Distal forelimb representations in primary motor cortex are redistributed after forelimb restriction: A longitudinal study in adult squirrel monkeys

Journal of Neurophysiology

Volumn 109, Issue 5, 2013, Pages 1268-1282

  Milliken, Garrett W ^a   Plautz, Erik J ^a   Nudo, Randolph J ^a  

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

Author keywords

Disuse; Hand; Motor cortex; Plasticity; Primate

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FINGER; FOREARM; FORELIMB; FUNCTIONAL MAGNETIC RESONANCE IMAGING; IMMOBILIZATION; JOINT FUNCTION; LONGITUDINAL STUDY; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOVEMENT (PHYSIOLOGY); MUSCLE TONE; NONHUMAN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SQUIRREL MONKEY; TRANSCRANIAL MAGNETIC STIMULATION; WRIST;

ANIMALS; BRAIN MAPPING; CASTS, SURGICAL; FORELIMB; LONGITUDINAL STUDIES; MALE; MOTOR CORTEX; MOTOR SKILLS; MOVEMENT; NEURONAL PLASTICITY; RESTRAINT, PHYSICAL; SAIMIRI;

EID: 84874583224     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00044.2012     Document Type: Article

References (54)

1. Adachi K, Lee JC, Hu JW, Yao D, Sessle BJ. Motor cortex neuroplasticity associated with lingual nerve injury in rats. Somatosens Mot Res 24: 97-109, 2007.
2. Boinski S. Habitat use by squirrel monkeys (Saimiri oerstedi) in Costa Rica. Folia Primatol (Basel) 49: 151-167, 1987.
3. Byl NN. Focal hand dystonia may result from aberrant neuroplasticity. Adv Neurol 94: 19-28, 2004.
4. Cheney PD, Fetz EE. Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimuli in primates: evidence for functional groups of CM cells. J Neurophysiol 53: 786-804, 1985.
5. Clark BC, Issac LC, Lane JL, Damron LA, Hoffman RL. Neuromuscular plasticity during and following 3 wk of human forearm cast immobilization. J Appl Physiol 105: 868-878, 2008.
6. Clark BC, Taylor JL, Hoffman RL, Dearth DJ, Thomas JS. Cast immobilization increases long-interval intracortical inhibition. Muscle Nerve 42: 363-372, 2010.
7. Cramer SC. A window into the molecular basis of human brain plasticity. J Physiol 586: 5601, 2008.
8. Dancause N. Neurophysiological and anatomical plasticity in the adult sensorimotor cortex. Rev Neurosci 17: 561-580, 2006.
9. Devanne H, Cohen LG, Kouchtir-Devanne N, Capaday C. Integrated motor cortical control of task-related muscles during pointing in humans. J Neurophysiol 87: 3006-3017, 2002.
10. Fetz EE, Cheney PD. Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J Neurophysiol 44: 751-772, 1980.
11. Franchi G. Time course of motor cortex reorganization following botulinum toxin injection into the vibrissal pad of the adult rat. Eur J Neurosci 16: 1333-1348, 2002.
12. Gould HJ 3rd, Cusick CG, Pons TP, Kaas JH. The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys. J Comp Neurol 247: 297-325, 1986.
13. Graziano MS, Taylor CS, Moore T. Complex movements evoked by microstimulation of precentral cortex. Neuron 34: 841-851, 2002.
14. Jankowska E, Padel Y, Tanaka R. The mode of activation of pyramidal tract cells by intracortical stimuli. J Physiol 249: 617-636, 1975.
15. Jones TA, Allred RP, Adkins DL, Hsu JE, O'Bryant A, Maldonado MA. Remodeling the brain with behavioral experience after stroke. Stroke 40: S136-S138, 2009.
16. Kaas JH. The reorganization of somatosensory and motor cortex after peripheral nerve or spinal cord injury in primates. Prog Brain Res 128: 173-179, 2000.
17. Kaneko F, Murakami T, Onari K, Kurumadani H, Kawaguchi K. Decreased cortical excitability during motor imagery after disuse of an upper limb in humans. Clin Neurophysiol 114: 2397-2403, 2003.
18. Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R, Ungerleider LG. The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci USA 95: 861-868, 1998.
19. Kleim JA, Barbay S, Nudo RJ. Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80: 3321-3325, 1998.
20. Kleim JA, Cooper NR, VandenBerg PM. Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res 934: 1-6, 2002.
21. Kleim JA, Jones TA. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J Speech Lang Hear Res 51: S225-S239, 2008.
22. Kleim JA, Lussnig E, Schwarz ER, Comery TA, Greenough WT. Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J Neurosci 16: 4529-4535, 1996.
23. Liepert J, Miltner WH, Bauder H, Sommer M, Dettmers C, Taub E, Weiller C. Motor cortex plasticity during constraint-induced movement therapy in stroke patients. Neurosci Lett 250: 5-8, 1998.
24. Liepert J, Tegenthoff M, Malin JP. Changes of cortical motor area size during immobilization. Electroencephalogr Clin Neurophysiol 97: 382-386, 1995.
25. Lundbye-Jensen J, Nielsen JB. Central nervous adaptations following 1 wk of wrist and hand immobilization. J Appl Physiol 105: 139-151, 2008.
26. Monfils MH, Plautz EJ, Kleim JA. In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience. Neuroscientist 11: 471-483, 2005.
27. Navarro X, Vivo M, Valero-Cabre A. Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol 82: 163-201, 2007.
28. Nudo RJ, Jenkins WM, Merzenich MM, Prejean T, Grenda R. Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys. J Neurosci 12: 2918-2947, 1992.
29. Nudo RJ, Milliken GW. Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J Neurophysiol 75: 2144-2149, 1996.
30. Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16: 785-807, 1996a.
31. Nudo RJ, Plautz EJ, Frost SB. Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle Nerve 24: 1000-1019, 2001.
32. Nudo RJ, Wise BM, SiFuentes F, Milliken GW. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272: 1791-1794, 1996b.
33. Okun MS, Nadeau SE, Rossi F, Triggs WJ. Immobilization dystonia. J Neurol Sci 201: 79-83, 2002.
34. Plautz EJ, Milliken GW, Nudo RJ. Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use vs. learning. Neurobiol Learn Mem 74: 27-55, 2000.
35. Remple MS, Bruneau RM, VandenBerg PM, Goertzen C, Kleim JA. Sensitivity of cortical movement representations to motor experience: evidence that skill learning but not strength training induces cortical reorganization. Behav Brain Res 123: 133-141, 2001.
36. Ricci R, Ramsey D, Johnson K, Borckardt JJ, Vallejo M, Roberts DR, George MS. A pilot feasibility study of daily rTMS to modify corticospinal excitability during lower limb immobilization. Ther Clin Risk Manag 4: 1127-1134, 2008.
37. Roberts DR, Ricci R, Funke FW, Ramsey P, Kelley W, Carroll JS, Ramsey D, Borckardt JJ, Johnson K, George MS. Lower limb immobilization is associated with increased corticospinal excitability. Exp Brain Res 181: 213-220, 2007.
38. Sanes JN, Suner S, Donoghue JP. Dynamic organization of primary motor cortex output to target muscles in adult rats. I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions. Exp Brain Res 79: 479-491, 1990.
39. Sawaki L, Butler AJ, Leng X, Wassenaar PA, Mohammad YM, Blanton S, Sathian K, Nichols-Larsen DS, Wolf SL, Good DC, Wittenberg GF. Constraint-induced movement therapy results in increased motor map area in subjects 3 to 9 months after stroke. Neurorehabil Neural Repair 22: 505-513, 2008.
40. Schieber MH, Deuel RK. Primary motor cortex reorganization in a long-term monkey amputee. Somatosens Mot Res 14: 157-167, 1997.
41. Sessle BJ, Adachi K, Avivi-Arber L, Lee J, Nishiura H, Yao D, Yoshino K. Neuroplasticity of face primary motor cortex control of orofacial movements. Arch Oral Biol 52: 334-337, 2007.
42. Siebner HR, Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148: 1-16, 2003.
43. Stoney SD Jr, Thompson WD, Asanuma H. Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. J Neurophysiol 31: 659-669, 1968.
44. Taub E, Crago JE, Burgio LD, Groomes TE, Cook EW 3rd, DeLuca SC, Miller NE. An operant approach to rehabilitation medicine: overcoming learned nonuse by shaping. J Exp Anal Behav 61: 281-293, 1994.
45. Taub E, Heitmann RD, Barro G. Alertness, level of activity, and purposive movement following somatosensory deafferentation in monkeys. Ann N Y Acad Sci 290: 348-365, 1977.
46. Taub E, Miller NE, Novack TA, Cook EW 3rd, Fleming WC, Nepomuceno CS, Connell JS, Crago JE. Technique to improve chronic motor deficit after stroke. Arch Phys Med Rehabil 74: 347-354, 1993.
47. Taub E, Uswatte G, Mark VW, Morris DM. The learned nonuse phenomenon: implications for rehabilitation. Eura Medicophys 42: 241-256, 2006.
48. Weibull A, Flondell M, Rosen B, Bjorkman A. Cerebral and clinical effects of short-term hand immobilisation. Eur J Neurosci 33: 699-704, 2011.
49. Wolf SL. Revisiting constraint-induced movement therapy: are we too smitten with the mitten? Is all nonuse "learned"? and other quandaries. Phys Ther 87: 1212-1223, 2007.
50. Woodlee MT, Schallert T. The interplay between behavior and neurodegeneration in rat models of Parkinson's disease and stroke. Restor Neurol Neurosci 22: 153-161, 2004.
51. Xu T, Yu X, Perlik AJ, Tobin WF, Zweig JA, Tennant K, Jones T, Zuo Y. Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462: 915-919, 2009.
52. Zanette G, Manganotti P, Fiaschi A, Tamburin S. Modulation of motor cortex excitability after upper limb immobilization. Clin Neurophysiol 115: 1264-1275, 2004.
53. Zanette G, Tinazzi M, Bonato C, di Summa A, Manganotti P, Polo A, Fiaschi A. Reversible changes of motor cortical outputs following immobilization of the upper limb. Electroencephalogr Clin Neurophysiol 105: 269-279, 1997.
54. Zar JH. Biostatistical Analysis. Englewood Cliffs, NJ: Prentice-Hall, 1984, p. 718.