Intermittent theta-burst stimulation rescues dopamine-dependent corticostriatal synaptic plasticity and motor behavior in experimental parkinsonism: Possible role of glial activity

Movement Disorders

Volumn 32, Issue 7, 2017, Pages 1035-1046

  Cacace, Fabrizio ^a   Mineo, Desirèe ^a   Viscomi, Maria Teresa ^a   Latagliata, Emanuele Claudio ^a   Mancini, Maria ^a   Sasso, Valeria ^a   Vannelli, Anna ^a   Pascucci, Tiziana ^a,b   Pendolino, Valentina ^a   Marcello, Elena ^c   Pelucchi, Silvia ^c   Puglisi Allegra, Stefano ^a,b   Molinari, Marco ^a   Picconi, Barbara ^a   Calabresi, Paolo ^d   Ghiglieri, Veronica ^a,d  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF PERUGIA   (Italy)

Author keywords

corticostriatal synaptic plasticity; glia; long term potentiation; Parkinson's disease; transcranial magnetic stimulation

Indexed keywords

DOPAMINE; OXIDOPAMINE; ADRENERGIC RECEPTOR STIMULATING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL PARKINSONISM; GLIA CELL; IMMEDIATE EARLY GENE; IN VITRO STUDY; LOCOMOTION; MALE; MICRODIALYSIS; NERVE CELL; NERVE CELL PLASTICITY; NERVE STIMULATION; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; THETA RHYTHM; WHOLE CELL PATCH CLAMP; ANIMAL; ANIMAL BEHAVIOR; ASTROCYTE; BRAIN CORTEX; CHEMICALLY INDUCED; CORPUS STRIATUM; METABOLISM; MICROGLIA; MOTOR ACTIVITY; PARKINSONISM; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; TRANSCRANIAL MAGNETIC STIMULATION; WISTAR RAT;

ADRENERGIC AGENTS; ANIMALS; ASTROCYTES; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; CORPUS STRIATUM; DOPAMINE; GENES, IMMEDIATE-EARLY; MALE; MICRODIALYSIS; MICROGLIA; MOTOR ACTIVITY; NEURONAL PLASTICITY; OXIDOPAMINE; PARKINSONIAN DISORDERS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 85017430822     PISSN: 08853185     EISSN: 15318257     Source Type: Journal    
DOI: 10.1002/mds.26982     Document Type: Article

References (41)

1. Hirsch EC, Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol 2009;8(4):382-397.
2. Barcia C. Glial-mediated inflammation underlying parkinsonism. Scientifica (Cairo) 2013;2013:357805.
3. Collins LM, Toulouse A, Connor TJ, Nolan YM. Contributions of central and systemic inflammation to the pathophysiology of Parkinson's disease. Neuropharmacology 2012;62(7):2154-2168.
4. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, Safety of TMSCG. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009;120(12):2008-2039.
5. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron 2005;45(2):201-206.
6. Benninger DH, Berman BD, Houdayer E, et al. Intermittent theta-burst transcranial magnetic stimulation for treatment of Parkinson disease. Neurology; 76(7):601-609.
7. Suppa A, Marsili L, Belvisi D, et al. Lack of LTP-like plasticity in primary motor cortex in Parkinson's disease. Exp Neurol; 227(2):296-301.
8. Trippe J, Mix A, Aydin-Abidin S, Funke K, Benali A. Theta burst and conventional low-frequency rTMS differentially affect GABAergic neurotransmission in the rat cortex. Exp Brain Res 2009;199(3-4):411-421.
9. Benali A, Trippe J, Weiler E, et al. Theta-burst transcranial magnetic stimulation alters cortical inhibition. J Neurosci 2011;31(4):1193-1203.
10. Calabresi P, Pisani A, Rothwell J, Ghiglieri V, Obeso JA, Picconi B. Hyperkinetic disorders and loss of synaptic downscaling. Nat Neurosci 2016;19(7):868-875.
11. Picconi B, Centonze D, Hakansson K, et al. Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat Neurosci 2003;6(5):501-506.
12. Strafella AP, Paus T, Fraraccio M, Dagher A. Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain 2003;126(Pt 12):2609-2615.
13. Khedr EM, Rothwell JC, Shawky OA, Ahmed MA, Foly N, Hamdy A. Dopamine levels after repetitive transcranial magnetic stimulation of motor cortex in patients with Parkinson's disease: preliminary results. Mov Disord 2007;22(7):1046-1050.
14. Keck ME, Welt T, Muller MB, et al. Repetitive transcranial magnetic stimulation increases the release of dopamine in the mesolimbic and mesostriatal system. Neuropharmacology 2002;43(1):101-109.
15. Kanno M, Matsumoto M, Togashi H, Yoshioka M, Mano Y. Effects of acute repetitive transcranial magnetic stimulation on dopamine release in the rat dorsolateral striatum. J Neurol Sci 2004;217(1):73-81.
16. Bagetta V, Sgobio C, Pendolino V, et al. Rebalance of striatal NMDA/AMPA receptor ratio underlies the reduced emergence of dyskinesia during D2-like dopamine agonist treatment in experimental Parkinson's disease. J Neurosci 2012;32(49):17921-17931.
17. Ghiglieri V, Pendolino V, Sgobio C, Bagetta V, Picconi B, Calabresi P. Theta-burst stimulation and striatal plasticity in experimental parkinsonism. Exp Neurol 2012;236(2):395-398.
18. Paille V, Picconi B, Bagetta V, et al. Distinct levels of dopamine denervation differentially alter striatal synaptic plasticity and NMDA receptor subunit composition. J Neurosci 2010;30(42):14182-14193.
19. Koopmans GC, Deumens R, Honig WM, Hamers FP, Steinbusch HW, Joosten EA. The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination. J Neurotrauma 2005;22(2):214-225.
20. Pascucci T, Ventura R, Latagliata EC, Cabib S, Puglisi-Allegra S. The medial prefrontal cortex determines the accumbens dopamine response to stress through the opposing influences of norepinephrine and dopamine. Cereb Cortex 2007;17(12):2796-2804.
21. Westerink BH, Enrico P, Feimann J, De Vries JB. The pharmacology of mesocortical dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and prefrontal cortex of the rat brain. J Pharmacol Exp Ther 1998;285(1):143-154.
22. Cerovic M, Bagetta V, Pendolino V, et al. Derangement of Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) and extracellular signal-regulated kinase (ERK) dependent striatal plasticity in L-DOPA-induced dyskinesia. Biol Psychiatry 2015;77(2):106-115.
23. Calabresi P, Pisani A, Mercuri NB, Bernardi G. Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels. Eur J Neurosci 1992;4(10):929-935.
24. Calabresi P, Maj R, Pisani A, Mercuri NB, Bernardi G. Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 1992;12(11):4224-4233.
25. Sasso V, Bisicchia E, Latini L, et al. Repetitive transcranial magnetic stimulation reduces remote apoptotic cell death and inflammation after focal brain injury. J Neuroinflammation 2016;13(1):150.
26. Zangen A, Hyodo K. Transcranial magnetic stimulation induces increases in extracellular levels of dopamine and glutamate in the nucleus accumbens. Neuroreport 2002;13(18):2401-2405.
27. Cho SS, Strafella AP. rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS One 2009;4(8):e6725.
28. Strafella AP, Paus T, Barrett J, Dagher A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci 2001;21(15):RC157.
29. Cardenas-Morales L, Volz LJ, Michely J, et al. Network connectivity and individual responses to brain stimulation in the human motor system. Cereb Cortex 2014;24(7):1697-1707.
30. Wang Z, Kai L, Day M, et al. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 2006;50(3):443-452.
31. Yin HH, Davis MI, Ronesi JA, Lovinger DM. The role of protein synthesis in striatal long-term depression. J Neurosci 2006;26(46):11811-11820.
32. Benali A, Trippe J, Weiler E, et al. Theta-burst transcranial magnetic stimulation alters cortical inhibition. J Neurosci 2011;31(4):1193-1203.
33. Cullen CL, Young KM. How does transcranial magnetic stimulation influence glial cells in the central nervous system? Front Neural Circuits 2016;10:26.
34. Cicchetti F, Brownell AL, Williams K, Chen YI, Livni E, Isacson O. Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur J Neurosci 2002;15(6):991-998.
35. McGeer PL, McGeer EG. Glial cell reactions in neurodegenerative diseases: pathophysiology and therapeutic interventions. Alzheimer Dis Assoc Disord 1998;12(suppl 2):S1-S6.
36. McGeer PL, Schwab C, Parent A, Doudet D. Presence of reactive microglia in monkey substantia nigra years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine administration. Ann Neurol 2003;54(5):599-604.
37. Orr CF, Rowe DB, Mizuno Y, Mori H, Halliday GM. A possible role for humoral immunity in the pathogenesis of Parkinson's disease. Brain 2005;128(Pt 11):2665-2674.
38. Inyushin MY, Huertas A, Kucheryavykh YV, et al. L-DOPA uptake in astrocytic endfeet enwrapping blood vessels in rat brain. Parkinsons Dis 2012;2012:321406.
39. Oliva I, Fernandez M, Martin ED. Dopamine release regulation by astrocytes during cerebral ischemia. Neurobiol Dis 2013;58:231-241.
40. Tsai MJ, Lee EH. Characterization of L-DOPA transport in cultured rat and mouse astrocytes. J Neurosci Res 1996;43(4):490-495.
41. Asanuma M, Miyazaki I, Murakami S, Diaz-Corrales FJ, Ogawa N. Striatal astrocytes act as a reservoir for L-DOPA. PLoS One 2014;9(9):e106362.