Ketamine Decreases Resting State Functional Network Connectivity in Healthy Subjects: Implications for Antidepressant Drug Action

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Scheidegger, Milan ^a,b   Walter, Martin ^c,d,e   Lehmann, Mick ^a   Metzger, Coraline ^c,e   Grimm, Simone ^b,f,g   Boeker, Heinz ^b   Boesiger, Peter ^a,h   Henning, Anke ^a,h   Seifritz, Erich ^b,h  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL OF PSYCHIATRY   (Switzerland)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^e Clinical Affective Neuroimaging Laboratory (CANLAB)   (Germany)

^f FREIE UNIVERSITÄT BERLIN   (Germany)

^g CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^h UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

KETAMINE; PLACEBO;

ADULT; ANTERIOR CINGULATE; ANTIDEPRESSANT ACTIVITY; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; CROSSOVER PROCEDURE; DEFAULT MODE NETWORK; DORSAL MEDIAL PREFRONTAL CORTEX; DORSAL NEXUS; DOUBLE BLIND PROCEDURE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NETWORK CONNECTIVITY; HUMAN; HUMAN EXPERIMENT; MALE; MEDIOPREFRONTAL CORTEX; NERVE CELL NETWORK; NORMAL HUMAN; OBSERVATIONAL STUDY; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PREGENUAL ANTERIOR CINGULATE; PROSPECTIVE STUDY; PSYCHOMETRY; RANDOMIZED CONTROLLED TRIAL; STEADY STATE;

ADULT; ANTIDEPRESSIVE AGENTS; BRAIN MAPPING; CROSS-OVER STUDIES; DEPRESSIVE DISORDER, MAJOR; DOUBLE-BLIND METHOD; FEMALE; GYRUS CINGULI; HUMANS; INJECTIONS, INTRAVENOUS; KETAMINE; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; PLACEBOS; PREFRONTAL CORTEX; SEPTAL NUCLEI;

EID: 84866720097     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044799     Document Type: Article

References (66)

1. Sanacora G, Zarate CA, Krystal JH, Manji HK, (2008) Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat Rev Drug Discov 7: 426-437 doi:10.1038/nrd2462.
2. Vollenweider FX, Kometer M, (2010) The neurobiology of psychedelic drugs: implications for the treatment of mood disorders. Nat Rev Neurosci 11: 642-651 doi:10.1038/nrn2884.
3. Berman RM, Cappiello A, Anand A, Oren DA, Heninger GR, et al. (2000) Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 47: 351-354.
4. Zarate CA, Singh JB, Carlson PJ, Brutsche NE, Ameli R, et al. (2006) A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 63: 856-864 doi:10.1001/archpsyc.63.8.856.
5. Phelps LE, Brutsche N, Moral JR, Luckenbaugh DA, Manji HK, et al. (2009) Family history of alcohol dependence and initial antidepressant response to an N-methyl-D-aspartate antagonist. Biol Psychiatry 65: 181-184 doi:10.1016/j.biopsych.2008.09.029.
6. Aan Het Rot M, Collins KA, Murrough JW, Perez AM, Reich DL, et al. (2010) Safety and efficacy of repeated-dose intravenous ketamine for treatment-resistant depression. Biol Psychiatry 67: 139-145 doi:10.1016/j.biopsych.2009.08.038.
7. Machado-Vieira R, Salvadore G, Diazgranados N, Zarate CA, (2009) Ketamine and the next generation of antidepressants with a rapid onset of action. Pharmacol Ther 123: 143-150 doi:10.1016/j.pharmthera.2009.02.010.
8. Li N, Lee B, Liu RJ, Banasr M, Dwyer JM, et al. (2010) mTOR-Dependent Synapse Formation Underlies the Rapid Antidepressant Effects of NMDA Antagonists. Science 329: 959-964 doi:10.1126/science.1190287.
9. Autry AE, Adachi M, Nosyreva E, Na ES, Los MF, et al. (2011) NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475: 91-95 doi:10.1038/nature10130.
10. Li N, Liu R-J, Dwyer JM, Banasr M, Lee B, et al. (2011) Glutamate N-methyl-D-aspartate receptor antagonists rapidly reverse behavioral and synaptic deficits caused by chronic stress exposure. Biol Psychiatry 69: 754-761 doi:10.1016/j.biopsych.2010.12.015.
11. Maeng S, Zarate CA, Du J, Schloesser RJ, McCammon J, et al. (2008) Cellular mechanisms underlying the antidepressant effects of ketamine: role of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors. Biol Psychiatry 63: 349-352 doi:10.1016/j.biopsych.2007.05.028.
12. Yüksel C, Ongür D, (2010) Magnetic resonance spectroscopy studies of glutamate-related abnormalities in mood disorders. Biol Psychiatry 68: 785-794 doi:10.1016/j.biopsych.2010.06.016.
13. Cotter D, Mackay D, Landau S, Kerwin R, Everall I, (2001) Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Arch Gen Psychiatry 58: 545-553.
14. Chana G, Landau S, Beasley C, Everall IP, Cotter D, (2003) Two-dimensional assessment of cytoarchitecture in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia: evidence for decreased neuronal somal size and increased neuronal density. Biol Psychiatry 53: 1086-1098.
15. Choudary PV, Molnar M, Evans SJ, Tomita H, Li JZ, et al. (2005) Altered cortical glutamatergic and GABAergic signal transmission with glial involvement in depression. Proc Natl Acad Sci USA 102: 15653-15658 doi:10.1073/pnas.0507901102.
16. Bechtholt-Gompf AJ, Walther HV, Adams MA, Carlezon WA, Ongür D, et al. (2010) Blockade of Astrocytic Glutamate Uptake in Rats Induces Signs of Anhedonia and Impaired Spatial Memory. Neuropsychopharmacology 35: 2049-2059 doi:10.1038/npp.2010.74.
17. Walter M, Henning A, Grimm S, Schulte RF, Beck J, et al. (2009) The relationship between aberrant neuronal activation in the pregenual anterior cingulate, altered glutamatergic metabolism, and anhedonia in major depression. Arch Gen Psychiatry 66: 478-486 doi:10.1001/archgenpsychiatry.2009.39.
18. Keedwell PA, Andrew C, Williams SCR, Brammer MJ, Phillips ML, (2005) The neural correlates of anhedonia in major depressive disorder. Biol Psychiatry 58: 843-853 doi:10.1016/j.biopsych.2005.05.019.
19. Portella MJ, de Diego-Adeliño J, Gómez-Ansón B, Morgan-Ferrando R, Vives Y, et al. (2011) Ventromedial prefrontal spectroscopic abnormalities over the course of depression: a comparison among first episode, remitted recurrent and chronic patients. J Psychiatr Res 45: 427-434 doi:10.1016/j.jpsychires.2010.08.010.
20. Drevets WC, Price JL, Furey ML, (2008) Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct 213: 93-118 doi:10.1007/s00429-008-0189-x.
21. Price JL, Drevets WC, (2010) Neurocircuitry of mood disorders. Neuropsychopharmacology 35: 192-216 doi:10.1038/npp.2009.104.
22. Mayberg HS, (1997) Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatry Clin Neurosci 9: 471-481.
23. Holtzheimer PE, Mayberg HS, (2011) Stuck in a rut: rethinking depression and its treatment. Trends Neurosci 34: 1-9 doi:10.1016/j.tins.2010.10.004.
24. Stone JM, Dietrich C, Edden R, Mehta MA, De Simoni S, et al. (2012) Ketamine effects on brain GABA and glutamate levels with 1H-MRS: relationship to ketamine-induced psychopathology. Mol Psychiatry doi:10.1038/mp.2011.171.
25. Kim S-Y, Lee H, Kim H-J, Bang E, Lee S-H, et al. (2011) In vivo and ex vivo evidence for ketamine-induced hyperglutamatergic activity in the cerebral cortex of the rat: Potential relevance to schizophrenia. NMR Biomed pp. n/a-n/a doi:10.1002/nbm.1681.
26. Rowland LM, Bustillo JR, Mullins PG, Jung RE, Lenroot R, et al. (2005) Effects of ketamine on anterior cingulate glutamate metabolism in healthy humans: a 4-T proton MRS study. Am J Psychiatry 162: 394-396 doi:10.1176/appi.ajp.162.2.394.
27. Lorrain DS, Baccei CS, Bristow LJ, Anderson JJ, Varney MA, (2003) Effects of ketamine and N-methyl-D-aspartate on glutamate and dopamine release in the rat prefrontal cortex: modulation by a group II selective metabotropic glutamate receptor agonist LY379268. NSC 117: 697-706.
28. Moghaddam B, Adams B, Verma A, Daly D, (1997) Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 17: 2921-2927.
29. Alt A, Nisenbaum ES, Bleakman D, Witkin JM, (2006) A role for AMPA receptors in mood disorders. Biochem Pharmacol 71: 1273-1288 doi:10.1016/j.bcp.2005.12.022.
30. Martinowich K, Manji H, Lu B, (2007) New insights into BDNF function in depression and anxiety. Nat Neurosci 10: 1089-1093 doi:10.1038/nn1971.
31. Garcia LSB, Comim CM, Valvassori SS, Réus GZ, Barbosa LM, et al. (2008) Acute administration of ketamine induces antidepressant-like effects in the forced swimming test and increases BDNF levels in the rat hippocampus. Prog Neuropsychopharmacol Biol Psychiatry 32: 140-144 doi:10.1016/j.pnpbp.2007.07.027.
32. Valentine GW, Sanacora G, (2009) Targeting glial physiology and glutamate cycling in the treatment of depression. Biochem Pharmacol 78: 431-439 doi:10.1016/j.bcp.2009.04.008.
33. Northoff G, Walter M, Schulte RF, Beck J, Dydak U, et al. (2007) GABA concentrations in the human anterior cingulate cortex predict negative BOLD responses in fMRI. Nature Publishing Group 10: 1515-1517 doi:10.1038/nn2001.
34. Muthukumaraswamy SD, Edden RAE, Jones DK, Swettenham JB, Singh KD, (2009) Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proceedings of the National Academy of Sciences 106: 8356-8361 doi:10.1073/pnas.0900728106.
35. Horn DI, Yu C, Steiner J, Buchmann J, Kaufmann J, et al. (2010) Glutamatergic and resting-state functional connectivity correlates of severity in major depression- the role of pregenual anterior cingulate cortex and anterior insula. Front Syst Neurosci 4doi:10.3389/fnsys.2010.00033.
36. Duncan NW, Enzi B, Wiebking C, Northoff G, (2011) Involvement of glutamate in rest-stimulus interaction between perigenual and supragenual anterior cingulate cortex: A combined fMRI-MRS study. Hum Brain Mapp pp. n/a-n/a doi:10.1002/hbm.21179.
37. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, et al. (2001) A default mode of brain function. Proc Natl Acad Sci USA 98: 676-682 doi:10.1073/pnas.98.2.676.
38. Grimm S, Boesiger P, Beck J, Schuepbach D, Bermpohl F, et al. (2009) Altered negative BOLD responses in the default-mode network during emotion processing in depressed subjects. Neuropsychopharmacology 34: 932-843 doi:10.1038/npp.2008.81.
39. Sheline YI, Barch DM, Price JL, Rundle MM, Vaishnavi SN, et al. (2009) The default mode network and self-referential processes in depression. Proceedings of the National Academy of Sciences 106: 1942-1947 doi:10.1073/pnas.0812686106.
40. Salvadore G, Cornwell BR, Colon-Rosario V, Coppola R, Grillon C, et al. (2009) Increased anterior cingulate cortical activity in response to fearful faces: a neurophysiological biomarker that predicts rapid antidepressant response to ketamine. Biol Psychiatry 65: 289-295 doi:10.1016/j.biopsych.2008.08.014.
41. Fox MD, Greicius M, (2010) Clinical applications of resting state functional connectivity. Front Syst Neurosci 4: 19 doi:10.3389/fnsys.2010.00019.
42. Friston K, (2011) Functional and Effective Connectivity: A Review. Brain Connect 1: 1-24 doi:10.1089/brain.2011.0008.
43. Anand A, Li Y, Wang Y, Wu J, Gao S, et al. (2005) Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. BPS 57: 1079-1088 doi:10.1016/j.biopsych.2005.02.021.
44. Greicius MD, Flores BH, Menon V, Glover GH, Solvason HB, et al. (2007) Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 62: 429-437 doi:10.1016/j.biopsych.2006.09.020.
45. Zhou Y, Yu C, Zheng H, Liu Y, Song M, et al. (2010) Increased neural resources recruitment in the intrinsic organization in major depression. J Affect Disord 121: 220-230 doi:10.1016/j.jad.2009.05.029.
46. Sheline YI, Price JL, Yan Z, Mintun MA, (2010) Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proceedings of the National Academy of Sciences 107: 11020-11025 doi:10.1073/pnas.1000446107.
47. Mccabe C, Mishor Z, Filippini N, Cowen PJ, Taylor MJ, et al. (2011) SSRI administration reduces resting state functional connectivity in dorso-medial prefrontal cortex. Mol Psychiatry 16: 592-594 doi:10.1038/mp.2010.138.
48. McCabe C, Mishor Z, (2011) Antidepressant medications reduce subcortical-cortical resting-state functional connectivity in healthy volunteers. NeuroImage 57: 1317-1323 doi:10.1016/j.neuroimage.2011.05.051.
49. Sinner B, Graf BM, (2008) Ketamine. Handb Exp Pharmacol pp. 313-333 doi:10.1007/978-3-540-74806-9_15.
50. Dittrich A, (1998) The standardized psychometric assessment of altered states of consciousness (ASCs) in humans. Pharmacopsychiatry 31 (Suppl 2):: 80-84 doi:10.1055/s-2007-979351.
51. Spielberger CD, Gorsuch RL, Edward LR (1970) STAI manual for the state-trait anxiety inventory ("Self-evaluation questionnaire").
52. Snaith RP, Hamilton M, Morley S, Humayan A, Hargreaves D, et al. (1995) A scale for the assessment of hedonic tone the Snaith-Hamilton Pleasure Scale. Br J Psychiatry 167: 99-103.
53. Chao-Gan Y, Yu-Feng Z, (2010) DPARSF: A MATLAB Toolbox for "Pipeline" Data Analysis of Resting-State fMRI. Front Syst Neurosci 4: 13 doi:10.3389/fnsys.2010.00013.
54. Song X-W, Dong Z-Y, Long X-Y, Li S-F, Zuo X-N, et al. (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE 6: e25031 doi:10.1371/journal.pone.0025031.
55. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, et al. (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15: 273-289 doi:10.1006/nimg.2001.0978.
56. Musso F, Brinkmeyer J, Ecker D, London MK, Thieme G, et al. (2011) Ketamine effects on brain function- Simultaneous fMRI/EEG during a visual oddball task. NeuroImage 58: 508-525 doi:10.1016/j.neuroimage.2011.06.045.
57. Nagels A, Kirner-Veselinovic A, Krach S, Kircher T, (2011) Neural correlates of S-ketamine induced psychosis during overt continuous verbal fluency. NeuroImage 54: 1307-1314 doi:10.1016/j.neuroimage.2010.08.021.
58. Abel KM, Allin MPG, Kucharska-Pietura K, Andrew C, Williams S, et al. (2003) Ketamine and fMRI BOLD signal: distinguishing between effects mediated by change in blood flow versus change in cognitive state. Hum Brain Mapp 18: 135-145 doi:10.1002/hbm.10064.
59. Abel KM, Allin MPG, Kucharska-Pietura K, David A, Andrew C, et al. (2003) Ketamine alters neural processing of facial emotion recognition in healthy men: an fMRI study. Neuroreport 14: 387-391 doi:10.1097/01.wnr.0000058031.29600.31.
60. Honey RAE, Honey GD, O'Loughlin C, Sharar SR, Kumaran D, et al. (2004) Acute ketamine administration alters the brain responses to executive demands in a verbal working memory task: an FMRI study. Neuropsychopharmacology 29: 1203-1214 doi:10.1038/sj.npp.1300438.
61. Northoff G, Richter A, Bermpohl F, Grimm S, Martin E, et al. (2005) NMDA hypofunction in the posterior cingulate as a model for schizophrenia: an exploratory ketamine administration study in fMRI. Schizophr Res 72: 235-248 doi:10.1016/j.schres.2004.04.009.
62. Fu CHY, Abel KM, Allin MPG, Gasston D, Costafreda SG, et al. (2005) Effects of ketamine on prefrontal and striatal regions in an overt verbal fluency task: a functional magnetic resonance imaging study. Psychopharmacology 183: 92-102 doi:10.1007/s00213-005-0154-9.
63. Buckner RL, Andrews-Hanna JR, Schacter DL, (2008) The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124: 1-38 doi:10.1196/annals.1440.011.
64. Hamilton JP, Furman DJ, Chang C, Thomason ME, Dennis E, et al. (2011) Default-Mode and Task-Positive Network Activity in Major Depressive Disorder: Implications for Adaptive and Maladaptive Rumination. Biol Psychiatry 70: 327-333 doi:10.1016/j.biopsych.2011.02.003.
65. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, et al. (2005) Deep brain stimulation for treatment-resistant depression. Neuron 45: 651-660 doi:10.1016/j.neuron.2005.02.014.
66. Drevets WC, Savitz J, Trimble M, (2008) The subgenual anterior cingulate cortex in mood disorders. CNS Spectr 13: 663-681.