Activation of the anti-inflammatory reflex blocks lipopolysaccharide-induced decrease in synaptic inhibition in the temporal cortex of the rat

Journal of Neuroscience Research

Volumn 93, Issue 6, 2015, Pages 859-865

  Garcia Oscos, Francisco ^a,b   Peña, David ^a   Housini, Mohammad ^a   Cheng, Derek ^a   Lopez, Diego ^c   Cuevas Olguin, Roberto ^d   Saderi, Nadia ^d   Salgado Delgado, Roberto ^d   Galindo Charles, Luis ^b   Salgado Burgos, Humberto ^e   Rose John, Stefan ^f   Flores, Gonzalo ^g   Kilgard, Michael P ^a   Atzori, Marco ^a,d  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

^d UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^e UNIVERSIDAD AUTÓNOMA DE YUCATÁN   (Mexico)

^f UNIVERSITY OF KIEL   (Germany)

^g BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

Author keywords

GABA; Nicotinic 7; PHA543613; Vagal nerve stimulation; VNS

Indexed keywords

LIPOPOLYSACCHARIDE; N (3 QUINUCLIDINYL)FURO[2,3 C]PYRIDINE 5 CARBOXAMIDE; ANTIINFLAMMATORY AGENT; FUSED HETEROCYCLIC RINGS; N-(1-AZABICYCLO(2.2.2)OCT-3-YL)FURO(2,3-C)PYRIDINE-5-CARBOXAMIDE; QUINUCLIDINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY REFLEX; ARTICLE; CONTROLLED STUDY; INFLAMMATION; NONHUMAN; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; RAT; REFLEX; STIMULUS RESPONSE; SYNAPTIC INHIBITION; TEMPORAL CORTEX; VAGUS NERVE; VAGUS NERVE STIMULATION; ANIMAL; BIOPHYSICS; CHEMICALLY INDUCED; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; ELECTROSTIMULATION; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; SYNAPSE; TEMPORAL LOBE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BICYCLO COMPOUNDS, HETEROCYCLIC; BIOPHYSICS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; IN VITRO TECHNIQUES; INFLAMMATION; INHIBITORY POSTSYNAPTIC POTENTIALS; LIPOPOLYSACCHARIDES; NEURONS; PATCH-CLAMP TECHNIQUES; QUINUCLIDINES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; TEMPORAL LOBE; VAGUS NERVE STIMULATION;

EID: 84927577482     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23550     Document Type: Article

References (56)

1. Allendorfer JB, Szaflarski JP. 2014. Contributions of fMRI towards our understanding of the response to psychosocial stress in epilepsy and psychogenic nonepileptic seizures. Epilepsy Behav 35:19-25.
2. Allendorfer JB, Heyse H, Mendoza L, Nelson EB, Eliassen JC, Storrs JM, Szaflarski JP. 2014. Physiologic and cortical response to acute psychosocial stress in left temporal lobe epilepsy: a pilot cross-sectional fMRI study. Epilepsy Behav 36:115-123.
3. Anacker C, Cattaneo A, Musaelyan K, Zunszain PA, Horowitz M, Molteni R, Luoni A, Calabrese F, Tansey K, Gennarelli M, Thuret S, Price J, Uher R, Riva MA, Pariante CM. 2013. Role for the kinase SGK1 in stress, depression, and glucocorticoid effects on hippocampal neurogenesis. Proc Natl Acad Sci U S A 110:8708-8713.
4. Atzori M, Lei S, Evans DI, Kanold PO, Phillips-Tansey E, McIntyre O, McBain CJ. 2001. Differential synaptic processing separates stationary from transient inputs to the auditory cortex. Nat Neurosci 4:1230-1237.
5. Atzori M, Kanold PO, Pineda JC, Flores-Hernandez J, Paz RD. 2005. Dopamine prevents muscarinic-induced decrease of glutamate release in the auditory cortex. Neuroscience 134:1153-1165.
6. Atzori M, Garcia-Oscos F, Mendez JA. 2012. Role of IL-6 in the etiology of hyperexcitable neuropsychiatric conditions: experimental evidence and therapeutic implications. Future Med Chem 4:2177-2192.
7. Beattie EC, Stellwagen D, Morishita W, Bresnahan JC, Ha BK, Von Zastrow M, Beattie MS, Malenka RC. 2002. Control of synaptic strength by glial TNFalpha. Science 295:2282-2285.
8. Bown C, Wang JF, MacQueen G, Young LT. 2000. Increased temporal cortex ER stress proteins in depressed subjects who died by suicide. Neuropsychopharmacology 22:327-332.
9. Cassimjee N, Fouche J-P, Burnett M, Lochner C, Warwick J, Dupont P, Stein DJ, Cloete KJ, Carey PD. 2010. Changes in regional brain volumes in social anxiety disorder following 12 weeks of treatment with escitalopram. Metab Brain Dis 25:369-374.
10. Craig IW. 2010. Genetic polymorphism in stress response. In: Fink G, editor. Stress science. San Diego: Elsevier. p 325-336.
11. Deidda G, Bozarth IF, Cancedda L. 2014. Modulation of GABAergic transmission in development and neurodevelopmental disorders: investigating physiology and pathology to gain therapeutic perspectives. Front Cell Neurosci 8:119.
12. Dhabhar FS. 2014. Effects of stress on immune function: the good, the bad, and the beautiful. Immunol Res 58:193-210.
13. Engineer ND, Riley JR, Seale JD, Vrana WA, Shetake JA, Sudanagunta SP, Borland SM, Kilgard M. 2010. Reversing pathological neural activity using targeted plasticity. Nature 470:101-104.
14. Faravelli C, Lo Sauro C, Lelli L, Pietrini F, Lazzeretti L, Godini L, Benni L, Fioravanti G, Talamba GA, Castellini G, Ricca V. 2012. The role of life events and HPA axis in anxiety disorders: a review. Curr Pharm Des 18:5663-5674.
15. Frick A, Howner K, Fischer H, Eskildsen SF, Kristiansson M, Furmark T. 2013. Cortical thickness alterations in social anxiety disorder. Neurosci Lett 536:52-55.
16. Fulham WR, Michie PT, Ward PB, Rasser PE, Todd J, Johnston PJ, Thompson PM, Schall U. 2014. Mismatch negativity in recent-onset and chronic schizophrenia: a current source density analysis. PLoS One 9:e100221.
17. Garcia-Oscos F, Salgado H, Hall S, Thomas F, Farmer GE, Bermeo J, Galindo LC, Ramirez RD, D'Mello S, Rose-John S, Atzori M. 2012. The stress-induced cytokine interleukin-6 decreases the inhibition/excitation ratio in the rat temporal cortex via transsignaling. Biol Psychiatry 71:574-582.
18. Garcia-Oscos F, Peña D, Housini M, Cheng D, Lopez D, Borland MS, Salgado-Delgado R, Salgado H, D&Mello S, Kilgard MP, Rose-John S, Atzori M. Vagal nerve stimulation blocks interleukin 6-dependent synaptic hyperexcitability induced by lipopolysaccharide-induced acute stress in the rodent prefrontal cortex. Brain Behav Immun 2015;43:149-158.
19. A benzodiazepine receptor binding in veterans with posttraumatic stress disorder. Mol Psychiatry 13:74-83.
20. Goldstein DS. 2010. Sympathetic noradrenergic and adrenomedullary hormonal systems in stress and distress. In: Fink G, editor. Stress science. San Diego: Elsevier. p 399-404.
21. Hains AB, Arnsten AF. 2008. Molecular mechanisms of stress-induced prefrontal cortical impairment: implications for mental illness. Learn Mem 15:551-564.
22. Harrison NA, Doeller DF, Voon V, Burgess N, Critchley HD. 2014. Preripheral inflammation impairs human spatial memory via actions on the medial temporal lobe glucose metabolism. Biol Psychiatry 76:585-93.
23. Herman J. 2010. Stress response: neural and feedback regulation of the hpa axis. In: Fink G, editor. Stress science. San Diego: Elsevier. p 75-80.
24. Hosoi T, Okuma Y, Nomura Y. 2002. The mechanisms of immune-to-brain communication in inflammation as a drug target. Curr Drug Targets Inflamm Allerg 1:257-262.
25. Inkster B, Rao AW, Ridler K, Nichols TE, Saemann PG, Auer DP, Holsboer F, Tozzi F, Muglia P, Merlo-Pich E, Matthews PM. 2011. Structural brain changes in patients with recurrent major depressive disorder presenting with anxiety symptoms. J Neuroimaging 21:375-382.
26. Ising M, Höhne N, Siebertz A, Parchmann A-M, Erhardt A, Keck M. 2012. Stress response regulation in panic disorder. Curr Pharm Des 18:5675-5684.
27. Jalbrzikowski M, Jonas R, Senturk D, Patel A, Chow C, Green MF, Bearden CE. 2013. Structural abnormalities in cortical volume, thickness, and surface area in 22q11.2 microdeletion syndrome: relationship with psychotic symptoms. Neuroimage Clin 3:405-415.
28. Jenkins FJ, Van Houten B, Bovbjerg DH. 2014. Effects on DNA damage and/or repair processes as biological mechanisms linking psychological stress to cancer risk. J Appl Biobehav Res 19:3-23.
29. Kawaguchi Y. 1995. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655.
30. Ketter TA, Post RM, Theodore WH. 1999. Positive and negative psychiatric effects of antiepileptic drugs in patients with seizure disorders. Neurology 53:S53-S67.
31. Krämer M, Seefeldt WL, Heinrichs N, Tuschen-Caffier B, Schmitz J, Wolf OT, Blechert J. 2012. Subjective, autonomic, and endocrine reactivity during social stress in children with social phobia. J Abnorm Child Psychol 40:95-104.
32. Kroes MCW, Rugg MD, Whalley MG, Brewin CR. 2011. Structural brain abnormalities common to posttraumatic stress disorder and depression. J Psychiatry Neurosci 36:256-265.
33. Kross EK, Gries CJ, Curtis JR. 2008. Posttraumatic stress disorder following critical illness. Crit Care Clin 24:875-887, ix-x.
34. Lai C-H, Wu Y-T. 2012. Frontal regional homogeneity increased and temporal regional homogeneity decreased after remission of first-episode drug-naïve major depressive disorder with panic disorder patients under duloxetine therapy for 6 weeks. J Affect Disord 136:453-458.
35. Leonard B, Song C. 2010. Cytokines, stress, and depression. In: Fink G, editor. Stress science. San Diego: Elsevier. p 560-565.
36. Maguire J. 2014. Stress-induced plasticity of GABAergic inhibition. Front Cell Neurosci 8:157.
37. Minen MT, Camprodon J, Nehme R, Chemali Z. 2014. The neuropsychiatry of tinnitus: a circuit-based approach to the causes and treatments available. J Neurol Neurosurg Psychiatry 85:1138-1144.
38. Misiak B, Frydecka D, Zawadzki M, Krefft M, Kiejna A. 2014. Refining and integrating schizophrenia pathophysiology: relevance of the allostatic load concept. Neurosci Biobehav Rev 45:183-201.
39. Müller N, Myint A-M, Schwarz MJ. 2011. Inflammatory biomarkers and depression. Neurotox Res 19:308-318.
40. Munhoz CD, Garcia-Bueno B, Madrigal JL, Lepsch LB, Scavone C, Leza JC. 2008. Stress-induced neuroinflammation: mechanisms and new pharmacological targets. Braz J Med Biol Res 41:1037-1046.
41. Nichols JA, Nichols AR, Smirnakis SM, Engineer ND, Kilgard MP, Atzori M. 2011. Vagus nerve stimulation modulates cortical synchrony and excitability through the activation of muscarinic receptors. Neuroscience 189:207-214.
42. Oke SL, Tracey KJ. 2009. The inflammatory reflex and the role of complementary and alternative medical therapies. Ann N Y Acad Sci 1172:172-180.
43. Pietersen CY, Mauney SA, Kim SS, Lim MP, Rooney RJ, Goldstein JM, Petryshen TL, Seidman LJ, Shenton ME, McCarley RW, Sonntag K-C, Woo T-UW. 2014a. Molecular profiles of pyramidal neurons in the superior temporal cortex in schizophrenia. J Neurogenet 28:53-69.
44. Pietersen CY, Mauney SA, Kim SS, Passeri E, Lim MP, Rooney RJ, Goldstein JM, Petreyshen TL, Seidman LJ, Shenton ME, Mccarley RW, Sonntag K-C, Woo T-UW. 2014b. Molecular profiles of parvalbumin-immunoreactive neurons in the superior temporal cortex in schizophrenia. J Neurogenet 28:70-85.
45. Salgado H, Garcia-Oscos F, Patel A, Martinolich L, Nichols JA, Dinh L, Roychowdhury S, Tseng KY, Atzori M. 2011a. Layer-specific noradrenergic modulation of inhibition in cortical layer II/III. Cereb Cortex 21:212-221.
46. Salgado H, Garcia-Oscos F, Dinh L, Atzori M. 2011b. Dynamic modulation of short-term synaptic plasticity in the auditory cortex: the role of norepinephrine. Hear Res 27:26-36.
47. Schmidt MJ, Mirnics K. 2014. Neurodevelopment, GABA system dysfunction, and schizophrenia. Neuropsychopharmacology 40:190-206.
48. Segarra R, Ojeda N, Zabala A, Garcia J, Catalan A, Eguiluz JI, Gutierrez M. 2012. Similarities in early course among men and women with a first episode of schizophrenia and schizophreniform disorder. Eur Arch Psychiatry Clin Neurosci 262:95-105.
49. Sellmann C, Villarín Pildaín L, Schmitt A, Leonardi-Essmann F, Durrenberger PF, Spanagel R, Arzberger T, Kretzschmar H, Zink M, Gruber O, Herrera-Marschitz M, Reynolds R, Falkai P, Gebicke-Haerter PJ, Matthäus F. 2014. Gene expression in superior temporal cortex of schizophrenia patients. Eur Arch Psychiatry Clin Neurosci 264:297-309.
50. Skilbeck KJ, Johnston GA, Hinton T. 2010. Stress and GABA receptors. J Neurochem 112:1115-1130.
51. Stellwagen D, Malenka RC. 2006. Synaptic scaling mediated by glial TNF-alpha. Nature 440:1054-1059.
52. Steptoe A, Hamer M, Chida Y. 2007. The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav Immun 21:901-912.
53. Tracey KJ. 2002. The inflammatory reflex. Nature 420:853-859.
54. Van Tol M-J, van der Wee NJA, van den Heuvel OA, Nielen MMA, Demenescu LR, Aleman A, Renken R, van Buchem MA, Zitman FG, Veltman DJ. 2010. Regional brain volume in depression and anxiety disorders. Arch Gen Psychiatry 67:1002-1011.
55. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ. 2003. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384-388.
56. Weinstein AA, Deuster PA, Francis JL, Bonsall RW, Tracy RP, Kop WJ. 2014. Neurohormonal and inflammatory hyperresponsiveness to acute mental stress in depression. Biol Psychol 84:228-234.