On the role of skeletal muscle acidosis and inorganic phosphates as determinants of central and peripheral fatigue: A 31P‐MRS study
Intramuscular hydrogen ion (H+) and inorganic phosphate (Pi) concentrations were dissociated during exercise to challenge their relationships with peripheral and central fatigue in vivo. Ten recreationally active, healthy men (27 ± 5 years; 180 ± 4 cm; 76 ± 10 kg) performed two consecutive intermitt...
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| Veröffentlicht in: | The Journal of physiology Jg. 600; H. 13; S. 3069 - 3081 |
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| Abstract | Intramuscular hydrogen ion (H+) and inorganic phosphate (Pi) concentrations were dissociated during exercise to challenge their relationships with peripheral and central fatigue in vivo. Ten recreationally active, healthy men (27 ± 5 years; 180 ± 4 cm; 76 ± 10 kg) performed two consecutive intermittent isometric single‐leg knee‐extensor trials (60 maximal voluntary contractions; 3 s contraction, 2 s relaxation) interspersed with 5 min of rest. Phosphorus magnetic resonance spectroscopy (31P‐MRS) was used to continuously quantify intramuscular [H+] and [Pi] during both trials. Using electrical femoral nerve stimulation, quadriceps twitch force (Qtw) and voluntary activation (VA) were quantified at rest and throughout both trials. Decreases in Qtw and VA from baseline were used to determine peripheral and central fatigue, respectively. Qtw was strongly related to both [H+] (β coefficient: −0.9, P < 0.0001) and [Pi] (−1.1, P < 0.0001) across trials. There was an effect of trial on the relationship between Qtw and [H+] (−0.5, P < 0.0001), but not Qtw and [Pi] (0.0, P = 0.976). This suggests that, unlike the unaltered association with [Pi], a given level of peripheral fatigue was associated with a different [H+] in Trial 1 vs. Trial 2. VA was related to [H+] (−0.3, P < 0.0001), but not [Pi] (−0.2, P = 0.243), across trials and there was no effect of trial (−0.1, P = 0.483). Taken together, these results support intramuscular Pi as a primary cause of peripheral fatigue, and muscle acidosis, probably acting on group III/IV muscle afferents in the interstitial space, as a contributor to central fatigue during exercise.
Key points
We investigated the relationship between intramuscular metabolites and neuromuscular function in humans performing two maximal, intermittent, knee‐extension trials interspersed with 5 min of rest.
Concomitant measurements of intramuscular hydrogen (H+) and inorganic phosphate (Pi) concentrations, as well as quadriceps twitch‐force (Qtw) and voluntary activation (VA), were made throughout each trial using phosphorus magnetic resonance spectroscopy (31P‐MRS) and electrical femoral nerve stimulations.
Although [Pi] fully recovered prior to the onset of the second trial, [H+] did not.
Qtw was strongly related to both [H+] and [Pi] across both trials. However, the relationship between Qtw and [H+] shifted leftward from the first to the second trial, whereas the relationship between Qtw and [Pi] remained unaltered. VA was related to [H+], but not [Pi], across both trials.
These in vivo findings support the hypotheses of intramuscular Pi as a primary cause of peripheral fatigue, and muscle acidosis, probably acting on group III/IV muscle afferents, as a contributor to central fatigue.
figure legend Schematic diagram illustrating the experimental design and major findings. |
|---|---|
| AbstractList | Intramuscular hydrogen ion (H+) and inorganic phosphate (Pi) concentrations were dissociated during exercise to challenge their relationships with peripheral and central fatigue in vivo. Ten recreationally active, healthy men (27±5 years; 180±4 cm; 76±10 kg) performed two consecutive intermittent isometric single-leg knee-extensor trials (60 maximal voluntary contractions; 3s-contraction, 2s-relaxation) interspersed with 5 min of rest. Phosphorus magnetic resonance spectroscopy (31P-MRS) was used to continuously quantify intramuscular [H+] and [Pi] during both trials. Using electrical femoral nerve stimulation, quadriceps twitch force (Qtw) and voluntary activation (VA) were quantified at rest and throughout both trials. Decreases in Qtw and VA from baseline were used to determine peripheral and central fatigue, respectively. Qtw was strongly related to both [H+] (β Coefficient: −0.9, P < 0.0001) and [Pi] (−1.1, P < 0.0001) across trials. There was an effect of trial on the relationship between Qtw and [H+] (−0.5, P < 0.0001), but not Qtw and [Pi] (0.0, P = 0.976). This suggests that, unlike the unaltered association with [Pi], a given level of peripheral fatigue was associated with a different [H+] in trial 1 vs trial 2. VA was related to [H+] (−0.3, P < 0.0001), but not [Pi] (−0.2, P = 0.243), across trials and there was no effect of trial (−0.1, P = 0.483). Taken together, these results support intramuscular Pi as a primary cause of peripheral fatigue, and muscle acidosis, likely acting on group III/IV muscle afferents in the interstitial space, as a contributor to central fatigue during exercise. Intramuscular hydrogen ion (H+) and inorganic phosphate (Pi) concentrations were dissociated during exercise to challenge their relationships with peripheral and central fatigue in vivo. Ten recreationally active, healthy men (27 ± 5 years; 180 ± 4 cm; 76 ± 10 kg) performed two consecutive intermittent isometric single‐leg knee‐extensor trials (60 maximal voluntary contractions; 3 s contraction, 2 s relaxation) interspersed with 5 min of rest. Phosphorus magnetic resonance spectroscopy (31P‐MRS) was used to continuously quantify intramuscular [H+] and [Pi] during both trials. Using electrical femoral nerve stimulation, quadriceps twitch force (Qtw) and voluntary activation (VA) were quantified at rest and throughout both trials. Decreases in Qtw and VA from baseline were used to determine peripheral and central fatigue, respectively. Qtw was strongly related to both [H+] (β coefficient: −0.9, P < 0.0001) and [Pi] (−1.1, P < 0.0001) across trials. There was an effect of trial on the relationship between Qtw and [H+] (−0.5, P < 0.0001), but not Qtw and [Pi] (0.0, P = 0.976). This suggests that, unlike the unaltered association with [Pi], a given level of peripheral fatigue was associated with a different [H+] in Trial 1 vs. Trial 2. VA was related to [H+] (−0.3, P < 0.0001), but not [Pi] (−0.2, P = 0.243), across trials and there was no effect of trial (−0.1, P = 0.483). Taken together, these results support intramuscular Pi as a primary cause of peripheral fatigue, and muscle acidosis, probably acting on group III/IV muscle afferents in the interstitial space, as a contributor to central fatigue during exercise. Key points We investigated the relationship between intramuscular metabolites and neuromuscular function in humans performing two maximal, intermittent, knee‐extension trials interspersed with 5 min of rest. Concomitant measurements of intramuscular hydrogen (H+) and inorganic phosphate (Pi) concentrations, as well as quadriceps twitch‐force (Qtw) and voluntary activation (VA), were made throughout each trial using phosphorus magnetic resonance spectroscopy (31P‐MRS) and electrical femoral nerve stimulations. Although [Pi] fully recovered prior to the onset of the second trial, [H+] did not. Qtw was strongly related to both [H+] and [Pi] across both trials. However, the relationship between Qtw and [H+] shifted leftward from the first to the second trial, whereas the relationship between Qtw and [Pi] remained unaltered. VA was related to [H+], but not [Pi], across both trials. These in vivo findings support the hypotheses of intramuscular Pi as a primary cause of peripheral fatigue, and muscle acidosis, probably acting on group III/IV muscle afferents, as a contributor to central fatigue. figure legend Schematic diagram illustrating the experimental design and major findings. Intramuscular hydrogen ion (H+) and inorganic phosphate (Pi) concentrations were dissociated during exercise to challenge their relationships with peripheral and central fatigue in vivo. Ten recreationally active, healthy men (27 ± 5 years; 180 ± 4 cm; 76 ± 10 kg) performed two consecutive intermittent isometric single‐leg knee‐extensor trials (60 maximal voluntary contractions; 3 s contraction, 2 s relaxation) interspersed with 5 min of rest. Phosphorus magnetic resonance spectroscopy (31P‐MRS) was used to continuously quantify intramuscular [H+] and [Pi] during both trials. Using electrical femoral nerve stimulation, quadriceps twitch force (Qtw) and voluntary activation (VA) were quantified at rest and throughout both trials. Decreases in Qtw and VA from baseline were used to determine peripheral and central fatigue, respectively. Qtw was strongly related to both [H+] (β coefficient: −0.9, P < 0.0001) and [Pi] (−1.1, P < 0.0001) across trials. There was an effect of trial on the relationship between Qtw and [H+] (−0.5, P < 0.0001), but not Qtw and [Pi] (0.0, P = 0.976). This suggests that, unlike the unaltered association with [Pi], a given level of peripheral fatigue was associated with a different [H+] in Trial 1 vs. Trial 2. VA was related to [H+] (−0.3, P < 0.0001), but not [Pi] (−0.2, P = 0.243), across trials and there was no effect of trial (−0.1, P = 0.483). Taken together, these results support intramuscular Pi as a primary cause of peripheral fatigue, and muscle acidosis, probably acting on group III/IV muscle afferents in the interstitial space, as a contributor to central fatigue during exercise.Key pointsWe investigated the relationship between intramuscular metabolites and neuromuscular function in humans performing two maximal, intermittent, knee‐extension trials interspersed with 5 min of rest.Concomitant measurements of intramuscular hydrogen (H+) and inorganic phosphate (Pi) concentrations, as well as quadriceps twitch‐force (Qtw) and voluntary activation (VA), were made throughout each trial using phosphorus magnetic resonance spectroscopy (31P‐MRS) and electrical femoral nerve stimulations.Although [Pi] fully recovered prior to the onset of the second trial, [H+] did not.Qtw was strongly related to both [H+] and [Pi] across both trials. However, the relationship between Qtw and [H+] shifted leftward from the first to the second trial, whereas the relationship between Qtw and [Pi] remained unaltered. VA was related to [H+], but not [Pi], across both trials.These in vivo findings support the hypotheses of intramuscular Pi as a primary cause of peripheral fatigue, and muscle acidosis, probably acting on group III/IV muscle afferents, as a contributor to central fatigue. |
| Author | Lewis, Matthew T. Broxterman, Ryan M. Layec, Gwenael Weavil, Joshua C. Amann, Markus Hureau, Thomas J. |
| AuthorAffiliation | 3 Department of Medicine, University of Utah, Salt Lake City, UT, USA 2 Geriatric Research, Education, and Clinical Center, Salt Lake City VAMC, UT, USA 4 University of Strasbourg, Faculty of Sport Sciences, UR 3072: Mitochondria, Oxidative Stress and Muscular Protection laboratory, Strasbourg, France 1 Department of Anesthesiology, University of Utah, Salt Lake City, UT, USA |
| AuthorAffiliation_xml | – name: 4 University of Strasbourg, Faculty of Sport Sciences, UR 3072: Mitochondria, Oxidative Stress and Muscular Protection laboratory, Strasbourg, France – name: 1 Department of Anesthesiology, University of Utah, Salt Lake City, UT, USA – name: 3 Department of Medicine, University of Utah, Salt Lake City, UT, USA – name: 2 Geriatric Research, Education, and Clinical Center, Salt Lake City VAMC, UT, USA |
| Author_xml | – sequence: 1 givenname: Thomas J. orcidid: 0000-0002-6993-5723 surname: Hureau fullname: Hureau, Thomas J. email: t.hureau@unistra.fr organization: Oxidative Stress and Muscular Protection Laboratory – sequence: 2 givenname: Ryan M. orcidid: 0000-0002-7388-2214 surname: Broxterman fullname: Broxterman, Ryan M. organization: Geriatric Research, Education, and Clinical Center – sequence: 3 givenname: Joshua C. orcidid: 0000-0002-2032-8498 surname: Weavil fullname: Weavil, Joshua C. organization: Geriatric Research, Education, and Clinical Center – sequence: 4 givenname: Matthew T. orcidid: 0000-0003-0580-6866 surname: Lewis fullname: Lewis, Matthew T. organization: Geriatric Research, Education, and Clinical Center – sequence: 5 givenname: Gwenael orcidid: 0000-0002-5029-2457 surname: Layec fullname: Layec, Gwenael organization: University of Utah – sequence: 6 givenname: Markus surname: Amann fullname: Amann, Markus organization: University of Utah |
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| Copyright | 2022 The Authors. The Journal of Physiology © 2022 The Physiological Society. Journal compilation © 2022 The Physiological Society. |
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| Notes | https://doi.org/10.1113/JP283036#support‐information‐section The peer review history is available in the Supporting information section of this article Linked articles: This article is highlighted in a Perspective article by Forbes. To read this article, visit https://doi.org/10.1113/JP283331 Edited by: Michael Hogan & Bruno Grassi T. J. Hureau and R. M. Broxterman contributed equally to this work. . ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 T.J.H., R.M.B. and M.A. contributed to conception and design of the work; all authors contributed to acquisition, analysis or interpretation of data for the work; all authors contributed to drafting the work or revising it critically for important intellectual content. All authors approved the final version of the manuscript and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All persons designated as authors qualify for authorship, and all those who qualify for authorship are listed. Authors contribution Shared first authorship, TJH and RMB contributed equally to this work |
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| References | 2014; 116 1974; 33 2020; 120 2013; 105 1976; 367 1978; 274 2019; 127 1954; 123 1998; 512 2009; 459 2014; 210 2006; 577 2008; 100 2008; Oct 22 2006; 575 2010; 23 1990; 3 1990; 40 2001; 81 2018; 18 2002; 25 2019a; 20 1997; 129 2014; 307 1993; 16 1987; 60 2021 2019b; 317 1987; 236 1991; 260 2018; 596 1997; 18 2020; 48 2019; 597 2016; 594 2011; 43 2008; 21 2008; 88 1988; 395 1982 1988; 64 2017; 122 2016; 48 1996; 156 1988; 82 2009; 587 2009; 39 |
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| Snippet | Intramuscular hydrogen ion (H+) and inorganic phosphate (Pi) concentrations were dissociated during exercise to challenge their relationships with peripheral... |
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| SubjectTerms | Acidosis exercise Fatigue Femur Hydrogen intramuscular metabolic by‐product Knee Magnetic resonance spectroscopy Muscle contraction neuromuscular fatigue Phosphorus Quadriceps muscle Skeletal muscle Spectrum analysis |
| Title | On the role of skeletal muscle acidosis and inorganic phosphates as determinants of central and peripheral fatigue: A 31P‐MRS study |
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