fil.ion.ucl.ac.uk/spm).

After realignment, the images were normalized to the Montreal Neurological Institute (MNI) template, re-sampled at voxel size 2x2x2 mm, and smoothed spatially using a 6 mm FWHM Gaussian kernel to fulfill General Linear Model statistical requirements. Random effect analysis was performed over the entire brain. Voxel-by-voxel parameter estimation for the smoothed data was carried out according to the general linear model. The resulting estimated beta maps were compared using linear contrasts of each active and control condition, in order to test hypotheses about regionally-specific effects. A map of t-statistic values, the SPM(t)-map was obtained from this analysis. After computing the contrast for single subjects, group data was analyzed using a random effect model. A threshold of p<0.05, corrected for multiple comparisons, with a voxel height threshold of p<0.001 was employed. SPM Anatomy toolbox (Eickhoff et al., 2005) was used for the anatomical interpretation of the functional results.


Section: Results

Task-related activations were compared before and after acupuncture needling. Regarding explicit motor execution tasks, stimulation of the middle 2/5 of the MS6 line on the left side, corresponding to the upper limb motor segment, selectively influenced hand-explicit task-related motor activations.

When contrasting post-SA versus pre-SA, selective activation of the right precuneus was observed. In the control tasks (tongue and feet movements), no significant activation was found for the same comparison. Contrasting the right hand-left hand post-SA versus pre-SA showed selective activation of the left putamen (Fig.3).

Fig. 3: FIG. 3: Top row: Comparison of post-SA versus pre-SA: selective activation of the right precuneus Bottom row: Comparison of right hand-left hand post-SA versus pre-SA: selective activation of the left putamen. References: Neuroradiology Department, AOUSMM Udine/Italy
References: Neuroradiology Department, Azienda Ospedaliero Universitaria S.M.Della Misericordia di Udine - Udine/IT

Regarding the implicit motor task (hand movement imagination): independently of the imaginative motor or visual task, when comparing the post-SA versus pre-SA, selective activation of the left putamen and of the right caudate head was observed.

When comparing the implicit motor task post-SA (versus visual task) as controlled for pre-SA, a selective activation of the left area 7a (superior parietal lobe) and of the right thalamus (Fig.4) was noted.

Fig. 4: FIG. 4: Top row: Comparison of post-SA versus pre-SA independently of the motor or visual task: selective activation of the left putamen and of the right caudate head. Bottom row: Comparison of implicit motor task post-SA (vs visual task) controlled for SA: selective activation of the left area 7a (SPL) and of the right thalamus. References: Neuroradiology Department, AOUSMM Udine/Italy
References: Neuroradiology Department, Azienda Ospedaliero Universitaria S.M.Della Misericordia di Udine - Udine/IT

Psychophysical response

Acupuncture is often associated with a variety of specific sensations called de qi.

Of the fifteen volunteers in the study who experienced mild sensations: Six experienced soreness, five experienced numbness, four experienced throbbing, three experienced deep pressure, and two experienced respectively: heaviness, fullness/distension, tingling and aching.  Of those who experienced moderate sensations, two volunteers experienced deep pressure. Finally, one volunteer experienced a strong wellbeing sensation, one experienced a strong warmth and one experienced a strong fullness/distension (Fig. 5).

Fig. 5: FIG. 5: Bar graph showing sensation descriptors. References: Neuroradiology Department, AOUSMM Udine/Italy
References: Neuroradiology Department, Azienda Ospedaliero Universitaria S.M.Della Misericordia di Udine - Udine/IT


It is noteworthy that response times (millisec) were reduced during implicit motor work (hand movement imagination) execution after scalp acupuncture (Fig 6).

Fig. 6: FIG. 6: Graphic displaying volunteers’ response time before and after scalp acupuncture. M= implicit motor task; V= control visual References: Neuroradiology Department, AOUSMM Udine/Italy
References: Neuroradiology Department, Azienda Ospedaliero Universitaria S.M.Della Misericordia di Udine - Udine/IT


Section: Conclusion

Acupuncture has been widely used in China for three millennia as an art of healing, but its biological mechanism is not well understood. Although the clinical effect of acupuncture is generally accepted for certain diagnoses (6), such as knee pain, low back pain etc., controversy exists regarding the precise effect of acupuncture, especially for specific acupuncture points and meridians. Since the late 1990s, fMRI has successfully been used in acupuncture studies. (More than 80 studies and a dozen review articles have been published in the past 10 years). Several studies have been conducted to observe which part of the brain is activated after a specific acupoint is needled (7), or after multiple acupoints are needled (8), and to identify whether different methods of needling trigger different brain activations (8). A previous study was designed to investigate brain activity after acupuncture needles are pulled out (9). To the best of our knowledge, no previous fMRI study exists comparing explicit and implicit motor tasks before and after scalp acupuncture. This study was designed to perform fMRI before and immediately after needle stimulation of the middle 2/5 of the MS6 line on the left side, considering that in the context of acupuncture studies, a repetition of the stimulus in an on-and-off design does not reflect the typical way in which acupuncture is usually delivered (10). Hence, the use of blocked design in acupuncture fMRI studies has recently been criticized by several authors (10). Acupuncture has been shown to manipulate sustained influence over the brain, even after cessation of the needling stimulation, suggesting that acupuncture effects have a time-variant feature at each functional brain region mapped after the needling manipulation, and may be acupoint-specific (11).

With regards to explicit motor tasks, stimulation of the middle 2/5 of the MS6 line on the left side, corresponding to the upper limb motor segment, showed selective influence on hand explicit motor tasks. Contrasting post-SA versus pre-SA showed selective activation of the right precuneus. In the control tasks (tongue and feet movements) no significant activation was found. Contrasting right hand-left hand post SA versus pre showed selective activation of the left putamen.

Regarding implicit motor tasks (hand movement imagination): independently of the imaginative motor or visual task, in general, comparison of post-SA versus pre-SA showed selective activation of the left putamen and of the right caudate head. Comparison of implicit imaginative motor task post-SA (versus control imaginative visual task) versus pre-SA showed selective activation of the left area 7a (superior parietal lobe) and of the right thalamus.

The superior parietal lobe (SPL) plays a role in movement planning and spatial coding of reaching movements. In order to monitor location and identity of contralateral body parts needed for adjusting posture or guiding motor acts, this region is likely to integrate somatosensory and visual information; moreover activation in the SPL could be evoked when mental rotation is combined with motor imagery of hands (12).

The medial aspect (precuneus) of the superior parietal cortex plays an important role in maintaining an accurate and up-to-date representation of the current postural state of the body (13). As previously reported, change in the posture of the upper-limb is associated with a significant increase in BOLD activation in only one brain region-the superior parietal cortex, particularly the medial aspect (precuneus).

The basal ganglia are a group of nuclei of varied origin in the brain that act as a cohesive functional unit. They are situated at the base of the forebrain and are strongly connected with the cerebral cortex, thalamus and other brain areas. The basal ganglia are associated with a variety of functions, including voluntary motor control, procedural learning relating to routine behaviors or "habits" such as eye movements, and cognitive, emotional functions. Currently popular theories implicate the basal ganglia primarily in action selection, that is, the decision of which of several possible behaviors to execute at a given time (14).

The thalamushas multiple functions. It may be thought of as a kind of information switchboard. It is generally believed to act as a relay between a variety of subcortical areas and the cerebral cortex. A major role of the thalamus is devoted to "motor" systems. Through investigations of the anatomy of the brains of primates, the nature of the interconnected tissues of the cerebellum to the multiple motor cortices suggested that the thalamus fulfills a key function in providing the specific channels from the basal ganglia and cerebellum to the cortical motor areas (15).

A post-SA response time reduction during implicit motor work (hand movement imagination) execution was also noted. As highlighted in previous studies on mental rotation, response times increase in line with increased angular disparities, which indicates that the subject solves the task by mentally rotating the stimuli (12). Scalp acupuncture, which conditions a reduction in response time, is likely to improve performance in implicit motor tasks.

This study evaluated scalp acupuncture effects by comparing pre and post acupuncture stimulation.

In summary, a specific influence on implicit motor tasks was observed, with an increase in activation in the superior parietal lobe and a specific influence on hand explicit motor tasks with an increase in activation in the precuneus. These regions play an important role in maintaining an accurate and up-to-date representation of the current postural state of the body and participate in the accurate control and planning of movements. During explicit and implicit tasks, an increase in activation in the basal ganglia, left putamen, right caudate head, and in the right thalamus was also noted. These findings may shed light on the scalp acupuncture effects. The observation of specific cerebral activation patterns might explain the therapeutic effects of scalp acupuncture and confirms that Scalp Acupuncture has sustained influence over the brain, even after cessation of needling stimulation. It confirms that it is possible to measure BOLD changes even after cessation of needling stimulation.


Section: References
  1. Liang F. Acupuncture and Moxibustion. Shanghai: Shanghai Scientific and Technical Publishers 2006.
  2. Shoukang L. Scalp acupuncture therapy and its clinical application. Journal of TCM, 11(4):272-280, 1991.
  3. Dhond RP, Kettner N, Napadow V. Neuroimaging acupuncture effects in the human brain. J Altern Complement Med 2007; 13: 603-616.
  4. Haller S, Bartsch AJ. Pitfalls in fMRI. Eur Radiol (2009); 19: 2689-2706.
  5. Kong J, Gollub R, Huang T, et al. Acupucture de qi, from qualitative history to quantitative measurement. J Altern Complemen Med. 2007;13:1059-1070.
  6. WHO Acupuncture: Review and Analysis of Reports on Controlled Clinical Trials: World Healt Organization. 2002 87 p.
  7. Hui KK, Liu J, Marina O, et al. The integrated response of the human cerebro-cerbellar and limbic system to acupuncture stimulation at ST 36 as evidenced by fMRI. Neuroimage 2005;27:479-496.
  8. Yan B, Li K, Xu J, et al. Acupoint-specific fMRI patterns in human brain. Neurosci Lett 2005;383:236-240
  9. Seong-UK Park, Ae-SooK Shin, Geon-Ho Jahng, et al. Effects of scalp acupuncture versus upper and lower limb acupuncture on signal activation of blood oxygen level dependent (BOLD) fMRI of the brain and somatosensory cortex. J Altern Complement Med. 2009;15:1193-1200.
  10. Beissner Florian. Functional magnetic resonance imaging studies of acupuncture mechanism: a critique. Focus on alternative and Complementary Therapies. 2010;16:3-11.
  11. Bai L, Qin W, Tian J, et al. Time varied characteristics of acupuncture effects in fMRI studies. Hum Brain Mapp 2009;30:3445-60.
  12. Wolbers T, Weiller C, Buchel C. Contralateral coding of imagined body parts in the superior parietal lobe. Cerebral Cortex 2003;13:392-399.
  13. Pellijeff A, Bonilha L, Morgan P, et al. Parietal updating of limb posture: an event-related  fMRI study. Neuropsychologia 2006;44:2685-2690.
  14. Stocco A, Lebiere C, Anderson J. Conditional routing of information to the cortex: a model of the basal ganglia’s role in cognitive coordination. Psychological Review 2010;117 (2): 541–74.
  15. Kurata, K ."Activity properties and location of neurons in the motor thalamus that project to the cortical motor areas in monkeys". Journal of neurophysiology 2005; 94 (1): 550–66.


Section: Personal Information

Romeo Zanardi, Neuroradiology Department, Azienda Ospedaliero Universitaria Santa Maria della Misericordia di  Udine, Italy;
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Marta Maieron, Healt Physics Department, AOUSMM, Udine, Italy;
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Carlo Maria Giovanardi, AMAB –Italian-Chinese Acupuncture School, San Lazzaro di Savena, Italy;
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 Barbara Tomasino, IRCCS “E.Medea”, San Vito al Tagliamento, Italy;
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