Adaptive plasticity in primate motor cortex as a consequence of behavioral experience and neuronal injury

Seminars in the Neurosciences

Volumn 9, Issue 1-2, 1997, Pages 13-23

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

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Learning; Motor cortex; Plasticity; Rehabilitation; Stroke

Indexed keywords

ANIMAL EXPERIMENT; BEHAVIOR; BRAIN INFARCTION; BRAIN INJURY; CONTROLLED STUDY; HUMAN; MOTOR CORTEX; MOTOR PERFORMANCE; MUSCLE DENERVATION; NERVE CELL PLASTICITY; NERVE INJURY; NONHUMAN; PERIPHERAL NERVE INJURY; REVIEW; SYNAPSE; TASK PERFORMANCE; TOPOGRAPHY; TRAINING;

EID: 0030931363     PISSN: 10445765     EISSN: None     Source Type: Journal    
DOI: 10.1006/smns.1997.0102     Document Type: Article

References (65)

1. Kaas J. H. Plasticity of sensory and motor maps in adult mammals. Annu. Rev. Neurosci. 14:1991;137-167.
2. Fritsch G., Hitzig E. Ueber die elektrische Erregbarkeit des Grosshirns. Arch. Anat. Physiol. Wiss. Med. 37:1870;300-332.
3. Woolsey C. N. Patterns of localization in sensory and motor areas of the cerebral cortex. Milbank Symposium: The Biology of Mental Health and Disease. 1952;Hoeber, New York. p. 193-206.
4. Donoghue J. P., Sanes J. N. Motor areas of the cerebral cortex. J. Clin. Neurophysiol. 11:1994;382-396.
5. Tanji J., Kurata K. Changing concepts of motor areas of the cerebral cortex. Brain Dev. 11:1989;374-377.
6. Wise S. P., DiPellegrino G., Boussaoud D. Primate premotor cortex: Dissociation of visuomotor from sensory signals. J. Neurophysiol. 68:1992;969-972.
7. Wise S. Evolutionary and comparative neurobiology of the supplementary sensorimotor area. Adv. Neurol. 70:1996;71-83.
8. Picard N., Strick P. L. Motor areas of the medial wall: A review of their location and functional activation. Cereb. Cortex. 6:1996;342-353.
9. Welker W. I., Benjamin R. M., Miles R. C., Woolsey C. N. Motor effects of stimulation of cerebral cortex of squirrel monkey (Saimiri sciureus. J. Neurophysiol. 20:1957;347-364.
10. Asanuma H., Rosén I. Topographical organization of cortical efferent zones projecting to distal forelimb muscles in the monkey. Exp. Brain Res. 14:1972;243-256.
11. Donoghue J. P., Leibovic S., Sanes J. N. Organization of the forelimb area in squirrel monkey motor cortex: Representation of digit, wrist, and elbow muscles. Exp. Brain Res. 89:1992;1-19.
12. Gould H. J. I., Cusick C. G., Pons T. P., Kaas J. H. 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. 247:1986;297-325.
13. Nudo R. J., Jenkins W. M., Merzenich M. M., Prejean T., Gedela R. Neurophysiological correlates of hand preference in primary motor cortex of squirrel monkeys. J. Neurosci. 12:1992;2918-2947.
14. Stepniewska I., Preuss T. M., Kaas J. H. Architectonics, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J. Comp. Neurol. 330:1993;238-271.
15. Sanes J. N., Donoghue J. P., Thangaraj V., Edelman R. R., Warach S. Shared neural substrates controlling hand movements in human motor cortex. Science. 268:1995;1775-1777.
16. Preuss T. M., Stepniewska I., Kaas J. H. Movement representation in the dorsal and ventral premotor areas of owl monkeys: A microstimulation study. J. Comp. Neurol. 371:1996;649-676.
17. Tanji J., Wise S. P. Submodality distribution in sensorimotor cortex of the unanesthetized monkey. J. Neurophysiol. 45:1981;467-481.
18. Strick P. L., Preston J. B. Two representations of the hand in area 4 of a primate. II. Somatosensory input organization. J. Neurophysiol. 48:1982;150-159.
19. Humphrey S. M., Gardner G. A., Raiszadeh R., Nudo R. J. Loss of sensory, but not motor responsiveness in intact cortex surrounding a focal ischemic infarct in area 4. Soc. Neurosci. Abstr. 20:1994;179.
20. Geyer S., Ledberg A., Schleicher A., Kinomura S., Schormann T., Bürgel U., Klingberg T., Larsson J., Zilles K., Roland P. E. Two different areas within the primary motor cortex of man. Nature. 382:1996;805-807.
21. Keller A. Intrinsic synaptic organization of the motor cortex. Cereb. Cortex. 3:1993;430-441.
22. Huntley G. W., Jones E. G. Relationship of intrinsic connections to forelimb movement representations in monkey motor cortex: A correlative anatomical and physiological study. J. Neurophysiol. 66:1991;390-413.
23. Plautz E. P., Milliken G. W., Nudo R. J. Anatomical connectivity of electrophysiologically identified movement representations in the M1 hand area of squirrel monkeys. Soc. Neurosci. Abstr. 22:1996;1083.
24. Graham Brown T., Sherrington C. S. On the instability of a cortical point. Proc. R. Soc. (London). 85:1912;250-277.
25. Nudo R. J., Jenkins W. M., Merzenich M. M. Repetitive microstimulation alters the cortical representation of movements in adult rats. Somatosens. Mot. Res. 7:1990;463-483.
26. Jacobs K. M., Donoghue J. P. Reshaping the cortical motor map by unmasking latent intracortical connections. Science. 251:1991;944-947.
27. Sanes J. N., Wang J., Donoghue J. P. Immediate and delayed changes of rat motor cortical output representation with new forelimb configurations. Cereb. Cortex. 2:1992;141-152.
28. Woody C. D., Engel J. Jr. Changes in unit activity and thresholds to electrical microstimulation at coronal-pericruciate cortex of cat with classical conditioning of different facial movements. J. Neurophysiol. 35:1972;230-241.
29. Fetz E. E., Baker M. A. Operantly conditioned patterns of precentral unit activity and correlated responses in adjacent cells and correlated muscles. J. Neurophysiol. 36:1973;179-204.
30. Nudo R. J., Milliken G. W., Jenkins W. M., Merzenich M. M. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J. Neurosci. 16:1996;785-807.
31. Plautz E. J., Milliken G. W., Nudo R. J. Differential effects of skill acquisition and motor use on the reorganization of motor representations in area 4 of adult squirrel monkeys. Soc. Neurosci. Abstr. 21:1995;1902.
32. Elbert T., Pantev C., Wienbruch C., Rockstroh B., Taub E. Increased cortical representation of the fingers of the left hand in string players. Science. 270:1995;305-307.
33. Grafton S. T., Mazziotta J. C., Presty S., Friston K. J., Frackowiak R. S. J., Phelps M. E. Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J. Neurosci. 12:1992;2542-2548.
34. Pascual-Leone A., Nguyet D., Cohen L. G., Brasil-Neto J. P., Cammarota A., Hallett M. Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J. Neurophysiol. 74:1995;1037-1045.
35. Pascual-Leone A., Torres F. Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. Brain. 116:1993;39-52.
36. Karni A., Meyer G., Jezzard P., Adams M. M., Turner R., Ungerleider L. G. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature. 377:1995;155-158.
37. Seitz R. J., Huang Y., Knorr U., Tellmann L., Herzog H., Freund H. J. Large-scale plasticity of the human motor cortex. Neuroreport. 6:1995;742-744.
38. Jenkins I. H., Brooks D. J., Nixon P. D., Frackowiak S. J., Passingham R. E. Motor sequence learning: A study with positron emission tomography. J. Neurosci. 14:1994;3775-3790.
39. Schlaug G., Knorr U., Seitz R. J. Inter-subject variability of cerebral activations in acquiring a motor skill: A study with positron emission tomography. Exp. Brain Res. 98:1994;523-534.
40. Pascual-Leone A., Grafman J., Hallett M. Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science. 263:1994;1287-1289.
41. Seitz R. J., Roland R. E., Bohm C., Greitz T., Stone-Elander S. Motor learning in man: A positron emission tomographic study. Neuroreport. 1:1990;57-60.
42. Donoghue J. P., Sanes J. N. Organization of adult motor cortex representation patterns following neonatal forelimb nerve injury in rats. J. Neurosci. 8:1988;3221-3232.
43. Sanes J. N., Suner S., Donoghue J. P. 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. 79:1990;479-491.
44. Sanes J. N., Suner S., Lando J. F., Donoghue J. P. Rapid reorganization of adult rat motor cortex somatic representation patterns after motor nerve injury. Proc. Natl. Acad. Sci. USA. 85:1988;2003-2007.
45. Donoghue J. P., Suner S., Sanes J. N. Dynamic organization of primary motor cortex output to target muscles in adult rats. II. Rapid reorganization following motor nerve lesions. Exp. Brain Res. 79:1990;492-503.
46. Ojemann J. G., Silbergeld D. L. Cortical stimulation mapping of phantom limb rolandic cortex. Case report. J. Neurosurg. 82:1995;641-644.
47. Brasil-Neto J. P., Valls-Sole J., Pascual-Leone A., Cammarota A., Amassion V. E., Cracco R., Maccabee P., Cracco L., Hallett M., Cohen L. G. Rapid modulation of human cortical motor outputs following ischaemic nerve block. Brain. 116:1993;511-525.
48. Cohen L. G., Brasil-Neto J. P., Pascual-Leone A., Hallett M. Plasticity of cortical motor output organization following deafferentation, cerebral lesions, and skill acquisition. Adv. Neurol. 63:1993;187-200.
49. Glees P., Cole J. Recovery of skilled motor functions after small repeated lesions in motor cortex in macaque. J. Neurophysiol. 13:1950;137-148.
50. Nudo R. J., Milliken G. W. Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J. Neurophysiol. 75:1996;2144-2149.
51. Nudo R. J., Wise B. M., SiFuentes F., Milliken G. W. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science. 272:1996;1791-1794.
52. Castro-Alamancos M. A., García-Segura L. M., Borrell J. Transfer of function to a specific area of the cortex after induced recovery from brain damage. Eur. J. Neurosci. 4:1992;853-863.
53. Taub E., Miller N. E., Novack T. A., Cook E. W. I., Fleming W. C., Nepomuceno C. S., Connell J. S., Crago J. E. Technique to improve chronic motor deficit after stroke. Arch. Phys. Med. Rehab. 74:1993;347-354.
54. Kozlowski D. A., James D. C., Schallert T. Use-dependent exaggeration of neuronal injury after unilateral sensorimotor cortex lesions. J. Neurosci. 16:1996;4776-4786.
55. Donoghue J. P. Plasticity of adult sensorimotor representations. Curr. Opinion Neurobiol. 5:1995;749-754.
56. Iriki A., Pavlides C., Keller A., Asanuma H. Long-term potentiation of thalamic input to the motor cortex induced by coactivation of thalamocortical and corticocortical afferents. J. Neurophysiol. 65:1991;1435-1441.
57. Aroniadou V. A., Keller A. The patterns and synaptic properties of horizontal intracortical connections in the rat motor cortex. J. Neurophysiol. 70:1993;1553-1569.
58. Hess G., Jacobs K. M., Donoghue J. P. ND. Neuroscience. 61:1994;225-235.
59. Hess G., Donoghue J. P. Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J. Neurophysiol. 71:1994;2543-2547.
60. Castro-Alamancos M. A., Donoghue J. P., Connors B. W. Different forms of plasticity in somatosensory and motor areas of the neocortex. J. Neurosci. 15:1995;5324-5333.
61. Jones E. G., Coulter J. D., Hendry S. H. C. Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J. Comp. Neurol. 181:1978;291-348.
62. Keller A. Intrinsic connections between representation zones in the cat motor cortex. Neuroreport. 4:1993;515-518.
63. Weiss D. S., Keller A. Specific patterns of intrinsic connections between representation zones in the rat motor cortex. Cereb. Cortex. 4:1994;205-214.
64. Kleim J. A., Lussnig E., Schwarz E. R., Comery T. A., Greenough W. T. Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J. Neurosci. 16:1996;4529-4535.
65. Bertelson J. A., Plautz E. J., Nudo R. J. Reorganization of muscle representations in motor cortex following a focal ischemic infarct. Soc. Neurosci. Abstr. 22:1996;2023.