Fatigue-sensitive afferents inhibit extensor but not flexor motoneurons in humans

Journal of Neuroscience

Volumn 26, Issue 18, 2006, Pages 4796-4802

  Martin, Peter G ^a   Smith, Janette L ^a   Butler, Jane E ^a   Gandevia, Simon C ^a   Taylor, Janet L ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Corticospinal; Fatigue; Group III and IV muscle afferents; Human; Ischemia; Motoneuron

Indexed keywords

ARTICLE; CONTROLLED STUDY; ELBOW FLEXION; ELECTROMYOGRAPHY; EXTENSOR MUSCLE; FEMALE; FLEXOR MUSCLE; HUMAN; HUMAN TISSUE; MALE; MOTONEURON; MUSCLE CONTRACTION; MUSCLE EXCITATION; MUSCLE FATIGUE; MUSCLE ISCHEMIA; MUSCLE SPINDLE AFFERENT NERVE; PRIORITY JOURNAL; PYRAMIDAL TRACT; REFLEX; TRICEPS BRACHII MUSCLE; ADULT; ANALYSIS OF VARIANCE; BRACHIAL PLEXUS; COMPARATIVE STUDY; CYTOLOGY; ELBOW; ELECTROSTIMULATION; EVOKED MUSCLE RESPONSE; INNERVATION; ISCHEMIA; METHODOLOGY; NERVE CELL INHIBITION; PATHOPHYSIOLOGY; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION RESPONSE; SKELETAL MUSCLE; TIME;

ADULT; ANALYSIS OF VARIANCE; BRACHIAL PLEXUS; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELBOW; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; ISCHEMIA; MALE; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL; NEURAL INHIBITION; PYRAMIDAL TRACTS; TIME FACTORS;

EID: 33646913261     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5487-05.2006     Document Type: Article

References (52)

1. Andersen OK, Sonnenborg FA, Arendt-Nielsen L (1999) Modular organization of human leg withdrawal reflexes elicited by electrical stimulation of the foot sole. Muscle Nerve 22:1520-1530.
2. Bigland-Ritchie B, Johansson R, Lippold OC, Smith S, Woods JJ (1983) Changes in motoneurone firing rates during sustained maximal voluntary contractions. J Physiol (Lond) 340:335-346.
3. 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 (Lond) 379:451-459.
4. Bongiovanni LG, Hagbarth KE (1990) Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man. J Physiol (Lond) 423:1-14.
5. 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.
6. de Noordhout AM, Rapisarda G, Bogacz D, Gerard P, De Pasqua V, Pennisi G, Delwaide PJ (1999) Corticomotoneuronal synaptic connections in normal man: an electrophysiological study. Brain 122:1327-1340.
7. Duchateau J, Hainaut K (1993) Behaviour of short and long latency reflexes in fatigued human muscles. J Physiol (Lond) 471:787-799.
8. Eccles JC, Lundberg A (1959) Synaptic actions in motoneurones by afferents which may evoke the flexion reflex. Arch Ital Biol 97:199-221.
9. Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725-1789.
10. Gandevia SC, Macefield G, Burke D, McKenzie DK (1990) Voluntary activation of human motor axons in the absence of muscle afferent feedback. The control of the deafferented hand. Brain 113:1563-1581.
11. Gandevia SC, Petersen N, Butler JE, Taylor JL (1999) Impaired response of human motoneurones to corticospinal stimulation after voluntary exercise. J Physiol (Lond) 521:749-759.
12. Garland SJ (1991) Role of small diameter afferents in reflex inhibition during human muscle fatigue. J Physiol (Lond) 435:547-558.
13. Garland SJ, Kaufman MP (1995) Role of muscle afferents in the inhibition of motoneurons during fatigue. Adv Exp Med Biol 384:271-278.
14. Garland SJ, McComas AJ (1990) Reflex inhibition of human soleus muscle during fatigue. J Physiol (Lond) 429:17-27.
15. Grimby L, Hannerz J, Hedman B (1981) The fatigue and voluntary discharge properties of single motor units in man. J Physiol (Lond) 316:545-554.
16. Hagbarth KE (1960) Spinal withdrawal reflexes in the human lower limbs. J Neurol Neurosurg Psychiatry 23:222-227.
17. Hayes SG, Kindig AE, Kaufman MP (2006) Cyclooxygenase blockade attenuates the responses of group III and IV muscle afferents to dynamic exercise in cats. Am J Physiol Heart Circ Physiol, in press.
18. Holmqvist B, Lundberg A (1961) Differential supraspinal control of synaptic actions evoked by volleys in the flexion reflex afferents in alpha motoneurones. Acta Physiol Scand:1-15.
19. Johnson KV, Edwards SC, Van Tongeren C, Bawa P (2004) Properties of human motor units after prolonged activity at a constant firing rate. Exp Brain Res 154:479-487.
20. Jovanovic K, Anastasijevic R, Vuco J (1990) Reflex effects on gamma fusimotor neurones of chemically induced discharges in small-diameter muscle afferents in decerebrate cats. Brain Res 521:89-94.
21. Kalezic I, Bugaychenko LA, Kostyukov AI, Pilyavskii AI, Ljubisavljevic M, Windhorst U, Johansson H (2004) Fatigue-related depression of the feline monosynaptic gastrocnemius-soleus reflex. J Physiol (Lond) 556:283-296.
22. Kaufman MP, Forster HV (1996) Reflexes controlling circulatory, ventilatory and airway responses to exercise. In: Handbook of physiology. Exercise: regulation and integration of multiple systems, pp 381-447. Bethesda, MD: American Physiology Society.
23. Kernell D, Monster AW (1982a) Motoneurone properties and motor fatigue. An intracellular study of gastrocnemius motoneurones of the cat. Exp Brain Res 46:197-204.
24. Kernell D, Monster AW (1982b) Time course and properties of late adaptation in spinal motoneurones of the cat. Exp Brain Res 46:191-196.
25. Kniffki KD, Schomburg ED, Steffens H (1979) Synaptic responses of lumbar alpha-motoneurones to chemical algesic stimulation of skeletal muscle in spinal cats. Brain Res 160:549-552.
26. Kniffki KD, Schomburg ED, Steffens H (1980) Action of muscular group III and IV afferents on spinal locomotor activity in cat. Brain Res 186:445-447.
27. Kniffki KD, Schomburg ED, Steffens H (1981a) Synaptic effects from chemically activated fine muscle afferents upon alpha-motoneurones in decerebrate and spinal cats. Brain Res 206:361-370.
28. Kniffki KD, Schomburg ED, Steffens H (1981b) Convergence in segmental reflex pathways from fine muscle afferents and cutaneous or group II muscle afferents to alpha-motoneurones. Brain Res 218:342-346.
29. Kuchinad RA, Ivanova TD, Garland SJ (2004) Modulation of motor unit discharge rate and H-reflex amplitude during submaximal fatigue of the human soleus muscle. Exp Brain Res 158:345-355.
30. Kukulka CG, Moore MA, Russell AG (1986) Changes in human alpha-motoneuron excitability during sustained maximum isometric contractions. Neurosci Lett 68:327-333.
31. Levinsson A, Garwicz M, Schouenborg J (1999) Sensorimotor transformation in cat nociceptive withdrawal reflex system. Eur J Neurosci 11:4327-4332.
32. Ljubisavljevic M, Jovanovic K, Anastasijevic R (1992) Changes in discharge rate of fusimotor neurones provoked by fatiguing contractions of cat triceps surae muscles. J Physiol (Lond) 445:499-513.
33. Loscher WN, Cresswell AG, Thorstensson A (1996) Excitatory drive to the alpha-motoneuron pool during a fatiguing submaximal contraction in man. J Physiol (Lond) 491:271-280.
34. Macefield G, Hagbarth KE, Gorman R, Gandevia SC, Burke D (1991) Decline in spindle support to alpha-motoneurones during sustained voluntary contractions. J Physiol (Lond) 440:497-512.
35. Nielsen J, Petersen N (1994) Is presynaptic inhibition distributed to corticospinal fibres in man? J Physiol (Lond) 477:47-58.
36. Palmer E, Ashby P (1992) Corticospinal projections to upper limb motoneurones in humans. J Physiol (Lond) 448:397-412.
37. Petersen NT, Taylor JL, Gandevia SC (2002) The effect of electrical stimulation of the corticospinal tract on motor units of the human biceps brachii. J Physiol (Lond) 544:277-284.
38. Pettorossi VE, Della Torre G, Bortolami R, Brunetti O (1999) The role of capsaicin-sensitive muscle afferents in fatigue-induced modulation of the monosynaptic reflex in the rat. J Physiol (Lond) 515:599-607.
39. Rossi A, Dechii B, Ginanneschi F (1999) Presynaptic excitability changes of group Ia fibres to muscle nociceptive stimulation in humans. Brain Res 818:12-22.
40. Rossi A, Mazzocchio R, Decchi B (2003) Effect of chemically activated fine muscle afferents on spinal recurrent inhibition in humans. Clin Neurophysiol 114:279-287.
41. Rudomin P, Schmidt RF (1999) Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129:1-37.
42. Sacco P, Newberry R, McFadden L, Brown T, McComas AJ (1997) Depression of human electromyographic activity by fatigue of a synergistic muscle. Muscle Nerve 20:710-717.
43. Sawczuk A, Powers RK, Binder MD (1997) Contribution of outward currents to spike-frequency adaptation in hypoglossal motoneurons of the rat. J Neurophysiol 78:2246-2253.
44. 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.
45. Spielmann JM, Laouris Y, Nordstrom MA, Robinson GA, Reinking RM, Stuart DG (1993) Adaptation of cat motoneurons to sustained and intermittent extracellular activation. J Physiol (Lond) 464:75-120.
46. Taylor JL, Gandevia SC (2004) Noninvasive stimulation of the human corticospinal tract. J Appl Physiol 96:1496-1503.
47. Taylor JL, Butler JE, Gandevia SC (1999) Altered responses of human elbow flexors to peripheral-nerve and cortical stimulation during a sustained maximal voluntary contraction. Exp Brain Res 127:108-115.
48. Taylor JL, Petersen N, Butler JE, Gandevia SC (2000) Ischaemia after exercise does not reduce responses of human motoneurones to cortical or corticospinal tract stimulation. J Physiol (Lond) 525:793-801.
49. Ugawa Y, Rothwell JC, Day BL, Thompson PD, Marsden CD (1991) Percutaneous electrical stimulation of corticospinal pathways at the level of the pyramidal decussation in humans. Ann Neurol 29:418-427.
50. Walton DM, Kuchinad RA, Ivanova TD, Garland SJ (2002) Reflex inhibition during muscle fatigue in endurance-trained and sedentary individuals. Eur J Appl Physiol 87:462-468.
51. Windhorst U, Kirmayer D, Soibelman F, Misri A, Rose R (1997) Effects of neurochemically excited group III-IV muscle afferents on motoneuron afterhyperpolarization. Neuroscience 76:915-929.
52. Woods JJ, Furbush F, Bigland-Ritchie B (1987) Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. J Neurophysiol 58:125-137.