Spinal μ-opioid receptor-sensitive lower limb muscle afferents determine corticospinal responsiveness and promote central fatigue in upper limb muscle

Journal of Physiology

Volumn 592, Issue 22, 2014, Pages 5011-5024

  Sidhu, Simranjit K ^a   Weavil, Joshua ^b   Venturelli, Massimo ^a   Garten, Ryan ^c   Rossman, Matthew ^b   Richardson, Russell ^a,b,c   Gmelch, Benjamin ^a   Morgan, David ^a   Amann, Markus ^a,b,c  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FENTANYL; MU OPIATE RECEPTOR;

ADULT; ARM WEAKNESS; ARTICLE; CONTROLLED STUDY; CORTICOSPINAL RESPONSIVENESS; CYCLING; ELBOW; EVOKED RESPONSE; EXHAUSTION; FEEDBACK SYSTEM; FLEXOR MUSCLE; HUMAN; HUMAN EXPERIMENT; LEG MUSCLE; MALE; MAXIMUM VOLUNTARY CONTRACTION; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCULOSKELETAL SYSTEM PARAMETERS; NERVOUS SYSTEM PARAMETERS; NORMAL HUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; SENSORY NERVE; TRANSCRANIAL MAGNETIC STIMULATION; AGONISTS; DRUG EFFECTS; EVOKED MUSCLE RESPONSE; INNERVATION; LIMB; PHYSIOLOGY; SKELETAL MUSCLE;

ADULT; AFFERENT PATHWAYS; EVOKED POTENTIALS, MOTOR; EXTREMITIES; FEEDBACK, PHYSIOLOGICAL; FENTANYL; HUMANS; MALE; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL; PYRAMIDAL TRACTS; RECEPTORS, OPIOID, MU;

EID: 84922910226     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.275438     Document Type: Article

References (31)

1. 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.
2. 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.
3. AmannM, VenturelliM, Ives SJ,McDaniel J, Layec G, Rossman MJ., Richardson RS (2013). Peripheral fatigue limits endurance exercise via a sensory feedback-mediated reduction in spinal motoneuronal output. J Appl Physiol (1985) 115, 355-364.
4. Amann M, Venturelli M, Ives SJ, Morgan DE, Gmelch B, Witman MA, Jonathan Groot H,WalterWray D, Stehlik J., Richardson RS (2014). Group III/IV muscle afferents impair limb blood in patients with chronic heart failure. Int J Cardiol 174, 368-375.
5. Balter JE., Zehr EP (2007). Neural coupling between the arms and legs during rhythmic locomotor-like cycling movement. J Neurophysiol 97, 1809-1818.
6. Bigland-Ritchie BR, Dawson NJ, Johansson RS., Lippold OC (1986). Reflex origin for the slowing of motoneurone firing rates in fatigue of human voluntary contractions. J Physiol 379, 451-459.
7. BirdsongWT, Fierro L, Williams FG, Spelta V, Naves LA, Knowles M, Marsh-Haffner J, Adelman JP, AlmersW, Elde RP., McCleskey EW(2010). Sensing muscle ischemia: coincident detection of acid and ATP via interplay of two ion channels. Neuron 68, 739-749.
8. Bruijnzeel AW(2009). ?-Opioid receptor signalling and brain reward function. Brain Res Rev 62, 127-146.
9. Fuglevand AJ,Winter DA., Patla AE (1993). Models of recruitment and rate coding organization in motor-unit pools. J Neurophysiol 70, 2470-2488.
10. Gandevia SC, Allen GM, Butler JE., Taylor JM (1996). Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol 490, 529-536.
11. 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.
12. Hilty L, Lutz K, Maurer K, Rodenkirch T, Spengler CM, Boutellier U, Jancke L., Amann M (2011). Spinal opioid receptor-sensitive muscle afferents contribute to the fatigue-induced increase in intracortical inhibition in healthy humans. Exp Physiol 96, 505-517.
13. Jankowski MP, Rau KK, Ekmann KM, Anderson CE., Koerber HR (2013). Comprehensive phenotyping of group III and IV muscle afferents in mouse. J Neurophysiol 109, 2374-2381.
14. Kennedy DS, McNeil CJ, Gandevia SC., Taylor JL (2013). Firing of antagonist small-diameter muscle afferents reduces voluntary activation and torque of elbow flexors. J Physiol 591, 3591-3604.
15. Kennedy DS, McNeil CJ, Gandevia SC., Taylor JL (2014). Fatigue-related firing of distal muscle nociceptors reduces voluntary activation of proximal muscles of the same limb. J Appl Physiol (1985) 116, 385-394.
16. Lalley PM (2008). Opioidergic and dopaminergic modulation of respiration. Respir Physiol Neurobiol 164, 160-167.
17. 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.
18. 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.
19. McNeil CJ, Giesebrecht S, Gandevia SC., Taylor JL (2011). Behaviour of the motoneurone pool in a fatiguing submaximal contraction. J Physiol 589, 3533-3544.
20. Millet GY, Martin V, Lattier G., Ballay Y (2003). Mechanisms contributing to knee extensor strength loss after prolonged running exercise. J Appl Physiol (1985) 94, 193-198.
21. Racinais S, Bishop D, Denis R., Lattier G (2007). Muscle deoxygenation and neural drive to the muscle during repeated sprint cycling. Med Sci Sports Exerc 39, 268-274.
22. Rasmussen P, Nielsen J, Overgaard M, Krogh-Madsen R, Gjedde A, Secher NH., Petersen NC (2010). Reducedmuscle activation during exercise related to brain oxygenation and metabolism in humans. J Physiol 588, 1985-1995.
23. Schabrun SM., Hodges PW (2012). Muscle pain differentially modulates short interval intracortical inhibition and intracortical facilitation in primary motor cortex. J Pain 13, 187-194.
24. Sidhu SK, Bentley DJ., Carroll TJ (2009). Locomotor exercise induces long-lasting impairments in the capacity of the human motor cortex to voluntarily activate knee extensor muscles. J Appl Physiol 106, 556-565.
25. Sidhu SK, Lauber B, Cresswell AG., Carroll TJ (2013). Sustained cycling exercise increases intracortical inhibition. Med Sci Sports Exerc 45, 654-662.
26. Todd G, Gorman RB., Gandevia SC (2004). Measurement and reproducibility of strength and voluntary activation of lower-limb muscles. Muscle Nerve 29, 834-842.
27. 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.
28. Yoon T, Schlinder-Delap B, Keller ML., Hunter SK (2012). Supraspinal fatigue impedes recovery from a low-intensity sustained contraction in old adults. J Appl Physiol (1985) 112, 849-858.
29. Zehr EP, Balter JE, Ferris DP, Hundza SR, Loadman PM., Stoloff RH (2007a). Neural regulation of rhythmic arm and leg movement is conserved across human locomotor tasks. J Physiol 582, 209-227.
30. Zehr EP., Duysens J (2004). Regulation of arm and leg movement during human locomotion. Neuroscientist 10, 347-361.
31. Zehr EP, Klimstra M, Johnson EA., Carroll TJ (2007b). Rhythmic leg cycling modulates forearm muscle H-reflex amplitude and corticospinal tract excitability. Neurosci Lett 419, 10-14.