Large-Scale Persistent Network Reconfiguration Induced by Ketamine in Anesthetized Monkeys: Relevance to Mood Disorders

Biological Psychiatry

Volumn 79, Issue 9, 2016, Pages 765-775

  Lv, Qian ^a   Yang, Liqin ^a   Li, Guoliang ^b   Wang, Zhiwei ^a   Shen, Zhuangming ^a   Yu, Wenwen ^a   Jiang, Qinying ^a   Hou, Baoyu ^a   Pu, Jian ^a   Hu, Hailan ^a   Wang, Zheng ^a  

^a Institute of Neuroscience   (China)

^b Department of Anesthesiology ^*  (China)

Author keywords

Functional connectivity; Graph theory; Ketamine; Macaque monkey; Mood disorders; Neural network plasticity

Indexed keywords

ANTIDEPRESSANT AGENT; KETAMINE; PLACEBO; SODIUM CHLORIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR CINGULATE; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DEPRESSION; DOWN REGULATION; ECHO PLANAR IMAGING; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GLOBUS PALLIDUS; GUSTATORY CORTEX; HYPOTHALAMUS; MACACA FASCICULARIS; MALE; MEDIAL PREFRONTAL CORTEX; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; NUCLEUS ACCUMBENS; ORBITAL CORTEX; POSTERIOR CINGULATE; POSTERIOR INSULA; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUTAMEN; REWARD; RHESUS MONKEY; SECONDARY SOMATOSENSORY CORTEX; TEMPORAL CORTEX; THALAMUS; THEORETICAL STUDY; WHOLE BODY MRI; WHOLE BODY SCANNER; ANIMAL; BIOLOGICAL MODEL; BRAIN; BRAIN MAPPING; DRUG EFFECTS; MOOD DISORDERS; NERVE CELL PLASTICITY; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES;

ANIMALS; ANTIDEPRESSIVE AGENTS; BRAIN; BRAIN MAPPING; FEMALE; KETAMINE; MACACA FASCICULARIS; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; MOOD DISORDERS; NEURAL PATHWAYS; NEURONAL PLASTICITY;

EID: 84925949874     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2015.02.028     Document Type: Article

References (67)

1. Price, J.L., Drevets, W.C., Neurocircuitry of mood disorders. Neuropsychopharmacology 35 (2010), 192–216.
2. Sesack, S.R., Grace, A.A., Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35 (2010), 27–47.
3. Krishnan, V., Nestler, E.J., Linking molecules to mood: new insight into the biology of depression. Am J Psychiatry 167 (2010), 1305–1320.
4. Castren, E., Neuronal network plasticity and recovery from depression. JAMA Psychiatry 70 (2013), 983–989.
5. Mayberg, H.S., Liotti, M., Brannan, S.K., McGinnis, S., Mahurin, R.K., Jerabek, P.A., et al. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 156 (1999), 675–682.
6. Nestler, E.J., Carlezon, W.A. Jr, The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59 (2006), 1151–1159.
7. Duman, R.S., Aghajanian, G.K., Synaptic dysfunction in depression: potential therapeutic targets. Science 338 (2012), 68–72.
8. Berman, R.M., Cappiello, A., Anand, A., Oren, D.A., Heninger, G.R., Charney, D.S., et al. Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 47 (2000), 351–354.
9. Zarate, C.A. Jr, Singh, J.B., Carlson, P.J., Brutsche, N.E., Ameli, R., Luckenbaugh, D.A., et al. A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 63 (2006), 856–864.
10. Price, R.B., Nock, M.K., Charney, D.S., Mathew, S.J., Effects of intravenous ketamine on explicit and implicit measures of suicidality in treatment-resistant depression. Biol Psychiatry 66 (2009), 522–526.
11. Autry, A.E., Adachi, M., Nosyreva, E., Na, E.S., Los, M.F., Cheng, P.F., et al. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475 (2011), 91–95.
12. Li, N., Lee, B., Liu, R.J., Banasr, M., Dwyer, J.M., Iwata, M., et al. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329 (2010), 959–964.
13. Murrough, J.W., Perez, A.M., Pillemer, S., Stern, J., Parides, M.K., aan het Rot, M., et al. Rapid and longer-term antidepressant effects of repeated ketamine infusions in treatment-resistant major depression. Biol Psychiatry 74 (2013), 250–256.
14. Sanacora, G., Zarate, C.A., Krystal, J.H., Manji, H.K., Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat Rev Drug Discov 7 (2008), 426–437.
15. Zunszain, P.A., Horowitz, M.A., Cattaneo, A., Lupi, M.M., Pariante, C.M., Ketamine: synaptogenesis, immunomodulation and glycogen synthase kinase-3 as underlying mechanisms of its antidepressant properties. Mol Psychiatry 18 (2013), 1236–1241.
16. Krystal, J.H., Sanacora, G., Duman, R.S., Rapid-acting glutamatergic antidepressants: the path to ketamine and beyond. Biol Psychiatry 73 (2013), 1133–1141.
17. Aan Het Rot, M., Zarate, C.A. Jr, Charney, D.S., Mathew, S.J., Ketamine for depression: where do we go from here?. Biol Psychiatry 72 (2012), 537–547.
18. Sinner, B., Graf, B.M., Ketamine. Handb Exp Pharmacol 182 (2008), 313–333.
19. Vincent, J.L., Patel, G.H., Fox, M.D., Snyder, A.Z., Baker, J.T., Van Essen, D.C., et al. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447 (2007), 83–86.
20. Margulies, D.S., Vincent, J.L., Kelly, C., Lohmann, G., Uddin, L.Q., Biswal, B.B., et al. Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci U S A 106 (2009), 20069–20074.
21. Matsui, T., Tamura, K., Koyano, K.W., Takeuchi, D., Adachi, Y., Osada, T., et al. Direct comparison of spontaneous functional connectivity and effective connectivity measured by intracortical microstimulation: an fMRI study in macaque monkeys. Cereb Cortex 21 (2011), 2348–2356.
22. Logothetis, N.K., Eschenko, O., Murayama, Y., Augath, M., Steudel, T., Evrard, H.C., et al. Hippocampal-cortical interaction during periods of subcortical silence. Nature 491 (2012), 547–553.
23. Hutchison, R.M., Womelsdorf, T., Gati, J.S., Everling, S., Menon, R.S., Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Hum Brain Mapp 34 (2013), 2154–2177.
24. Wang, Z., Chen, L.M., Negyessy, L., Friedman, R.M., Mishra, A., Gore, J.C., et al. The relationship of anatomical and functional connectivity to resting-state connectivity in primate somatosensory cortex. Neuron 78 (2013), 1116–1126.
25. Mars, R.B., Jbabdi, S., Sallet, J., O׳Reilly, J.X., Croxson, P.L., Olivier, E., et al. Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J Neurosci 31 (2011), 4087–4100.
26. Hutchison, R.M., Hutchison, M., Manning, K.Y., Menon, R.S., Everling, S., Isoflurane induces dose-dependent alterations in the cortical connectivity profiles and dynamic properties of the brain׳s functional architecture. Hum Brain Mapp 35 (2014), 5754–5775.
27. Sallet, J., Mars, R.B., Noonan, M.P., Neubert, F.X., Jbabdi, S., O׳Reilly, J.X., et al. The organization of dorsal frontal cortex in humans and macaques. J Neurosci 33 (2013), 12255–12274.
28. Hutchison, R.M., Everling, S., Monkey in the middle: why non-human primates are needed to bridge the gap in resting-state investigations. Front Neuroanat, 6, 2012, 29.
29. Groman, S.M., Jentsch, J.D., Identifying the molecular basis of inhibitory control deficits in addictions: neuroimaging in non-human primates. Curr Opin Neurobiol 23 (2013), 625–631.
30. Berton, O., Hahn, C.G., Thase, M.E., Are we getting closer to valid translational models for major depression?. Science 338 (2012), 75–79.
31. Capitanio, J.P., Emborg, M.E., Contributions of non-human primates to neuroscience research. Lancet 371 (2008), 1126–1135.
32. Gil-da-Costa, R., Stoner, G.R., Fung, R., Albright, T.D., Nonhuman primate model of schizophrenia using a noninvasive EEG method. Proc Natl Acad Sci U S A 110 (2013), 15425–15430.
33. Driesen, N.R., McCarthy, G., Bhagwagar, Z., Bloch, M.H., Calhoun, V.D., D׳Souza, D.C., et al. The impact of NMDA receptor blockade on human working memory-related prefrontal function and connectivity. Neuropsychopharmacology 38 (2013), 2613–2622.
34. Scheidegger, M., Walter, M., Lehmann, M., Metzger, C., Grimm, S., Boeker, H., et al. Ketamine decreases resting state functional network connectivity in healthy subjects: implications for antidepressant drug action. PLoS One, 7, 2012, e44799.
35. Gass, N., Schwarz, A.J., Sartorius, A., Schenker, E., Risterucci, C., Spedding, M., et al. Sub-anesthetic ketamine modulates intrinsic BOLD connectivity within the hippocampal-prefrontal circuit in the rat. Neuropsychopharmacology 39 (2014), 895–906.
36. Bullmore, E., Sporns, O., Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10 (2009), 186–198.
37. Zalesky, A., Fornito, A., Bullmore, E.T., Network-based statistic: identifying differences in brain networks. Neuroimage 53 (2010), 1197–1207.
38. Yamamoto, S., Ohba, H., Nishiyama, S., Harada, N., Kakiuchi, T., Tsukada, H., et al. Subanesthetic doses of ketamine transiently decrease serotonin transporter activity: a PET study in conscious monkeys. Neuropsychopharmacology 38 (2013), 2666–2674.
39. Van Essen, D.C., Drury, H.A., Dickson, J., Harwell, J., Hanlon, D., Anderson, C.H., An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inform Assoc 8 (2001), 443–459.
40. Rohlfing, T., Kroenke, C.D., Sullivan, E.V., Dubach, M.F., Bowden, D.M., Grant, K.A., et al. The INIA19 template and NeuroMaps atlas for primate brain image parcellation and spatial normalization. Front Neuroinform, 6, 2012, 27.
41. Achard, S., Bullmore, E., Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3 (2007), 174–183.
42. Bassett, D.S., Bullmore, E., Verchinski, B.A., Mattay, V.S., Weinberger, D.R., Meyer-Lindenberg, A., Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci 28 (2008), 9239–9248.
43. Watts, D.J., Strogatz, S.H., Collective dynamics of ׳small-world׳ networks. Nature 393 (1998), 440–442.
44. Rubinov, M., Sporns, O., Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52 (2010), 1059–1069.
45. Maslov, S., Sneppen, K., Specificity and stability in topology of protein networks. Science 296 (2002), 910–913.
46. Zhang, J., Wang, J., Wu, Q., Kuang, W., Huang, X., He, Y., et al. Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biol Psychiatry 70 (2011), 334–342.
47. Pizzagalli, D.A., Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology 36 (2011), 183–206.
48. Leistedt, S.J., Coumans, N., Dumont, M., Lanquart, J.P., Stam, C.J., Linkowski, P., Altered sleep brain functional connectivity in acutely depressed patients. Hum Brain Mapp 30 (2009), 2207–2219.
49. Ma, Y., Neuropsychological mechanism underlying antidepressant effect: a systematic meta-analysis. Mol Psychiatry 20 (2015), 311–319.
50. Greicius, M.D., Flores, B.H., Menon, V., Glover, G.H., Solvason, H.B., Kenna, H., et al. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 62 (2007), 429–437.
51. Sheline, Y.I., Price, J.L., Yan, Z., Mintun, M.A., Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proc Natl Acad Sci U S A 107 (2010), 11020–11025.
52. Hasler, G., Northoff, G., Discovering imaging endophenotypes for major depression. Mol Psychiatry 16 (2011), 604–619.
53. Posner, J., Hellerstein, D.J., Gat, I., Mechling, A., Klahr, K., Wang, Z., et al. Antidepressants normalize the default mode network in patients with dysthymia. JAMA Psychiatry 70 (2013), 373–382.
54. Frodl, T., Bokde, A.L., Scheuerecker, J., Lisiecka, D., Schoepf, V., Hampel, H., et al. Functional connectivity bias of the orbitofrontal cortex in drug-free patients with major depression. Biol Psychiatry 67 (2010), 161–167.
55. Hasler, G., Drevets, W.C., Manji, H.K., Charney, D.S., Discovering endophenotypes for major depression. Neuropsychopharmacology 29 (2004), 1765–1781.
56. Meng, C., Brandl, F., Tahmasian, M., Shao, J.M., Manoliu, A., Scherr, M., et al. Aberrant topology of striatum׳s connectivity is associated with the number of episodes in depression. Brain 137 (2014), 598–609.
57. Li, B., Piriz, J., Mirrione, M., Chung, C., Proulx, C.D., Schulz, D., et al. Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature 470 (2011), 535–539.
58. Li, K., Zhou, T., Liao, L., Yang, Z., Wong, C., Henn, F., et al. betaCaMKII in lateral habenula mediates core symptoms of depression. Science 341 (2013), 1016–1020.
59. Hamani, C., Mayberg, H., Stone, S., Laxton, A., Haber, S., Lozano, A.M., The subcallosal cingulate gyrus in the context of major depression. Biol Psychiatry 69 (2011), 301–308.
60. Mayberg, H.S., Targeted electrode-based modulation of neural circuits for depression. J Clin Invest 119 (2009), 717–725.
61. Mayberg, H.S., Lozano, A.M., Voon, V., McNeely, H.E., Seminowicz, D., Hamani, C., et al. Deep brain stimulation for treatment-resistant depression. Neuron 45 (2005), 651–660.
62. Bewernick, B.H., Hurlemann, R., Matusch, A., Kayser, S., Grubert, C., Hadrysiewicz, B., et al. Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression. Biol Psychiatry 67 (2010), 110–116.
63. Koenigs, M., Grafman, J., The functional neuroanatomy of depression: distinct roles for ventromedial and dorsolateral prefrontal cortex. Behav Brain Res 201 (2009), 239–243.
64. Schaefer, A., Burmann, I., Regenthal, R., Arelin, K., Barth, C., Pampel, A., et al. Serotonergic modulation of intrinsic functional connectivity. Curr Biol 24 (2014), 2314–2318.
65. McCabe, C., Mishor, Z., Filippini, N., Cowen, P.J., Taylor, M.J., Harmer, C.J., SSRI administration reduces resting state functional connectivity in dorso-medial prefrontal cortex. Mol Psychiatry 16 (2011), 592–594.
66. McCabe, C., Mishor, Z., Antidepressant medications reduce subcortical-cortical resting-state functional connectivity in healthy volunteers. Neuroimage 57 (2011), 1317–1323.
67. Krystal, J.H., Karper, L.P., Seibyl, J.P., Freeman, G.K., Delaney, R., Bremner, J.D., et al. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 51 (1994), 199–214.