Scalp Acupuncture Synchronizing Dual Task Gait for Enhancing Prefrontal Cortex Response

Jun Su; Yuanyuan Guo; Biyi Zhao; Yongchun Jiang; Xi Qin; Meilian Zhong; Dathan Nevin Dychingco Leung; Junxiao Yin; Qiang Lin; Ke Chen

doi:10.3791/66944

JoVE Journal > Neuroscience

Neurociencias

Scalp Acupuncture Synchronizing Dual Task Gait for Enhancing Prefrontal Cortex Response

Published: August 09, 2024

doi:

10.3791/66944

Jun Su¹, Yuanyuan Guo², Biyi Zhao³, Yongchun Jiang^2,4,5, Xi Qin⁶, Meilian Zhong^2,4,5, Dathan Nevin Dychingco Leung⁷, Junxiao Yin⁸, Qiang Lin*⁴, Ke Chen*⁹

¹Department of Orthopaedics,Anshun Hospital of Traditional Chinese Medicine, ²The Fifth Affiliated Hospital of Guangzhou Medical University, ³School of Traditional Chinese Medicine,Jinan University, ⁴Department of Rehabilitation Medicine,The Seventh Affiliated Hospital of Sun Yat-sen University, ⁵Guangzhou Medical University, ⁶Panzhihua Central Hospital, ⁷Department of Physical Therapy, College of Rehabilitation Sciences,University of Santo Tomas, ⁸Clinical Medical College of Acupuncture and Rehabilitation,Guangzhou University of Traditional Chinese Medicine, ⁹Department of Spine Surgery,Zhongshan Torch Development Zone People’s Hospital

Summary

This protocol demonstrates the standardized procedure of scalp acupuncture synchronizing motor-cognitive dual task and motor-cognitive dual task. This can provide an important reference for the clinical exploration of the new and effective non-drug treatment of integrated Chinese and Western medicine.

Abstract

Studies have shown that motor-cognitive dual task can greatly improve motor/cognitive function. However, the therapeutic effect of motor-cognitive dual task is still limited. How to improve dual-task performance is the key to solving this problem. Scalp acupuncture is a non-drug intervention method of traditional Chinese medicine to treat brain-derived diseases by acupuncturing the corresponding projection area of cerebral cortex function on the scalp. Studies have shown that scalp acupuncture helps improve neuronal damage and cognitive dysfunction and plays a neuroprotective function in central nervous system diseases. However, no relevant studies have discussed the synergistic gain effect of motor-cognitive dual task and scalp acupuncture. Therefore, this protocol aims to demonstrate the standardized operation of scalp acupuncture synchronizing motor-cognitive dual task and motor-cognitive dual task and compares the differences between these two tasks in healthy subjects through a randomized cross-over trial. This protocol initially revealed the possible influence mechanism of scalp acupuncture synchronizing motor-cognitive dual task on cognitive performance, gait control, and cortical brain function, which can provide new ideas and a theoretical basis for clinical exploration of new and effective non-drug treatment of integrated Chinese and Western medicine.

Introduction

Motor-cognitive dual task refers to the synchronous execution of a motor task and a cognitive task, requiring the synchronous participation of both motor and cognitive systems¹^,². Studies have shown that compared with a single motor task/cognitive task, a motor-cognitive dual task can greatly improve motor/cognitive function³^,⁴. Anson et al.⁵ randomly divided 20 Parkinson's patients into a single-task group (gait and cognitive training in sequence) and a dual-task group (gait and cognitive training synchronously) for an 8-week rehabilitation training. The results showed that both groups could significantly reduce the Movement Disorder Society-Unified Parkinson's Disease Rating Scale motor subscale score. Still, the dual-task group had a greater decrease, and the improvement of motor performance could last at least for 4 weeks. Shah et al.⁶ randomly divided 224 elderly community members into a physical exercise group, a computer cognitive training group, a motor-cognitive training group, and a blank control group for a 16-week rehabilitation training. All subjects received positron emission computed tomography scans before and after training. The results found that compared with the other three groups, the motor-cognitive training group had improved verbal memory function and significantly increased brain glucose metabolism in the left sensorimotor cortex. Moreover, higher brain glucose metabolism in this brain region was positively correlated with improved verbal memory, suggesting that a specific combination of motor-cognitive training can improve cognition and increase brain glucose metabolism. In addition, in terms of movement, the motor-cognitive dual task can improve balance function and reduce the risk of falls⁷^,⁸. Amanda et al.⁹ randomly divided 21 Parkinson's patients into single-task and dual-task groups for an 8-week rehabilitation training. The results showed that both groups could significantly improve clinical scores of motor function, but only the dual-task group significantly reduced falls by 60%.

However, the motor-cognitive dual task is a behavioral intervention, andalthough clinical studies have shown that its therapeutic efficacy is better than that of a single motor task/cognitive task, the therapeutic effect of the motor-cognitive dual task is still limited. Therefore, improving dual task performance is the key to solving this problem. At present, relevant studies have proved that combined central interventions on the basis of motor-cognitive dual tasks can improve motor-cognitive dual task performance¹⁰^,¹¹^,¹²^,¹³. Common central interventions include transcranial direct current stimulation (tDCS) and transcranial magnetic stimulation (TMS)¹¹. However, tDCS or TMS cannot be performed synchronously with motor-cognitive dual tasks. It can only be performed before and after dual tasks, and instruments are relatively expensive, leading to limited clinical promotion. Therefore, the key to improving dual-task performance is to find an alternative intervention that can be performed synchronously with dual-task and has a therapeutic effect similar to that of combined tDCS or TMS at a reasonable price. The study found that scalp acupuncture had an immediate effect similar to that of tDCS to some extent. Zhang et al.¹⁴ explored the short-term performance differences between tDCS and scalp acupuncture in working memory and included 44 college students in a randomized crossover experiment design. The results showed no statistical difference in the accuracy (ACC) or response time of tDCS and scalp acupuncture before or after intervention in the 0-back task and 1-back task. It is suggested that the therapeutic effect of scalp acupuncture on cognitive function is similar to that of tDCS.

Scalp acupuncture is a non-drug intervention method of traditional Chinese medicine to treat brain-derived diseases by acupuncturing the corresponding projection area of cerebral cortex function on the scalp. Scalp acupuncture is one of the stroke treatments recommended by the World Health Organization and has been shown to improve cognitive function in patients with post-stroke cognitive impairment (PSCI)¹⁵. Studies have shown that scalp acupuncture helps improve neuronal damage and cognitive dysfunction and plays a neuroprotective function in central nervous system diseases¹⁶. Chen et al.¹⁵ randomly assigned 56 patients with PSCI to a treatment group (receiving scalp acupuncture in addition to medication) or control group (receiving medication only) for a period of 4 weeks. The results of the study found that the application of scalp acupuncture in addition to medication significantly improved cognitive function and increased brain hemoglobin levels compared to patients who received medication only. Xiong et al.¹⁷ randomly divided 70 patients with post-stroke cognitive dysfunction into a scalp acupuncture group (scalp acupuncture + cognitive training) and a control group (sham scalp acupuncture + cognitive training) for 12 weeks of rehabilitation training. The results found that Mini-Mental Status Exam (MMSE), Loewenstein Occupational Therapy Cognitive Assessment (LOTCA), and Fugl-Meyer Assessment (FMA) scores in the scalp acupuncture group were significantly higher than those in the control group, suggesting that scalp acupuncture combined with cognitive training can improve stroke patients' cognitive and motor functions.

However, no relevant studies have discussed the synergistic gain effect of motor-cognitive dual task and scalp acupuncture. Therefore, this protocol aims to include 39 healthy subjects to demonstrate the standardized operation of scalp acupuncture synchronizing motor-cognitive dual task and motor-cognitive dual task and compares the differences between these two tasks in healthy subjects through a randomized cross-over trial. The Gaitrite gait analysis system and functional Near-infrared spectroscopy (fNIRS) are utilized to explore the synergistic gain effect of scalp acupuncture on synchronous dual tasks. This protocol seeks to uncover the mechanism behind how scalp acupuncture synchronizing motor-cognitive dual task affects gait control and cortical brain function, providing a novel idea and theoretical basis for clinical exploration of new effective non-drug therapies.

Protocol

This project was approved by the Medical Ethics Association of the Fifth Affiliated Hospital of Guangzhou Medical University (approval No. KY01-2023-11-02) on December 05, 2023. The trial was registered in the Chinese Clinical Trials Registry (registration number: NO. ChiCTR2400079574) on January 06, 2024. All participants signed the informed consent form.

1. Recruitment

Inclusion criteria
1. Recruit healthy subjects aged 20-35 years.
2. Recruit healthy subjects with Montreal Cognitive Assessment (MoCA) ≥ 26¹⁸.
3. Recruit healthy subjects without a history of mental illness.
4. Recruit healthy subjects without aphasia.
5. Recruit healthy subjects without obvious organ function injury.
6. Recruit healthy subjects with voluntarily signed informed consent.
Exclusion criteria
1. Exclude subjects with diseases affecting gait, such as hemiplegia, Parkinson's disease, fractures, knee lesions, and lower limb joint injuries.
2. Exclude subjects with a history of mental illness or antipsychotic drug use.
3. Exclude women during pregnancy and lactation.

2. Baseline information collection

Randomly divide the subject into healthy group-1 (n = 19) and healthy group-2 (n = 20).
Collect the baseline characteristic data for both groups, including sex, age, height, weight, bilateral leg length, and MoCA score.

3. Intervention stage

NOTE: Inform the subjects of the relevant experimental procedures, purposes, and precautions to ensure the experiment's smooth conduct and quality.

Healthy Group 1
1. Motor-cognitive dual task
  1. Ask the subject to stand at the beginning of the footpath and listen to the computer's and the researcher's instructions.
    NOTE: The footpath is from the Gaitrite gait analysis system. The system is a 4.6 m long electronic footpath that connects to the serial port of a Windows XP computer. The footpath is 1/8 inch thick and contains 16,128 sensors sandwiched between the thin vinyl top cover and the rubber bottom, with an effective sensor area of 0.61 m wide and 3.66 m long. The footpath is portable and can be rolled up when the experiment is over, saving space.
  2. Let the subject remain standing when hearing the "stand" prompt from the computer. This process lasts for 30 s.
  3. Let the subject walk along the footpath at a natural and comfortable pace when the subject hears "random number -7" from the researcher, and dictate the result of continuously subtracting seven from the "random number" (for example, the researcher says "385-7", the subject replies "385 minus 7 equals 378, another minus 7 equals 371, another minus 7 equals 364, and so on"). This process lasts for 30 seconds. Record the results of the cognitive task and calculate the total number of calculations, the correct number, and the ACC.
    NOTE: The random number is any integer >300.
  4. Let the subject stop counting when hearing "continue walking" from the computer and continue walking for 30 s.
  5. Repeat 3.1.1.3-3.1.1.4 to complete the "random number -7" cognitive task three times.
  6. Let the subject stop walking when hearing "end". The experiment is over.
2. Scalp acupuncture synchronizing motor-cognitive dual task
  NOTE: The "Scalp acupuncture synchronizing motor-cognitive dual task" will be performed after a 1 week washout. The tasks "Motor cognitive dual task" and "Scalp acupuncture synchronizing motor cognitive dual task" were performed separately, with a one-week washout period in between. The experiment was a randomized cross-over trial in which the same individual received different interventions at different stages. The washout period is the second stage of treatment after the effect of the first stage has completely disappeared. The washout period prevents the therapeutic effects of the first stage from affecting the second stage, making the experimental results more accurate.
  1. Choose Baihui¹⁹, Shenting²⁰, and Sishencong²¹ as the key acupoints (Figure 1).
    NOTE: Baihui and Shenting acupoints are vital meridian, Sishencong belongs to extraordinary points; acupuncture at these points can regulate body's "Yang", awake the brain, calm the spirit, and improve cognitive function¹⁹^,²⁰^,²¹. Baihui Point is located in the middle of the head hairline , straight up 5 inches (16.7 cm), about the middle point of the connection between the two ear tips, the intersection point between the middle line of the head and the bilateral ear tips. Acupuncture at Baihui Point can improve memory loss, dizziness, headache, heart palpitation, and other symptoms¹⁹. Shenting Point is located in the middle of the head hairline 0.5 inches (1.7 cm), located on the middle line of the head, 1.7 cm above the midpoint of the front hairline. Acupuncture at the Shenting Point can be used to treat headache, dizziness, insomnia, nasal deep, rhinitis, epilepsy, memory loss, schizophrenia, and other symptoms²⁰. Sishencong is a group of four acupoints located 1 inch (3.3 cm) in front, behind, left, and right of Baihui Point on the top of the head, a total of four acupoints. Each point is arranged around the Baihui point, and each point is about 1 inch (3.3 cm) away from the Baihui point. Acupuncture at Sishencong can be used to treat headache, insomnia, vertigo, neurasthenia, forgetfulness, and other symptoms²¹.
  2. Disinfect the skin of the acupuncture point with alcohol and disinfect it in a circle from the center to the outside.
  3. Take a 1.5 inch needle (5 cm) and place it 15° from the skin under the cap aponeurosis. Insert the needle to a depth of 1 inch (3.3 cm), twist it to "Deqi" for 1 min, and leave the needle.
    NOTE: When Shenting, front Shencong, and Baihui enter the scalp, the tip of the needle is forward, and the tip of the left and right Shencong and the back Shencong are toward Baihui. The follow-up procedure is the same as 3.1.1.1-3.1.1.6. "Deqi" is a unique compound sensation that is interpreted as the flow of "qi" or "life energy.""Deqi" can be manifested as pain, soreness, swelling, heaviness, warmth, dull pain, numbness, etc²².
Healthy Group 2
NOTE: The intervention order in Healthy Group 2 was the opposite of that in Healthy Group 1.
1. Scalp acupuncture synchronizing motor-cognitive dual task
  1. Perform the experimental procedure as described in step 3.1.2.
2. Motor-cognitive dual task
  1. Perform the experimental procedure as described in step 3.1.1.

4. Assessment

Gait analysis system
Ensure that the researcher masters the equipment operation skills in advance, including Gaitrite's working principle, scope of application, subject requirements, and experimental operation specifications, and be familiar with precautions, such as ensuring the safety of subjects while walking and preventing the risk of falling.
1. Subject preparation
  1. Prepare suitable experimental clothes for the subject and fold the pant leg above the subject's ankle joint to avoid interference with the collection of gait parameters.
  2. Measure the length of the subject's left and right legs.
    NOTE: The subject stands with his legs shoulder-width apart, and the vertical distance between the subject's left or right leg rotors and the ground is taken as the leg length.
  3. Ask the subjects to stand at the beginning of the footpath and listen to the computer's and the researcher's instructions.
2. Software operation
  1. Open the software Gaitrite, click the New Subject button, and enter the basic information of the subject (name, gender, age, height, weight, left and right leg length).
  2. Click the New Test button to create a test task.
3. Gait parameter acquisition
  1. Ask the subject to stand at the beginning of the footpath and explain how the experiment proceeds.
    NOTE: The subjects need to walk from one side of the footpath to the other, and the starting and end points should be outside the footpath as a trial. A total of 3-4 trials will be carried out.
  2. Click the Start Walk button to synchronize gait data collection.
    NOTE: The Start Walk button needs to be pressed before each trial begins. The gait data of the subjects during "Motor-cognitive dual task" and "Scalp acupuncture synchronizing motor-cognitive dual task" were collected, respectively. The specific gait data include Ambulation Time, Step Time, Step Length, Step/Extremity, Cycle_Time, Stride Length, Heel-Heel Base Support, Angle of Toe, StrideVelocity, Stride Velocity, Left: Right Foot Step Time Ratio, Left: Right Foot Step Length Ratio, Left: Right Foot Cycle Time Ratio, Functional Amb. Profile, Velocity Normalized using Leg Length, Swing Percent of Cycle, Swing Time, Swing_Time, Stance Percent of Cycle, Stance Time, Single Support percent of Cycle, Single Support Time, Double Support percent of Cycle, Double Support Time, Heel Off On Time, Heel Off On Percent, Double Support Load Time, Double Support Load Percent Gait Cycle, Double Support Unload Time, Double Support Unload Percent Gait Cycle.
  3. Click the Save button to save the data. Each subject will have gait data for two walking tasks.
Synchronizing the fNIRS brain function assessment
1. Regions of interest selection
  1. Set sources and detectors according to the 10-20 system. Place a total of 10 sources and 12 detectors. Set the protocol to monitor the following 6 areas of Interest (ROIs), including the bilateral dorsolateral prefrontal cortex (DLPFC), the dorsolateral promoter cortex (PMC), and the dorsolateral primary motor cortex (M1).
    NOTE: The DLPFC is mainly responsible for cognitive, emotional, and sensory processing; PMC involves motion planning; M1 is in charge of movement execution²³^,²⁴^,²⁵^,²⁶.
2. Researcher preparation
  1. Ensure that the researchers are trained to master fNIRS equipment operation skillsand be familiar with experimental operation procedures and precautions to ensure accurate and true data collection results.
3. Subject preparation
  1. Wear an fNIRS cap on the subject.
  2. Ensure that the Cz point is correctly positioned.
    NOTE: The Cz point on the fNIRS cap is located at the fourth point on the midline of the cap from the forehead to the occipital lobe. The Cz point on the subject's head is located at the intersection of the nasal root and the occipital processor the intersection of the upper ear fossa (ear cone).
  3. Adjust the position of the fNIRS cap so that the Cz point on the subject's head coincides with the Cz point on the cap.
  4. Tighten the straps on both sides of the ear cap according to the size of the subject's skull so that the subject's ears protrude through the gap.
  5. Put a portable fNIRS backpack on the subject and ensure that the backpack does not affect the subject's normal walking.
  6. Turn on the power button on the fNIRS backpack when the subject is ready for the task.
  7. Ask the subject to stand at the start of the footpath and listen to the computer and the researcher.
4. Software preparation
  1. Open the Nirsmart software, select the experiment paradigm, and input the subject information and remarks (name, gender, age, task type).
  2. Click on Pre-acquisition to test the signal source quality of all brain channels. Suppose the signal source quality is not optimal (the channel in the brain area is marked green to indicate that the signal source quality is optimal). In that case, adjust the hair of the subject by pushing it away with a hair stringer.
  3. Click the Automatic Gain button to complete the acquisition when the signal source quality of all brain channels is optimal.
5. fNIRS brain function data acquisition
  1. Ask the subject to stand at the start of the footpath. Synchronously collect brain function data by clicking the fNIRS Start button.
    NOTE: The fNIRS brain function is synchronized with the Gaitrite gait analysis system for data acquisition. Both these systems are used simultaneously when the subject performs the tasks mentioned in section 3.
  2. Click the fNIRS End button to save the data when the experiment is over.

5. Statistical analysis

Use statistical analysis software to analyze all data. Test the normality of the measurement data by Kolmogorov-Smirnov. Represent data with normal distribution as mean ± standard deviation and with non-normal distribution as median (interquartile distance).
For the data conforming to the normal distribution, use the paired sample T-test to compare the influence of the two intervention methods on the results.
Compare the data that do not conform to a normal distribution using the rank sum test. Use the χ² test to compare the adoption rate or composition ratio of the data. Consider P < 0.05 as statistically significant.

Representative Results

This protocol used a randomized controlled crossover design, recruiting 39 healthy subjects aged 20 to 35, including 14 males and 25 females. These participants were randomly assigned into Health Group 1 (n = 19) and Health Group 2 (n = 20). Baseline data for both groups were gathered (Table 1). No significant differences were observed between the groups regarding gender, age, height, weight, length of left and right legs, and MoCA assessment scores (all P > 0.05).

Cognitive task outcomes revealed that the scalp acupuncture synchronizing motor-cognitive dual task outperformed the motor-cognitive dual task in terms of higher ACC (P = 0.022), more correct answers (P < 0.001), and a larger total calculation count (P < 0.001) (Table 2).

The analysis of gait parameters showed that compared to the motor-cognitive dual task, scalp acupuncture synchronizing motor-cognitive dual task showed an increase in Velocity, Cadence, Step Length, Step/Extremity, Stride Velocity_L, Stride Velocity_R, and Velocity normalized using leg length. The data showed a decrease in Ambulation Time, Step_Time_L, Step_Time_R, Angle of toe, Left: Right foot Step time ratio, Cycle_Time_L, Cycle_Time_R, Swing_Time_L, Stance_Time_L, Stance_Time_R, Single Support Time_R, Double Support percent of Cycle_L, Double Support percent of Cycle_R, Double Support Time_L, Double Support Time_R, Double Support Load Time_L, Double Support Load Time_R, Double Support Load Percent Gait Cycle_L, Double Support Load Percent Gait Cycle_R, Double Support Unload Time_L, Double Support Unload Time_R, Double Support Unload Percent Gait Cycle_L, and Double Support Unload Percent Gait Cycle_R (all P < 0.05) (Table 3). For a comprehensive overview of all gait parameters, refer to Supplementary Table 1.

The ΔHbO comparison results of each ROI under different interventions showed that in the scalp acupuncture synchronizing motor-cognitive dual task, the change in oxygenated hemoglobin (Δ HbO) levels in the left promoter cortex (L-PMC), the right primary motor cortex (R-M1), and the left primary motor cortex (L-M1) were lower compared to the motor-cognitive dual task (L-PMC: P = 0.041; R-M1: P = 0.001; L-M1: P = 0.008), as detailed in Table 4 and Figure 2.

Figure 1: Schematic showing the selected acupoints. (A,B) Select Baihui, Shenting, and Sishencong for stimulation. Locate the acupoints according to the positioning standards of the People's Republic of China: "The name and positioning of the acupoint." "Baihui Point" is the intersection point between the middle line of the head and the bilateral ear tips. "Shenting Point" is located on the middle line of the head, 1.7 cm above the midpoint of the front hairline. "Sishencong" is a group of four acupoints located 1 inch (3.3 cm) in front, behind, left, and right of Baihui Point on the top of the head, a total of four acupoints. Please click here to view a larger version of this figure.

Figure 2. Comparison of ΔHbO for each ROI with different interventions. (A) Motor-cognitive dual Task. (B) Scalp acupuncture synchronizing motor-cognitive dual task. The ΔHbO levels of L-PMC, R-M1, and L-M1 were lower in the scalp acupuncture synchronizing motor-cognitive dual task compared to the motor-cognitive dual task. Abbreviations ΔHbO, change in oxygenated hemoglobin; DLPFC, dorsolateral prefrontal cortex; PMC, promoter cortex; M1, primary motor cortex; S1, primary sensory cortex; R, right; L, left. Please click here to view a larger version of this figure.

Table 1: Comparison of clinical characteristics between two groups. Baseline data for Health Group-1 (n = 19) and Health Group-2 (n = 20) were gathered, and no significant differences were observed between the groups regarding gender, age, height, weight, length of left and right legs, and MoCA assessment scores. Abbreviations: cm, centimeter; kg, kilogram; MoCA, Montreal Cognitive Assessment. n (%) or mean and standard deviation are shown. Please click here to download this Table.

Table 2: Completion of cognitive tasks under different interventions. Subjects walk along the footpath at a natural and comfortable pace when hearing "random number -7", and dictate the result of continuously subtracting seven from the "random number". The researcher records the results of the cognitive task and calculates the total number of calculations, the correct number, and the ACC. Abbreviations: ACC, Accuracy Rate. Mean and standard deviation are shown. The significance level is set at P < 0.05. Significant correlations are marked with *P < 0.05, ***P < 0.001. Please click here to download this Table.

Table 3: Performance of gait parameters under different interventions. Subjects walk from one side of the footpath to the other, and the gait analysis system synchronizes gait data collection. Abbreviations: Amb_Time, Ambulation Time; Step_Time, Step Time (s); Step_Len, Step Length (cm); Step_Extrem, Step/Extremity (ratio); Cycle_Time, Cycle Time (s); ToeInOut, Angle of Toe; StrideVelocity, Stride Velocity; Step_Time_Dif, Left: Right foot Step time ratio; NormVelocity, Velocity normalized using leg length; Swing_Time, Swing Time (s); Stance_Time, stance Time (s); S_Supp_Time, Single Support Time (s); D_Supp_Perc, Double Support percent of Cycle; D_Supp_Time, Double Support Time (s); D_SuppLoadTm, Double Support Load Time; D_SuppLoadPerc, Double Support Load Percent Gait Cycle; D_SuppUnloadTm, Double Support Unload Time; D_SuppUnloadPerc, Double Support Unload Percent Gait Cycle; _R, right; _L, left. Mean and standard deviation are shown. The significance level is set at P < 0.05. Significant correlations are marked with *P < 0.05, **P < 0.01, ***P < 0.001. Please click here to download this Table.

Table 4: Comparison of ΔHbO in various ROIs under different interventions. The ΔHbO levels of L-PMC, R-M1, and L-M1 were lower in the "scalp acupuncture synchronizing motor-cognitive dual task" compared to the "motor-cognitive dual task". Abbreviations: ΔHbO, change in oxygenated hemoglobin; ROIs, regions of interest; DLPFC, dorsolateral prefrontal cortex; PMC, promoter cortex; M1, primary motor cortex; R, right; L, left. Mean and standard deviation are shown. The significance level is set at P < 0.05. Significant correlations are marked with *P < 0.05, **P < 0.01, ***P < 0.001. Please click here to download this Table.

Supplementary Table 1: Performance of gait parameters under different interventions. Subjects walk from one side of the footpath to the other, and the gait analysis system synchronizes gait data collection. Abbreviations Amb_Time, Ambulation Time; Step_Count, Step Count; Step_Time, Step Time (s); Step_Len,Step Length (cm); Step_Extrem, Step/Extremity (ratio); Cycle_Time, Cycle Time (s); Stride_Len, Stride Length (cm); Supp_Base, Heel-Heel Base Support; ToeInOut, Angle of toe; StrideVelocity, Stride Velocity; Step_Time_Dif, Left: Right foot Step time ratio; Step_Len_Dif, Left: Right foot Step Length ratio; Cycle_Time_Dif, Left: Right foot Cycle time ratio; FAP, Functional Amb. Profile; NormVelocity, Velocity normalized using leg length; Swing_Perc, Swing percent of Cycle; Swing_Time, Swing Time (s); Swing_Time, Swing Time (s); Stance_Perc, stance percent of Cycle; Stance_Time, stance Time (s); S_Supp_Perc, Single Support percent of Cycle; S_Supp_Time, Single Support Time (s); D_Supp_Perc, Double Support percent of Cycle; D_Supp_Time, Double Support Time (s); HeelOffOnTime, Heel Off On Time; HeelOffOnPerc, Heel Off On Percent; D_SuppLoadTm, Double Support Load Time; D_SuppLoadPerc, Double Support Load Percent Gait Cycle; D_SuppUnloadTm, Double Support Unload Time; D_SuppUnloadPerc, Double Support Unload Percent Gait Cycle; _R, right; _L, left. Mean and standard deviation are shown. The significance level is set at P < 0.05. Significant correlations are marked with *P < 0.05, **P < 0.01, ***P < 0.001. Please click here to download this File.

Discussion

Previous studies have not seen combining scalp acupuncture with the motor-cognitive dual task". This protocol explored the synergistic gain effect of synchronous motor-cognitive dual task combined with scalp acupuncture. It examined the therapeutic differences between scalp acupuncture synchronizing motor-cognitive dual task and motor-cognitive dual task. Scalp acupuncture operation is the key technology of this protocol. Baihui Point, Shenting Point, and Sishencong are selected as crucial acupoints. Baihui Point and Shenting Point are vital meridian, which contributes to invigorating the body's "Yang," calming the mind and alleviating mental disorders associated with brain dysfunction²⁷^,²⁸. Sishencong belongs to extraordinary points, and acupuncture at "Sishencong" can regulate the body's "Yang" and has the effect of tranquilizing²⁹. Therefore, this protocol hypothesized that scalp acupuncture could synergistically enhance the effectiveness of motor-cognitive dual task and improve gait performance and cognitive function.

The results from this protocol support this hypothesis by demonstrating that scalp acupuncture synchronizing motor-cognitive dual task significantly enhances cognitive performance tasks while improving gait performance by increasing walking speed and reducing walking time. Additionally, fNIRS results indicate that compared to performing a motor-cognitive dual task, scalp acupuncture synchronizing motor-cognitive dual task leads to a significantly lower increase in HbO concentration within relevant brain areas such as R-M1, L-M1, and L-PMC.

M1 is the primary part of the motor cortex, located in the anterior central gyrus, and coordinates with other brain motor regions to control movement²⁴^,²⁵^,²⁶. PMC is a functional area associated with movement in the frontal lobe, responsible for controlling certain movement characteristics, including preparation for movement, sensory orientation during movement, spatial orientation, and partial movement of the body's proximal and trunk muscles²⁴^,²⁵^,²⁶. It is suggested that scalp acupuncture synchronizing motor-cognitive dual task may improve the efficiency of neural activity and the planning executive function and motor function so that the HbO concentration of PMC and M1 can complete motor tasks and cognitive tasks with high quality without drastic changes, which fully proves the synergistic gain effect of scalp acupuncture. Previous studies also showed similar results²³. Finn et al.²³ conducted working memory training on 25 healthy elderly and randomly divided them into a high and low-load training groups. After 5 weeks of training, both groups showed better memory than before the training. MRI before and after training showed that activation of specific brain regions was decreased in both groups, especially in the high-load training group. It shows that when the efficiency of neural activity is increased, fewer neurons are recruited to perform the task, and the task is performed better.

Potential risks in this protocol are needle faintness and broken needles. When needle fainting occurs, subjects may experience dizziness, palpitation, nausea, or syncope. The researcher should immediately remove needles, ask subjects to lie down and rest, drink warm water, and inhale oxygen at low flow if necessary. Hunger increases the risk of needle fainting³⁰. Therefore, before the start of the experiment, the subjects can eat properly to reduce their sense of hunger. At the same time, the researcher should explain the experimental procedures to the subjects, especially those who receive acupuncture for the first time, and try to eliminate their fear of acupuncture³¹. In the implementation process, the needle should be injected according to the standard to ensure the comfort and safety of the subject. When the needle breaks, the researcher should ask the subject to relax, not move, to prevent the broken end from sinking deep into the muscle. The broken end can be removed by finger or tweezers if the broken end is still outside the body. If the broken end is flat with the skin, both sides of the pinhole can be squeezed to expose the fractured end to the body and remove it with tweezers. Before the experiment, the researcher should carefully check the needles, those not meeting the quality requirements should be stripped and removed. When selecting a needle, the length of the needle body should be 1.3 cm longer than the depth to be pierced. When needling, do not pierce the whole needle body but leave part of it outside the body. When inserting the needle, it should be removed immediately if it bends. Do not force insertion. In addition, due to the abundance of blood vessels in the scalp, close attention should be paid to whether there is bleeding during the needle withdrawal process. After the needle withdrawal, a sterile dry cotton ball should be used to press the needle hole lightly to prevent bleeding. If scalp bleeds after needle withdrawal, apply light pressure to the bleeding point with a clean, sterilized cotton ball or gauze immediately until the bleeding stops, and ensure that the acupuncture area is kept clean to prevent infection. For several hours after bleeding, avoid rubbing or stimulating the acupuncture area and closely observe whether other symptoms, such as swelling or persistent bleeding, occur at the bleeding site³¹.

Another potential impact of this protocol is the correct setting of the washout period. Because this experiment was a randomized cross-over trial, the same individual received different interventions at different stages. In order to avoid the effect of the first phase of treatment affecting the second phase, we set the washout period of the regimen to 1 week, which can make the experimental results more accurate.

The experimental subjects included in this protocol are healthy, which can effectively eliminate the heterogeneity among patients caused by central nervous system diseases. By exploring the performance difference between scalp acupuncture synchronizing motor-cognitive dual task and motor-cognitive dual task in healthy subjects, the results are initially obvious, proving that the scalp acupuncture synchronizing motor-cognitive dual task has a synergistic gain. However, it needs to be further verified in patients in the future. Additionally, this protocol solely explored the immediate effects of the scalp acupuncture synchronizing motor-cognitive dual task compared to the motor-cognitive dual task. Future research should explore its long-term benefits to provide more evidence-based support for the clinical promotion and application of scalp acupuncture synchronizing motor-cognitive dual task.

At present, it has been proved that simple scalp acupuncture stimulation and simple motor-cognitive dual task can effectively improve motor or cognitive function¹^,¹⁵. However, no clinical studies have been conducted on combining these two therapies. In addition, related research has demonstrated that motor-cognitive dual task combined with central intervention can improve dual task performance. Commonly employed interventions include TMS and tDCS³²^,³³^,³⁴. However, it is essential to note that TMS and tDCS can not be synchronized with motor-cognitive dual tasks; they can only be applied before or after the dual task, thus limiting their clinical applicability. Therefore, this study innovatively combined scalp acupuncture technology with a motor-cognitive dual task and carried out simultaneously, and the research results were initially effective. Besides, scalp acupuncture technology is more economical than central intervention means and has great potential for clinical promotion.

In this study, a randomized cross-over trial was conducted to demonstrate the synergistic gain effect of scalp acupuncture synchronizing motor-cognitive dual task in healthy subjects. Therefore, the scalp acupuncture synchronizing motor-cognitive dual task in this study can provide an important reference for future clinical patients to implement treatment plans and has guiding significance.

This protocol initially revealed the possible influence mechanism of scalp acupuncture synchronizing motor-cognitive dual task on cognitive performance, gait control, and cortical brain function. It proves the synergistic gain effect of scalp acupuncture in central nervous regulation and peripheral biomechanics. It can provide new ideas and a theoretical basis for the clinical exploration of the new and effective non-drug treatment of integrated Chinese and Western medicine.

Divulgaciones

The authors have nothing to disclose.

Acknowledgements

This study was supported by the Guangdong Provincial Key Laboratory of Traditional Chinese Medicine Informatization (2021B1212040007), Guangzhou clinical characteristic technology construction project (2023C-TS19), Science and Technology Fund project of Guizhou Provincial Health Commission (gzwkj2023-390), 2022 Guangzhou Medical University Student Innovation Ability Improvement Plan project (PX-66221494/02-408-2304-19062XM), Chinese medicine research project of Guangdong Provincial Chinese Medicine Bureau (20241182). We want to thank Yuxin Zheng (an employee of the Seventh Affiliated Hospital of Sun Yat-sen University) for the data analysis, Siqing Wang (an undergraduate of Guangzhou Medical University), and Yuting Lin (an undergraduate of Sun Yat-sen University) for the article translation. Sihao Chen, Weijie Lin, Zhiqing Qiu, Ziwei Wu, Shasha Tang (undergraduates of Guangzhou Medical University), and Guibing Tang (an employee of the Fifth Affiliated Hospital of Guangzhou Medical University) for data collection.

Materials

Disposable acupuncture needles	Huan Qiu, China	N/A	Scalp acupuncture
GAITRite	CIR Systems Inc, America	https://www.gaitrite.com/	Gaitrite gait analysis system
NirSmart-500	Hui Chuang, China	N/A	fNIRS

Referencias

Gallou-Guyot, M., Mandigout, S., Combourieu-Donnezan, L., Bherer, L., Perrochon, A. Cognitive and physical impact of cognitive-motor dual-task training in cognitively impaired older adults: An overview. Neurophysiol Clin. 50 (6), 441-453 (2020).
Xiao, Y., Yang, T., Shang, H. The impact of motor-cognitive dual-task training on physical and cognitive functions in Parkinson’s disease. Brain Sci. 13 (3), 437 (2023).
Wollesen, B., Wildbredt, A., van Schooten, K. S., Lim, M. L., Delbaere, K. The effects of cognitive-motor training interventions on executive functions in older people: a systematic review and meta-analysis. Eur Rev Aging Phys Act. 17, 9 (2020).
Zhu, X., Yin, S., Lang, M., He, R., Li, J. The more the better? A meta-analysis on effects of combined cognitive and physical intervention on cognition in healthy older adults. Ageing Res Rev. 31, 67-79 (2016).
Rosenfeldt, A. B., Penko, A. L., Streicher, M. C., Zimmerman, N. M., Koop, M. M., Alberts, J. L. Improvements in temporal and postural aspects of gait vary following single- and multi-modal training in individuals with Parkinson’s disease. Parkinsonism Relat Disord. 64, 280-285 (2019).
Shah, T., et al. A combination of physical activity and computerized brain training improves verbal memory and increases cerebral glucose metabolism in the elderly. Transl Psychiatry. 4 (12), e487 (2014).
Booth, V., Hood, V., Kearney, F. Interventions incorporating physical and cognitive elements to reduce falls risk in cognitively impaired older adults: a systematic review. JBI Database System Rev Implement Rep. 14 (5), 110-135 (2016).
Lipardo, D. S., Aseron, A. M. C., Kwan, M. M., Tsang, W. W. Effect of exercise and cognitive training on falls and fall-related factors in older adults with mild cognitive impairment: A systematic review. Arch Phys Med Rehabil. 98 (10), 2079-2096 (2017).
Penko, A. L., Barkley, J. E., Rosenfeldt, A. B., Alberts, J. L. Multimodal training reduces fall frequency as physical activity increases in individuals with Parkinson’s disease. J Phys Act Health. 16 (12), 1085-1091 (2019).
Zhou, D., Zhou, J., Chen, H., Manor, B., Lin, J., Zhang, J. Effects of transcranial direct current stimulation (tDCS) on multiscale complexity of dual-task postural control in older adults. Exp Brain Res. 233 (8), 2401-2409 (2015).
Manor, B., Zhou, J., Jor’dan, A., Zhang, J., Fang, J., Pascual-Leone, A. Reduction of dual-task costs by noninvasive modulation of prefrontal activity in healthy elders. J Cogn Neurosci. 28 (2), 275-281 (2016).
Zheng, Y., Wang, Y., Yue, Z., Wang, X., Zhang, J., Fang, J. Transcranial direct current stimulation modulates the brain’s response to foot stimuli under dual-task condition: A fMRI study in elderly adults. Neurosci Lett. 692, 225-230 (2019).
Zhou, J., et al. Transcranial direct current stimulation reduces the cost of performing a cognitive task on gait and postural control. Eur J Neurosci. 39 (8), 1343-1348 (2014).
Zhang, W., Lang, S., Zheng, Y., Qin, X., Chen, H., You, Y., Ou, H. The effects of transcranial direct current stimulation versus electroacupuncture on working memory in healthy subjects. J Altern Complement Med. 25 (6), 637-642 (2019).
Chen, J., Li, H., Zeng, C., Li, J., Zhao, B. Evaluation of the recovery outcome of poststroke cognitive impairment after cluster needling of scalp acupuncture therapy based on functional near-infrared spectroscopy. Brain Behav. 10 (8), e01731 (2020).
Du, S. Q., et al. Acupuncture inhibits TXNIP-associated oxidative stress and inflammation to attenuate cognitive impairment in vascular dementia rats. CNS Neurosci Ther. 24 (1), 39-46 (2018).
Xiong, J., et al. The effect of combined scalp acupuncture and cognitive training in patients with stroke on cognitive and motor functions. NeuroRehabilitation. 46 (1), 75-82 (2020).
Nasreddine, Z. S., et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 53 (4), 695-699 (2005).
Lin, R., et al. Electroacupuncture at the Baihui acupoint alleviates cognitive impairment and exerts neuroprotective effects by modulating the expression and processing of brain-derived neurotrophic factor in APP/PS1 transgenic mice. Mol Med Rep. 13 (2), 1611-1617 (2016).
Wen, T., Zhang, X., Liang, S., Li, Z., Xing, X., Liu, W., Tao, J. Electroacupuncture ameliorates cognitive impairment and spontaneous low-frequency brain activity in rats with ischemic stroke. J Stroke Cerebrovasc Dis. 27 (10), 2596-2605 (2018).
Tong, T., Pei, C., Chen, J., Lv, Q., Zhang, F., Cheng, Z. Efficacy of acupuncture therapy for chemotherapy-related cognitive impairment in breast cancer patients. Med Sci Monit. 24, 2919-2927 (2018).
Hui, K. K., et al. Characterization of the "deqi" response in acupuncture. BMC Complement Altern Med. 7, 33 (2007).
Finn, M., McDonald, S. Computerised cognitive training for older persons with mild cognitive impairment: A pilot study using a randomised controlled trial design. Brain Impairment. 12 (3), 187-199 (2011).
Jones, E. G., Coulter, J. D., Hendry, S. H. C. Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol. 181 (2), 291-347 (1978).
Stinear, C. M., Coxon, J. P., Byblow, W. D. Primary motor cortex and movement prevention: where Stop meets Go. Neurosci Biobehav Rev. 33 (5), 662-673 (2009).
Barhoun, P., et al. The role of the primary motor cortex in motor imagery: A theta burst stimulation study. Psychophysiology. 59 (10), e14077 (2022).
Jianyi, X. U. E., et al. Scalp acupuncture Yikang therapy on Baihui (GV20), Sishencong (EX-HN1), Zhisanzhen, Niesanzhen improves neurobehavior in young rats with cerebral palsy through Notch signaling pathway. J Tradit Chin Med. 43 (2), 337-342 (2023).
Wang, Y. F., et al. Combinations of scalp acupuncture location for the treatment of post-stroke hemiparesis: A systematic review and Apriori algorithm-based association rule analysis. Front Neurosci. 16, 956854 (2022).
Liu, Z. H., Qi, Y. C., Pan, P. G., Ma, M. M., Qian, X., Fu, W. J. Clinical observation on treatment of clearing the Governor Vessel and refreshing the mind needling in neural development and remediation of children with cerebral palsy. Chin J Integr Med. 19 (7), 505-509 (2013).
Chen, F. P., Hwang, S. J., Lee, H. P., Yang, H. Y., Chung, C. Clinical study of syncope during acupuncture treatment. Acupunct Electrother Res. 15 (2), 107-119 (1990).
Zhang, Y., Zhao, X., Chen, M. L., Chen, W., Xu, X. Case report: Fainting during acupuncture treatment. Altern Ther Health Med. 26 (3), 58-60 (2020).
Manor, B., et al. Transcranial direct current stimulation may improve cognitive-motor function in functionally limited older adults. Neurorehabil Neural Repair. 32 (9), 788-798 (2018).
Schabrun, S. M., Lamont, R. M., Brauer, S. G. Transcranial direct current stimulation to enhance dual-task gait training in Parkinson’s disease: A pilot RCT. PLoS One. 11 (6), e0158497 (2016).
Swank, C., Mehta, J., Criminger, C. Transcranial direct current stimulation lessens dual task cost in people with Parkinson’s disease. Neurosci Lett. 626, 1-5 (2016).