Motor unit synchronization in FDI and biceps brachii muscles of strength-trained males

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Abstract

Motor unit (MU) synchronization is the simultaneous or near-simultaneous firing of two MUs which occurs more often than would be expected by chance. The present study sought to investigate the effects of exercise training, muscle group, and force level, by comparing the magnitude of synchronization in the biceps brachii (BB) and first dorsal interosseous (FDI) muscles of untrained and strength-trained college-aged males at two force levels, 30% of maximal voluntary contraction (MVC) and 80% MVC. MU action potentials were recorded directly via an intramuscular needle electrode. The magnitude of synchronization was assessed using previously-reported synchronization indices: k′, E, and CIS. Synchronization was significantly higher in the FDI than in the BB. Greater synchronization was observed in the strength-trained group with CIS, but not with E or k′. Also, synchronization was significantly greater at 80% MVC than at 30% MVC with E, but only moderately greater with CIS and there was no force difference with k′. Synchronization prevalence was found to be greater in the BB (80.1%) than in the FDI (71.5%). Thus, although the evidence is a bit equivocal, it appears that MU synchronization is greater at higher forces, and greater in strength-trained individuals than in untrained subjects.

Introduction

Short-term motor unit synchronization is defined as the near-simultaneous discharge (±10 ms) of action potentials by two motor neurons more often than would be expected due to chance. The most frequently offered explanation for synchronization is that branched inputs from presynaptic neurons produce a common synaptic input that increases the probability of simultaneous discharge in the motor neurons sharing these inputs. In short-term synchronization, activity along these branched inputs results in a narrow central peak (⩽10 ms) in a cross-correlogram. The phenomenon of short-term synchronization has been investigated under numerous conditions. For example, although motor unit synchronization appears to be unaffected by advancing age once adult maturity has been achieved (Kamen and Roy, 2000, Semmler et al., 2006), it is greater during lengthening contractions than shortening contractions (Semmler et al., 2002), and greater during finger extension than finger flexion (Bremner et al., 1991). It should be noted, however, that it is frequently difficult to compare the magnitude of synchronization across studies due to the use of different synchronization indices by investigators.

Neural adaptations in motor unit discharge behavior as a result of resistance exercise training include changes in activation level (Knight and Kamen, 2004), motor unit firing rate (Kamen and Knight, 2004) and increases in doublet firing (Van Cutsem et al., 1998). Synchronization is also believed to enhance muscular force output and several studies have focused on synchronization using a subject’s training status as the main independent factor. One of the earliest studies in this area found that weight lifters exhibited greater synchronization in the first dorsal interosseous muscle (FDI) than control subjects (Milner-Brown et al., 1975). The Milner-Brown study also showed an increase in synchronization following a brief 6-week strength training protocol. However, this study utilized an indirect method of averaging the surface EMG signal with respect to motor unit discharge to provide a global estimate of synchronization and the validity of this surface EMG technique has been challenged (Yue et al., 1995). Felici et al. (2001) observed burst-like activity in resistance-trained individuals which they interpreted as indirect evidence for synchronization. A more recent study using direct motor unit measurements (Semmler and Nordstrom, 1998) compared motor unit synchronization in weight lifters, untrained subjects, and highly-trained musicians. Similar to the earlier Milner-Brown et al. findings (Milner-Brown et al., 1975), strength-trained weight lifters displayed the highest magnitude of synchronization while skill-trained musicians revealed the least amount of synchronization. These findings further support the idea that synchronization may be an adaptation that occurs as a result of strength training, allowing for greater muscular force production. However, in an effort to extend these findings, (Kidgell et al., 2006) required subjects to undertake a short-term strength training program (4–8 weeks) and found that training produced no change in the magnitude of synchronization in the FDI muscle, despite significant increases in the maximal voluntary contraction (MVC). Thus, one interpretation is that the magnitude of motor unit synchronization is an innate measure, reflecting the number of common descending inputs to motoneurons.

Although previous work has advanced our understanding regarding the occurrence and underlying mechanisms of motor unit synchronization, there have been certain limitations in studies performed thus far. The overwhelming majority of studies have examined motor units recruited at low relative force levels (2–30% MVC), limiting the understanding of how force output may influence synchronization. Along with these low force levels, the FDI has been the most frequently studied muscle, raising questions whether adaptations observed in this muscle are consistent with those observed throughout the rest of the body. In particular, motor unit adaptations that occur in a muscle specifically targeted during a typical resistance training program need to be further investigated. Selection of an appropriate synchronization index, and the relationship between these indices, has also been difficult to assess. Therefore, the purpose of this study is to compare both the magnitude and prevalence of motor unit synchronization in the biceps brachii (BB) and the FDI of untrained and strength-trained males at both submaximal (30% MVC) and near maximal (80% MVC) force levels utilizing three different synchronization indices.

Section snippets

Subjects

Twenty males were recruited for this study, consisting of 10 strength-trained individuals (age: 21.3 ± 2.96 years, height: 70.6 ± 2.73 in., weight: 178.9 ± 16.97 lbs), defined as weightlifters who frequently participated (mean = 5 h/week, 4.4 years) in resistive strength training involving the upper extremities, and 10 individuals (age: 20.2 ± 2.53 years, height: 69.4 ± 3.03 in., weight: 159.5 ± 25.22 lbs) with no resistive strength training activity within the past 3 years. All participants were free of any

Force

As expected maximal voluntary contractile force (MVC) was significantly higher (p < 0.001) in the trained group than in the untrained group for both index finger abduction (trained (T): 19.2 ± 2.72 N; untrained (U): 17.1 ± 3.32 N) and elbow flexion (T: 266.2 ± 56.84 N; U: 180.8 ± 50.16 N).

Motor unit sample

A total of 436 motor units (202 T, 234 U) were obtained for this experiment from twenty subjects, allowing for synchronization analysis of 473 motor unit pairs (217 T, 256 U). The characteristics of the motor unit set

Discussion

The present results provide additional support for the existence of greater synchronization in trained individuals and extend these findings to a larger muscle trained heavily in weightlifters, the biceps brachii (Fig. 2). Both CIS and E indexes were greater in the trained group than in the untrained group. Although the group differences were statistically significant (at α < 0.05) only for E, analysis of effect sizes produced a medium effect size for CIS (η2 = 0.06) and a large effect size (η2 = 

Conclusion

The present results are consistent with previous studies demonstrating greater magnitude of motor unit synchronization in the FDI than in the BB. However, in contrast to previous studies the prevalence of synchronization was greater in the BB than in the FDI. The bulk of the evidence supports the observation that synchronization magnitude is greater in strength-trained individuals, although the effect size may vary depending upon the choice of synchronization index. These results also support

Acknowledgement

This research was supported by an ACSM Foundation Research Grant from the American College of Sports Medicine Foundation.

Brett W. Fling research interests are focused on attempting to better understand neural adaptations that occur in individuals with voluntary movement disorders and applying this knowledge to improve their quality of life. I currently use several neuroimaging techniques, such as functional MRI and diffusion tensor imaging, as an important tool in my research at the University of Michigan. Our current research is a collaborative effort with Dr. Robert Welsh, a research investigator in the

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    Brett W. Fling research interests are focused on attempting to better understand neural adaptations that occur in individuals with voluntary movement disorders and applying this knowledge to improve their quality of life. I currently use several neuroimaging techniques, such as functional MRI and diffusion tensor imaging, as an important tool in my research at the University of Michigan. Our current research is a collaborative effort with Dr. Robert Welsh, a research investigator in the Department of Radiology. Projects include a longitudinal study examining cortical plasticity during real and imagined hand movements in individuals with amyotrophic lateral sclerosis (ALS). The end result of this study will culminate in an attempt at designing a more refined brain–computer interface to allow “locked-in” ALS individuals the ability to communicate. Another on-going project is investigating neural correlates of complexity on both unimanual and multiple bimanual motor tapping tasks in healthy young and older adults.

    Anita Christie completed her undergraduate degree in Neuroscience and her Master’s degree in Applied Health Sciences at Brock University. She is currently working on her doctoral degree in the Department of Kinesiology at the University of Massachusetts, Amherst, under the direction of Dr. Gary Kamen. Her research interests include the neural control of movement and neuromuscular adaptations to exercise and aging.

    Gary Kamen received his Ph.D. in Exercise Science from the University of Massachusetts. Following academic appointments at Indiana University and Boston University, he joined the Department of Exercise Science (now Kinesiology) at UMass Amherst in 1995. Many of his research activities have been designed to understand how processes such as long-term exercise, fatigue and aging produce adaptations in neural control and the neuromuscular system. These projects, supported by NIH, ACSM and other sponsors, have culminated in the publication of over 100 books, book chapters, articles and research abstracts at national and international meetings. He serves as a reviewer for over 20 journals and numerous granting agencies. He is currently a Fellow of the AAHPERD Research Consortium, the American College of Sports Medicine, and the American Academy of Kinesiology and Physical Education.

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