Firing of antagonist small-diameter muscle afferents reduces voluntary activation and torque of elbow flexors

Journal of Physiology

Volumn 591, Issue 14, 2013, Pages 3591-3604

  Kennedy, David S ^a,b   Mcneil, Chris J ^a,c   Gandevia, Simon C ^a,b   Taylor, Janet L ^a,b  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARM MOVEMENT; ARTICLE; BIOMECHANICS; BLOOD PRESSURE; CELL SIZE; CONTROLLED STUDY; FEMALE; FLEXOR MUSCLE; HUMAN; HUMAN EXPERIMENT; MALE; MAXIMAL VOLUNTARY CONTRACTION; MUSCLE ACTION POTENTIAL; MUSCLE BLOOD FLOW; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE ISCHEMIA; MUSCLE SPINDLE AFFERENT NERVE; MUSCLE TWITCH; MUSCULOSKELETAL SYSTEM PARAMETERS; NORMAL HUMAN; PRIORITY JOURNAL; TORQUE; TRANSCRANIAL MAGNETIC STIMULATION; VOLUNTARY MOVEMENT;

ADULT; ELBOW; ELECTRIC STIMULATION; FEMALE; HUMANS; ISCHEMIA; MALE; MIDDLE AGED; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL; TORQUE; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84880720031     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.248559     Document Type: Article

References (53)

1. Adreani CM, Hill JM & Kaufman MP (1997). Responses of group III and IV muscle afferents to dynamic exercise. J Appl Physiol 82, 1811-1817.
2. Alam M & Smirk FH (1937). Observations in man upon a blood pressure raising reflex arising from the voluntary muscles. J Physiol 89, 372-383.
3. Allen DG, Lamb GD & Westerblad H (2008). Skeletal muscle fatigue: Cellular mechanisms. Physiol Rev 88, 287-332.
4. Amann M, Proctor LT, Sebranek JJ, Pegelow DF & Dempsey JA (2009). Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 587, 271-283.
5. Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF & Dempsey JA (2011). Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. J Physiol 589, 5299-5309.
6. Beltman JGM, Sargeant AJ, Van Mechelen W & De Haan A (2004). Voluntary activation level and muscle fibre recruitment of human quadriceps during lengthening contractions. J Appl Physiol 97, 619-626.
7. Bigland-Ritchie BR, Dawson NJ, Johansson RS & Lippold OCJ (1986). Reflex origin for the slowing of motoneurone firing rates in fatigue of human voluntary contractions. J Physiol 379, 451-459.
8. Butler JE, Taylor JL & Gandevia SC (2003). Responses of human motoneurons to corticospinal stimulation during maximal voluntary contractions and ischemia. J Neurosci 23, 10224-10230.
9. Coote JH, Hilton SM & Perez-Gonzalez JF (1971). The reflex nature of the pressor response to muscular exercise. J Physiol 215, 789-804.
10. Creed RS, Denny-Brown D, Eccles JC, Liddell EGT & Sherrinton CS (1932). The flexor reflex. In Reflex Activity of the Spinal Cord, 1st edn, pp. 17-46. Oxford University Press, London.
11. 3-induced alkalosis reduces the phosphocreatine slow component during heavy-intensity forearm exercise. J Appl Physiol 99, 1668-1675.
12. Gandevia SC (2001). Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81, 1725-1789.
13. Gandevia SC, Allen GM, Butler JE & Taylor JL (1996). Supraspinal factors in human muscle fatigue: Evidence for suboptimal output from the motor cortex. J Physiol 490, 529-536.
14. Garland SJ & Kaufman MP (1995). Role of muscle afferents in the inhibition of motoneurons during fatigue. Adv Exp Med Biol 384, 271-278.
15. Graven-Nielsen T, Jansson Y, Segerdahl M, Kristensen JD, Mense S, Arendt-Nielsen L & Sollevi A (2003). Experimental pain by ischaemic contractions compared with pain by intramuscular infusions of adenosine and hypertonic saline. Eur J Pain 7, 93-102.
16. Graven-Nielsen T, Lund H, Arendt-Nielsen L, Danneskiold-Samsøe B & Bliddal H (2002). Inhibition of maximal voluntary contraction force by experimental muscle pain: A centrally mediated mechanism. Muscle Nerve 26, 708-712.
17. Hayward L, Wesselmann U & Rymer WZ (1991). Effects of muscle fatigue on mechanically sensitive afferents of slow conduction velocity in the cat triceps surae. J Neurophysiol 65, 360-370.
18. Henderson LA, Bandler R, Gandevia SC & Macefield VG (2006). Distinct forebrain activity patterns during deep versus superficial pain. Pain 120, 286-296.
19. Hug F, Grélot L, Le Fur Y, Cozzone PJ & Bendahan D (2006). Recovery kinetics throughout successive bouts of various exercises in elite cyclists. Med Sci Sports Exerc 38, 2151-2158.
20. Ichinose M, Delliaux S, Watanabe K, Fujii N & Nishiyasu T (2011). Evaluation of muscle metaboreflex function through graded reduction in forearm blood flow during rhythmic handgrip exercise in humans. Am J Physiol Heart Circ Physiol 301, H609-H616.
21. Kaufman MP, Longhurst JC, Rybicki KJ, Wallach JH & Mitchell JH (1983). Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. J Appl Physiol 55, 105-112.
22. Kaufman MP, Rybicki KJ, Waldrop TG & Ordway GA (1984). Effect of ischemia on responses of group III and IV afferents to contraction. J Appl Physiol 57, 644-650.
23. Kellgren JH (1938). Observation on referred pain arising from muscle. Clin Sci 3, 175-190.
24. Khan SI, McNeil CJ, Gandevia SC & Taylor JL (2011). Effect of experimental muscle pain on maximal voluntary activation of human biceps brachii muscle. J Appl Physiol 111, 743-750.
25. Kniffki KD, Mense S & Schmidt RF (1978). Responses of group IV afferent units from skeletal muscle to stretch, contraction and chemical stimulation. Exp Brain Res 31, 511-522.
26. Kniffki KD, Schomburg ED & Steffens H (1981). Synaptic effects from chemically activated fine muscle afferents upon alpha-motoneurones in decerebrate and spinal cats. Brain Res 206, 361-370.
27. Lanza IR, Wigmore DM, Befroy DE & Kent-Braun JA (2006). In vivo ATP production during free-flow and ischaemic muscle contractions in humans. J Physiol 577, 353-367.
28. Laursen RJ, Graven-Nielsen T, Jensen TS & Arendt-Nielsen L (1999). The effect of differential and complete nerve block on experimental muscle pain in humans. Muscle Nerve 22, 1564-1570.
29. Lewis T, Pickering GW & Rothschild P (1931). Observations on muscular pain in intermittent claudication. Heart 15, 359-383.
30. Light AR, Hughen RW, Zhang J, Rainier J, Liu Z & Lee J (2008). Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TRPV1. J Neurophysiol 100, 1184-1201.
31. Marsh GD, Paterson DH, Potwarka JJ & Thompson RT (1993). Transient changes in muscle high-energy phosphates during moderate exercise. J Appl Physiol 75, 648-656.
32. Martin PG, Marino FE, Rattey J, Kay D & Cannon J (2005). Reduced voluntary activation of human skeletal muscle during shortening and lengthening contractions in whole body hyperthermia. Exp Physiol 90, 225-236.
33. Martin PG, Smith JL, Butler JE, Gandevia SC & Taylor JL (2006). Fatigue-sensitive afferents inhibit extensor but not flexor motoneurons in humans. J Neurosci 26, 4796-4802.
34. Martin PG, Weerakkody N, Gandevia SC & Taylor JL (2008). Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans. J Physiol 586, 1277-1289.
35. McNeil CJ, Martin PG, Gandevia SC & Taylor JL (2009). The response to paired motor cortical stimuli is abolished at a spinal level during human muscle fatigue. J Physiol 587, 5601-5612.
36. McNeil CJ, Giesebrecht S, Gandevia SC & Taylor JL (2011a). Behaviour of the motoneurone pool in a fatiguing submaximal contraction. J Physiol 589, 3533-3544.
37. McNeil CJ, Giesebrecht S, Khan SI, Gandevia SC & Taylor JL (2011b). The reduction in human motoneurone responsiveness during muscle fatigue is not prevented by increased muscle spindle discharge. J Physiol 589, 3731-3738.
38. Mense S (2009). Algesic agents exciting muscle nociceptors. Exp Brain Res 196, 89-100.
39. Mills KR, Newham DJ & Edwards RHT (1982). Force, contraction frequency and energy metabolism as determinants of ischaemic muscle pain. Pain 14, 149-154.
40. Paintal AS (1960). Functional analysis of Group III afferent fibres of mammalian muscles. J Physiol 152, 250-270.
41. Rotto DM & Kaufman MP (1988). Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J Appl Physiol 64, 2306-2313.
42. Schomburg ED & Steffens H (2002). Only minor spinal motor reflex effects from feline group IV muscle nociceptors. Neurosci Res 44, 213-223.
43. Schomburg ED, Steffens H & Kniffki KD (1999). Contribution of group III and IV muscle afferents to multisensorial spinal motor control in cats. Neurosci Res 33, 195-206.
44. Schomburg ED, Steffens H, Dibaj P & Sears TA (2012). Major contribution of Aδ and C fibres to increased reflex transmission in the feline spinal cord during acute muscle inflammation. Neurosci Res 72, 155-162.
45. Stephens TJ, McKenna MJ, Canny BJ, Snow RJ & McConell GK (2002). Effect of sodium bicarbonate on muscle metabolism during intense endurance cycling. Med Sci Sports Exerc 34, 614-621.
46. Taylor JL & Gandevia SC (2008). A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104, 542-550.
47. Taylor JL, Butler JE, Allen GM & Gandevia SC (1996). Changes in motor cortical excitability during human muscle fatigue. J Physiol 490, 519-528.
48. Taylor JL, Butler JE & Gandevia SC (2000). Changes in muscle afferents, motoneurons and motor drive during muscle fatigue. Eur J Appl Physiol 83, 106-115.
49. Todd G, Taylor JL & Gandevia SC (2003). Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J Physiol 551, 661-671.
50. Todd G, Taylor JL & Gandevia SC (2004). Reproducible measurement of voluntary activation of human elbow flexors with motor cortical stimulation. J Appl Physiol 97, 236-242.
51. Todd G, Butler JE, Taylor JL & Gandevia SC (2005). Hyperthermia: A failure of the motor cortex and the muscle. J Physiol 563, 621-631.
52. Wiles CM & Edwards RHT (1982). The effect of temperature, ischaemia and contractile activity on the relaxation rate of human muscle. Clin Physiol 2, 485-497.
53. Woods JJ, Furbush F & Bigland-Ritchie B (1987). Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. J Neurophysiol 58, 125-137.