Adaptations of motoneuron properties to chronic compensatory muscle overload

Journal of Neurophysiology

Volumn 113, Issue 7, 2015, Pages 2769-2777

  Krutki, P ^a   Haluszka A ^a   Mrowczynski W ^a   Gardiner, P F ^b   Celichowski, J ^a  

^a POZNAN UNIVERSITY OF PHYSICAL EDUCATION   (Poland)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Membrane properties; Rat

Indexed keywords

ACTION POTENTIAL; ADAPTATION; ADULT; AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDROMIC STIMULATION; ARTICLE; BODY MASS; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; INTRACELLULAR RECORDING; MALE; MOTONEURON; MUSCLE FUNCTION; MUSCLE HYPERTROPHY; MUSCLE MASS; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PLANTARIS MUSCLE; PRIORITY JOURNAL; RAT; SOLEUS MUSCLE; STEADY STATE; TENOTOMY; ANIMAL; HYPERTROPHY; INNERVATION; MUSCLE CONTRACTION; NERVE CELL PLASTICITY; NEUROMUSCULAR JUNCTION; PATHOLOGY; PATHOPHYSIOLOGY; SKELETAL MUSCLE; SYNAPTIC TRANSMISSION; WISTAR RAT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; HYPERTROPHY; MALE; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; NEURONAL PLASTICITY; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 84982061153     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00968.2014     Document Type: Article

References (51)

1. Allbrook D. Skeletal muscle regeneration. Muscle Nerve 4: 234-245, 1981.
2. Antonio J, Gonyea WJ. Skeletal muscle fiber hyperplasia. Med Sci Sports Exerc 25: 1333-1345, 1993.
3. Baçzyk M, Hałuszka A, Mrówczynski W, Celichowski J, Krutki P. The influence of a 5-wk whole body vibration on electrophysiological properties of rat hindlimb spinal motoneurons. J Neurophysiol 109: 2705-2711, 2013.
4. Bakels R, Kernell D. Matching between motoneurone and muscle unit properties in rat medial gastrocnemius. J Physiol 463: 307-324, 1993.
5. Baldwin KM, Valdez V, Herrick RE, Maclntosh AM, Roy RR. Biochemical properties of overload fast-twitch skeletal muscle. J Appl Physiol 52: 467-472, 1982.
6. Barrett EF, Barret JN. Separation of two voltage-sensitive potassium currents, and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurones. J Physiol 255: 737-774, 1976.
7. Bawa P, Calancie B. Repetitive doublets in human flexor carpi radialis muscle. J Physiol 339: 123-132, 1983.
8. Beaumont E, Gardiner PF. Effects of daily spontaneous running on the electrophysiological properties of hindlimb motoneurones in rats. J Physiol 540: 129-138, 2002.
9. Beaumont E, Gardiner PF. Endurance training alters the biophysical properties of hindlimb motoneurons in rats. Muscle Nerve 27: 228-236, 2003.
10. Beaumont E, Houle JD, Peterson Gardiner PF CA. Passive exercise and fetal spinal cord transplant both help to restore motoneuronal properties after spinal cord transection in rats. Muscle Nerve 29: 234-242, 2004.
11. Cavalcanti RA, da Pureza DY, de Melo MP, de Souza RR, Bergamaschi CT, do Amaral SL, Tang H, Loesch A, Riberio A. A Low-intensity treadmill exercise-related changes in the rat stellate ganglion neurons. J Neurosci Res 87: 1334-1342, 2009.
12. Celichowski J, Drzymała-Celichowska H. The number of motor units in the medial gastrocnemius muscle of male and female rats. J Physiol Pharmacol 58: 821-828, 2007.
13. Cormery B, Beaumont E, Csukly K, Gardiner P. Hindlimb unweighting for 2 wk alters physiological properties of rat hindlimb motoneurones. J Physiol 568: 841-850, 2005.
14. Cormery B, Marini JF, Gardiner PF. Changes in electrophysiological properties of tibial motoneurones in the rat following 4 weeks of tetrodotoxin-induced paralysis. Neurosci Lett 287: 21-24, 2000.
15. Dearth CL, Goh Q, Marino JS, Cicinelli PA, Torresa-Palsa MJ, Pierre P, Worth RG, Pizza FX. Skeletal muscle cells express ICAM-1 after muscle overload and ICAM-1 contributes to the ensuing hypertrophic response. PLoS One 8: e58486, 2013.
16. Degens H, Meessen NE, Wirtz P, Binkhorst RA. The development of compensatory hypertrophy in the plantaris muscle of the rat. Ann Anat 177: 285-289, 1995.
17. De Luca CJ, Lefever RS, Cue MP, Xenaius AP. Behavior of human motor units in different muscles during linearly varying contractions. J Physiol Lond 329: 113-128, 1982.
18. Finkel RS. Electrophysiological and motor function scale association in a pre-symptomatic infant with spinal muscular atrophy type I. Neuromuscul Disord 23: 112-115, 2013.
19. Finkelstein DI, Lang JG, Luff AR. Functional and structural changes of rat plantaris motoneurons following compensatory hypertrophy of the muscle. Anat Rec 229: 129-137, 1991.
20. Fry AC. The role of resistance exercise intensity on muscle fibre adaptation. Sports Med 34: 663-679, 2004.
21. Gardiner P, Beaumont E, Cormery B. Motoneurones "learn" B, "forget" physical activity. Can J Appl Physiol 30: 352-370, 2005.
22. Gardiner PF, Jasmin BJ, Corriveau P. Rostrocaudal pattern of fiber-type changes in an overloaded rat ankle extensor. J Appl Physiol 71: 558-64, 1991.
23. Gardiner PF, Dai Y, Heckman CJ. Effects of exercise training on alphamotoneurons. J Appl Physiol 101: 1228-1236, 2006.
24. Gardiner PF, Kernell D. The "fastness" of rat motoneurons: time-course of afterhyperpolarization in relation to axonal conduction velocity and muscle unit contractile speed. Pflügers Arch 415: 762-766, 1990.
25. Gardiner PF. Physiological properties of motoneurons innervating different muscle unit types in rat gastrocnemius. J Neurophysiol 69: 1160-1170, 1993.
26. Gollvik L, Kellerth JO, Ulfhake B. The effects of tenotomy and overload on the postnatal development of medial gastrocnemius motor units in the cat. Acta Physiol Scand 128: 485-494, 1986.
27. Gustafsson B, Pinter MJ. Relations among passive electrical properties of lumbar alpha-motoneurones of cat. J Physiol 357: 453-483, 1984.
28. Heckman CJ, Binder MD. Computer simulation of the steadystate inputoutput function of the cat medial gastrocnemius motoneuron pool. J Neurophysiol 65: 952-967, 1991.
29. Hennig R, Lømo T. Firing patterns of motor units in normal rats. Nature 314: 164-166, 1985.
30. Henry G, Chambers MD. The surgical treatment of spasticity. Muscle Nerve 20: 121-128, 1997.
31. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to induction and excitation in nerve. J Physiol 117: 500-544, 1952.
32. Huey KA, Burdette S, Zhong H, Roy RR. Early response of heat shock proteins to functional overload of the soleus and plantaris in rats and mice. Exp Physiol 95: 1145-1155, 2010.
33. Ianuzzo CD, Chen V. Metabolic character of hypertrophied rat muscle. J Appl Physiol 46: 738-742, 1979.
34. Kalmar JM, Button DC, Gardiner K, Cahill F, Gardiner PF. Caloric restriction does not offset age-associated changes in the biophysical properties of motoneurons. J Neurophysiol 101: 548-557, 2009.
35. Kirkwood PA, Munson JB. The incidence of initial doublets in the discharges of motoneurones of two different inspiratory muscles in the cat. J Physiol 493: 577-587, 1996.
36. Krutki P, Celichowski J, Lochynski D, Pogrzebna M, Mrówczynski W. Interspecies differences of motor units properties in the medial gastrocnemius muscle of cat and rat. Arch Ital Biol 144: 11-23, 2006.
37. Krysciak K, Celichowski J, Drzymała-Celichowska H, Gardiner P, Krutki P. Force regulation and electrical properties of motor units in overloaded muscle. Muscle Nerve. In press.
38. Kudina LP, Alexeeva NL. After-potentials and control of repetitive firing in human motoneurones. Electroencephalogr Clin Neurophysiol 85: 345-353, 1992.
39. Lehmann MJ, Lormes W, Opitz-Gress A, Steinacker JM, Netzer N, Foster C, Gustmann U. Training and overtraining: an overview and experimental results in endurance sports. J Sports Med Phys Fitness 37: 7-17, 1997.
40. McDonagh MJN, Davies CTM. Adaptive response of mammalian skeletal muscle to exercise with high loads. Eur J Appl Physiol 52: 139-155, 1984.
41. Mrówczynski W, Krutki P, Chakarov V, Celichowski J. Doublet of action potentials evoked by intracellular injection of rectangular depolarization current into rat motoneurones. Exp Brain Res 205: 95-102, 2010.
42. Noble EG, Pettigrew FP. Appearance of "transitional" motor units in overloaded rat skeletal muscle. J Appl Physiol 67: 2049-2054, 1989.
43. Nunez-Abades PA, Patillo JM, Hodgson TM, Cameron WE. Role of synaptic inputs in determining input resistance of developing brainsteam motoneurons. J Neurophysiol 84: 2317-2329, 2000.
44. Olha AE, Jasmin BJ, Michel RN, Gardiner PF. Physiological responses of rat plantaris motor units to overload induced by surgical removal of its synergists. J Neurophysiol 60: 2138-2151, 1988.
45. Powers RK, Binder MD. Summation of effective synaptic currents and firing rate modulation in cat spinal motoneurons. J Neurophysiol 83: 483-500, 2000.
46. Roy RR, Ishihara A, Kim JA, lee M, Fox K, Edgerton VR. Metabolic and morphological stability of motoneurons in response to chronically elevated neuromuscular activity. Neuroscience 92: 361-366, 1999.
47. Seynnes OR, de Boer A, Narici MV. Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol 102: 368-373, 2006.
48. Siegelbaum SA, Koester J. Ion channels. In: Principles of Neural Science (5th ed.), edited by Kandel ER, Schwartz JH, and Jessell TM. New York, NY: McGraw-Hill, 2013, p. 100-125.
49. Silva GJ, Brum PC, Negrão CE, Krieger EM. Acute and chronic effects of exercise on baroreflexes in spontaneously hypertensive rats. Hypertension 30: 714-719, 1997.
50. Viana F, Bayliss DA, Berger AJ. Multiple potassium conductances and their role in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. J Neurophysiol 69: 2150-2163, 1993.
51. Walsh JV Jr, Burke RE, Rymer WZ, Tsairis P. Effect of compensatory hypertrophy studied in individual motor units in medial gastrocnemius muscle of the cat. J Neurophysiol 41: 496-508, 1978.