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Post‐exercise recovery of contractile function and endurance in humans and mice is accelerated by heating and slowed by cooling skeletal muscle

Key points We investigated whether intramuscular temperature affects the acute recovery of exercise performance following fatigue‐induced by endurance exercise. Mean power output was better preserved during an all‐out arm‐cycling exercise following a 2 h recovery period in which the upper arms were...

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Published in:The Journal of physiology 2017-12, Vol.595 (24), p.7413-7426
Main Authors: Cheng, Arthur J., Willis, Sarah J., Zinner, Christoph, Chaillou, Thomas, Ivarsson, Niklas, Ørtenblad, Niels, Lanner, Johanna T., Holmberg, Hans‐Christer, Westerblad, Håkan
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cited_by cdi_FETCH-LOGICAL-c7058-afa84c29b1156b535cfa0305482046e4701d25b83ce3c330af7abbf3397075b43
cites cdi_FETCH-LOGICAL-c7058-afa84c29b1156b535cfa0305482046e4701d25b83ce3c330af7abbf3397075b43
container_end_page 7426
container_issue 24
container_start_page 7413
container_title The Journal of physiology
container_volume 595
creator Cheng, Arthur J.
Willis, Sarah J.
Zinner, Christoph
Chaillou, Thomas
Ivarsson, Niklas
Ørtenblad, Niels
Lanner, Johanna T.
Holmberg, Hans‐Christer
Westerblad, Håkan
description Key points We investigated whether intramuscular temperature affects the acute recovery of exercise performance following fatigue‐induced by endurance exercise. Mean power output was better preserved during an all‐out arm‐cycling exercise following a 2 h recovery period in which the upper arms were warmed to an intramuscular temperature of ̴ 38°C than when they were cooled to as low as 15°C, which suggested that recovery of exercise performance in humans is dependent on muscle temperature. Mechanisms underlying the temperature‐dependent effect on recovery were studied in intact single mouse muscle fibres where we found that recovery of submaximal force and restoration of fatigue resistance was worsened by cooling (16–26°C) and improved by heating (36°C). Isolated whole mouse muscle experiments confirmed that cooling impaired muscle glycogen resynthesis. We conclude that skeletal muscle recovery from fatigue‐induced by endurance exercise is impaired by cooling and improved by heating, due to changes in glycogen resynthesis rate. Manipulation of muscle temperature is believed to improve post‐exercise recovery, with cooling being especially popular among athletes. However, it is unclear whether such temperature manipulations actually have positive effects. Accordingly, we studied the effect of muscle temperature on the acute recovery of force and fatigue resistance after endurance exercise. One hour of moderate‐intensity arm cycling exercise in humans was followed by 2 h recovery in which the upper arms were either heated to 38°C, not treated (33°C), or cooled to ∼15°C. Fatigue resistance after the recovery period was assessed by performing 3 × 5 min sessions of all‐out arm cycling at physiological temperature for all conditions (i.e. not heated or cooled). Power output during the all‐out exercise was better maintained when muscles were heated during recovery, whereas cooling had the opposite effect. Mechanisms underlying the temperature‐dependent effect on recovery were tested in mouse intact single muscle fibres, which were exposed to ∼12 min of glycogen‐depleting fatiguing stimulation (350 ms tetani given at 10 s interval until force decreased to 30% of the starting force). Fibres were subsequently exposed to the same fatiguing stimulation protocol after 1–2 h of recovery at 16–36°C. Recovery of submaximal force (30 Hz), the tetanic myoplasmic free [Ca2+] (measured with the fluorescent indicator indo‐1), and fatigue resistance were all impaired by cooling
doi_str_mv 10.1113/JP274870
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Mean power output was better preserved during an all‐out arm‐cycling exercise following a 2 h recovery period in which the upper arms were warmed to an intramuscular temperature of ̴ 38°C than when they were cooled to as low as 15°C, which suggested that recovery of exercise performance in humans is dependent on muscle temperature. Mechanisms underlying the temperature‐dependent effect on recovery were studied in intact single mouse muscle fibres where we found that recovery of submaximal force and restoration of fatigue resistance was worsened by cooling (16–26°C) and improved by heating (36°C). Isolated whole mouse muscle experiments confirmed that cooling impaired muscle glycogen resynthesis. We conclude that skeletal muscle recovery from fatigue‐induced by endurance exercise is impaired by cooling and improved by heating, due to changes in glycogen resynthesis rate. Manipulation of muscle temperature is believed to improve post‐exercise recovery, with cooling being especially popular among athletes. However, it is unclear whether such temperature manipulations actually have positive effects. Accordingly, we studied the effect of muscle temperature on the acute recovery of force and fatigue resistance after endurance exercise. One hour of moderate‐intensity arm cycling exercise in humans was followed by 2 h recovery in which the upper arms were either heated to 38°C, not treated (33°C), or cooled to ∼15°C. Fatigue resistance after the recovery period was assessed by performing 3 × 5 min sessions of all‐out arm cycling at physiological temperature for all conditions (i.e. not heated or cooled). Power output during the all‐out exercise was better maintained when muscles were heated during recovery, whereas cooling had the opposite effect. Mechanisms underlying the temperature‐dependent effect on recovery were tested in mouse intact single muscle fibres, which were exposed to ∼12 min of glycogen‐depleting fatiguing stimulation (350 ms tetani given at 10 s interval until force decreased to 30% of the starting force). Fibres were subsequently exposed to the same fatiguing stimulation protocol after 1–2 h of recovery at 16–36°C. Recovery of submaximal force (30 Hz), the tetanic myoplasmic free [Ca2+] (measured with the fluorescent indicator indo‐1), and fatigue resistance were all impaired by cooling (16–26°C) and improved by heating (36°C). In addition, glycogen resynthesis was faster at 36°C than 26°C in whole flexor digitorum brevis muscles. We conclude that recovery from exhaustive endurance exercise is accelerated by raising and slowed by lowering muscle temperature. Key points We investigated whether intramuscular temperature affects the acute recovery of exercise performance following fatigue‐induced by endurance exercise. Mean power output was better preserved during an all‐out arm‐cycling exercise following a 2 h recovery period in which the upper arms were warmed to an intramuscular temperature of ̴ 38°C than when they were cooled to as low as 15°C, which suggested that recovery of exercise performance in humans is dependent on muscle temperature. Mechanisms underlying the temperature‐dependent effect on recovery were studied in intact single mouse muscle fibres where we found that recovery of submaximal force and restoration of fatigue resistance was worsened by cooling (16–26°C) and improved by heating (36°C). Isolated whole mouse muscle experiments confirmed that cooling impaired muscle glycogen resynthesis. We conclude that skeletal muscle recovery from fatigue‐induced by endurance exercise is impaired by cooling and improved by heating, due to changes in glycogen resynthesis rate.</description><identifier>ISSN: 0022-3751</identifier><identifier>ISSN: 1469-7793</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/JP274870</identifier><identifier>PMID: 28980321</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Adult ; Animals ; Athletes ; Calcium ; Calcium - metabolism ; Cells, Cultured ; Cold-water immersion ; Contractility ; Cooling ; Cooling effects ; Cooling rate ; Cycles ; Exercise ; Fatigue ; Fatigue strength ; Female ; Fibers ; Glycogen ; Glycogen - metabolism ; Humans ; Hyperthermia, Induced - adverse effects ; Hyperthermia, Induced - methods ; Hypothermia, Induced - adverse effects ; Hypothermia, Induced - methods ; Indo-1 ; Male ; Medicin och hälsovetenskap ; Mice ; Mice, Inbred C57BL ; Muscle ; Muscle Contraction ; Muscle Fatigue ; Muscle recovery ; Muscle, Skeletal - metabolism ; Muscle, Skeletal - physiology ; Muscles ; Musculoskeletal system ; Recovery ; Recovery of Function ; Research Paper ; Skeletal muscle ; Stimulation ; Temperature ; Temperature effects</subject><ispartof>The Journal of physiology, 2017-12, Vol.595 (24), p.7413-7426</ispartof><rights>2017 The Authors. 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Mean power output was better preserved during an all‐out arm‐cycling exercise following a 2 h recovery period in which the upper arms were warmed to an intramuscular temperature of ̴ 38°C than when they were cooled to as low as 15°C, which suggested that recovery of exercise performance in humans is dependent on muscle temperature. Mechanisms underlying the temperature‐dependent effect on recovery were studied in intact single mouse muscle fibres where we found that recovery of submaximal force and restoration of fatigue resistance was worsened by cooling (16–26°C) and improved by heating (36°C). Isolated whole mouse muscle experiments confirmed that cooling impaired muscle glycogen resynthesis. We conclude that skeletal muscle recovery from fatigue‐induced by endurance exercise is impaired by cooling and improved by heating, due to changes in glycogen resynthesis rate. Manipulation of muscle temperature is believed to improve post‐exercise recovery, with cooling being especially popular among athletes. However, it is unclear whether such temperature manipulations actually have positive effects. Accordingly, we studied the effect of muscle temperature on the acute recovery of force and fatigue resistance after endurance exercise. One hour of moderate‐intensity arm cycling exercise in humans was followed by 2 h recovery in which the upper arms were either heated to 38°C, not treated (33°C), or cooled to ∼15°C. Fatigue resistance after the recovery period was assessed by performing 3 × 5 min sessions of all‐out arm cycling at physiological temperature for all conditions (i.e. not heated or cooled). Power output during the all‐out exercise was better maintained when muscles were heated during recovery, whereas cooling had the opposite effect. Mechanisms underlying the temperature‐dependent effect on recovery were tested in mouse intact single muscle fibres, which were exposed to ∼12 min of glycogen‐depleting fatiguing stimulation (350 ms tetani given at 10 s interval until force decreased to 30% of the starting force). Fibres were subsequently exposed to the same fatiguing stimulation protocol after 1–2 h of recovery at 16–36°C. Recovery of submaximal force (30 Hz), the tetanic myoplasmic free [Ca2+] (measured with the fluorescent indicator indo‐1), and fatigue resistance were all impaired by cooling (16–26°C) and improved by heating (36°C). In addition, glycogen resynthesis was faster at 36°C than 26°C in whole flexor digitorum brevis muscles. We conclude that recovery from exhaustive endurance exercise is accelerated by raising and slowed by lowering muscle temperature. Key points We investigated whether intramuscular temperature affects the acute recovery of exercise performance following fatigue‐induced by endurance exercise. Mean power output was better preserved during an all‐out arm‐cycling exercise following a 2 h recovery period in which the upper arms were warmed to an intramuscular temperature of ̴ 38°C than when they were cooled to as low as 15°C, which suggested that recovery of exercise performance in humans is dependent on muscle temperature. Mechanisms underlying the temperature‐dependent effect on recovery were studied in intact single mouse muscle fibres where we found that recovery of submaximal force and restoration of fatigue resistance was worsened by cooling (16–26°C) and improved by heating (36°C). Isolated whole mouse muscle experiments confirmed that cooling impaired muscle glycogen resynthesis. 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Mean power output was better preserved during an all‐out arm‐cycling exercise following a 2 h recovery period in which the upper arms were warmed to an intramuscular temperature of ̴ 38°C than when they were cooled to as low as 15°C, which suggested that recovery of exercise performance in humans is dependent on muscle temperature. Mechanisms underlying the temperature‐dependent effect on recovery were studied in intact single mouse muscle fibres where we found that recovery of submaximal force and restoration of fatigue resistance was worsened by cooling (16–26°C) and improved by heating (36°C). Isolated whole mouse muscle experiments confirmed that cooling impaired muscle glycogen resynthesis. We conclude that skeletal muscle recovery from fatigue‐induced by endurance exercise is impaired by cooling and improved by heating, due to changes in glycogen resynthesis rate. Manipulation of muscle temperature is believed to improve post‐exercise recovery, with cooling being especially popular among athletes. However, it is unclear whether such temperature manipulations actually have positive effects. Accordingly, we studied the effect of muscle temperature on the acute recovery of force and fatigue resistance after endurance exercise. One hour of moderate‐intensity arm cycling exercise in humans was followed by 2 h recovery in which the upper arms were either heated to 38°C, not treated (33°C), or cooled to ∼15°C. Fatigue resistance after the recovery period was assessed by performing 3 × 5 min sessions of all‐out arm cycling at physiological temperature for all conditions (i.e. not heated or cooled). Power output during the all‐out exercise was better maintained when muscles were heated during recovery, whereas cooling had the opposite effect. Mechanisms underlying the temperature‐dependent effect on recovery were tested in mouse intact single muscle fibres, which were exposed to ∼12 min of glycogen‐depleting fatiguing stimulation (350 ms tetani given at 10 s interval until force decreased to 30% of the starting force). Fibres were subsequently exposed to the same fatiguing stimulation protocol after 1–2 h of recovery at 16–36°C. Recovery of submaximal force (30 Hz), the tetanic myoplasmic free [Ca2+] (measured with the fluorescent indicator indo‐1), and fatigue resistance were all impaired by cooling (16–26°C) and improved by heating (36°C). In addition, glycogen resynthesis was faster at 36°C than 26°C in whole flexor digitorum brevis muscles. We conclude that recovery from exhaustive endurance exercise is accelerated by raising and slowed by lowering muscle temperature. Key points We investigated whether intramuscular temperature affects the acute recovery of exercise performance following fatigue‐induced by endurance exercise. Mean power output was better preserved during an all‐out arm‐cycling exercise following a 2 h recovery period in which the upper arms were warmed to an intramuscular temperature of ̴ 38°C than when they were cooled to as low as 15°C, which suggested that recovery of exercise performance in humans is dependent on muscle temperature. Mechanisms underlying the temperature‐dependent effect on recovery were studied in intact single mouse muscle fibres where we found that recovery of submaximal force and restoration of fatigue resistance was worsened by cooling (16–26°C) and improved by heating (36°C). Isolated whole mouse muscle experiments confirmed that cooling impaired muscle glycogen resynthesis. We conclude that skeletal muscle recovery from fatigue‐induced by endurance exercise is impaired by cooling and improved by heating, due to changes in glycogen resynthesis rate.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>28980321</pmid><doi>10.1113/JP274870</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-8180-3029</orcidid><orcidid>https://orcid.org/0000-0003-3862-2967</orcidid><orcidid>https://orcid.org/0000-0002-5322-4150</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 0022-3751
ispartof The Journal of physiology, 2017-12, Vol.595 (24), p.7413-7426
issn 0022-3751
1469-7793
1469-7793
language eng
recordid cdi_swepub_primary_oai_swepub_ki_se_493584
source Wiley-Blackwell Read & Publish Collection; PubMed Central
subjects Adult
Animals
Athletes
Calcium
Calcium - metabolism
Cells, Cultured
Cold-water immersion
Contractility
Cooling
Cooling effects
Cooling rate
Cycles
Exercise
Fatigue
Fatigue strength
Female
Fibers
Glycogen
Glycogen - metabolism
Humans
Hyperthermia, Induced - adverse effects
Hyperthermia, Induced - methods
Hypothermia, Induced - adverse effects
Hypothermia, Induced - methods
Indo-1
Male
Medicin och hälsovetenskap
Mice
Mice, Inbred C57BL
Muscle
Muscle Contraction
Muscle Fatigue
Muscle recovery
Muscle, Skeletal - metabolism
Muscle, Skeletal - physiology
Muscles
Musculoskeletal system
Recovery
Recovery of Function
Research Paper
Skeletal muscle
Stimulation
Temperature
Temperature effects
title Post‐exercise recovery of contractile function and endurance in humans and mice is accelerated by heating and slowed by cooling skeletal muscle
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