Two cellular hypotheses explaining the initiation of ketamine's antidepressant actions: Direct inhibition and disinhibition

Neuropharmacology

Volumn 100, Issue , 2016, Pages 17-26

  Miller, Oliver H ^a   Moran, Jacqueline T ^a   Hall, Benjamin J ^a,b  

^a Tulane University   (United States)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Ambient glutamate; AMPA receptor; AMPAR; Cortex; Depression; Disinhibition; GluN2B; Homeostatic synaptic plasticity; Inhibition; Ketamine; NMDA receptor; NMDAR; Protein synthesis

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; GLUTAMIC ACID; KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NEUROTRANSMITTER; AMINO ACID RECEPTOR BLOCKING AGENT; AMPA RECEPTOR; ANTIDEPRESSANT AGENT; PROTEIN SUBUNIT;

ANTIDEPRESSANT ACTIVITY; BRAIN REGION; DRUG BINDING; ELECTROCONVULSIVE THERAPY; GAMMA RHYTHM; GENETIC MANIPULATION; HUMAN; IN VITRO STUDY; INTERNEURON; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE EXCITABILITY; NEUROTRANSMITTER RELEASE; NONHUMAN; OSCILLATION; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PYRAMIDAL NERVE CELL; REVIEW; SYNAPTIC TRANSMISSION; ANIMAL; BIOLOGICAL MODEL; BRAIN; DEPRESSIVE DISORDER, MAJOR; DEPRESSIVE DISORDER, TREATMENT-RESISTANT; DRUG EFFECTS; METABOLISM; NERVE CELL; NERVE CELL INHIBITION; PROTEIN SUBUNIT;

ANIMALS; ANTIDEPRESSIVE AGENTS; BRAIN; DEPRESSIVE DISORDER, MAJOR; DEPRESSIVE DISORDER, TREATMENT-RESISTANT; ELECTROCONVULSIVE THERAPY; EXCITATORY AMINO ACID ANTAGONISTS; GLUTAMIC ACID; HUMANS; INTERNEURONS; KETAMINE; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURONAL PLASTICITY; NEURONS; PROTEIN SUBUNITS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84942367095     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.07.028     Document Type: Review

References (100)

1. C.C. Abbott, and et al. Hippocampal structural and functional changes associated with electroconvulsive therapy response Transl. Psychiatry 4 2014 e483
2. C.C. Abbott, P. Gallegos, N. Rediske, N.T. Lemke, and D.K. Quinn A review of longitudinal electroconvulsive therapy: neuroimaging investigations J. Geriatr. Psychiatry Neurol. 27 2014 33 46
3. M.C. Angulo, J. Rossier, and E. Audinat Postsynaptic glutamate receptors and integrative properties of fast-spiking interneurons in the rat neocortex J. Neurophysiol. 82 1999 1295 1302
4. D. Atasoy, and et al. Spontaneous and evoked glutamate release activates two populations of NMDA receptors with limited overlap J. Neurosci. 28 2008 10151 10166
5. A.E. Autry, and et al. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses Nature 475 2011 91 95
6. M. Bal, and et al. Reelin mobilizes a VAMP7-dependent synaptic vesicle pool and selectively augments spontaneous neurotransmission Neuron 80 2013 934 946
7. M. Banasr, and R.S. Duman Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors Biol. Psychiatry 64 2008 863 870
8. M. Banasr, and et al. Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole Mol. Psychiatry 15 2010 501 511
9. J.E. Belforte, and et al. Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes Nat. Neurosci. 13 2010 76 83
10. R.M. Berman, and et al. Antidepressant effects of ketamine in depressed patients Biol. Psychiatry 47 2000 351 354
11. F. Bouckaert, and et al. ECT: its brain enabling effects: a review of electroconvulsive therapy-induced structural brain plasticity J. ECT 30 2014 143 151
12. C. Boudaba, D.M. Linn, K.C. Halmos, and J.G. Tasker Increased tonic activation of presynaptic metabotropic glutamate receptors in the rat supraoptic nucleus following chronic dehydration J. Physiol. 551 2003 815 823
13. B.P. Brennan, and et al. Rapid enhancement of glutamatergic neurotransmission in bipolar depression following treatment with riluzole Neuropsychopharmacology 35 2010 834 846
14. G. Buzsáki, and J.J. Chrobak Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks Curr. Opin. Neurobiol. 5 1995 504 510
15. F.V. Caixeta, A.M. Cornélio, R. Scheffer-Teixeira, S. Ribeiro, and A.B.L. Tort Ketamine alters oscillatory coupling in the hippocampus Sci. Rep. 3 2013 2348
16. M. Carlén, and et al. A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior Mol. Psychiatry 17 2012 537 548
17. 13C]-nuclear magnetic resonance spectroscopy measures of ketamine's effect on amino acid neurotransmitter metabolism Biol. Psychiatry 71 2012 1022 1025
18. R.S. Ehrlichman, and et al. N-methyl-d-aspartic acid receptor antagonist-induced frequency oscillations in mice recreate pattern of electrophysiological deficits in schizophrenia Neuroscience 158 2009 705 712
19. F. Farzan, N.N. Boutros, D.M. Blumberger, and Z.J. Daskalakis What does the electroencephalogram tell us about the mechanisms of action of ECT in major depressive disorders? J. ECT 30 2014 98 106
20. P. Fatt, and B. Katz Spontaneous subthreshold activity at motor nerve endings J. Physiol. 117 1952 109 128
21. Frankowska, M., Filip, M., Przegaliński, E. Effects of GABAB receptor ligands in animal tests of depression and anxiety. Pharmacol. Rep. 59, 645-655.
22. M.E. Frizzo, S. dos, L.P. Dall'Onder, K.B. Dalcin, and D.O. Souza Riluzole enhances glutamate uptake in rat astrocyte cultures Cell. Mol. Neurobiol. 24 2004 123 128
23. E. Fumagalli, M. Funicello, T. Rauen, M. Gobbi, and T. Mennini Riluzole enhances the activity of glutamate transporters GLAST, GLT1 and EAAC1 Eur. J. Pharmacol. 578 2008 171 176
24. G. Gonzalez-Burgos, and D.A. Lewis NMDA receptor hypofunction, parvalbumin-positive neurons, and cortical gamma oscillations in schizophrenia Schizophr. Bull. 38 2012 950 957
25. S.L. Gourley, J.W. Espitia, G. Sanacora, and J.R. Taylor Antidepressant-like properties of oral riluzole and utility of incentive disengagement models of depression in mice Psychopharmacology (Berl.). 219 2012 805 814
26. J.A. Gray, and et al. Distinct modes of AMPA receptor suppression at developing synapses by GluN2A and GluN2B: single-cell NMDA receptor subunit deletion in vivo Neuron 71 2011 1085 1101
27. H. Guo, and et al. Increased expression of the glial glutamate transporter EAAT2 modulates excitotoxicity and delays the onset but not the outcome of ALS in mice Hum. Mol. Genet. 12 2003 2519 2532
28. A. Gupta, L.A. Devi, and I. Gomes Potentiation of μ-opioid receptor-mediated signaling by ketamine J. Neurochem. 119 2011 294 302
29. T. Hakami, and et al. NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness PLoS One 4 2009 e6755
30. J.E. Hanson, and et al. GluN2B antagonism affects interneurons and leads to immediate and persistent changes in synaptic plasticity, oscillations, and behavior Neuropsychopharmacology 38 2013 1221 1233
31. J.E. Heuser, and et al. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release J. Cell Biol. 81 1979 275 300
32. H. Homayoun, and B. Moghaddam NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons J. Neurosci. 27 2007 11496 11500
33. L.E. Hong, and et al. Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine Neuropsychopharmacology 35 2009 632 640
34. C. Hull, H. Adesnik, and M. Scanziani Neocortical disynaptic inhibition requires somatodendritic integration in interneurons J. Neurosci. 29 2009 8991 8995
35. L. Ibrahim, and et al. Course of improvement in depressive symptoms to a single intravenous infusion of ketamine vs add-on riluzole: results from a 4-week, double-blind, placebo-controlled study Neuropsychopharmacology 37 2012 1526 1533
36. L. Jiménez-Sánchez, L. Campa, Y.P. Auberson, and A. Adell The role of GluN2A and GluN2B subunits on the effects of NMDA receptor antagonists in modeling schizophrenia and treating refractory depression Neuropsychopharmacology 39 2014 2673 2680
37. M.M. Karnani, M. Agetsuma, and R. Yuste A blanket of inhibition: functional inferences from dense inhibitory connectivity Curr. Opin. Neurobiol. 26 2014 96 102
38. K. Kashiwagi Channel blockers acting at n-methyl-d-aspartate receptors: differential effects of mutations in the vestibule and ion channel pore Mol. Pharmacol. 61 2002 533 545
39. O. Kekesi, and et al. Long-lasting, distinct changes in central opioid receptor and urinary bladder functions in models of schizophrenia in rats Eur. J. Pharmacol. 661 2011 35 41
40. C. Kiselycznyk, and et al. NMDA receptor subunits and associated signaling molecules mediating antidepressant-related effects of NMDA-GluN2B antagonism Behav. Brain Res. 2015 10.1016/j.bbr.2015.03.023
41. B. Kocsis Differential role of NR2A and NR2B subunits in N-methyl-D-aspartate receptor antagonist-induced aberrant cortical gamma oscillations Biol. Psychiatry 71 2012 987 995
42. B. Kocsis State-dependent increase of cortical gamma activity during REM sleep after selective blockade of NR2B subunit containing NMDA receptors Sleep 35 2012 1011 1016
43. H. Koike, M. Iijima, and S. Chaki Involvement of AMPA receptor in both the rapid and sustained antidepressant-like effects of ketamine in animal models of depression Behav. Brain Res. 224 2011 107 111
44. T. Korotkova, E.C. Fuchs, A. Ponomarenko, J. von Engelhardt, and H. Monyer NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory Neuron 68 2010 557 569
45. S.E. Kotermanski, and J.W. Johnson Mg2+ imparts NMDA receptor subtype selectivity to the Alzheimer's drug memantine J. Neurosci. 29 2009 2774 2779
46. N. Li, and et al. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists Science 329 2010 959 964
47. Q. Li, S. Clark, D.V. Lewis, and W.A. Wilson NMDA receptor antagonists disinhibit rat posterior cingulate and retrosplenial cortices: a potential mechanism of neurotoxicity J. Neurosci. 22 2002 3070 3080
48. B.K. Lim, K.W. Huang, B.A. Grueter, P.E. Rothwell, and R.C. Malenka Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens Nature 487 2012 183 189
49. T.-Y. Liu, and et al. Different patterns of abnormal gamma oscillatory activity in unipolar and bipolar disorder patients during an implicit emotion task Neuropsychologia 50 2012 1514 1520
50. S. Maeng, and et al. Cellular mechanisms underlying the antidepressant effects of ketamine: role of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors Biol. Psychiatry 63 2008 349 352
51. E.O. Mann, and I. Mody Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons Nat. Neurosci. 13 2009 205 212
52. J.M. Mateos, and et al. Synaptic modifications at the CA3-CA1 synapse after chronic AMPA receptor blockade in rat hippocampal slices J. Physiol. 581 2007 129 138
53. R.A. McKinney Excitatory amino acid involvement in dendritic spine formation, maintenance and remodelling J. Physiol. 588 2010 107 116
54. R.A. McKinney, M. Capogna, R. Dürr, B.H. Gähwiler, and S.M. Thompson Miniature synaptic events maintain dendritic spines via AMPA receptor activation Nat. Neurosci. 2 1999 44 49
55. O.H. Miller, and et al. GluN2B-containing NMDA receptors regulate depression-like behavior and are critical for the rapid antidepressant actions of ketamine Elife 3 2014
56. M.J. Niciu, and et al. Riluzole likely lacks antidepressant efficacy in ketamine non-responders J. Psychiatr. Res. 58 2014 197 199
57. M.J. Niciu, and et al. Ketamine's antidepressant efficacy is extended for at least four weeks in subjects with a family history of an alcohol use disorder Int. J. Neuropsychopharmacol. 18 2014
58. E. Nosyreva, and et al. Acute suppression of spontaneous neurotransmission drives synaptic potentiation J. Neurosci. 33 2013 6990 7002
59. G. NyÍri, F. Stephenson, T. Freund, and P. Somogyi Large variability in synaptic n-methyl-d-aspartate receptor density on interneurons and a comparison with pyramidal-cell spines in the rat hippocampus Neuroscience 119 2003 347 363
60. T. Papouin, and et al. Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists Cell 150 2012 633 646
61. D. Pinault N-methyl d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex Biol. Psychiatry 63 2008 730 735
62. A.J. Pocklington, M. Cumiskey, J.D. Armstrong, and S.G.N. Grant The proteomes of neurotransmitter receptor complexes form modular networks with distributed functionality underlying plasticity and behaviour Mol. Syst. Biol. 2 2006 2006.0023
63. N.V. Povysheva, and J.W. Johnson Tonic NMDA receptor-mediated current in prefrontal cortical pyramidal cells and fast-spiking interneurons J. Neurophysiol. 107 2012 2232 2243
64. L. Pozzi, I.P. Dorocic, X. Wang, M. Carlén, and K. Meletis Mice lacking NMDA receptors in parvalbumin neurons display normal depression-related behavior and response to antidepressant action of NMDAR antagonists PLoS One 9 2014 e83879
65. S.H. Preskorn, and et al. An innovative design to establish proof of concept of the antidepressant effects of the NR2B subunit selective N-methyl-D-aspartate antagonist, CP-101,606, in patients with treatment-refractory major depressive disorder J. Clin. Psychopharmacol. 28 2008 631 637
66. M.C. Quirk, D.L. Sosulski, C.E. Feierstein, N. Uchida, and Z.F. Mainen A defined network of fast-spiking interneurons in orbitofrontal cortex: responses to behavioral contingencies and ketamine administration Front. Syst. Neurosci. 3 2009 13
67. J. Raingo, and et al. VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission Nat. Neurosci. 15 2012 738 745
68. G. Rajkowska, and J.J. Miguel-Hidalgo Gliogenesis and glial pathology in depression CNS Neurol. Disord. Drug Targets 6 2007 219 233
69. D.M.O. Ramirez, M. Khvotchev, B. Trauterman, and E.T. Kavalali Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission Neuron 73 2012 121 134
70. D.C. Rotaru, H. Yoshino, D.A. Lewis, G.B. Ermentrout, and G. Gonzalez-Burgos Glutamate receptor subtypes mediating synaptic activation of prefrontal cortex neurons: relevance for schizophrenia J. Neurosci. 31 2011 142 156
71. J.D. Rothstein, and et al. Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression Nature 433 2005 73 77
72. B. Rudy, G. Fishell, S. Lee, and J. Hjerling-Leffler Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons Dev. Neurobiol. 71 2011 45 61
73. H.a. Sackeim, and et al. The effects of electroconvulsive therapy on quantitative electroencephalograms. Relationship to clinical outcome Arch. Gen. Psychiatry 53 1996 814 824
74. P. Sah, S. Hestrin, and R.A. Nicoll Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons Science 246 1989 815 818
75. G. Sanacora, and et al. Preliminary evidence of riluzole efficacy in antidepressant-treated patients with residual depressive symptoms Biol. Psychiatry 61 2007 822 825
76. G. Sanacora, and et al. Lanicemine: a low-trapping NMDA channel blocker produces sustained antidepressant efficacy with minimal psychotomimetic adverse effects Mol. Psychiatry 19 2014 978 985
77. G. Sanacora, and A.F. Schatzberg Ketamine: promising path or false prophecy in the development of novel therapeutics for mood disorders? Neuropsychopharmacology 40 2015 259 267
78. Y. Sara, T. Virmani, F. Deák, X. Liu, and E.T. Kavalali An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission Neuron 45 2005 563 573
79. D.A. Slattery, S. Desrayaud, and J.F. Cryan GABAB receptor antagonist-mediated antidepressant-like behavior is serotonin-dependent J. Pharmacol. Exp. Ther. 312 2005 290 296
80. D.A. Slattery, I.D. Neumann, and J.F. Cryan Transient inactivation of the infralimbic cortex induces antidepressant-like effects in the rat J. Psychopharmacol. 25 2011 1295 1303
81. V.S. Sohal, F. Zhang, O. Yizhar, and K. Deisseroth Parvalbumin neurons and gamma rhythms enhance cortical circuit performance Nature 459 2009 698 702
82. J.M. Stone, and et al. Ketamine effects on brain GABA and glutamate levels with 1H-MRS: relationship to ketamine-induced psychopathology Mol. Psychiatry 17 2012 664 665
83. M.A. Sutton, and et al. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis Cell 125 2006 785 799
84. M.A. Sutton, N.R. Wall, G.N. Aakalu, and E.M. Schuman Regulation of dendritic protein synthesis by miniature synaptic events Science 304 2004 1979 1983
85. M.A. Sutton, A.M. Taylor, H.T. Ito, A. Pham, and E.M. Schuman Postsynaptic decoding of neural activity: eEF2 as a biochemical sensor coupling miniature synaptic transmission to local protein synthesis Neuron 55 2007 648 661
86. K. Takahashi, and et al. Riluzole rapidly attenuates hyperemotional responses in olfactory bulbectomized rats, an animal model of depression Behav. Brain Res. 216 2011 46 52
87. V. Volman, M.M. Behrens, and T.J. Sejnowski Downregulation of parvalbumin at cortical GABA synapses reduces network gamma oscillatory activity J. Neurosci. 31 2011 18137 18148
88. C.-C. Wang, and et al. A critical role for GluN2B-containing NMDA receptors in cortical development and function Neuron 72 2011 789 805
89. H.-X. Wang, and W.-J. Gao Cell type-specific development of NMDA receptors in the interneurons of rat prefrontal cortex Neuropsychopharmacology 34 2009 2028 2040
90. S.-J. Wang, K.-Y. Wang, and W.-C. Wang Mechanisms underlying the riluzole inhibition of glutamate release from rat cerebral cortex nerve terminals (synaptosomes) Neuroscience 125 2004 191 201
91. C.-C. Wang, R.G. Held, and B.J. Hall SynGAP regulates protein synthesis and homeostatic synaptic plasticity in developing cortical networks PLoS One 8 2013 e83941
92. M.R. Warden, and et al. A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge Nature 492 2012 428 432
93. E.R. Workman, F. Niere, and K.F. Raab-Graham mTORC1-dependent protein synthesis underlying rapid antidepressant effect requires GABABR signaling Neuropharmacology 73 2013 192 203
94. J.-G. Xue, and et al. NMDA receptor activation enhances inhibitory GABAergic transmission onto hippocampal pyramidal neurons via presynaptic and postsynaptic mechanisms J. Neurophysiol. 105 2011 2897 2906
95. C.A. Zarate, and et al. An open-label trial of riluzole in patients with treatment-resistant major depression Am. J. Psychiatry 161 2004 171 174
96. C.A. Zarate, and et al. An open-label trial of the glutamate-modulating agent riluzole in combination with lithium for the treatment of bipolar depression Biol. Psychiatry 57 2005 430 432
97. C.A. Zarate, and et al. A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression Arch. Gen. Psychiatry 63 2006 856 864
98. C.A. Zarate, and et al. A randomized trial of a low-trapping nonselective N-methyl-D-aspartate channel blocker in major depression Biol. Psychiatry 74 2013 257 264
99. M. Zink, B. Vollmayr, P.J. Gebicke-Haerter, and F.A. Henn Reduced expression of glutamate transporters vGluT1, EAAT2 and EAAT4 in learned helpless rats, an animal model of depression Neuropharmacology 58 2010 465 473
100. K. Zito, V. Scheuss, G. Knott, T. Hill, and K. Svoboda Rapid functional maturation of nascent dendritic spines Neuron 61 2009 247 258