Theta-burst transcranial magnetic stimulation alters cortical inhibition

Journal of Neuroscience

Volumn 31, Issue 4, 2011, Pages 1193-1203

  Benali, Alia ^a,b   Trippe, Jörn ^a   Weiler, Elke ^a   Mix, Annika ^a   Petrasch Parwez, Elisabeth ^a   Girzalsky, Wolfgang ^a   Eysel, Ulf T ^a   Erdmann, Ralf ^a   Funke, Klaus ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALBINDIN; CALRETININ; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; ELECTRIC ACTIVITY; ELECTROENCEPHALOGRAPHY; EVOKED SOMATOSENSORY RESPONSE; INTEGRATION; INTERNEURON; MALE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 79251590532     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1379-10.2011     Document Type: Article

References (76)

1. Allen EA, Pasley BN, Duong T, Freeman RD (2007) Transcranial magnetic stimulation elicits coupled neural and hemodynamic consequences. Science 317:1918-1921.
2. Allison T (1962) Recovery functions of somatosensory evoked responses in man. Electroencephalogr Clin Neurophysiol 14:331-343.
3. Aydin-Abidin S, Trippe J, Funke K, Eysel UT, Benali A (2008) High- and low-frequency repetitive transcranial magnetic stimulation differentially activates c-fos and zif268 protein expression in the rat brain. Exp Brain Res 188:249-261.
4. Baumgärtel K, Tweedie-Cullen RY, Grossmann J, Gehrig P, Livingstone- Zatchej M, Mansuy IM (2009) Changes in the proteome after neuronal zif268 overexpression. J Proteome Res 8:3298-3316.
5. Beaulieu C (1993) Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res 609:284-292.
6. Benali A, Leefken I, Eysel UT, Weiler E (2003) A computerized image analysis system for quantitative analysis of cells in histological brain sections. J Neurosci Methods 125:33-43. (Pubitemid 36579330)
7. Bender R, Hoffmann MC, Frotscher M, Nitsch C (2000) Species-specific expression of parvalbumin in the entorhinal cortex of the Mongolian gerbil: dependence on local activity but not extrinsic afferents. Neuroscience 99:423-431.
8. Blatow M, Rozov A, Katona I, Hormuzdi SG, Meyer AH, Whittington MA, Caputi A, Monyer H (2003) A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 38:805-817.
9. Caillard O, Moreno H, Schwaller B, Llano I, Celio MR, Marty A (2000) Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc Natl Acad Sci U S A 97:13372-13377.
10. Cardin JA Carlén M, Meletis K Knoblich U, Zhang F Deisseroth K, Tsai LH Moore CI (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663-667.
11. Chaudhury S, Nag TC, Wadhwa S (2008) Calbindin D-28K and parvalbumin expression in embryonic chick hippocampus is enhanced by prenatal auditory stimulation. Brain Res 1191:96-106.
12. Cho RY, Konecky RO, Carter CS (2006) Impairments in frontal cortical synchrony and cognitive control in schizophrenia. Proc Natl Acad Sci U S A 103:19878-19883.
13. Clement EA, Richard A, Thwaites M, Ailon J, Peters S, Dickson CT (2008) Cyclic and sleep-like spontaneous alternations of brain state under urethane anaesthesia. PLoS One 3:e2004.
14. Di Lazzaro V, Pilato F, Saturno E, Oliviero A, Dileone M, Mazzone P, Insola A, Tonali PA, Ranieri F, Huang YZ, Rothwell JC (2005) Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol 565:945-950.
15. Di Lazzaro V, Pilato F, Dileone M, Profice P, Oliviero A, Mazzone P, Insola A, Ranieri F, Meglio M, Tonali PA, Rothwell JC (2008) The physiological basis of the effects of intermittent theta burst stimulation of the human motor cortex. J Physiol 586:3871-3879.
16. Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76-88.
17. Farzan F, Barr MS, Levinson AJ, Chen R, Wong W, Fitzgerald PB, Daskalakis ZJ (2010) Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia. Brain 133:1505-1514.
18. Fitzgerald PB, Fountain S, Daskalakis ZJ (2006) A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol 117:2584-2596.
19. Freund TF (2003) Interneuron diversity series: Rhythm and mood in perisomatic inhibition. Trends Neurosci 28:489-495.
20. Funke K, Benali A (2009) Short-latency afferent inhibition varies with cortical state in rat somatosensory cortex. Neuroreport 20:1313-1318.
21. Griffiths R, Norman RI (1993) Effects of anaesthetics on uptake, synthesis and release of transmitters. Br J Anaesth 71:96-107.
22. Hakami T, Jones NC, Tolmacheva EA, Gaudias J, Chaumont J, Salzberg M, O'Brien TJ, Pinault D (2009) NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness. PLoS One 4:e6755.
23. Hara K, Harris A (2002) The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anaesth Pharmacol 94:313-318.
24. Härtig W, Brauer K, Brückner G (1992) Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. Neuroreport 3:869-872.
25. Hartmann M, Heumann R, Lessmann V (2002) Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 20:5887-5897.
26. Hiscock JJ, Mackenzie L, Willoughby JO (1998) Laminar distribution of Fos/calcium-binding protein and Fos/neurofilament protein-labeled neurons in rat motor and sensory cortex after picrotoxin-induced seizures. Exp Neurol 149:373-383.
27. Hong LE, Summerfelt A, Buchanan RW, O'Donnell P, Thaker GK, Weiler MA, Lahti AC (2010) Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine. Neuropsychopharmacology 35:632-640.
28. Hoshiyama M, Kakigi R (2003) Changes in somatosensory evoked responses by repetition of the median nerve stimulation. Clin Neurophysiol 114:2251-2257. (Pubitemid 37494923)
29. Howard A, Tamas G, Soltesz I (2005) Lighting the chandelier: new vistas for axo-axonic cells. Trends Neurosci 28:310-316. (Pubitemid 40775776)
30. Huang YZ, Edwards MJ, Rounis E, Bhatia KP Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201-206. (Pubitemid 40128115)
31. Jiang B, Kitamura A, Yasuda H, Sohya K, Maruyama A, Yanagawa Y, Obata K, Tsumoto T (2004) Brain-derived neurotrophic factor acutely depresses excitatory synaptic transmission to GABAergic neurons in visual cortical slices. Eur J Neurosci 20:709-718.
32. Kawaguchi Y, Kubota Y (1998) Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85:677-701. (Pubitemid 28223633)
33. Krieg WJ (1946) Cortical areas of the albino rat. Arch Neurol Psych 56:739.
34. Kullmann DM, Lamsa KP (2007) Long-term synaptic plasticity in hippocampal interneurons. Nat Rev Neurosci 8:687-699. (Pubitemid 47283146)
35. Kwon JS, O'Donnell BF, Wallenstein GV, Greene RW, Hirayasu Y, Nestor PG, Hasselmo ME, Potts GF, Shenton ME, McCarley RW (1999) Gammafrequency-range abnormalities to auditory stimulation in schizophrenia. Arch Gen Psychiatry 56:1001-1005.
36. Lamsa K, Taira T (2003) Use-dependent shift from inhibitory to excitatory GABAA receptor action in SP-O interneurons in the rat hippocampal CA3 area. J Neurophysiol 90:1983-1995. (Pubitemid 37129402)
37. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory interneurons and schizophrenia. Trends Neurosci 6:312-324.
38. Lodge DJ, Behrens MM, Grace AA (2009) A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci 29:2344-2354.
39. Lu JT, Li CY, Zhao JP, Poo MM, Zhang XH (2007) Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type. J Neurosci 27:9711-9720.
40. Maccabee PJ, Amassian VE, Eberle LP, Cracco RQ (1993) Magnetic coil stimulation of straight and bent amphibian and mammalian peripheral nerve in vitro: locus of excitation. J Physiol Lond 460:201-219.
41. Mainardi M, Landi S, Berardi N, Maffei L, Pizzorusso T (2009) Reduced responsiveness to long-term monocular deprivation of parvalbumin neurons assessed by c-Fos staining in rat visual cortex. PLoS One 4:e4342.
42. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
43. Michaluk J, Antkiewicz-Michaluk L, Vetulani J (2001) Conditions of application of repeated transcranial magnetic stimulation to rats may mask the effects of the treatment. Pol J Pharmacol 53:685-687. (Pubitemid 34065779)
44. Minchin MC (1981) The effect of anaesthetics on the uptake and release of gamma-aminobutyrate and D-aspartate in rat brain slices. Br J Pharmacol 73:681-689. (Pubitemid 11067905)
45. Mix A, Benali A, Eysel UT, Funke K (2010) Continuous and intermittent transcranial magnetic theta burst stimulation modify tactile learning performance and cortical protein expression in the rat differently. Eur J Neurosci 32:1575-1586.
46. Moliadze V, Zhao Y, Eysel U, Funke K (2003) Effect of transcranial magnetic stimulation on single-unit activity in the cat primary visual cortex. J Physiol 553:665-679. (Pubitemid 37527562)
47. Morris BJ, Cochran SM, Pratt JA (2005) PCP: from pharmacology to modelling schizophrenia. Curr Opin Pharmacol 5:101-106.
48. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. San Diego: Academic.
49. Petrasch-Parwez E, Nguyen HP, Löbbecke-Schumacher M, Habbes HW, Wieczorek S, Riess O, Andres KH, Dermietzel R, Von Hörsten S (2007) Cellular and subcellular localization of Huntingtin aggregates in the brain of a rat transgenic for Huntington disease. J Comp Neurol 501:716-730.
50. Petrasch-Parwez E, Habbes HW, Weickert S, Löbbecke-Schumacher M, Striedinger K, Wieczorek S, Dermietzel R, Epplen JT (2004) Fine-structural analysis and connexin expression in the retina of a transgenic model of Huntington's disease. J Comp Neurol 479:181-197.
51. Pratt JA, Winchester C, Egerton A, Cochran SM, Morris BJ (2008) Modelling prefrontal cortex deficits in schizophrenia: implications for treatment. Br J Pharmacol 153:S465-S470.
52. Ragert P, Becker M, Tegenthoff M, Pleger B, Dinse HR (2004) Sustained increase of somatosensory cortex excitability by 5 Hz repetitive transcranial magnetic stimulation studied by paired median nerve stimulation in humans. Neurosci Lett 356:91-94.
53. Roopun AK, Cunningham MO, Racca C, Alter K, Traub RD, Whittington MA (2008) Region-specific changes in gamma and beta2 rhythms in NMDA receptor dysfunction models of schizophrenia. Schizophr Bull 34:962-973.
54. Rotem A, Moses E (2006) Magnetic stimulation of curved nerves. IEEE Trans Biomed Eng 53:414-420.
55. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531:807-826.
56. Sakai T, Oshima A, Nozaki Y, Ida I, Haga C, Akiyama H, Nakazato Y, Mikuni M (2008) Changes in density of calcium-binding-protein-immunoreactive GABAergic neurons in prefrontal cortex in schizophrenia and bipolar disorder. Neuropathology 28:143-150.
57. 2+-buffers. Cell Mol Life Sci 66:275-300.
58. Schwaller B, Dick J, Dhoot G, Carroll S, Vrbova G, Nicotera P, Pette D, Wyss A, Bluethmann H, Hunziker W, Celio MR (1999) Prolonged contraction- relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. Am J Physiol 276:C395-403.
59. Sinclair MD (2003) A review of the physiological effects of alpha2-agonists related to the clinical use of medetomidine in small animal practice. Can Vet J 44:885-897.
60. Skoglund TS, Pascher R, Berthold CH (1997) The existence of a layer IV in the rat motor cortex. Cereb Cortex 7:178-180.
61. Stagg CJ, Wylezinska M, Matthews PM, Johansen-Berg H, Jezzard P, Rothwell JC, Bestmann S (2009) Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J Neurophysiol 101:2872-2877.
62. Sun QQ (2009) Experience-dependent intrinsic plasticity in interneurons of barrel cortex layer IV. J Neurophysiol 102:2955-2973.
63. Thickbroom GW (2007) Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp Brain Res 180:583-593.
64. Tokimura H, Di Lazzaro V, Tokimura Y, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (2000) Short latency inhibition of human hand motor cortex by somatosensory input from the hand. J Physiol 523:503-513.
65. Trippe J, Mix A, Aydin-Abidin S, Funke K, Benali A (2009) Theta burst and conventional low frequency rTMS differentially affect GABAergic neuro-transmission in the rat cortex. Exp Brain Res 199:411-421.
66. Tropea D, Kreiman G, Lyckman A, Mukherjee S, Yu H, Horng S, Sur M (2006) Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex. Nat Neurosci 9:660-668.
67. Tsumoto T (1992) Long-term potentiation and long-term depression in the neocortex. Prog Neurobiol 39:209-228.
68. van Brederode JF, Helliesen MK, Hendrickson AE (1991) Distribution of the calcium-binding proteins parvalbumin and calbindin-D28k in the sensorimotor cortex of the rat. Neuroscience 44:157-171.
69. Vierling-Claassen D, Siekmeier P, Stufflebeam S, Kopell N (2008) Modeling GABA alterations in schizophrenia: a link between impaired inhibition and altered gamma and beta range auditory entrainment. J Neurophysiol 99:2656-2671.
70. Vreugdenhil M, Jefferys JG, Celio MR, Schwaller B (2003) Parvalbumin-deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus. J Neurophysiol 89:1414-1422.
71. Weiler E, Benali A (2005) Olfactory epithelia differentially express neuronal markers. J Neurocytol 34:217-240.
72. Weiser M, Bueno E, Sekirnjak C, Martone ME, Baker H, Hillman D, Chen S, Thornhill W, Ellisman M, Rudy B (1995) The potassium channel sub-unit Kv3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons. J Neurosci 15:4298-4314.
73. Weissman JD, Epstein CM, Davey KR (1992) Magnetic brain stimulation and brain size: relevance to animal studies. Electroencephalogr Clin Neurophysiol 85:215-219.
74. Winsky L, Kuźnicki J (1996) Antibody recognition of calcium-binding proteins depends on their calcium-binding status. J Neurochem 66:764-771. (Pubitemid 126578436)
75. Zilles K (1985) The cortex of the rat - a stereotaxic atlas. Berlin: Springer.
76. Zilles K, Wree A (1995) Cortex: areal and laminar structure. In: The rat nervous system (Paxinos G, ed), pp 649-685. San Diego: Academic.