Modulation of inhibitory activity markers by intermittent theta-burst stimulation in rat cortex is NMDA-receptor dependent

Brain Stimulation

Volumn 7, Issue 3, 2014, Pages 394-400

  Labedi, Adnan ^a,b   Benali, Alia ^a,c   Mix, Annika ^a   Neubacher, Ute ^a   Funke, Klaus ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b ST JOSEF HOSPITAL   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

c Fos; Calcium binding proteins; GAD67; Inhibitory systems; Neocortex

Indexed keywords

BIOLOGICAL MARKER; CALBINDIN; GLUTAMATE DECARBOXYLASE 67; KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PARVALBUMIN; RECEPTOR SUBTYPE; URETHAN; AMPA RECEPTOR; GLUTAMATE DECARBOXYLASE; ISOPROTEIN; N METHYLASPARTIC ACID;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEPTH STIMULATION; CELL TYPE; IMMUNOHISTOCHEMISTRY; INTERNEURON; NERVE CELL; NEUROMODULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION; ANIMAL; FRONTAL LOBE; HUMAN; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; CALBINDINS; CEREBRAL CORTEX; FRONTAL LOBE; GLUTAMATE DECARBOXYLASE; HUMANS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; N-METHYLASPARTATE; NEURONS; PARVALBUMINS; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84899930869     PISSN: 1935861X     EISSN: 18764754     Source Type: Journal    
DOI: 10.1016/j.brs.2014.02.010     Document Type: Article

References (63)

1. G.W. Thickbroom Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models Exp Brain Res 180 2007 583 593
2. U. Ziemann, B. Corwell, and L.G. Cohen Modulation of plasticity in human motor cortex after forearm ischemic nerve block J Neurosci 18 1998 1115 1123
3. M.B. Iyer, N. Schleper, and E.M. Wassermann Priming stimulation enhances the depressant effect of low-frequency repetitive transcranial magnetic stimulation J Neurosci 23 2003 10867 10872
4. N. Lang, H.R. Siebner, and D. Ernst et al. Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction of after-effects Biol Psychiatry 56 2004 634 639
5. H.R. Siebner, N. Lang, and V. Rizzo et al. Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex J Neurosci 24 2004 3379 3385
6. R. Gentner, K. Wankerl, C. Reinsberger, D. Zeller, and J. Classen Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity Cereb Cortex 18 2008 2046 2053
7. T. Tsumoto Long-term potentiation and long-term depression in the neocortex Prog Neurobiol 39 1992 209 228
8. T.V. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 1993 31 39
9. P.B. Fitzgerald, S. Fountain, and Z.J. Daskalakis A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition Clin Neurophysiol 117 2006 2584 2596
10. Y.Z. Huang, M.J. Edwards, E. Rounis, K.P. Bhatia, and J.C. Rothwell Theta burst stimulation of the human motor cortex Neuron 45 2005 201 206
11. M.C. Ridding, and U. Ziemann Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects J Physiol 588 2010 2291 2304
12. H.R. Siebner A primer on priming the human motor cortex Clin Neurophysiol 121 2010 461 463
13. Y.Z. Huang, R.S. Chen, J.C. Rothwell, and H.Y. Wen The after-effect of human theta burst stimulation is NMDA receptor dependent Clin Neurophysiol 118 2007 1028 1032
14. J.T. Teo, O.B. Swayne, and J.C. Rothwell Further evidence for NMDA-dependence of the after-effects of human theta burst stimulation Clin Neurophysiol 118 2007 1649 1651
15. R. Dingledine, K. Borges, D. Bowie, and S.F. Traynelis The glutamate receptor ion channels Pharmacol Rev 51 1999 7 61
16. P. Schwenkreis, K. Witscher, B. Pleger, J.P. Malin, and M. Tegenthoff The NMDA antagonist memantine affects training induced motor cortex plasticity - a study using transcranial magnetic stimulation BMC Neurosci 6 2005 35
17. J. Trippe, A. Mix, S. Aydin-Abidin, K. Funke, and A. Benali Theta burst and conventional low-frequency rTMS differentially affect GABAergic neurotransmission in the rat cortex Exp Brain Res 199 2009 411 421
18. J. Wei, and J.Y. Wu Post-translational regulation of L-glutamic acid decarboxylase in the brain Neurochem Res 33 2008 1459 1465
19. Y. Kawaguchi, and Y. Kubota Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin and calbindin D28k immunoreactive neurons in layer V of rat frontal cortex J Neurophysiol 70 1993 387 396
20. H. Markram, M. Toledo-Rodriguez, Y. Wang, A. Gupta, G. Silberberg, and C. Wu Interneurons of the neocortical inhibitory system Nat Rev Neurosci 5 2004 793 807
21. A. Benali, J. Trippe, and E. Weiler et al. Theta-burst transcranial magnetic stimulation alters cortical inhibition J Neurosci 31 2011 1193 1203
22. A. Mix, A. Benali, and K. Funke Strain differences in the effect of rTMS on cortical expression of calcium binding proteins in rats Exp Brain Res 232 2014 435 442 http://dx.doi.org/10.1007/s00221-013-3751-6
23. L.J. Volz, A. Benali, A. Mix, U. Neubacher, and K. Funke Dose-dependence of changes in cortical protein expression induced with repeated transcranial magnetic theta-burst stimulation in the rat Brain Stimul 6 2013 598 606
24. K. Hoppenrath, and K. Funke Time-course of changes in neuronal activity markers following iTBS-TMS of the rat neocortex Neurosci Lett 536 2013 19 23
25. S. Patz, J. Grabert, T. Gorba, M.J. Wirth, and P. Wahle Parvalbumin expression in visual cortical interneurons depends on neuronal activity and TrkB ligands during an early period of postnatal development Cereb Cortex 14 2004 342 351
26. R. Bender, M.C. Hoffmann, M. Frotscher, and C. Nitsch Species-specific expression of parvalbumin in the entorhinal cortex of the Mongolian gerbil: dependence on local activity but not extrinsic afferents Neuroscience 99 2000 423 431
27. B. Schwaller The continuing disappearance of "pure" Ca2+ buffers Cell Mol Life Sci 66 2009 275 300
28. S. Chaudhury, T.C. Nag, and S. Wadhwa Calbindin D-28K and parvalbumin expression in embryonic chick hippocampus is enhanced by prenatal auditory stimulation Brain Res 1191 2008 96 106
29. M.M. Behrens, S.S. Ali, D.N. Dao, J. Lucero, G. Shekhtman, and K.L. Quick et al. Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase Science 318 2007 1645 1647
30. D.A. Lewis, T. Hashimoto, and D.W. Volk Cortical inhibitory interneurons and schizophrenia Trends Neurosci 6 2005 312 324
31. T. Sakai, A. Oshima, and Y. Nozaki et al. Changes in density of calcium-binding-protein-immunoreactive GABAergic neurons in prefrontal cortex in schizophrenia and bipolar disorder Neuropathology 28 2008 143 150
32. J.H. Krystal, L.P. Karper, and J.P. Seibyl et al. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans Arch Gen Psychiatry 51 3 1994 199 214
33. J.W. Olney, and N.B. Farber Glutamate receptor dysfunction and schizophrenia Arch Gen Psychiatry 52 12 1995 998 1007
34. J.T. Kantrowitz, and D.C. Javitt N-methyl-D-aspartate (NMDA) receptor dysfunction or dysregulation: the final common pathway on the road to schizophrenia? Brain Res Bull 83 2010 108 121
35. J.A. Pratt, C. Winchester, A. Egerton, S.M. Cochran, and B.J. Morris Modelling prefrontal cortex deficits in schizophrenia: implications for treatment Br J Pharmacol 153 2008 465 470
36. G. Keilhoff, A. Becker, G. Grecksch, G. Wolf, and H.G. Bernstein Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS similar to those found in human schizophrenia Neuroscience 126 2004 591 598
37. J.W. Kinney, C.N. Davis, I. Tabarean, B. Conti, T. Bartfai, and M.M. Behrens A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons J Neurosci 26 2006 1604 1615
38. T. Hakami, N.C. Jones, and E.A. Tolmacheva et al. NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness PLoS One 4 2009 e6755
39. D. Pinault N-methyl-d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex Biol Psychiatry 63 2008 730 735
40. L.E. Hong, A. Summerfelt, and R.W. Buchanan et al. Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine Neuropsychopharmacology 35 2009 632 640
41. J.S. Kwon, B.F. O'Donnel, and G.V. Wallenstein et al. Gamma frequency-range abnormalities to auditory stimulation in schizophrenia Arch Gen Psychiatry 56 1999 1001 1005
42. D. Vierling-Claassen, P. Siekmeier, S. Stufflebeam, and N. Kopell Modeling GABA alterations in schizophrenia: a link between impaired inhibition and altered gamma and beta range auditory entrainment J Neurophysiol 99 2008 2656 2671
43. J.A. Cardin, M. Carlén, and K. Meletis et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses Nature 459 2009 663 668
44. M. Carlén, K. Meletis, and J.H. Siegle et al. A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior Mol Psychiatry 17 5 2012 537 548
45. G. Gonzalez-Burgos, and D.A. Lewis NMDA receptor hypofunction, parvalbumin-positive neurons, and cortical gamma oscillations in schizophrenia Schizophr Bull 38 2012 950 957
46. A. Breier, A.K. Malhotra, D.A. Pinals, N.I. Weisenfeld, and D. Pickar Association of ketamine-induced psychosis with focal activation of the prefrontal cortex in healthy volunteers Am J Psychiatry 154 1997 805 811
47. H. Homayoun, and B. Moghaddam NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons J Neurosci 27 43 2007 11496 11500
48. J. Michaluk, L. Antkiewicz-Michaluk, and J. Vetulani Conditions of application of repeated transcranial magnetic stimulation to rats may mask the effects of the treatment Pol J Pharmacol 53 2001 685 687
49. J.D. Weissman, C.M. Epstein, and K.R. Davey Magnetic brain stimulation and brain size: relevance to animal studies Electroencephalogr Clin Neurophysiol 85 1992 215 219
50. A. Mix, A. Benali, U.T. Eysel, and K. Funke Continuous and intermittent transcranial magnetic theta-burst stimulation differently modify tactile learning performance and cortical protein expression in the rat Eur J Neurosci 32 2010 1575 1586
51. B.K. Bitanihirwe, M.P. Lim, J.F. Kelley, T. Kaneko, and T.U. Woo Glutamatergic deficits and parvalbumin-containing inhibitory neurons in the prefrontal cortex in schizophrenia BMC Psychiatry 9 2009 71
52. J.W. Olney, J.W. Newcomer, and N.B. Farber NMDA receptor hypofunction model of schizophrenia J Psychiatr Res 33 1999 523 533
53. J.F. Staiger, W. Zuschratter, H.J. Luhmann, and D. Schubert Local circuits targeting parvalbumin-containing interneurons in layer IV of rat barrel cortex Brain Struct Funct 214 2009 1 13
54. D. Orduz, D.P. Bischop, B. Schwaller, S.N. Schiffmann, and D. Gall Parvalbumin tunes spike-timing and efferent short-term plasticity in striatal fast spiking interneurons J Physiol 591 2013 3215 3232
55. D.M. Kullmann, and K.P. Lamsa LTP and LTD in cortical GABAergic interneurons: emerging rules and roles Neuropharmacology 60 2011 712 719
56. K. Funke, and A. Benali Modulation of cortical inhibition by rTMS - findings obtained from animal models J Physiol 589 2011 4423 4435
57. A. Obenaus, M. Esclapez, and C.R. Houser Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures J Neurosci 13 1993 4470 4485
58. C.E. Ribak, R.M. Bradburne, and A.B. Harris A preferential loss of GABAergic, symmetric synapses in epileptic foci: a quantitative ultrastructural analysis of monkey neocortex J Neurosci 2 1982 1725 1735
59. R. Kuruba, B. Hattiangady, V.K. Parihar, B. Shuai, and A.K. Shetty Differential susceptibility of interneurons expressing neuropeptide Y or parvalbumin in the aged hippocampus to acute seizure activity PLoS One 6 2011 e24493
60. C. Gavrilovici, E. Pollock, M. Everest, and M.O. Poulter The loss of interneuron functional diversity in the piriform cortex after induction of experimental epilepsy Neurobiol Dis 48 2012 317 328
61. K. Hara, and R.A. Harris The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels Anesth Analg 94 2002 313 318
62. A. Bacci, J.R. Huguenard, and D.A. Prince Modulation of neocortical interneurons: extrinsic influences and exercises in self-control Trends Neurosci 28 2005 602 610
63. D.S. Melchitzky, and D.A. Lewis Pyramidal neuron local axon terminals in monkey prefrontal cortex: differential targeting of subclasses of GABA neurons Cereb Cortex 13 2003 452 460