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Manuscript Clarification

Greater Electromyographic Responses Do Not Imply Greater Motor Unit Recruitment and ‘Hypertrophic Potential’ Cannot Be Inferred

Vigotsky, Andrew D.; Beardsley, Chris; Contreras, Bret; Steele, James; Ogborn, Dan; Phillips, Stuart M.

Journal of Strength and Conditioning Research: January 2017 - Volume 31 - Issue 1 - p e1-e4
doi: 10.1519/JSC.0000000000001249
Erratum

In the January 2017 issue of the in the manuscript clarification by Vigotsky, Beardsley, Contreras, Steele, Ogborn, and Phillips, “Greater Electromyographic Responses Do Not Imply Greater Motor Unit Recruitment and ‘Hypertrophic Potential’ Cannot Be Inferred”, the second reference should have read as follows: Behm DG. Neuromuscular implications and applications of resistance training. 9: 264-274, 1995.

This has been corrected online.

The Journal of Strength & Conditioning Research. 31(2):e66, February 2017.

To the Editor:

We read with interest the study by Looney et al. (13), investigating the effects of load on electromyographic (EMG) amplitude and rating of perceived exertion (RPE) during squats taken to muscular failure. There are numerous interesting takeaways from this study, including the similar RPE outcomes of different loads when sets are taken to failure; however, we demur with the authors' interpretation of the findings.

In the title and the body of the article, the term motor unit (MU) recruitment is used synonymously with EMG amplitude. This is an incorrect assumption, but regrettably a common mistake in sports and exercise science. We find this mistake being made especially when dealing with fatiguing and dynamic conditions, such as those investigated by Looney et al. (13). In fact, Enoka and Duchateau (7) recently described how numerous studies have misinterpreted surface EMG signals by inferring specific MU recruitment. More than 2 decades previously, De Luca (4) stated, “To its detriment, electromyography is too easy to use and consequently too easy to abuse.” Looney et al. (13) state that MU firing rate decreases with fatigue (10,15) and consequently that the increase in EMG amplitude is caused by increased MU recruitment (19–21) and has applied that same logic to the subsequent interpretation of the findings, as the authors repeatedly state that the greater EMG amplitude observed in the heavier conditions is indicative of greater MU recruitment. Regrettably, the interpretation of EMG is not so straightforward. Moreover, different quadriceps muscles may use different neural strategies to maintain force generation during repeated concentric contractions (6), which makes the findings of Looney et al. (13) particularly difficult to interpret.

Although EMG amplitude is influenced by MU recruitment, MU recruitment cannot be inferred from changes in surface EMG amplitude. The recruitment threshold of high threshold MUs is reduced during sustained, fatiguing contractions (1), and the subsequent recruitment of these MUs assists in the maintenance force production. However, MU cycling may momentarily derecruit fatigued MUs to reduce fatigue (22). This means that, in scenarios that require less force output, such as low-load conditions, there may be lower simultaneous MU recruitment compared with high-load conditions. Ultimately, a comparable complement of the MU population of a particular muscle may be recruited, but not simultaneously as in high-load conditions. This would explain the observation of reduced peak EMG amplitude in low-load training, as reported by Looney et al. (13). These factors, including the reduced recruitment threshold of high threshold MUs, in addition to MU cycling during fatiguing contractions, may also explain other recent work showing differences in peak amplitude measured during surface EMG for high-load and low-load conditions (12,16).

Electromyographic amplitude during fatiguing conditions can be extraordinarily misleading, as EMG measures consist not only of multiple neural components (MU recruitment, rate coding, and possibly MU synchronization) but also of multiple peripheral constituents: muscle fiber propagation velocity and intracellular action potentials (5). Intracellular action potentials are of particular interest during fatiguing conditions, as the ensuing increase in length of intracellular action potentials may augment surface EMG signals, despite a decrease in intracellular action potential magnitude. These inherent limitations make it impossible to discern MU recruitment from increases in EMG amplitude during fatiguing, dynamic conditions (2,5,8,9). It may be true that greater loads induce greater MU recruitment, but to measure this, more advanced methods are needed, such as spike-triggered averaging (3) or initial wavelet analysis followed by principal component classification of major frequency properties and optimization to tune wavelets to these frequencies (11).

In addition to our concerns regarding the confusion of EMG amplitude with MU recruitment, we note that inferring chronic adaptations from acute, mechanistic variables is very difficult. Looney et al. (13) suggest that their findings support the use of heavier loads for hypertrophy. Such a conclusion is unwarranted, as the literature does not currently differentiate between the long-term effects of heavy and light loads on increases in muscular size (18). Data from Mitchell et al. (14) also demonstrated comparable growth of type I and II fibers after 10 weeks of strength training at either low (30% 1 repetition maximum [1RM]) or high-loads (80% 1RM). If the differential EMG amplitude between high and low-load training observed by Looney et al. (13) and others (12,16) is representative of greater recruitment of presumably high threshold MUs, then one would expect a differential hypertrophic response between low and high threshold MUs, which is presently not supported. In fact, from an evidence-based perspective, Schoenfeld et al. (18), in their meta-analysis, showed no difference between studies that have used lighter or heavier loads to induce hypertrophy. A recent study by the same author confirmed that this was true even in well trained participants (17). Thus, longitudinal trials are clearly needed to elucidate these mechanisms, in addition to comparing individual loading with combined loading schemes.

The findings of Looney et al. (13) provide more data that unequal EMG amplitudes are obtained during fatiguing contractions with low-load and high-load conditions and the novel finding that both conditions elicit similar RPE. What these data do not provide, however, is evidence that heavier load contractions recruit more MUs and that this can be inferred to result in greater hypertrophy. We hope that our letter helps put these findings into a clearer perspective.

References

1. Adam A, De Luca CJ. Recruitment order of motor units in human vastus lateralis muscle is maintained during fatiguing contractions. J Neurophysiol 90: 2919–2927, 2003.
2. Behm DG. Neuromuscular implications and applications of resistance training. J Strength Cond Res 9: 264–274, 1995.
3. Boe SG, Stashuk DW, Doherty TJ. Motor unit number estimation by decomposition-enhanced spike-triggered averaging: Control data, test-retest reliability, and contractile level effects. Muscle Nerve 29: 693–699, 2004.
4. De Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 13: 135–163, 1997.
5. Dimitrova NA, Dimitrov GV. Interpretation of EMG changes with fatigue: Facts, pitfalls, and fallacies. J Electromyogr Kinesiol 13: 13–36, 2003.
6. Ebersole KT, O'Connor KM, Wier AP. Mechanomyographic and electromyographic responses to repeated concentric muscle actions of the quadriceps femoris. J Electromyogr Kinesiol 16: 149–157, 2006.
7. Enoka RM, Duchateau J. Inappropriate interpretation of surface EMG signals and muscle fiber characteristics impedes understanding of the control of neuromuscular function. J Appl Physiol (1985). 119:1516–1518, 2015.
8. Ertas M, Stalberg E, Falck B. Can the size principle be detected in conventional EMG recordings? Muscle Nerve 18: 435–439, 1995.
9. Freund HJ. Motor unit and muscle activity in voluntary motor control. Physiol Rev 63: 387–436, 1983.
10. Harwood B, Choi I, Rice CL. Reduced motor unit discharge rates of maximal velocity dynamic contractions in response to a submaximal dynamic fatigue protocol. J Appl Physiol (1985) 113: 1821–1830, 2012.
11. Hodson-Tole EF, Wakeling JM. Variations in motor unit recruitment patterns occur within and between muscles in the running rat (Rattus norvegicus). J Exp Biol 210: 2333–2345, 2007.
12. Jenkins ND, Housh TJ, Bergstrom HC, Cochrane KC, Hill EC, Smith CM, Johnson GO, Schmidt RJ, Cramer JT. Muscle activation during three sets to failure at 80 vs. 30 % 1RM resistance exercise. Eur J Appl Physiol 2015.
13. Looney DP, Kraemer WJ, Joseph MF, Comstock BA, Denegar CR, Flanagan SD, Newton RU, Szivak TK, DuPont WH, Hooper DR, Häkkinen K, Maresh CM. Electromyographical and Perceptual Responses to Different Resistance Intensities in a Squat Protocol: Does Performing Sets to Failure With Light Loads Produce the Same Activity? J Strength Cond Res 30: 792–799, 2016.
14. Mitchell CJ, Churchward-Venne TA, West DW, Burd NA, Breen L, Baker SK, Phillips SM. Resistance exercise load does not determine training-mediated hypertrophic gains in young men. J Appl Physiol (1985) 113: 71–77, 2012.
15. Mottram CJ, Jakobi JM, Semmler JG, Enoka RM. Motor-unit activity differs with load type during a fatiguing contraction. J Neurophysiol 93: 1381–1392, 2005.
16. Schoenfeld BJ, Contreras B, Willardson JM, Fontana F, Tiryaki-Sonmez G. Muscle activation during low- versus high-load resistance training in well-trained men. Eur J Appl Physiol 114: 2491–2497, 2014.
17. Schoenfeld BJ, Peterson MD, Ogborn D, Contreras B, Sonmez GT. Effects of low- versus high-load resistance training on muscle strength and hypertrophy in well-trained men. J Strength Cond Res 2015.
18. Schoenfeld BJ, Wilson JM, Lowery RP, Krieger JW. Muscular adaptations in low-versus high-load resistance training: A meta-analysis. Eur J Sport Sci: 1–10, 2014.
19. Smilios I, Hakkinen K, Tokmakidis SP. Power output and electromyographic activity during and after a moderate load muscular endurance session. J Strength Cond Res 24: 2122–2131, 2010.
20. Stock MS, Beck TW, Defreitas JM. Effects of fatigue on motor unit firing rate versus recruitment threshold relationships. Muscle Nerve 45: 100–109, 2012.
21. Toigo M, Boutellier U. New fundamental resistance exercise determinants of molecular and cellular muscle adaptations. Eur J Appl Physiol 97: 643–663, 2006.
22. Westad C, Westgaard RH, De Luca CJ. Motor unit recruitment and derecruitment induced by brief increase in contraction amplitude of the human trapezius muscle. J Physiol 552: 645–656, 2003.

In Response:

We certainly appreciated the interest of Vigotsky et al. on our study and for their comments on our recent study, which explored the effects of load on muscle activation and perceived exertion during the completion of fatiguing squat exercise protocols. Although the manuscript clarification (MC) letter raises a few interesting considerations, overall, the remarks convey a number of conceptual anomalies regarding basic principles of neuromuscular physiology that are worth further attention.

The request of Vigotsky for MC addresses the limitations of surface electromyography of which we are well aware. We agree it is an oversimplification to draw a direct parallel between a measure of electrical energy at the skin and the nature of motor unit recruitment in muscles. However, the purpose of our study was to compare surface electromyography between different relative loads and sets when submaximal and taken to failure. As pointed out in the request for clarification, there are some interesting outcomes with important practical implications.

The authors mention a number of important caveats in the interpretation of muscle activity during fatigue. However, this issue was deliberately addressed through the use of load-equated submaximal trials before the fatiguing resistance exercise protocols. Consequently, we demonstrated higher peak electromyographic (EMG) amplitudes in the presence of fatigue, which is consistent with observations of reduced recruitment thresholds during fatiguing contractions (1,6), as confirmed by work referenced in the MC. Moreover, although the authors of the MC question our contention of reduced motor unit firing rates during fatigue and implicitly question the maintenance of motor unit recruitment order under such conditions, the literature used to support their rebuttal precisely affirms these conclusions (1,6).

We agree with the statement of Vigotsky et al. that different muscles are likely to use different neural strategies to maintain force production. This is why we used the same muscles and electrode positions. The authors' difficulty in interpreting our findings is paradoxical when the literature used to justify their arguments conflicts with our experiment on that very basis (e.g., use of trapezius, anconeus, quadriceps, and other muscles with varying contractile properties). The issues with EMG signal interpretation, as discussed by groups cited in their MC letter (5), are minimized through the use of standardized acute program variables and a within-subject design. These experimental controls largely eliminate the variability associated with subcutaneous tissue thickness, the spatial distribution of muscle fibers and their conduction velocities, electrode location, and condition-specific action potential shapes. As Farina points out, these factors produce some uncertainty in amplitude-based estimates of neural drive to muscle. However, these concerns are also more relevant in between-group experiments, comparisons of different muscles, or acute program variables, or when minute aspects of motor unit activity are being investigated, especially when single unit techniques are used. We agree that surface EMG amplitude may serve as a “crude” indicator of neural drive to muscle; however, with respect to more general questions such as ours, with the appropriate experimental design, these estimates may also be more robust and meaningful.

As previously noted, a reduction in the recruitment threshold of higher threshold motor units may occur during fatiguing exercise to assist in the maintenance of force production. This would explain why identical movements and loads produced larger EMG amplitudes in the presence of fatigue. In contrast, this does not explain the observation of substantially lower peak amplitudes at lower loads compared with higher loads, regardless of the presence or absence of fatigue. It is important to emphasize the protocols resulted in similar total exercise volumes and postexercise force reductions. When these realities are considered in conjunction with the design of the experiment, the relevance of factors, such as motor unit cycling, synchronization, rate coding, propagation velocity, and intracellular action potentials, becomes questionable.

In light of arguments of Vigotsky, their choice of evidence is somewhat ironic. For example, despite providing no explanation of how our study misinterprets surface EMG signals in the manner outlined by (3), work by Enoka and De Luca generally supports our arguments (1–3,5). In recent discussion of common surface EMG misinterpretations by Enoka, the amplitude of the EMG signal is interpreted as “…the summation of motor unit action potentials, providing an index of muscle activation.” The purpose of Enoka's review was directed toward the limited ability to directly translate muscle fiber types into motor unit types on the basis of contractile properties. These issues and any related claims were not raised or implied in our investigation. Thus, although the provocative title of the article would seem to fit Vigotsky's narrative, the actual content leads us to question its relevance altogether.

In another example, as cited in the letter, Ertas et al. (4) suggested that the surface electrode measurement area is relatively small when compared with the overall motor unit territory. A within-group study with strict electrode positioning minimizes signaling differences resulting from this property. Moreover, as opposed to the measurement of the first 4 motor unit potentials, which reflects a relatively homogenous group of the lowest threshold motor units, the gross recording incorporates the combined activity of a large motor unit spectrum. In the vastus lateralis, there may be over one thousand motor units, with a maximum recruitment threshold of close to 95% 1 repetition maximum (1RM). In regard to the writers' argument, we highlight Ertas' finding that amplitude “tended to increase” between consecutively recruited motor unit potentials, despite the acknowledged use of a small number of highly homogenous low-threshold motor units.

Farina also made important observations on the contributions of amplitude cancellation, where the opposing polarities of different motor unit action potentials reduce the amplitude of surface signals. First, when measured using surface EMG, lower-threshold motor units produce smaller amplitude action potentials, which supports the contributions of higher threshold motor units to the larger EMG amplitudes observed with higher loads. As De Luca (2) observed over 35 years ago, this electrophysiological distinction reflects structural differences in muscle: the amplitude of action potentials increases as a function of muscle fiber diameter. As reported many times before, when the diameter of a muscle fiber increases, input resistance decreases and capacitance increases. Consequently, the muscle fibers are less excitable, ergo higher threshold. Second, because amplitude cancellation disproportionally affects low-threshold motor units, surface EMG amplitude is relatively insensitive to changes in these motor units, and therefore predominantly reflects changes in the activity of high-threshold motor units. Despite the lowering of recruitment thresholds as evidenced in the fatiguing protocols, this explains why higher loads always produced larger EMG amplitudes, and why a single set to failure at 50% 1RM did not produce more EMG activity when compared with heavier loads, or the same load, despite the completion of substantially more repetitions to failure. This also contradicts the argument of Vigotsky that the contributions of a comparable motor unit complement were obscured by differences in lower-threshold motor unit cycling properties.

In summary, dynamic muscle actions performed against lighter external resistance require activation of a lower percentage of the total motor units. This has been demonstrated in a very large number of studies, and is reaffirmed using a novel experimental paradigm that allowed us to discriminate the contributions of fatigue at different levels of muscle activation, ceteris paribus. The size principle dictates that higher threshold motor units are recruited less when lower muscle tension is required, and this remains evident in the presence of fatigue. In this study, we report higher signal energy in the surface electromyogram with heavier loads, and this is due to greater activation of the motor unit pool and by definition, the recruitment of larger, higher threshold motor units. The authors of the MC letter provide no counter to this finding or interpretation. Hence our recommendation of heavier loads for the activation of a larger spectrum of motor units, development of muscle strength, and ostensibly a favorable hypertrophic response.

We readily admit that neuromuscular fatigue induces several adjustments in motor unit activation strategies and intramuscular chemical alterations, which impact the electrical signal measured at the skin; this was not addressed in our study. Nevertheless, we report the energy in this signal is less for muscle contractions at 50% taken to failure compared to 90% 1RM; regardless of the contributing mechanisms, they are different and this has important implications. As the writers of the MC letter discuss, RPE was not different between the conditions, leading to our conclusion that heavier loads to failure involve the same perceived exertion but are superior in terms of time efficiency as well-being more effective for strength development, as demonstrated by Schoenfeld et al. (8) in a study cited in the letter. The same outcome of superior strength development was also reported by Dr. Phillips' group, as reported by Mitchell et al. (7), again cited in the MC letter.

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