Vagus nerve stimulation has antidepressant effects in the kainic acid model for temporal lobe epilepsy

Brain Stimulation

Volumn 8, Issue 1, 2015, Pages 13-20

  Grimonprez, Annelies ^a   Raedt, Robrecht ^a   Dauwe, Ine ^a   Mollet, Lies ^a   Larsen, Lars Emil ^a   Meurs, Alfred ^a   De Herdt, Veerle ^a   Wadman, Wytse ^b   Delbeke, Jean ^a   Vonck, Kristl ^a   Boon, Paul ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Anhedonia; Depression; Kainic acid model; Temporal lobe epilepsy; Vagus nerve stimulation

Indexed keywords

KAINIC ACID; QUININE; SACCHARIN; SODIUM CHLORIDE; WATER;

ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVERSION; CONTROLLED STUDY; EPILEPTIC STATE; EXPERIMENTAL BEHAVIORAL TEST; EXPERIMENTAL EPILEPSY; FLUID INTAKE; MAJOR DEPRESSION; MALE; NONHUMAN; PSYCHOTHERAPY; QUININE AVERSION TEST; RAT; RAT MODEL; SACCHARIN PREFERENCE TEST; SHAM PROCEDURE; TASTE; TEMPORAL LOBE EPILEPSY; VAGUS NERVE STIMULATION; ANIMAL; CHEMICALLY INDUCED; COMPLICATION; DECISION MAKING; DEPRESSIVE DISORDER, MAJOR; DISEASE MODEL; EPILEPSY, TEMPORAL LOBE; STATUS EPILEPTICUS;

RATTUS;

ANHEDONIA; ANIMALS; CHOICE BEHAVIOR; DEPRESSIVE DISORDER, MAJOR; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; KAINIC ACID; MALE; RATS; STATUS EPILEPTICUS; VAGUS NERVE STIMULATION;

EID: 84919625092     PISSN: 1935861X     EISSN: 18764754     Source Type: Journal    
DOI: 10.1016/j.brs.2014.09.013     Document Type: Article

References (136)

1. A.M. Kanner, and A. Balabanov Depression and epilepsy: how closely related are they? Neurology 58 2002 S27 S39
2. A.M. Kanner The complex epilepsy patient: intricacies of assessment and treatment Epilepsia 44 Suppl. 5 2003 3 8
3. A.M. Kanner Can neurobiological pathogenic mechanisms of depression facilitate the development of seizure disorders? Lancet Neurol 11 2012 1093 1102
4. A.M. Kanner, and J.C. Nieto Depressive disorders in epilepsy Neurology 53 1999 S26 S32
5. C.L. Harden Depression and anxiety in epilepsy patients Epilepsy Behav 3 2002 296
6. W.A. Swinkels, J. Kuyk, R. van Dyck, and P. Spinhoven Psychiatric comorbidity in epilepsy Epilepsy Behav 7 2005 37 50
7. C. Hoppe, C.E. Elger, and C. Helmstaedter Long-term memory impairment in patients with focal epilepsy Epilepsia 48 Suppl. 9 2007 26 29
8. A. Mazarati, D. Shin, S. Auvin, R. Caplan, and R. Sankar Kindling epileptogenesis in immature rats leads to persistent depressive behavior Epilepsy Behav 10 2007 377 383
9. M.T. Berlim, and G. Turecki Definition, assessment, and staging of treatment-resistant refractory major depression: a review of current concepts and methods Can J Psychiatry 52 2007 46 54
10. D.C. Hesdorffer, and A.M. Kanner The FDA alert on suicidality and antiepileptic drugs: fire or false alarm? Epilepsia 50 2009 978 986
11. B.S. Judge, and L.L. Rentmeester Antidepressant overdose-induced seizures Neurol Clin 29 2011 565 580
12. E. Ben-Menachem Vagus-nerve stimulation for the treatment of epilepsy Lancet Neurol 1 2002 477 482
13. A randomized controlled trial of chronic vagus nerve stimulation for treatment of medically intractable seizures. The Vagus Nerve Stimulation Study Group Neurology 45 1995 224 230
14. A. Handforth, and C.M. DeGiorgio Vagus nerve stimulation therapy for partial-onset seizures: a randomized active-control trial Neurology 51 1998 48 55
15. C.M. DeGiorgio, S.C. Schachter, and A. Handforth Prospective long-term study of vagus nerve stimulation for the treatment of refractory seizures Epilepsia 41 2000 1195 1200
16. G.L. Morris 3rd, and W.M. Mueller Long-term treatment with vagus nerve stimulation in patients with refractory epilepsy. The Vagus Nerve Stimulation Study Group E01-E05 Neurology 53 1999 1731 1735
17. R. Raedt, R. Clinckers, and L. Mollet Increased hippocampal noradrenaline is a biomarker for efficacy of vagus nerve stimulation in a limbic seizure model J Neurochem 117 2011 461 469
18. V. De Herdt, J. De Waele, and R. Raedt Modulation of seizure threshold by vagus nerve stimulation in an animal model for motor seizures Acta Neurol Scand 121 2010 271 276
19. L. Mollet, A. Grimonprez, and R. Raedt Intensity-dependent modulatory effects of vagus nerve stimulation on cortical excitability Acta Neurol Scand 128 2013 391 396
20. S.E. Krahl, K.B. Clark, D.C. Smith, and R.A. Browning Locus coeruleus lesions suppress the seizure-attenuating effects of vagus nerve stimulation Epilepsia 39 1998 709 714
21. G.M. Alexander, and J.O. McNamara Vagus nerve stimulation elevates seizure threshold in the kindling model Epilepsia 53 2012 2043 2052
22. K. Rijkers, M. Aalbers, and G. Hoogland Acute seizure-suppressing effect of vagus nerve stimulation in the amygdala kindled rat Brain Res 1319 2010 155 163
23. S.E. Krahl, S.S. Senanayake, and A. Handforth Right-sided vagus nerve stimulation reduces generalized seizure severity in rats as effectively as left-sided Epilepsy Res 56 2003 1 4
24. S.E. Krahl, S.S. Senanayake, and A. Handforth Destruction of peripheral C-fibers does not alter subsequent vagus nerve stimulation-induced seizure suppression in rats Epilepsia 42 2001 586 589
25. D. Sahin, G. Ilbay, M. Imal, O. Bozdogan, and N. Ates Vagus nerve stimulation suppresses generalized seizure activity and seizure-triggered postictal cardiac rhythm changes in rats Physiol Res 58 2009 345 350
26. M. Takaya, W.J. Terry, and D.K. Naritoku Vagus nerve stimulation induces a sustained anticonvulsant effect Epilepsia 37 1996 1111 1116
27. M. Aalbers, J. Vles, S. Klinkenberg, G. Hoogland, M. Majoie, and K. Rijkers Animal models for vagus nerve stimulation in epilepsy Exp Neurol 230 2011 167 175
28. J. Zabara Inhibition of experimental seizures in canines by repetitive vagal stimulation Epilepsia 33 1992 1005 1012
29. J.W. Woodbury, and D.M. Woodbury Vagal stimulation reduces the severity of maximal electroshock seizures in intact rats: use of a cuff electrode for stimulating and recording Pacing Clin Electrophysiol 14 1991 94 107
30. G. Elger, C. Hoppe, P. Falkai, A.J. Rush, and C.E. Elger Vagus nerve stimulation is associated with mood improvements in epilepsy patients Epilepsy Res 42 2000 203 210
31. S. Klinkenberg, H.J. Majoie, M.M. van der Heijden, K. Rijkers, L. Leenen, and A.P. Aldenkamp Vagus nerve stimulation has a positive effect on mood in patients with refractory epilepsy Clin Neurol Neurosurg 114 2012 336 340
32. A.J. Rush, L.B. Marangell, and H.A. Sackeim Vagus nerve stimulation for treatment-resistant depression: a randomized, controlled acute phase trial Biol Psychiatry 58 2005 347 354
33. A.J. Rush, M.S. George, and H.A. Sackeim Vagus nerve stimulation (VNS) for treatment-resistant depressions: a multicenter study Biol Psychiatry 47 2000 276 286
34. H.A. Sackeim, A.J. Rush, and M.S. George Vagus nerve stimulation (VNS) for treatment-resistant depression: efficacy, side effects, and predictors of outcome Neuropsychopharmacology 25 2001 713 728
35. Z. Nahas, L.B. Marangell, and M.M. Husain Two-year outcome of vagus nerve stimulation (VNS) for treatment of major depressive episodes J Clin Psychiatry 66 2005 1097 1104
36. T.E. Schlaepfer, C. Frick, and A. Zobel Vagus nerve stimulation for depression: efficacy and safety in a European study Psychol Med 38 2008 651 661
37. M. Bajbouj, A. Merkl, and T.E. Schlaepfer Two-year outcome of vagus nerve stimulation in treatment-resistant depression J Clin Psychopharmacol 30 2010 273 281
38. A.J. Rush, H.A. Sackeim, and L.B. Marangell Effects of 12 months of vagus nerve stimulation in treatment-resistant depression: a naturalistic study Biol Psychiatry 58 2005 355 363
39. M.S. George, A.J. Rush, and L.B. Marangell A one-year comparison of vagus nerve stimulation with treatment as usual for treatment-resistant depression Biol Psychiatry 58 2005 364 373
40. L.B. Marangell, A.J. Rush, and M.S. George Vagus nerve stimulation (VNS) for major depressive episodes: one year outcomes Biol Psychiatry 51 2002 280 287
41. P. Cristancho, M.A. Cristancho, G.H. Baltuch, M.E. Thase, and J.P. O'Reardon Effectiveness and safety of vagus nerve stimulation for severe treatment-resistant major depression in clinical practice after FDA approval: outcomes at 1 year J Clin Psychiatry 72 2011 1376 1382
42. H.A. Sackeim, S.K. Brannan, A.J. Rush, M.S. George, L.B. Marangell, and J. Allen Durability of antidepressant response to vagus nerve stimulation (VNS) Int J Neuropsychopharmacol 10 2007 817 826
43. P.J. Goodnick, A.J. Rush, M.S. George, L.B. Marangell, and H.A. Sackeim Vagus nerve stimulation in depression Expert Opin Pharmacother 2 2001 1061 1063
44. P. Mohr, M. Rodriguez, A. Slavickova, and J. Hanka The application of vagus nerve stimulation and deep brain stimulation in depression Neuropsychobiology 64 2011 170 181
45. P.E. Holtzheimer, and H.S. Mayberg Neuromodulation for treatment-resistant depression F1000 Med Rep 4 2012 22
46. S.E. Krahl, S.S. Senanayake, A.E. Pekary, and A. Sattin Vagus nerve stimulation (VNS) is effective in a rat model of antidepressant action J Psychiatr Res 38 2004 237 240
47. H. Furmaga, A. Shah, and A. Frazer Serotonergic and noradrenergic pathways are required for the anxiolytic-like and antidepressant-like behavioral effects of repeated vagal nerve stimulation in rats Biol Psychiatry 70 2011 937 945
48. R.D. Porsolt, M. Le Pichon, and M. Jalfre Depression: a new animal model sensitive to antidepressant treatments Nature 266 1977 730 732
49. A. Mazarati, P. Siddarth, R.A. Baldwin, D. Shin, R. Caplan, and R. Sankar Depression after status epilepticus: behavioural and biochemical deficits and effects of fluoxetine Brain 131 2008 2071 2083
50. American Psychiatric Association APATFoDSMIV Diagnostic and statistical manual of mental disorders: DSM-IV-TR 2000 American Psychiatric Association Washington, DC
51. A. Harkin, D.D. Houlihan, and J.P. Kelly Reduction in preference for saccharin by repeated unpredictable stress in mice and its prevention by imipramine J Psychopharmacol 16 2002 115 123
52. N.F. Forbes, C.A. Stewart, K. Matthews, and I.C. Reid Chronic mild stress and sucrose consumption: validity as a model of depression Physiol Behav 60 1996 1481 1484
53. M.N. Jayatissa, C. Bisgaard, A. Tingstrom, M. Papp, and O. Wiborg Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression Neuropsychopharmacology 31 2006 2395 2404
54. P. Willner Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation Psychopharmacology 134 1997 319 329
55. M. El Yacoubi, S. Bouali, and D. Popa Behavioral, neurochemical, and electrophysiological characterization of a genetic mouse model of depression Proc Natl Acad Sci U S A 100 2003 6227 6232
56. R. El Tahry, L. Mollet, and R. Raedt Repeated assessment of larynx compound muscle action potentials using a self-sizing cuff electrode around the vagus nerve in experimental rats J Neurosci Methods 198 2011 287 293
57. J.L. Hellier, P.R. Patrylo, P.S. Buckmaster, and F.E. Dudek Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy Epilepsy Res 31 1998 73 84
58. R.J. Racine Modification of seizure activity by electrical stimulation. II. Motor seizure Electroencephalogr Clin Neurophysiol 32 1972 281 294
59. T. Strekalova, R. Spanagel, D. Bartsch, F.A. Henn, and P. Gass Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration Neuropsychopharmacology 29 2004 2007 2017
60. M.N. Jayatissa, K. Henningsen, M.J. West, and O. Wiborg Decreased cell proliferation in the dentate gyrus does not associate with development of anhedonic-like symptoms in rats Brain Res 1290 2009 133 141
61. O. Wiborg Chronic mild stress for modeling anhedonia Cell Tissue Res 354 2013 155 169
62. K.Y. Sarkisova, I.S. Midzianovskaia, and M.A. Kulikov Depressive-like behavioral alterations and c-fos expression in the dopaminergic brain regions in WAG/Rij rats with genetic absence epilepsy Behav Brain Res 144 2003 211 226
63. N.C. Jones, M.R. Salzberg, G. Kumar, A. Couper, M.J. Morris, and T.J. O'Brien Elevated anxiety and depressive-like behavior in a rat model of genetic generalized epilepsy suggesting common causation Exp Neurol 209 2008 254 260
64. E.A. Pineda, J.G. Hensler, R. Sankar, D. Shin, T.F. Burke, and A.M. Mazarati Interleukin-1beta causes fluoxetine resistance in an animal model of epilepsy-associated depression Neurotherapeutics 9 2012 477 485
65. J. Tchekalarova, D. Pechlivanova, T. Atanasova, P. Markova, V. Lozanov, and A. Stoynev Diurnal variations in depression-like behavior of Wistar and spontaneously hypertensive rats in the kainate model of temporal lobe epilepsy Epilepsy Behav 20 2011 277 285
66. A. Vezzani, J. French, T. Bartfai, and T.Z. Baram The role of inflammation in epilepsy Nat Rev Neurol 7 2011 31 40
67. H.M. Abelaira, G.Z. Reus, F. Petronilho, T. Barichello, and J. Quevedo Neuroimmunomodulation in depression: a review of inflammatory cytokines involved in this process Neurochem Res 39 9 2014 1634 1639
68. M.M. Lee, A. Reif, and A.G. Schmitt Major depression: a role for hippocampal neurogenesis? Curr Top Behav Neurosci 14 2013 153 179
69. J.M. Parent, and M.M. Kron Neurogenesis and epilepsy 2012
70. R. Holderbach, K. Clark, J.L. Moreau, J. Bischofberger, and C. Normann Enhanced long-term synaptic depression in an animal model of depression Biol Psychiatry 62 2007 92 100
71. R. Schwarcz, R. Zaczek, and J.T. Coyle Microinjection of kainic acid into the rat hippocampus Eur J Pharmacol 50 1978 209 220
72. G. Sperk, H. Lassmann, H. Baran, F. Seitelberger, and O. Hornykiewicz Kainic acid-induced seizures: dose-relationship of behavioural, neurochemical and histopathological changes Brain Res 338 1985 289 295
73. M. Kang, K.H. Pyun, C.G. Jang, H. Kim, H. Bae, and I. Shim Nelumbinis semen reverses a decrease in hippocampal 5-HT release induced by chronic mild stress in rats J Pharm Pharmacol 57 2005 651 656
74. S. Bekris, K. Antoniou, S. Daskas, and Z. Papadopoulou-Daifoti Behavioural and neurochemical effects induced by chronic mild stress applied to two different rat strains Behav Brain Res 161 2005 45 59
75. J.M. Li, L.D. Kong, Y.M. Wang, C.H. Cheng, W.Y. Zhang, and W.Z. Tan Behavioral and biochemical studies on chronic mild stress models in rats treated with a Chinese traditional prescription Banxia-houpu decoction Life Sci 74 2003 55 73
76. M. Papp, V. Klimek, and P. Willner Effects of imipramine on serotonergic and beta-adrenergic receptor binding in a realistic animal model of depression Psychopharmacology 114 1994 309 314
77. J.L. Moreau, M. Bos, F. Jenck, J.R. Martin, P. Mortas, and J. Wichmann 5HT2C receptor agonists exhibit antidepressant-like properties in the anhedonia model of depression in rats Eur Neuropsychopharmacol 6 1996 169 175
78. G. Sperk, H. Lassmann, H. Baran, S.J. Kish, F. Seitelberger, and O. Hornykiewicz Kainic acid induced seizures: neurochemical and histopathological changes Neuroscience 10 1983 1301 1315
79. S. Koh, R. Magid, H. Chung, C.D. Stine, and D.N. Wilson Depressive behavior and selective down-regulation of serotonin receptor expression after early-life seizures: reversal by environmental enrichment Epilepsy Behav 10 2007 26 31
80. G. Di Chiara, P. Loddo, and G. Tanda Reciprocal changes in prefrontal and limbic dopamine responsiveness to aversive and rewarding stimuli after chronic mild stress: implications for the psychobiology of depression Biol Psychiatry 46 1999 1624 1633
81. G. Di Chiara, and G. Tanda Blunting of reactivity of dopamine transmission to palatable food: a biochemical marker of anhedonia in the CMS model? Psychopharmacology 134 1997 351 353 discussion 371-7
82. A.J. Grippo, E.S. Na, R.F. Johnson, T.G. Beltz, and A.K. Johnson Sucrose ingestion elicits reduced Fos expression in the nucleus accumbens of anhedonic rats Brain Res 1019 2004 259 264
83. M. Dziedzicka-Wasylewska, P. Willner, and M. Papp Changes in dopamine receptor mRNA expression following chronic mild stress and chronic antidepressant treatment Behav Pharmacol 8 1997 607 618
84. M.E. Bardgett, J.L. Jackson, G.T. Taylor, and J.G. Csernansky Kainic acid decreases hippocampal neuronal number and increases dopamine receptor binding in the nucleus accumbens: an animal model of schizophrenia Behav Brain Res 70 1995 153 164
85. M.E. Bardgett, S.L. Salaris, J.L. Jackson, J. Harding, and J.G. Csernansky The effects of kainic acid lesions on dopaminergic responses to haloperidol and clozapine Psychopharmacology 133 1997 142 151
86. N. Ando, K. Morimoto, T. Watanabe, T. Ninomiya, and H. Suwaki Enhancement of central dopaminergic activity in the kainate model of temporal lobe epilepsy: implication for the mechanism of epileptic psychosis Neuropsychopharmacology 29 2004 1251 1258
87. M.M. Holm, J.L. Nieto-Gonzalez, and I. Vardya Hippocampal GABAergic dysfunction in a rat chronic mild stress model of depression Hippocampus 21 2011 422 433
88. S. Alvestad, J. Hammer, E. Eyjolfsson, H. Qu, O.P. Ottersen, and U. Sonnewald Limbic structures show altered glial-neuronal metabolism in the chronic phase of kainate induced epilepsy Neurochem Res 33 2008 257 266
89. A. Rodriguez-Moreno, and J. Lerma Kainate receptor modulation of GABA release involves a metabotropic function Neuron 20 1998 1211 1218
90. V.R. Clarke, B.A. Ballyk, and K.H. Hoo A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission Nature 389 1997 599 603
91. R. Delgado y Palacios, A. Campo, and K. Henningsen Magnetic resonance imaging and spectroscopy reveal differential hippocampal changes in anhedonic and resilient subtypes of the chronic mild stress rat model Biol Psychiatry 70 2011 449 457
92. A.J. Grippo, J. Francis, T.G. Beltz, R.B. Felder, and A.K. Johnson Neuroendocrine and cytokine profile of chronic mild stress-induced anhedonia Physiol Behav 84 2005 697 706
93. J.T. Jarvela, F.R. Lopez-Picon, A. Plysjuk, S. Ruohonen, and I.E. Holopainen Temporal profiles of age-dependent changes in cytokine mRNA expression and glial cell activation after status epilepticus in postnatal rat hippocampus J Neuroinflammation 8 2011 29
94. M.N. Jayatissa, C.F. Bisgaard, M.J. West, and O. Wiborg The number of granule cells in rat hippocampus is reduced after chronic mild stress and re-established after chronic escitalopram treatment Neuropharmacology 54 2008 530 541
95. J. Alonso, M.C. Angermeyer, and S. Bernert Prevalence of mental disorders in Europe: results from the European Study of the Epidemiology of Mental Disorders (ESEMeD) project Acta Psychiatr Scand Suppl 2004 21 27
96. W.P. Gray, and L.E. Sundstrom Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat Brain Res 790 1998 52 59
97. S. Jessberger, B. Romer, H. Babu, and G. Kempermann Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells Exp Neurol 196 2005 342 351
98. H. Dong, C.A. Csernansky, B. Goico, and J.G. Csernansky Hippocampal neurogenesis follows kainic acid-induced apoptosis in neonatal rats J Neurosci 23 2003 1742 1749
99. S. Manta, J. Dong, G. Debonnel, and P. Blier Enhancement of the function of rat serotonin and norepinephrine neurons by sustained vagus nerve stimulation J Psychiatry Neurosci 34 2009 272 280
100. S. Manta, M. El Mansari, G. Debonnel, and P. Blier Electrophysiological and neurochemical effects of long-term vagus nerve stimulation on the rat monoaminergic systems Int J Neuropsychopharmacol 16 2013 459 470
101. A.E. Dorr, and G. Debonnel Effect of vagus nerve stimulation on serotonergic and noradrenergic transmission J Pharmacol Exp Ther 318 2006 890 898
102. S. Manta, M. El Mansari, and P. Blier Novel attempts to optimize vagus nerve stimulation parameters on serotonin neuronal firing activity in the rat brain Brain Stimul 5 2012 422 429
103. D.A. Groves, E.M. Bowman, and V.J. Brown Recordings from the rat locus coeruleus during acute vagal nerve stimulation in the anaesthetised rat Neurosci Lett 379 2005 174 179
104. R.W. Roosevelt, D.C. Smith, R.W. Clough, R.A. Jensen, and R.A. Browning Increased extracellular concentrations of norepinephrine in cortex and hippocampus following vagus nerve stimulation in the rat Brain Res 1119 2006 124 132
105. P. Follesa, F. Biggio, and G. Gorini Vagus nerve stimulation increases norepinephrine concentration and the gene expression of BDNF and bFGF in the rat brain Brain Res 1179 2007 28 34
106. S.M. Florin-Lechner, J.P. Druhan, G. Aston-Jones, and R.J. Valentino Enhanced norepinephrine release in prefrontal cortex with burst stimulation of the locus coeruleus Brain Res 742 1996 89 97
107. D.L. Hassert, T. Miyashita, and C.L. Williams The effects of peripheral vagal nerve stimulation at a memory-modulating intensity on norepinephrine output in the basolateral amygdala Behav Neurosci 118 2004 79 88
108. R. Ruffoli, F.S. Giorgi, C. Pizzanelli, L. Murri, A. Paparelli, and F. Fornai The chemical neuroanatomy of vagus nerve stimulation J Chem Neuroanat 42 2011 288 296
109. S.E. Krahl, and K.B. Clark Vagus nerve stimulation for epilepsy: a review of central mechanisms Surg Neurol Int 3 2012 S255 S259
110. D. Labar Vagus nerve stimulation for 1 year in 269 patients on unchanged antiepileptic drugs Seizure 13 2004 392 398
111. J. Liporace, D. Hucko, and R. Morrow Vagal nerve stimulation: adjustments to reduce painful side effects Neurology 57 2001 885 886
112. L.L. Carpenter, F.A. Moreno, and M.A. Kling Effect of vagus nerve stimulation on cerebrospinal fluid monoamine metabolites, norepinephrine, and gamma-aminobutyric acid concentrations in depressed patients Biol Psychiatry 56 2004 418 426
113. F. Marrosu, A. Serra, A. Maleci, M. Puligheddu, G. Biggio, and M. Piga Correlation between GABA(A) receptor density and vagus nerve stimulation in individuals with drug-resistant partial epilepsy Epilepsy Res 55 2003 59 70
114. E. Ben-Menachem, A. Hamberger, and T. Hedner Effects of vagus nerve stimulation on amino acids and other metabolites in the CSF of patients with partial seizures Epilepsy Res 20 1995 221 227
115. J.A. Nichols, A.R. Nichols, S.M. Smirnakis, N.D. Engineer, M.P. Kilgard, and M. Atzori Vagus nerve stimulation modulates cortical synchrony and excitability through the activation of muscarinic receptors Neuroscience 189 2011 207 214
116. L. Detari, G. Juhasz, and T. Kukorelli Effect of stimulation of vagal and radial nerves on neuronal activity in the basal forebrain area of anaesthetized cats Acta Physiol Hung 61 1983 147 154
117. J.A. Shetake, N.D. Engineer, W.A. Vrana, J.T. Wolf, and M.P. Kilgard Pairing tone trains with vagus nerve stimulation induces temporal plasticity in auditory cortex Exp Neurol 233 2012 342 349
118. B.A. Porter, N. Khodaparast, and T. Fayyaz Repeatedly pairing vagus nerve stimulation with a movement reorganizes primary motor cortex Cereb Cortex 22 2012 2365 2374
119. D. De Ridder, S. Vanneste, N.D. Engineer, and M.P. Kilgard Safety and efficacy of vagus nerve stimulation paired with tones for the treatment of tinnitus: a case series Neuromodulation 17 2014 170 179
120. S.A. Hays, R.L. Rennaker, and M.P. Kilgard Targeting plasticity with vagus nerve stimulation to treat neurological disease Prog Brain Res 207 2013 275 299
121. N. Khodaparast, S.A. Hays, and A.M. Sloan Vagus nerve stimulation during rehabilitative training improves forelimb strength following ischemic stroke Neurobiol Dis 60 2013 80 88
122. N.D. Engineer, J.R. Riley, and J.D. Seale Reversing pathological neural activity using targeted plasticity Nature 470 2011 101 104
123. V. De Herdt, S. Bogaert, and K.R. Bracke Effects of vagus nerve stimulation on pro- and anti-inflammatory cytokine induction in patients with refractory epilepsy J Neuroimmunol 214 2009 104 108
124. V. De Herdt, L. Puimege, and J. De Waele Increased rat serum corticosterone suggests immunomodulation by stimulation of the vagal nerve J Neuroimmunol 212 2009 102 105
125. V. O'Keane, T.G. Dinan, L. Scott, and C. Corcoran Changes in hypothalamic-pituitary-adrenal axis measures after vagus nerve stimulation therapy in chronic depression Biol Psychiatry 58 2005 963 968
126. K.J. Tracey The inflammatory reflex Nature 420 2002 853 859
127. D.L. Feinstein, E. Galea, and D.J. Reis Norepinephrine suppresses inducible nitric oxide synthase activity in rat astroglial cultures J Neurochem 60 1993 1945 1948
128. J.B. O'Sullivan, K.M. Ryan, N.M. Curtin, A. Harkin, and T.J. Connor Noradrenaline reuptake inhibitors limit neuroinflammation in rat cortex following a systemic inflammatory challenge: implications for depression and neurodegeneration Int J Neuropsychopharmacol 12 2009 687 699
129. L.V. Borovikova, S. Ivanova, and M. Zhang Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin Nature 405 2000 458 462
130. B. Bonaz, C. Picq, V. Sinniger, J.F. Mayol, and D. Clarencon Vagus nerve stimulation: from epilepsy to the cholinergic anti-inflammatory pathway Neurogastroenterol Motil 25 2013 208 221
131. J. Meregnani, D. Clarencon, and M. Vivier Anti-inflammatory effect of vagus nerve stimulation in a rat model of inflammatory bowel disease Auton Neurosci 160 2011 82 89
132. E.P. Van Der Zanden, G.E. Boeckxstaens, and W.J. de Jonge The vagus nerve as a modulator of intestinal inflammation Neurogastroenterol Motil 21 2009 6 17
133. D. Revesz, M. Tjernstrom, E. Ben-Menachem, and T. Thorlin Effects of vagus nerve stimulation on rat hippocampal progenitor proliferation Exp Neurol 214 2008 259 265
134. F. Biggio, G. Gorini, and C. Utzeri Chronic vagus nerve stimulation induces neuronal plasticity in the rat hippocampus Int J Neuropsychopharmacol 12 2009 1209 1221
135. N. Gebhardt, K.J. Bar, and M.K. Boettger Vagus nerve stimulation ameliorated deficits in one-way active avoidance learning and stimulated hippocampal neurogenesis in bulbectomized rats Brain Stimul 6 2013 78 83
136. H. Furmaga, F.R. Carreno, and A. Frazer Vagal nerve stimulation rapidly activates brain-derived neurotrophic factor receptor TrkB in rat brain PLoS One 7 2012 e34844