Utility of intracerebral theta burst electrical stimulation to attenuate interhemispheric inhibition and to promote motor recovery after cortical injury in an animal model

Experimental Neurology

Volumn 261, Issue , 2014, Pages 258-266

  Barry, Melissa D ^a   Boddington, Laura J ^a   Igelström, Kajsa M ^a   Gray, Jason P ^a   Shemmell, Jon ^a   Tseng, Kuei Y ^b   Oorschot, Dorothy E ^a   Reynolds, John N J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Electrical stimulation; Interhemispheric inhibition; Motor cortex; Rehabilitation; Stroke; Theta burst stimulation

Indexed keywords

CANNABINOID RECEPTOR; 1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DAMAGE; BRAIN DEPTH STIMULATION; BRAIN INJURY; ELECTRODE; ELECTROSTIMULATION THERAPY; IMPLANTATION; INTERHEMISPHERIC INHIBITION; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; NERVE EXCITABILITY; NERVOUS SYSTEM PARAMETERS; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; THERAPY EFFECT; THETA BURST STIMULATION; ANIMAL; BIOPHYSICS; COMPLICATION; CONVALESCENCE; DISEASE MODEL; DRUG EFFECTS; ELECTROENCEPHALOGRAPHY; HEMISPHERIC DOMINANCE; MEMBRANE POTENTIAL; MOVEMENT DISORDERS; NERVE CELL INHIBITION; PATHOLOGY; PHYSIOLOGY; PROCEDURES; TRANSCRANIAL MAGNETIC STIMULATION; WISTAR RAT; ANIMAL TISSUE; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; ELECTRODE IMPLANT; EXCITABILITY; MOTOR COORDINATION; NERVE CELL PLASTICITY; THETA BURST ELECTRICAL STIMULATION;

ANIMALS; BIOPHYSICS; BRAIN INJURIES; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; FUNCTIONAL LATERALITY; MALE; MEMBRANE POTENTIALS; MOTOR CORTEX; MOVEMENT DISORDERS; NEURAL INHIBITION; PIPERIDINES; PYRAZOLES; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84905494356     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.05.023     Document Type: Article

References (48)

1. Abush H., Akirav I. Cannabinoids modulate hippocampal memory and plasticity. Hippocampus 2010, 20(10):1126-1138.
2. Ackerley S.J., Stinear C.M., Barber P.A., Byblow W.D. Combining theta burst stimulation with training after subcortical stroke. Stroke 2010, 41(7):1568-1572.
3. Bestmann S., Baudewig J., Siebner H.R., Rothwell J.C., Frahm J. Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits. Eur. J. Neurosci. 2004, 19(7):1950-1962.
4. Brownjohn P.W., Reynolds J.N., Matheson N., Fox J., Shemmell J.B. The effects of individualized theta burst stimulation on the excitability of the human motor system. Brain Stimul. 2014, 7(2):260-268.
5. Chagnac-Amitai Y., Luhmann H.J., Prince D.A. Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J. Comp. Neurol. 1990, 296(4):598-613.
6. 1 receptor antagonist, AM 251, causes a sustained reduction of daily food intake in the rat. Physiol. Behav. 2004, 82(5):863-869.
7. Clarkson A.N., Huang B.S., MacIsaac S.E., Mody I., Carmichael S.T. Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 2010, 468(7321):305-309.
8. Daskalakis Z.J., Christensen B.K., Fitzgerald P.B., Roshan L., Chen R. The mechanisms of interhemispheric inhibition in the human motor cortex. J. Physiol. Lond. 2002, 543(1):317-326.
9. Degenetais E., Thierry A.M., Glowinski J., Gioanni Y. Electrophysiological properties of pyramidal neurons in the rat prefrontal cortex: an in vivo intracellular recording study. Cereb. Cortex 2002, 12(1):1-16.
10. Di Lazzaro V., Oliviero A., Profice P., Insola A., Mazzone P., Tonali P., et al. Direct demonstration of interhemispheric inhibition of the human motor cortex produced by transcranial magnetic stimulation. Exp. Brain Res. 1999, 124(4):520-524.
11. Dobkin B.H. Training and exercise to drive poststroke recovery. Nat. Clin. Pract. Neurol. 2008, 4(2):76-85.
12. Donoghue J.P., Wise S.P. The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J. Comp. Neurol. 1982, 212(1):76-88.
13. Fabri M., Manzoni T. Glutamic acid decarboxylase immunoreactivity in callosal projecting neurons of cat and rat somatic sensory areas. Neuroscience 2004, 123(2):557-566.
14. Ferbert A., Priori A., Rothwell J.C., Day B.L., Colebatch J.G., Marsden C.D. Interhemispheric inhibition of the human motor cortex. J. Physiol. Lond. 1992, 453:525-546.
15. Funke K., Benali A. Modulation of cortical inhibition by rTMS - findings obtained from animal models. J. Physiol. 2011, 589(Pt 18):4423-4435.
16. Gonchar Y.A., Johnson P.B., Weinberg R.J. GABA-immunopositive neurons in rat neocortex with contralateral projections to S-I. Brain Res. 1995, 697(1-2):27-34.
17. Gross C.E., Boraud T., Guehl D., Bioulac B., Bezard E. From experimentation to the surgical treatment of Parkinson's disease: prelude or suite in basal ganglia research?. Prog. Neurobiol. 1999, 59(5):509-532.
18. Hamada M., Murase N., Hasan A., Balaratnam M., Rothwell J.C. The role of interneuron networks in driving human motor cortical plasticity. Cereb. Cortex 2013, 23(7):1593-1605.
19. Hao Z., Wang D., Zeng Y., Liu M. Repetitive transcranial magnetic stimulation for improving function after stroke. Cochrane Database Syst. Rev. 2013, 5:CD008862.
20. Harkany T., Mackie K., Doherty P. Wiring and firing neuronal networks: endocannabinoids take center stage. Curr. Opin. Neurobiol. 2008, 18(3):338-345.
21. Hashimotodani Y., Ohno-Shosaku T., Kano M. Endocannabinoids and synaptic function in the CNS. Neuroscientist 2007, 13(2):127-137.
22. Horikawa K., Armstrong W.E. A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J. Neurosci. Methods 1988, 25(1):1-11.
23. Huang Y.Z., Edwards M.J., Rounis E., Bhatia K.P., Rothwell J.C. Theta burst stimulation of the human motor cortex. Neuron 2005, 45(2):201-206.
24. B agonists on interhemispheric inhibition in man. Clin. Neurophysiol. 2007, 118(2):308-316.
25. Lan R., Liu Q., Fan P., Lin S., Fernando S.R., McCallion D., et al. Structure-activity relationships of pyrazole derivatives as cannabinoid receptor antagonists. J. Med. Chem. 1999, 42(4):769-776.
26. McGeorge A.J., Faull R.L.M. The organization and collateralization of corticostriate neurons in the motor and sensory cortex of the rat brain. Brain Res. 1987, 423(1-2):318-324.
27. McGeorge A.J., Faull R.L.M. The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 1989, 29(3):503-537.
28. McLaughlin P.J., Winston K., Swezey L., Wisniecki A., Aberman J., Tardif D.J., et al. The cannabinoid CB1 antagonists SR 141716A and AM 251 suppress food intake and food-reinforced behavior in a variety of tasks in rats. Behav. Pharmacol. 2003, 14(8):583-588.
29. Meehan S.K., Dao E., Linsdell M.A., Boyd L.A. Continuous theta burst stimulation over the contralesional sensory and motor cortex enhances motor learning post-stroke. Neurosci. Lett. 2011, 500(1):26-30.
30. Meyer B.-U., Röricht S., Woiciechowsky C. Topography of fibers in the human corpus callosum mediating interhemispheric inhibition between the motor cortices. Ann. Neurol. 1998, 43(3):360-369.
31. Muller-Dahlhaus J.F.M., Liu Y., Ziemann U. Inhibitory circuits and the nature of their interactions in the human motor cortex - a pharmacological TMS study. J. Physiol. Lond. 2008, 586(2):495-514.
32. Murase N., Duque J., Mazzocchio R., Cohen L.G. Influence of interhemispheric interactions on motor function in chronic stroke. Ann. Neurol. 2004, 55(3):400-409.
33. Nowak D.A., Grefkes C., Ameli M., Fink G.R. Interhemispheric competition after stroke: brain stimulation to enhance recovery of function of the affected hand. Neurorehabil. Neural Repair 2009, 23(7):641-656.
34. B-mediated interhemispheric inhibition. Science 2012, 335(6071):989-993.
35. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Academic Press, Sydney; Orlando. 6th ed.
36. Reiner A., Hart N.M., Lei W., Deng Y. Corticostriatal projection neurons - dichotomous types and dichotomous functions. Front. Neuroanat. 2010, 4:142.
37. Reynolds J.N.J., Hyland B.I., Wickens J.R. A cellular mechanism of reward-related learning. Nature 2001, 413(6851):67-70.
38. Schaar K., Brenneman M., Savitz S. Functional assessments in the rodent stroke model. Exp. Transl. Stroke Med. 2010, 2(1):13.
39. Schulz J.M., Redgrave P., Mehring C., Aertsen A., Clements K.M., Wickens J.R., et al. Short-latency activation of striatal spiny neurons via subcortical visual pathways. J. Neurosci. 2009, 29(19):6336-6347.
40. Schulz J.M., Oswald M.J., Reynolds J.N. Visual-induced excitation leads to firing pauses in striatal cholinergic interneurons. J. Neurosci. 2011, 31(31):11133-11143.
41. Sharples S.A., Kalmar J.M. Modulation of cortical excitability and interhemispheric inhibition prior to rhythmic unimanual contractions. J. Neurosci. Methods 2012, 210(2):178-186.
42. Suppa A., Ortu E., Zafar N., Deriu F., Paulus W., Berardelli A., et al. Theta burst stimulation induces after-effects on contralateral primary motor cortex excitability in humans. J. Physiol. 2008, 586(Pt 18):4489-4500.
43. Talelli P., Greenwood R.J., Rothwell J.C. Exploring theta burst stimulation as an intervention to improve motor recovery in chronic stroke. Clin. Neurophysiol. 2007, 118(2):333-342.
44. Talelli P., Wallace A., Dileone M., Hoad D., Cheeran B., Oliver R., et al. Theta burst stimulation in the rehabilitation of the upper limb: a semirandomized, placebo-controlled trial in chronic stroke patients. Neurorehabil. Neural Repair 2012, 26(8):976-987.
45. The European Stroke Organisation (ESO) Executive Committee and the ESO Writing Committee Guidelines for management of ischaemic stroke and transient ischaemic attack 2008. Cerebrovasc. Dis. 2008, 25(5):457-507.
46. Udupa K., Ni Z., Gunraj C., Chen R. Effect of long interval interhemispheric inhibition on intracortical inhibitory and facilitatory circuits. J. Physiol. Lond. 2010, 588(14):2633-2641.
47. Wilson C.J. Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J. Comp. Neurol. 1987, 263(4):567-580.
48. Wilson M.T., Goodwin D.P., Brownjohn P.W., Shemmell J., Reynolds J.N. Numerical modelling of plasticity induced by transcranial magnetic stimulation. J. Comput. Neurosci. 2014, 36(3):499-514.