Overflow of Muscle Activation by Proprioceptive Neuromuscular Facilitation in Standing Position: A Cross-Sectional Electromyographic Investigation in Healthy Individuals


 Background Although in several studies has been observed the principle of overflow of muscle activation, no one explored if this principle occurs in a standing position. This study aimed to investigate the occurrence and the condition of the overflow from upper limb migrating to inferior contralateral supported limb in standing position in healthy subjects.Methods Cross-sectional study with one sample. Eleven healthy individuals with a mean age of 22 (± 5.6) years were evaluated during 5 tasks applying the proprioceptive neuromuscular facilitation in left side 1) rest, 2) active diagonal primitive3) isotonic resistive diagonal primitive, 4) isometric resistive diagonal primitive, 5) active primitive diagonal with active extension of the right lower limb. The right side was monitored by electromyography activity of the tibial anterior, soleus, vastus medial oblique, rectus abdominis, tensor fasciae latae, gluteus maximus, gluteus medius, adductor longus muscles.Results Results showed a difference between tasks for soleus muscle (p < 0.001), with higher clinical relevance (d = 0.87), and the task with diagonal primitive against isotonic resistance produced more electromyography activity (p < 0.001). For all muscles there was a clinical relevance (d > 0.55). Conclusion The approach used in this study could improve the condition of distal muscles, mainly soleus, facilitating the acquisition of a standing position as soon as possible.


Introduction
Over ow of muscle activation or irradiation is the propagation of synergic muscle coactivation proceeding from a resisted movement [1]. The over ow begins in the stronger muscle groups and can reach any segments from proprioceptive inputs [2].
In healthy subjects, the irradiation occurred from trunk exion, increasing dorsi exion in the right, and left lower limbs [3]. Trunk extension increased plantar exion in both lower limbs. Also, it was observed that the irradiation occurred from the left lower limb to the right lower limb, measured by the increase in tibialis anterior activity [4]. So, the contralateral muscular activity in the non-exercised limb is the result of the irradiation process.
In addition, another study showed that force irradiation during upper limb diagonal exercises is affected by diagonal direction, contraction intensity, and gender when performed by healthy participants [5]. Our results in a previous article [6] match with some of these ndings. The position to elicit muscle response at a distance, ipsilateral, and contralateral to the stimulus. We also observed higher contralateral muscle recruitment for trunk and shoulder muscles during lower limb isometric diagonal compared to movements in other conditions. However, no one of these previous studies investigated this principle in a standing position, which is very functional in the rehabilitation process. Here, we hypothesized that distinct electromyographic activity on lower limb muscles would be observed during different tasks applying the proprioceptive neuromuscular facilitation (PNF) in the contralateral upper limb in standing position. Also, we hypothesized that muscle recruitment would be superior during diagonal against maximum isometric resistance, and would be different between the muscles. Therefore, this study aimed to investigate the occurrence and the condition of the over ow from upper limb migrating to inferior contralateral supported limb muscles in standing position. This study can be the rst step in the knowledge of the over ow principle in stand position.

Methods
Participants This is a cross-sectional study with one sample in different tasks using proprioceptive neuromuscular facilitation by the primitive diagonal for the upper limb. The Research Ethics Committee of the University approved this study (no. 1647/2010), and it was conducted on a motor control laboratory at the same University. The convenience sample recruited from university community, were eleven healthy individuals (5 females) with an average age of 22 (± 5.6) years. The exclusion criteria were the presence of any musculoskeletal or neuromuscular disorders.

Experimental set-up and data processing
The tests were performed in the following position: partially seated at a height-adjustable table, keeping the left lower limb with hip and knee exed at 90°. The right lower limb was positioned resting on the oor with the knee exed at 15° and hip in the neutral position.
Each subject was asked to perform 5 different tasks: 1) to remain at rest in the above position (R); 2) perform the diagonal primitive (DP) of the left upper limb in the main pattern, with exion, abduction and external rotation of the shoulder, elbow extension and total extension of the wrist and ngers [7]; 3) perform the same diagonal against isotonic resistance (DIR), where the therapist resists the patient's active movement through the entire range of motion (concentric contraction) of the same limb; 4) perform the same diagonal against maximum isometric resistance (DISO) in the 90 ° range of the shoulder, total elbow extension and neutral wrist of the same limb; 5) perform a diagonal of the left upper limb and, concomitantly, perform an active extension of the right lower limb that was exed at 15°(DEXT).
Positioning was done, according to [8]. An inter-electrode distance of 2 cm was kept constant. All EMG data were digitized at 1000 frames/s using Optotrak software and a synchronization unit.
The EMG data were processed o ine using Matlab software (Math Works Inc., version 6.0). The EMG signals were recti ed, ltered (low-pass at 20 Hz using a second-order Butterworth lter), and normalized to the averaged EMG signal recorded for the tested muscle during maximum voluntary isometric contraction (MVIC). The averaged EMG of the MVIC was calculated within the 500-1000 ms interval from the beginning of the isometric contraction.

Statistical analysis
To calculate the sample size was used the F tests family, ANOVA: repeated measures, within factors, effect size f = 0.50, α error probability = 0.05 1 -β error probability = 0.95 for one group. It was determinate that the sample size should be at least 10 participants with power 0.95. The data normality was tested and con rmed by the Kolmogorov-Smirnov test. We used a repeated-measures ANOVA test for each muscle in different tasks that were applied [muscle x (5 tasks)]. The pair-wise comparisons with Bonferroni's correction were used to verify the main effects. All tests were performed in IBM© SPSS© (version 22.0.0.0), and we used for statistical signi cance level at 0.05 for all comparisons. Also, the clinical relevance of the ndings was assessed using Cohen's test. According to Cohen [9], d < 0.50 indicate small effects, 0.50 ≤ d < 0.80 indicate medium effects, and d ≥ 0.80 indicate large effects .

Results
The repeated measures ANOVA test reveals that TFL and SO muscles showed statistical difference between the tasks proposed ( Table 1)

Discussion
This study aimed to investigate the occurrence and the condition of the over ow from upper limb migrating to inferior contralateral supported limb in standing position. Our rst hypothesis was con rmed just for the SO muscle although we found a clinical relevance for the other muscles. The higher EMG activity for SO muscle was in the following order. First, the DIR task (with isotonic contraction), followed by DEXT task (free diagonal, but with an extension of the right lower limb), then the DISO task (an isometric diagonal), followed by DP task (free diagonal), and nally, the lower EMG activity was in R task (just a proposed posture without diagonals, but maintained weight support). So, the second hypothesis was also con rmed because the muscle recruitment was superior in PNF diagonals (with the use of resistance) compared to free voluntary movement, but with differences between the muscles.
The results con rm the over ow of muscle activation from the upper limb to the contralateral supported lower limb. That occurrence was mainly during the DIR task (isotonic diagonal) as the condition with a more signi cant impact on the increase in muscle activity. The use of isometric diagonal is widespread to promote over ow principle (Gardner, 1963;Moore, 1975;Pink, 1981;Gontijo et al., 2012), but the performance of isotonic PNF diagonals can also change muscular activity in distant regions (Pink, 1981 Although the other muscles did not show statistical differences, the moderate and high clinical relevance indicates they participated in over ow. Looking at under kinesiology viewpoint, we can say that all muscles contributed to joint stability to support the movement on the left upper limb. To elevate the upper limb above to head (diagonal primitive), it is necessary trunk extension, and that extension needs the trunk and pelvis stability. While the upper limb moves, the stability was provided by gluteus muscles, AD, RA, and TFL muscles [16]. The GMAX help to hip extension and the GMED and AD muscles to maintain the hip in a neutral position, followed by TFL, while the RA helped to keep the trunk and pelvis stability.
Muscle activation also was necessary to achieve body stability during movement. First, SO activation produced plantar exion, and foot moved against the ground. However, the TA activation produced a balance of SO activation and as a result, the ankle stability [17]. Finally, the VMO was activated to avoid increased exion of the knee, maintained close to an extension [17].
The results of this study have a clinical application since many patients cannot stay standing in initial phases of recuperation of an orthopedic, traumatic, or neurological condition. The use of the present approach could improve the condition of distal muscles, mainly soleus, facilitating the acquisition of a standing position as soon as possible. Some examples of situations that could bene t from this approach can be postoperative surgery of knee, ankle when the load is released and cases of stroke or traumatic brain injury in acute or subacute phases.
It is possible to observe several limitations in this study. First, the small sample size does not allow us to generalize the results, but indicates the importance of soleus activity, after over ow intervention. Second, there was no study of kinematic and kinetic variables, which would provide a better understanding of the effects of over ow. It can be indicative of future studies. However, a rst step, exploring EMG activity, gives us a start in the knowledge of the over ow effects in an important muscle for the stand position.

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The results suggest that there is an over ow of the muscles from upper limb migrating to inferior contralateral supported limb muscles in a standing position, especially during diagonal against isotonic resistance. The approach used in this study could improve the condition of distal muscles, mainly soleus, facilitating the acquisition of a standing position as soon as possible.

Declarations
Ethics approval and consent to participate All participants signed to inform consent approved by the Research Ethics Committee of the Federal University of Triângulo Mineiro, Brazil (no. 1647/2010).