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Counterpoint: The interpolated twitch does not provide a valid measure of the voluntary activation of muscle

2009; American Physiological Society; Volume: 107; Issue: 1 Linguagem: Inglês

10.1152/japplphysiol.91220.2008a

ISSN

8750-7587

Autores

A. de Haan, K. H. L. Gerrits, Cornelis J. de Ruiter,

Tópico(s)

Advanced Sensor and Energy Harvesting Materials

Resumo

POINT-COUNTERPOINTCounterpoint: The interpolated twitch does not provide a valid measure of the voluntary activation of muscleA. de Haan, K. H. L. Gerrits, and C. J. de RuiterA. de Haan, K. H. L. Gerrits, and C. J. de RuiterPublished Online:01 Jul 2009https://doi.org/10.1152/japplphysiol.91220.2008aMoreSectionsPDF (105 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations The interpolated twitch technique (ITT) was first used by Merton (17) who superimposed an evoked stimulation on a voluntary contraction to detect muscle fibers not activated by the voluntary effort. The method has since been applied, mainly during isometric contractions, to determine how much of the muscles' potential can be used voluntarily. When no extra force is produced on a superimposed stimulus, this is usually taken as sign that "full activation" was achieved. Different methodological issues related to the measurement of voluntary activation have been addressed in the past, such as timing of, potentiation of, and type (single, doublet, multiple pulses) of the superimposed stimulus (6, 12, 18, 19), intermuscular differences (5), the method of extrapolation used to determine maximal muscle capacity (linear or curvilinear (4, 12), the influence of series elastic structures, synergistic and antagonist activation (2, 16), etc. Overall, these methodological reports indicate that the method can provide a valid estimation of voluntary activation, but that it should be used with care. In this Point:Counterpoint, we want to point out some major limitations of the ITT technique. The main issue addressed in this Counterpoint is what "full activation" signifies.The first point is the low sensitivity of the ITT method at near maximal contraction intensities (13). It should be noted that in accordance with the s-shaped stimulation frequency-force relation, the superimposed stimulus leads to relatively large increases in isometric force during submaximal contractions (with nonsaturating intracellular calcium concentrations, [Ca2+]i), but that only very small increases can be expected when maximal effort is approached. Clearly there is a low sensitivity of the ITT method at near maximal contraction intensities (13). "Full activation" in relation to the ITT method thus seems defined as the level of excitation ([Ca2+]i) needed to produce maximal force under the given contractile conditions. Surface EMG data show that for many subjects the EMG-force relationship is linear up to the near maximal voluntary isometric force (23). However, subjects with a high ability to "voluntarily activate" their muscles (e.g., with a high neural drive) show steep increases in EMG during contractions >80% of their maximal force, illustrating that much more extra excitation ([Ca2+]i ) is needed to completely use the force generating potential of the muscle (1, 14). Therefore, it can be expected that under those conditions (>80% maximal force capacity) in many experimental set ups a single superimposed twitch does not result in a measurable force increase. Consequently the force at which "full activation" is obtained is substantially underestimated in many studies.The second point is that it is not allowed to generalize findings based on a specific measurement of voluntary activation. Usually, measurements of voluntary activation have been carried out under isometric conditions and at a single specific joint angle. Such data cannot be extrapolated to other conditions. For instance, voluntary activation at one joint angle can be different from other angles, especially at angles where muscle length is short. The stimulation frequency-force relation shifts to the right at shorter muscle lengths (8), consequently higher levels of excitation are needed to obtain maximal force. It will therefore probably be more difficult to reach high levels of voluntary activation at shorter muscle lengths. Indeed, voluntary activation was measured to be lower at shorter muscle length in large muscle groups, such as the quadriceps femoris, which are relatively difficult to activate (3, 15). The poor ability to generalize voluntary activation established under isometric conditions is also illustrated by data during rapid fast "explosive" force attempts. Muscle excitation, inferred from surface EMG, is very short and much higher during jumping (10) and during fast isometric force rise (9, 22), compared with excitation at the plateau of an isometric contraction. The capacity to voluntarily activate muscles during explosive isometric contractions can be measured by comparing the initial fast-increasing force response during voluntary and electrically evoked contractions. In subjects who all had "high" voluntary activation, as established with ITT at the isometric force plateau during MVCs of the quadriceps muscles (96.5 ± 2.9%), large variations were seen in the capacity of initial activation during maximal fast contractions (9). The observed variation in this capacity was highly correlated with the initial EMG, indicating that differences in neural drive underlie this variation (9). Moreover, these findings show that the level of excitation, high enough for a near 100% activation at the plateau of an isometric contraction (full activation), is far from "full" under other conditions.The third point is that the implicit consequence of the measurement of voluntary activation is that maximal capacity is obtained at 100% voluntary activation. For the estimation of the maximal capacity, linear and curvilinear extrapolations of the superimposed force-voluntary force relation are used (7, 11). The differences in optimal curve fitting may be a consequence of variation in the ability of subject groups to "voluntarily activate" their muscles, leading to linear or curvilinear EMG-force relationships (1, 14). In almost all reports, curve fitting is performed for data of whole groups of subjects, which may mask relationships for individual subjects. Data from Kooistra et al. (14) indicate that for single subjects there might be a linear phase in the relationship between superimposed and voluntary torque, which in subjects with a very high neural drive is followed by a second (linear) phase (14 resp. Fig. 1), during which increases in EMG are much steeper than increases in voluntary force. For subjects with a very high neural drive, high voluntary activation levels (>95%) can be calculated using linear extrapolations from submaximal contraction levels, resulting in maximal capacity estimations, which are far below their real maximal capacity. From the inset in Fig. 2 it can be seen that the (very small) superimposed forces decline linearly and similarly with increasing voluntary forces on two different days. The consequence of the data for the subject displayed in Fig. 2 is that for the measurement with a torque of ∼150 Nm and extrapolating the linear relation between voluntary and superimposed torque below 150 Nm, a voluntary activation level of ∼96% is calculated, whereas in reality 150 Nm is only ∼75% of the measured maximal torque, which would indicate a voluntary activation level of ∼75%. Clearly, there is a mismatch between calculated voluntary activation levels and maximal torque capacity. Thus, even at the isometric force plateau, an almost full activation may be far from complete, at least in some subjects and in large muscle groups. In the scarce reports that show examples of data for individual subjects, linear relationships can be seen for the submaximal contractions, but there are additional data points having a low superimposed force at near maximal voluntary forces. The voluntary forces of these latter data points seem to be higher than the maximal force capacity calculated from the submaximal data (2, 19–21). Although only for subjects who are consistently very well able to activate their muscles, overestimation of voluntary activation can be demonstrated, it is conceivable that this in fact occurs for all subjects. Many subjects will not be able to further increase muscle excitation and despite measured levels of voluntary activation of ∼95% most of them do not approach their real maximal force capacity. The ITT method clearly overestimates the true voluntary activation and therewith underestimates maximal force capacity in many subjects. Fig. 2.Schematic illustration of the relationship between the amplitude of the superimposed twitch evoked by twitch interpolation and contraction strength. An inverse linear relationship is ideal. Nonlinearity can be introduced by various methodological and physiological factors.Download figureDownload PowerPointREFERENCES1 Alkner BA, Tesch PA, Berg HE. Quadriceps EMG/force relationship in knee extension and leg press. Med Sci Sports Exerc 32: 459–463, 2000.Crossref | PubMed | ISI | Google Scholar2 Allen GM, McKenzie DK, Gandevia SC. Twitch interpolation of the elbow flexor muscles at high forces. Muscle Nerve 21: 318–328, 1998.Crossref | PubMed | ISI | Google Scholar3 Becker R, Awiszus F. Physiological alterations of maximal voluntary quadriceps activation by changes of knee joint angle. 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Novel Perspectives from Mechanomyographic Data27 October 2022 | Medicine & Science in Sports & Exercise, Vol. 55, No. 3The effect of constant load cycling at extreme- and severe-intensity domains on performance fatigability and its determinants in young femaleScience & Sports, Vol. 74Determining voluntary activation in synergistic muscles: a novel mechanomyographic approach24 May 2022 | European Journal of Applied Physiology, Vol. 122, No. 8Acute Neuromuscular and Hormonal Responses to Power, Strength, and Hypertrophic Protocols and Training Background14 July 2022 | Frontiers in Sports and Active Living, Vol. 4Increase in Volitional Muscle Activation from Childhood to Adulthood: A Systematic Review and Meta-analysis30 December 2021 | Medicine & Science in Sports & Exercise, Vol. 54, No. 5A voluntary activation deficit in m. abductor hallucis exists in asymptomatic feetJournal of Biomechanics, Vol. 130Quantification of central fatigue: a central debate15 May 2021 | European Journal of Applied Physiology, Vol. 121, No. 9Comparison Between Isometric and Concentric Motor Fatigability in Persons With Multiple Sclerosis and Healthy Controls – exploring central and peripheral contributions of motor fatigability22 May 2021 | Neurorehabilitation and Neural Repair, Vol. 35, No. 7Specific motor cortex hypoexcitability and hypoactivation in COPD patients with peripheral muscle weakness3 January 2020 | BMC Pulmonary Medicine, Vol. 20, No. 1Peripheral Electrical Stimulation Paired With Movement-Related Cortical Potentials Improves Isometric Muscle Strength and Voluntary Activation Following Stroke15 May 2020 | Frontiers in Human Neuroscience, Vol. 14Quantification of Neuromuscular Fatigue: What Do We Do Wrong and Why?12 November 2019 | Sports Medicine, Vol. 50, No. 3Neuromuscular Factors Contributing to Reductions in Muscle Force After Repeated, High-Intensity Muscular Efforts24 June 2019 | Frontiers in Physiology, Vol. 10Neural Adaptations to Endurance Training1 November 2018Neural and Muscular Function in the Heat7 March 2019The role of the nervous system in neuromuscular fatigue induced by ultra-endurance exerciseApplied Physiology, Nutrition, and Metabolism, Vol. 43, No. 11Estimating Voluntary Activation Of The Elbow And Wrist Muscles In Chronic Hemiparetic Stroke Using Twitch Interpolation MethodologyPlasticity in central neural drive with short-term disuse and recovery - effects on muscle strength and influence of agingExperimental Gerontology, Vol. 106The Effects of Sex and Motoneuron Pool on Central FatigueMedicine & Science in Sports & Exercise, Vol. 50, No. 5Neurophysiological Mechanisms Underpinning Stretch-Induced Force Loss24 January 2017 | Sports Medicine, Vol. 47, No. 8Voluntary activation of biceps-to-triceps and deltoid-to-triceps transfers in quadriplegia2 March 2017 | PLOS ONE, Vol. 12, No. 3Original Research: Central and peripheral quadriceps fatigue in young and middle-aged untrained and endurance-trained men: A comparative study24 July 2016 | Experimental Biology and Medicine, Vol. 241, No. 16Voluntary muscle activation improves with power training and is associated with changes in gait speed in mobility-limited older adults — A randomized controlled trialExperimental Gerontology, Vol. 80Muscle Fatigue Affects the Interpolated Twitch Technique When Assessed Using Electrically-Induced Contractions in Human and Rat Muscles28 June 2016 | Frontiers in Physiology, Vol. 7Is the notion of central fatigue based on a solid foundation?Paola Contessa, Alessio Puleo, and Carlo J. De Luca16 February 2016 | Journal of Neurophysiology, Vol. 115, No. 2Task-specific neural adaptations to isoinertial resistance training31 July 2014 | Scandinavian Journal of Medicine & Science in Sports, Vol. 25, No. 5Children have a reduced maximal voluntary activation level of the adductor pollicis muscle compared to adults19 February 2015 | European Journal of Applied Physiology, Vol. 115, No. 7Evaluation of Central and Peripheral Fatigue in the Quadriceps Using Fractal Dimension and Conduction Velocity in Young Females16 April 2015 | PLOS ONE, Vol. 10, No. 4Activation deficit correlates with weakness in chronic stroke: Evidence from evoked and voluntary EMG recordingsClinical Neurophysiology, Vol. 125, No. 12The influence of strength training on muscle activation in elderly persons: A systematic review and meta-analysisExperimental Gerontology, Vol. 58Time Course of Central and Peripheral Alterations after Isometric Neuromuscular Electrical Stimulation-Induced Muscle Damage12 September 2014 | PLoS ONE, Vol. 9, No. 9Combining heat stress and moderate hypoxia reduces cycling time to exhaustion without modifying neuromuscular fatigue characteristics19 April 2014 | European Journal of Applied Physiology, Vol. 114, No. 7Insights into the neural control of eccentric contractionsJacques Duchateau, and Stéphane Baudry1 June 2014 | Journal of Applied Physiology, Vol. 116, No. 11Neuromuscular Adjustments of the Quadriceps Muscle after Repeated Cycling Sprints1 May 2013 | PLoS ONE, Vol. 8, No. 5Hot conditions improve power output during repeated cycling sprints without modifying neuromuscular fatigue characteristics29 June 2012 | European Journal of Applied Physiology, Vol. 113, No. 2Potential interests and limits of magnetic and electrical stimulation techniques to assess neuromuscular fatigueNeuromuscular Disorders, Vol. 22Distinct profiles of neuromuscular fatigue during muscle contractions below and above the critical torque in humansMark Burnley, Anni Vanhatalo, and Andrew M. 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Horstman1 July 2009 | Journal of Applied Physiology, Vol. 107, No. 1Last Word on Point:Counterpoint: The interpolated twitch does/does not provide a valid measure of the voluntary activation of muscleA. de Haan, K. H. L. Gerrits, and C. J. de Ruiter1 July 2009 | Journal of Applied Physiology, Vol. 107, No. 1 More from this issue > Volume 107Issue 1July 2009Pages 355-357 Copyright & PermissionsCopyright © 2009 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.91220.2008aPubMed19567806History Published online 1 July 2009 Published in print 1 July 2009 Metrics

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