Sub-anesthetic ketamine modulates intrinsic BOLD connectivity within the hippocampal-prefrontal circuit in the rat

Neuropsychopharmacology

Volumn 39, Issue 4, 2014, Pages 895-906

  Gass, Natalia ^a   Schwarz, Adam James ^b,c   Sartorius, Alexander ^a   Schenker, Esther ^d   Risterucci, Celine ^e   Spedding, Michael ^d   Zheng, Lei ^a,f   Meyer Lindenberg, Andreas ^a   Weber Fahr, Wolfgang ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Eli Lilly   (United States)

^c INDIANA UNIVERSITY   (United States)

^d INSTITUT DE RECHERCHES INTERNATIONALES SERVIER   (France)

^e F HOFFMANN LA ROCHE LTD   (Switzerland)

^f UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

functional connectivity; hippocampal prefrontal; ketamine; preclinical

Indexed keywords

ANALGESICS; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; HEART RATE; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; KETAMINE; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; OXYGEN; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; STATISTICS AS TOPIC;

EID: 84894042786     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.290     Document Type: Article

References (50)

1. Autry AE, Adachi M, Nosyreva E, Na ES, Los MF, Cheng PF et al (2011). NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475: 91-95.
2. Bandyopadhyaya D, Nizamie SH, Pradhan N, Bandyopadhyaya A (2011). Spontaneous gamma coherence as a possible trait marker of schizophrenia-An explorative study. Asian J Psychiatr 4: 172-177.
3. Chin CL, Upadhyay J, Marek GJ, Baker SJ, Zhang M, Mezler M et al (2011). Awake rat pharmacological magnetic resonance imaging as a translational pharmacodynamic biomarker: metabotropic glutamate 2/3 agonist modulation of ketamine-induced blood oxygenation level dependence signals. J Pharmacol Exp Ther 336: 709-715.
4. Cornwell BR, Salvadore G, Furey M, Marquardt CA, Brutsche NE, Grillon C et al (2012). Synaptic potentiation is critical for rapid antidepressant response to ketamine in treatment-resistant major depression. Biol Psychiatry 72: 555-561.
5. Crespo-Facorro B, Kim J, Andreasen NC, O'Leary DS, Bockholt HJ, Magnotta V (2000). Insular cortex abnormalities in schizophrenia: a structural magnetic resonance imaging study of firstepisode patients. Schizophr Res 46: 35-43.
6. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004). Neural systems supporting interoceptive awareness. Nat Neurosci 7: 189-195.
7. Crossley NA, Mechelli A, Fusar-Poli P, Broome MR, Matthiasson P, Johns LC et al (2009). Superior temporal lobe dysfunction and frontotemporal dysconnectivity in subjects at risk of psychosis and in first-episode psychosis. Hum Brain Mapp 30: 4129-4137.
8. Doyle OM, De Simoni S, Schwarz AJ, Brittain C, O'Daly OG, Williams SC et al (2013). Quantifying the attenuation of the ketamine pharmacological magnetic resonance imaging response in humans: a validation using antipsychotic and glutamatergic agents. J Pharmacol Exp Ther 345: 151-160.
9. Driesen NR, McCarthy G, Bhagwagar Z, Bloch M, Calhoun V, D'Souza DC et al (2013). Relationship of resting brain hyperconnectivity and schizophrenia-like symptoms produced by the NMDA receptor antagonist ketamine in humans. Mol Psychiatry.
10. Duncan GE, Moy SS, Knapp DJ, Mueller RA, Breese GR (1998). Metabolic mapping of the rat brain after subanesthetic doses of ketamine: potential relevance to schizophrenia. Brain Res 787: 181-190.
11. Egerton A, Brugger S, Raffin M, Barker GJ, Lythgoe DJ, McGuire PK et al (2012). Anterior cingulate glutamate levels related to clinical status following treatment in first-episode schizophrenia. Neuropsychopharmacology 37: 2515-2521.
12. Fell MJ, Katner JS, Johnson BG, Khilevich A, Schkeryantz JM, Perry KW et al (2010). Activation of metabotropic glutamate (mGlu)2 receptors suppresses histamine release in limbic brain regions following acute ketamine challenge. Neuropharmacology 58: 632-639.
13. Gass N, Schwarz AJ, Sartorius A, Cleppien D, Zheng L, Schenker E et al (2012). Haloperidol modulates midbrain-prefrontal functional connectivity in the rat brain. Eur Neuropsychopharmacol 23: 1310-1319.
14. Godsil BP, Kiss JP, Spedding M, Jay TM (2013). The hippocampalprefrontal pathway: The weak link in psychiatric disorders? Eur Neuropsychopharmacol 23: 1165-1181.
15. Goveas JS, Xie C, Ward BD, Wu Z, Li W, Franczak M et al (2011). Recovery of hippocampal network connectivity correlates with cognitive improvement in mild Alzheimer's disease patients treated with donepezil assessed by resting-state fMRI. J Magn Reson Imaging 34: 764-773.
16. Gozzi A, Schwarz A, Crestan V, Bifone A (2008). Drug-anaesthetic interaction in phMRI: the case of the psychotomimetic agent phencyclidine. Magn Reson Imaging 26: 999-1006.
17. Grunze HC, Rainnie DG, Hasselmo ME, Barkai E, Hearn EF, McCarley RW et al (1996). NMDA-dependent modulation of CA1 local circuit inhibition. J Neurosci 16: 2034-2043.
18. Grutzner C, Wibral M, Sun L, Rivolta D, Singer W, Maurer K et al (2013). Deficits in high- (460 Hz) gamma-band oscillations during visual processing in schizophrenia. Front Hum Neurosci 7: 88.
19. Hasler G, Northoff G (2011). Discovering imaging endophenotypes for major depression. Mol Psychiatry 16: 604-619.
20. Hodkinson DJ, de Groote C, McKie S, Deakin JF, Williams SR (2012). Differential effects of anaesthesia on the phMRI response to acute ketamine challenge. Br J Med Med Res 2: 373-385.
21. Immordino-Yang MH, McColl A, Damasio H, Damasio A (2009). Neural correlates of admiration and compassion. Proc Natl Acad Sci USA 106: 8021-8026.
22. Isnard J, Magnin M, Jung J, Mauguiere F, Garcia-Larrea L (2011). Does the insula tell our brain that we are in pain? Pain 152: 946-951.
23. Javitt DC, Zukin SR, Heresco-Levy U, Umbricht D (2012). Has an angel shown the way? Etiological and therapeutic implications of the PCP/NMDA model of schizophrenia. Schizophr Bull 38: 958-966.
24. Jones TB, Bandettini PA, Birn RM (2008). Integration of motion correction and physiological noise regression in fMRI. Neuroimage 42: 582-590.
25. Kamiyama H, Matsumoto M, Otani S, Kimura SI, Shimamura KI, Ishikawa S et al (2011). Mechanisms underlying ketamineinduced synaptic depression in rat hippocampus-medial prefrontal cortex pathway. Neuroscience 177: 159-169.
26. Kubota T, Anzawa N, Hirota K, Yoshida H, Kushikata T, Matsuki A (1999). Effects of ketamine and pentobarbital on noradrenaline release from the medial prefrontal cortex in rats. Can J Anaesth 46: 388-392.
27. Large CH (2007). Do NMDA receptor antagonist models of schizophrenia predict the clinical efficacy of antipsychotic drugs? J Psychopharmacol 21: 283-301.
28. Levanen J, Makela ML, Scheinin H (1995). Dexmedetomidine premedication attenuates ketamine-induced cardiostimulatory effects and postanesthetic delirium. Anesthesiology 82: 1117-1125.
29. Littlewood CL, Jones N, O'Neill MJ, Mitchell SN, Tricklebank M, Williams SC (2006). Mapping the central effects of ketamine in the rat using pharmacological MRI. Psychopharmacology (Berl) 186: 64-81.
30. 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. Neuroscience 117: 697-706.
31. Marsman A, van den Heuvel MP, Klomp DW, Kahn RS, Luijten PR, Hulshoff Pol HE (2013). Glutamate in schizophrenia: a focused review and meta-analysis of (1)H-MRS studies. Schizophr Bull 39: 120-129.
32. Meyer-Lindenberg AS, Olsen RK, Kohn PD, Brown T, Egan MF, Weinberger DR et al (2005). Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia. Arch Gen Psychiatry 62: 379-386.
33. Mion G, Villevieille T (2013). Ketamine pharmacology: an update (pharmacodynamics and molecular aspects, recent findings). CNS Neurosci Ther 19: 370-380.
34. 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.
35. Moore JW, Cambridge VC, Morgan H, Giorlando F, Adapa R, Fletcher PC (2013). Time, action and psychosis: using subjective time to investigate the effects of ketamine on sense of agency. Neuropsychologia 51: 377-384.
36. Nasrallah FA, Tan J, Chuang KH (2012). Pharmacological modulation of functional connectivity: alpha2-adrenergic receptor agonist alters synchrony but not neural activation. Neuroimage 60: 436-446.
37. Niesters M, Khalili-Mahani N, Martini C, Aarts L, van Gerven J, van Buchem MA et al (2012). Effect of subanesthetic ketamine on intrinsic functional brain connectivity: a placebo-controlled functional magnetic resonance imaging study in healthy male volunteers. Anesthesiology 117: 868-877.
38. Phillips KG, Cotel MC, McCarthy AP, Edgar DM, Tricklebank M, O'Neill MJ et al (2012). Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia. Neuropharmacology 62: 1359-1370.
39. Pinault D (2008). N-methyl d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex. Biol Psychiatry 63: 730-735.
40. Rotarska-Jagiela A, van de Ven V, Oertel-Knochel V, Uhlhaas PJ, Vogeley K, Linden DE (2010). Resting-state functional network correlates of psychotic symptoms in schizophrenia. Schizophr Res 117: 21-30.
41. Sato K, Wu J, Kikuchi T, Wang Y, Watanabe I, Okumura F (1996). Differential effects of ketamine and pentobarbitone on acetylcholine release from the rat hippocampus and striatum. Br J Anaesth 77: 381-384.
42. Scheidegger M, Walter M, Lehmann M, Metzger C, Grimm S, Boeker H et al (2012). Ketamine decreases resting state functional network connectivity in healthy subjects: implications for antidepressant drug action. PLoS One 7: e44799.
43. Schwarz AJ, Danckaert A, Reese T, Gozzi A, Paxinos G, Watson C et al (2006). A stereotaxic MRI template set for the rat brain with tissue class distribution maps and co-registered anatomical atlas: application to pharmacological MRI. Neuroimage 32: 538-550.
44. Schwarz AJ, Gass N, Sartorius A, Zheng L, Spedding M, Schenker E et al (2013). The low-frequency blood oxygenation level-dependent functional connectivity signature of the hippocampal- prefrontal network in the rat brain. Neuroscience 228: 243-258.
45. Seamans J (2008). Losing inhibition with ketamine. Nat Chem Biol 4: 91-93.
46. Tagliazucchi E, von Wegner F, Morzelewski A, Brodbeck V, Laufs H (2012). Dynamic BOLD functional connectivity in humans and its electrophysiological correlates. Front Hum Neurosci 6: 339.
47. van Buuren M, Gladwin TE, Zandbelt BB, van den Heuvel M, Ramsey NF, Kahn RS et al (2009). Cardiorespiratory effects on default-mode network activity as measured with fMRI. Hum Brain Mapp 30: 3031-3042.
48. Williams KA, Magnuson M, Majeed W, LaConte SM, Peltier SJ, Hu X et al (2010). Comparison of alpha-chloralose, medetomidine and isoflurane anesthesia for functional connectivity mapping in the rat. Magn Reson Imaging 28: 995-1003.
49. Zarate CA Jr, Singh JB, Carlson PJ, Brutsche NE, Ameli R, Luckenbaugh DA et al (2006). A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 63: 856-864.
50. Zhou Y, Shu N, Liu Y, Song M, Hao Y, Liu H et al (2008). Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr Res 100: 120-132.