Motor cortical stimulation promotes synaptic plasticity and behavioral improvements following sensorimotor cortex lesions

Experimental Neurology

Volumn 212, Issue 1, 2008, Pages 14-28

  Adkins, DeAnna L ^a   Hsu, J Edward ^a   Jones, Theresa A ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Motor rehabilitation; Multisynaptic boutons; Perforated synapses; Skilled reaching; Stroke; Synaptic plasticity

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX LESION; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; CONVALESCENCE; DISEASE SEVERITY; ELECTRON MICROSCOPY; MALE; MOTOR CORTEX STIMULATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORIMOTOR CORTEX; TASK PERFORMANCE; TRAINING;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN DAMAGE, CHRONIC; DENDRITES; ELECTRIC STIMULATION THERAPY; ELECTRODES, IMPLANTED; FORELIMB; MALE; MICROELECTRODES; MOTOR CORTEX; MOTOR SKILLS DISORDERS; MOVEMENT; NEURAL PATHWAYS; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; RATS; RATS, LONG-EVANS; RECOVERY OF FUNCTION; SEVERITY OF ILLNESS INDEX; STROKE; SYNAPTIC TRANSMISSION; TREATMENT OUTCOME;

EID: 40749128163     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.01.031     Document Type: Article

References (65)

1. Adkins D.L., Voorhies A.C., and Jones T.A. Behavioral and neuroplastic effects of focal endothelin-1 induced sensorimotor cortex lesions. Neuroscience 128 (2004) 473-486
2. Adkins D.L., Boychuk J., Remple M.S., and Kleim J.A. Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J. Appl. Physiol. 101 (2006) 1776-1782
3. Adkins D.L., Campos P., Quach D., Borromeo M., Schallert K., and Jones T.A. Epidural cortical stimulation enhances motor function after sensorimotor cortical infarcts in rats. Exp. Neurol. 200 (2006) 356-370
4. Adkins-Muir D.L., and Jones T.A. Cortical electrical stimulation combined with rehabilitative training: enhanced functional recovery and dendritic plasticity following focal cortical ischemia in rats. Neurol. Res. 25 (2003) 780-788
5. Adkins-Muir D.L., Luke L., Fowler B., and Jones T.A. Electrical stimulation of the peri-lesion cortical surface during motor skills training improves behavioral function after ischemic lesions of the sensorimotor cortex in adult rats. Soc. Neurosci. Abstr. 28 (2002) 489.4
6. Brown J.A., and Pilitsis J.G. Motor cortex stimulation. Pain Med. 7 Suppl. 1 (2006) S140-S145
7. Brown J.A., Lutsep H., Cramer S.C., and Weinand M. Motor cortex stimulation for enhancement of recovery after stroke: case report. Neurol. Res. 25 (2003) 815-818
8. Brown J.A., Lutsep H.L., Weinand M., and Cramer S.C. Motor cortex stimulation for the enhancement of recovery from stroke: a prospective, multicenter safety study. Neurosurgery 58 (2006) 464-473
9. Bury S.D., and Jones T.A. Unilateral sensorimotor cortex lesions in adult rats facilitate motor skill learning with the "unaffected" forelimb and training-induced dendritic structural plasticity in the motor cortex. J. Neurosci. 22 (2002) 8597-8606
10. Carmichael S.T. Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann. Neurol. 59 (2006) 735-742
11. Conner J.M., Chiba A.A., and Tuszynski M.H. The basal forebrain cholinergic system is essential for cortical plasticity and functional recovery following brain injury. Neuron 46 (2005) 173-179
12. Connor S., Williams P.T., Armstrong B., Petit T.L., Ivanco T.L., and Weeks A.C. Long-term potentiation is associated with changes in synaptic ultrastructure in the rat neocortex. Synapse 59 (2006) 378-382
13. Dietrich W.D., Ginsberg M.D., Busto R., and Watson B.D. Photochemically induced cortical infarction in the rat. 2. Acute and subacute alterations in local glucose utilization. J. Cereb. Blood Flow Metab. 6 (1986) 195-202
14. Dobkin B.H. Neurobiology of rehabilitation. Ann. N.Y. Acad. Sci. 1038 (2004) 148-170
15. Duncan P.W., Lai S.M., and Keighley J. Defining post-stroke recovery: implications for design and interpretation of drug trials. Neuropharmacology 39 (2000) 835-841
16. Eshkol N., and Wachmann A. Movement Notation (1958), Weidenfeld and Nicolson, London, UK
17. Friel K.M., Heddings A.A., and Nudo R.J. Effects of postlesion experience on behavioral recovery and neurophysiologic reorganization after cortical injury in primates. Neurorehabil. Neural Repair 14 (2000) 187-198
18. Fuxe K., Bjelke B., Andbjer B., Grahn H., Rimondini R., and Agnati L.F. Endothelin-1 induced lesions of the frontoparietal cortex of the rat. A possible model of focal cortical ischemia. Neuroreport 8 (1997) 2623-2629
19. Ganeshina O., Berry R.W., Petralia R.S., Nicholson D.A., and Geinisman Y. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J. Comp. Neurol. 468 (2004) 86-95
20. Geinisman Y., Morrell F., and deToledo-Morrell L. Increase in the relative proportion of perforated axospinous synapses following hippocampal kindling is specific for the synaptic field of stimulated axons. Brain Res. 507 (1990) 325-331
21. Geinisman Y., Berry R.W., Disterhoft J.F., Power J.M., and Van der Zee E.A. Associative learning elicits the formation of multiple-synapse boutons. J. Neurosci. 21 (2001) 5568-5573
22. Gharbawie O.A., Gonzalez C.L., and Whishaw I.Q. Skilled reaching impairments from the lateral frontal cortex component of middle cerebral artery stroke: a qualitative and quantitative comparison to focal motor cortex lesions in rats. Behav. Brain Res. 156 (2005) 125-137
23. Greenough W.T., Larson J.R., and Withers G.S. Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. Behav. Neural Biol. 44 (1985) 301-314
24. Gundersen H.J., Bendtsen T.F., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96 (1988) 379-394
25. Humm J.L., Kozlowski D.A., James D.C., Gotts J.E., and Schallert T. Use-dependent exacerbation of brain damage occurs during an early post-lesion vulnerable period. Brain Res. 783 (1998) 286-292
26. Hummel F.C., and Cohen L.G. Improvement of motor function with noninvasive cortical stimulation in a patient with chronic stroke. Neurorehabil. Neural Repair 19 (2005) 14-19
27. Hummel F.C., and Cohen L.G. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke?. Lancet Neurol. 5 (2006) 708-712
28. Jablonka J.A., Witte O.W., and Kossut M. Photothrombotic infarct impairs experience-dependent plasticity in neighboring cortex. Neuroreport 18 (2007) 165-169
29. Jones T.A. Multiple synapse formation in the motor cortex opposite unilateral sensorimotor cortex lesions in adult rats. J. Comp. Neurol. 414 (1999) 57-66
30. Jones T.A., Klintsova A.Y., Kilman V.L., Sirevaag A.M., and Greenough W.T. Induction of multiple synapses by experience in the visual cortex of adult rats. Neurobiol. Learn. Mem. 68 (1997) 13-20
31. Jones T.A., Chu C.J., Grande L.A., and Gregory A.D. Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J. Neurosci. 19 (1999) 10153-10163
32. Kleim J.A., Swain R.A., Armstrong K.A., Napper R.M., Jones T.A., and Greenough W.T. Selective synaptic plasticity within the cerebellar cortex following complex motor skill learning. Neurobiol. Learn. Mem. 69 (1998) 274-289
33. Kleim J.A., Barbay S., Cooper N.R., Hogg T.M., Reidel C.N., Remple M.S., and Nudo R.J. Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol. Learn. Mem. 77 (2002) 63-77
34. Kleim J.A., Bruneau R., Calder K., Pocock D., VandenBerg P.M., MacDonald E., Monfils M.H., Sutherland R.J., and Nader K. Functional organization of adult motor cortex is dependent upon continued protein synthesis. Neuron 40 (2003) 167-176
35. Kleim J.A., Bruneau R., VandenBerg P., MacDonald E., Mulrooney R., and Pocock D. Motor cortex stimulation enhances motor recovery and reduces peri-infarct dysfunction following ischemic insult. Neurol. Res. 25 (2003) 789-793
36. Kleim J.A., Hogg T.M., VandenBerg P.M., Cooper N.R., Bruneau R., and Remple M. Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J. Neurosci. 24 (2004) 628-633
37. Kobayashi M., Hutchinson S., Théoret H., Schlaug G., and Pascual-Leone A. Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements. Neurology 62 (2004) 91-98
38. Kolb B. Overview of cortical plasticity and recovery from brain injury. Phys. Med. Rehabil. Clin. North Am. 14 (2003) S7-S25 viii
39. Luft A.R., Buitrago M.M., Ringer T., Dichgans J., and Schulz J.B. Motor skill learning depends on protein synthesis in motor cortex after training. J. Neurosci. 24 (2004) 6515-6520
40. Macrae I.M., Robinson M.J., Graham D.I., Reid J.L., and McCulloch J. Endothelin-1-induced reductions in cerebral blood flow: dose dependency, time course, and neuropathological consequences. J. Cereb. Blood Flow Metab. 13 (1993) 276-284
41. McKenna J.E., and Whishaw I.Q. Complete compensation in skilled reaching success with associated impairments in limb synergies, after dorsal column lesion in the rat. J. Neurosci. 19 (1999) 1885-1894
42. Metz G.A., and Whishaw I.Q. Skilled reaching an action pattern: stability in rat (Rattus norvegicus) grasping movements as a function of changing food pellet size. Behav. Brain Res. 116 (2000) 111-122
43. Miklyaeva E.I., and Whishaw I.Q. HemiParkinson analogue rats display active support in good limbs versus passive support in bad limbs on a skilled reaching task of variable height. Behav. Neurosci. 110 (1996) 117-125
44. Monfils M.H., Plautz E.J., and Kleim J.A. In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience. Neuroscientist 11 (2005) 471-483
45. Nair D.G., Hamelin S., Pascual-Leone A., and Schlaug G. Direct current stimulation in combination with occupational therapy for 5 consecutive days improves motor function in chronic stroke patients. International Stroke Conference (2007)
46. Neumann-Haefelin T., and Witte O.W. Periinfarct and remote excitability changes after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 20 (2000) 45-52
47. Neumann-Haefelin T., Hagemann G., and Witte O.W. Cellular correlates of neuronal hyperexcitability in the vicinity of photochemically induced cortical infarcts in rats in vitro. Neurosci. Lett. 193 (1995) 101-104
48. Nudo R.J. Functional and structural plasticity in motor cortex: implications for stroke recovery. Phys. Med. Rehabil. Clin. North Am. 14 (2003) S57-S76
49. Nudo R.J., and 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
50. Nudo R.J., Milliken G.W., Jenkins W.M., and Merzenich M.M. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J. Neurosci. 16 (1996) 785-807
51. Pascual-Leone A. Disrupting the brain to guide plasticity and improve behavior. Prog. Brain Res. 157 (2006) 315-329
52. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1998), Academic Press, New York
53. Peterson G., and Devine J. Transfer on handedness in the rat resulting from small cortical lesions after limited forced practice. J. Comp. Physiol. Psychol. 56 (1963) 752-756
54. Plautz E.J., Barbay S., Frost S.B., Friel K.M., Dancause N., Zoubina E.V., Stowe A.M., Quaney B.M., and Nudo R.J. Post-infarct cortical plasticity and behavioral recovery using concurrent cortical stimulation and rehabilitative training: a feasibility study in primates. Neurol. Res. 25 (2003) 801-810
55. Purpura D.P., and McMurtry J.G. Intracellular activities and evoked potential changes during polarization of motor cortex. J. Neurophysiol. 28 (1965) 166-185
56. Ramanathan D., Conner J.M., and Tuszynski M.H. A form of motor cortical plasticity that correlates with recovery of function after brain injury. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 11370-11375
57. Teskey G.C., Flynn C., Goertzen C.D., Monfils M.H., and Young N.A. Cortical stimulation improves skilled forelimb use following a focal ischemic infarct in the rat. Neurol. Res. 25 (2003) 794-800
58. Thom T., Haase N., Rosamond W., Howard V.J., Rumsfeld J., Manolio T., Zheng Z.J., Flegal K., O'Donnell C., Kittner S., Lloyd-Jones D., Goff Jr. D.C., Hong Y., Adams R., Friday G., Furie K., Gorelick P., Kissela B., Marler J., Meigs J., Roger V., Sidney S., Sorlie P., Steinberger J., Wasserthiel-Smoller S., Wilson M., and Wolf P. Heart disease and stroke statistics-2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 113 (2006) e85-e151
59. Toni N., Buchs P.A., Nikonenko I., Povilaitite P., Parisi L., and Muller D. Remodeling of synaptic membranes after induction of long-term potentiation. J. Neurosci. 21 (2001) 6245-6251
60. West M.J., and Gundersen H.J. Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296 (1990) 1-22
61. Whishaw I.Q. Activation, travel distance, and environmental change influence food carrying in rats with hippocampal, medial thalamic and septal lesions: implications for studies on hoarding and theories of hippocampal function. Hippocampus 3 (1993) 373-385
62. Whishaw I.Q., Pellis S.M., Gorny B., Kolb B., and Tetzlaff W. Proximal and distal impairments in rat forelimb use in reaching follow unilateral pyramidal tract lesions. Behav. Brain Res. 56 (1993) 59-76
63. Whishaw I.Q., Pellis S.M., Gorny B.P., and Pellis V.C. The impairments in reaching and the movements of compensation in rats with motor cortex lesions: an endpoint, videorecording, and movement notation analysis. Behav. Brain Res. 42 (1991) 77-91
64. Wise S.P., and Donoghue J.P. Motor cortex of rodents. In: Jones E.G., and Peters A. (Eds). Cerebral Cortex 5 (1986), Plenum, New York 243-270
65. Withers G.S., and Greenough W.T. Reach training selectively alters dendritic branching in subpopulations of layer II-III pyramids in rat motor-somatosensory forelimb cortex. Neuropsychologia 27 (1989) 61-69