Shared reduction of oscillatory natural frequencies in bipolar disorder, major depressive disorder and schizophrenia

Journal of Affective Disorders

Volumn 184, Issue , 2015, Pages 111-115

  Canali, Paola ^a   Sarasso, Simone ^b   Rosanova, Mario ^b,e   Casarotto, Silvia ^b   Sferrazza Papa, Giovanna ^a   Gosseries, Olivia ^c,d   Fecchio, Matteo ^b   Massimini, Marcello ^b   Mariotti, Maurizio ^b   Cavallaro, Roberto ^a   Smeraldi, Enrico ^a   Colombo, Cristina ^a   Benedetti, Francesco ^a  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e Fondazione Europea di Ricerca Biomedica   (Italy)

Author keywords

GABAergic circuits; Gamma oscillations; Neuropsychiatric disorders; TMS EEG

Indexed keywords

ANTIDEPRESSANT AGENT; ATYPICAL ANTIPSYCHOTIC AGENT; BENZODIAZEPINE DERIVATIVE; LITHIUM SALT; MOOD STABILIZER; NEUROLEPTIC AGENT;

ADULT; ARTICLE; BETA RHYTHM; BIPOLAR DISORDER; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EVENT RELATED POTENTIAL; FEMALE; GAMMA RHYTHM; HAMILTON DEPRESSION RATING SCALE; HUMAN; MAJOR DEPRESSION; MALE; OSCILLATION; POSITIVE AND NEGATIVE SYNDROME SCALE; PRIORITY JOURNAL; PSYCHOPHARMACOTHERAPY; SCHIZOPHRENIA; SUPERIOR FRONTAL GYRUS; TRANSCRANIAL MAGNETIC STIMULATION; CASE CONTROL STUDY; ELECTROENCEPHALOGRAPHY; FRONTAL LOBE; MIDDLE AGED; NERVE TRACT; PATHOPHYSIOLOGY; PHYSIOLOGY; THALAMUS;

ADULT; BIPOLAR DISORDER; BRAIN WAVES; CASE-CONTROL STUDIES; DEPRESSIVE DISORDER, MAJOR; ELECTROENCEPHALOGRAPHY; FEMALE; FRONTAL LOBE; HUMANS; MALE; MIDDLE AGED; NEURAL PATHWAYS; SCHIZOPHRENIA; THALAMUS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84930935437     PISSN: 01650327     EISSN: 15732517     Source Type: Journal    
DOI: 10.1016/j.jad.2015.05.043     Document Type: Article

References (70)

1. S. Akbarian, and H.S. Huang Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders Brain Res. Rev. 52 2006 293 304
2. M.S. Barr, F. Farzan, P.M. Rusjan, R. Chen, P.B. Fitzgerald, and Z.J. Daskalakis Potentiation of gamma oscillatory activity through repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex Neuropsychopharmacology 34 2009 2359 2367
3. M. Bartos, I. Vida, and P. Jonas Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks Nat. Rev. Neurosci. 8 2007 45 56
4. E. Basar Brain oscillations in neuropsychiatric disease Dialogues Clin. Neurosci. 15 2013 291 300
5. E. Basar, and B. Guntekin A review of brain oscillations in cognitive disorders and the role of neurotransmitters Brain Res. 1235 2008 172 193
6. E. Basar, M. Schurmann, C. Basar-Eroglu, and T. Demiralp Selectively distributed gamma band system of the brain Int. J. Psychophysiol. 39 2001 129 135
7. F.M. Benes, and S. Berretta Gabaergic interneurons. implications for understanding schizophrenia and bipolar disorder Neuropsychopharmacology 25 2001 1 27
8. Z. Bhagwagar, M. Wylezinska, P. Jezzard, J. Evans, F. Ashworth, A. Sule, P.M. Matthews, and P.J. Cowen Reduction in occipital cortex gamma-aminobutyric acid concentrations in medication-free recovered unipolar depressed and bipolar subjects Biol. Psychiatry 61 2007 806 812
9. C.A. Brenner, P.D. Kieffaber, B.A. Clementz, J.K. Johannesen, A. Shekhar, B.F. O'Donnell, and W.P. Hetrick Event-related potential abnormalities in schizophrenia: a failure to "gate in" salient information? Schizophr. Res. 113 2009 332 338
10. G. Buzsaki, and B.O. Watson Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease Dialogues Clin. Neurosci. 14 2012 345 367
11. P. Canali A role for TMS/EEG in neuropsychiatric disorders Neurol. Psychiatry Brain Res. 20 2014 37 40
12. J.A. Cardin, M. Carlen, K. Meletis, U. Knoblich, F. Zhang, K. Deisseroth, L.H. Tsai, and C.I. Moore Driving fast-spiking cells induces gamma rhythm and controls sensory responses Nature 459 2009 663 667
13. A.G. Casali, S. Casarotto, M. Rosanova, M. Mariotti, and M. Massimini General indices to characterize the electrical response of the cerebral cortex to TMS Neuroimage 49 2010 1459 1468
14. R.Y. Cho, R.O. Konecky, and C.S. Carter Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia Proc. Natl. Acad. Sci. USA 103 2006 19878 19883
15. Z.J. Daskalakis, B.K. Christensen, R. Chen, P.B. Fitzgerald, R.B. Zipursky, and S. Kapur Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation Arch. Gen. Psychiatry 59 2002 347 354
16. Z.J. Daskalakis, B.K. Christensen, P.B. Fitzgerald, and R. Chen Transcranial magnetic stimulation: a new investigational and treatment tool in psychiatry J. Neuropsychiatry Clin. Neurosci. 14 2002 406 415
17. Z.J. Daskalakis, B. Moller, B.K. Christensen, P.B. Fitzgerald, C. Gunraj, and R. Chen The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects Exp. Brain Res. 174 2006 403 412
18. A. Delorme, and S. Makeig EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis J. Neurosci. Methods 134 2004 9 21
19. J. Downar, and Z.J. Daskalakis New targets for rTMS in depression: a review of convergent evidence Brain Stimul. 6 2013 231 240
20. S.K. Esser, R. Huber, M. Massimini, M.J. Peterson, F. Ferrarelli, and G. Tononi A direct demonstration of cortical LTP in humans: a combined TMS/EEG study Brain Res. Bull. 69 2006 86 94
21. F. Ferrarelli, M. Massimini, M.J. Peterson, B.A. Riedner, M. Lazar, M.J. Murphy, R. Huber, M. Rosanova, A.L. Alexander, N. Kalin, and G. Tononi Reduced evoked gamma oscillations in the frontal cortex in schizophrenia patients: a TMS/EEG study Am. J. Psychiatry 165 2008 996 1005
22. F. Ferrarelli, S. Sarasso, Y. Guller, B.A. Riedner, M.J. Peterson, M. Bellesi, M. Massimini, B.R. Postle, and G. Tononi Reduced natural oscillatory frequency of frontal thalamocortical circuits in schizophrenia Arch. Gen. Psychiatry 69 2012 766 774
23. P.B. Fitzgerald, and Z.J. Daskalakis A review of repetitive transcranial magnetic stimulation use in the treatment of schizophrenia Can. J. Psychiatry 53 2008 567 576
24. J. Gallinat, G. Winterer, C.S. Herrmann, and D. Senkowski Reduced oscillatory gamma-band responses in unmedicated schizophrenic patients indicate impaired frontal network processing Clin. Neurophysiol. 115 2004 1863 1874
25. G. Gonzalez-Burgos, and D.A. Lewis GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia Schizophr. Bull. 34 2008 944 961
26. C.M. Gray, and D.A. McCormick Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex Science 274 1996 109 113
27. A.R. Haig, E. Gordon, V. De Pascalis, R.A. Meares, H. Bahramali, and A. Harris Gamma activity in schizophrenia: evidence of impaired network binding? Clin. Neurophysiol. 111 2000 1461 1468
28. G. Hasler, J.W. van der Veen, T. Tumonis, N. Meyers, J. Shen, and W.C. Drevets Reduced prefrontal glutamate/glutamine and gamma-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy Arch. Gen. Psychiatry 64 2007 193 200
29. C.S. Herrmann, and T. Demiralp Human EEG gamma oscillations in neuropsychiatric disorders Clin. Neurophysiol. 116 2005 2719 2733
30. T. Hill, and P. Lewicki General linear models StatSoft ed. Statistics: Methods and Applications: A Comprehensive Reference for Science, Industry, and Data Mining 2006 StatSoft. Tulsa, OK 245 276
31. S. Komssi, P. Savolainen, J. Heiskala, and S. Kahkonen Excitation threshold of the motor cortex estimated with transcranial magnetic stimulation electroencephalography NeuroReport 18 2007 13 16
32. P.S. Lee, Y.S. Chen, J.C. Hsieh, T.P. Su, and L.F. Chen Distinct neuronal oscillatory responses between patients with bipolar and unipolar disorders: a magnetoencephalographic study J. Affect. Disord. 123 2010 270 275
33. J.S. Kwon, B.F. O'Donnell, G.V. Wallenstein, R.W. Greene, Y. Hirayasu, P.G. Nestor, M.E. Hasselmo, G.F. Potts, M.WE. Shenton, and R.W McCarley Gamma frequency-range abnormalities to auditory stimulation in schizophrenia Arch Gen Psychiatry 56 1999 1001 1005
34. J.P. Lefaucheur, B. Lucas, F. Andraud, J.Y. Hogrel, F. Bellivier, A. Del Cul, A. Rousseva, M. Leboyer, and M.L. Paillere-Martinot Inter-hemispheric asymmetry of motor corticospinal excitability in major depression studied by transcranial magnetic stimulation J. Psychiatr. Res. 42 2008 389 398
35. A.J. Levinson, P.B. Fitzgerald, G. Favalli, D.M. Blumberger, M. Daigle, and Z.J. Daskalakis Evidence of cortical inhibitory deficits in major depressive disorder Biol. Psychiatry 67 2010 458 464
36. A.J. Levinson, L.T. Young, P.B. Fitzgerald, and Z.J. Daskalakis Cortical inhibitory dysfunction in bipolar disorder: a study using transcranial magnetic stimulation J. Clin. Psychopharmacol. 27 2007 493 497
37. D.A. Lewis, T. Hashimoto, and D.W. Volk Cortical inhibitory neurons and schizophrenia Nat. Rev. Neurosci. 6 2005 312 324
38. Light G.A., Hsu xJ.L., Hsieh M.H., Meyer-Gomes K., Sprock J., Swerdlow N.R., and Braff D.L., Gamma band oscillations reveal neural network cortical coherence dysfunction in schizophrenia patients Biol Psychiatry 2006 1231 1240
39. S.K. Liu, P.B. Fitzgerald, M. Daigle, R. Chen, and Z.J. Daskalakis The relationship between cortical inhibition, antipsychotic treatment, and the symptoms of schizophrenia Biol. Psychiatry 65 2009 503 509
40. T.Y. Liu, J.C. Hsieh, Y.S. Chen, P.C. Tu, T.P. Su, and L.F. Chen Different patterns of abnormal gamma oscillatory activity in unipolar and bipolar disorder patients during an implicit emotion task Neuropsychologia 50 2012 1514 1520
41. K. Maharajh, D. Abrams, D.C. Rojas, P. Teale, and M.L. Reite Auditory steady state and transient gamma band activity in bipolar disorder Int. Congr. Ser. 1300 2007 707 710
42. G.S. Malhi, M. Tanious, P. Das, C.M. Coulston, and M. Berk Potential mechanisms of action of lithium in bipolar disorder. Current understanding CNS Drugs 27 2013 135 153
43. Z. Merali, L. Du, P. Hrdina, M. Palkovits, G. Faludi, M.O. Poulter, and H. Anisman Dysregulation in the suicide brain: mRNA expression of corticotropin-releasing hormone receptors and GABA(A) receptor subunits in frontal cortical brain region J. Neurosci. 24 2004 1478 1485
44. M.J. Minzenberg, A.J. Firl, J.H. Yoon, G.C. Gomes, C. Reinking, and C.S. Carter Gamma oscillatory power is impaired during cognitive control independent of medication status in first-episode schizophrenia Neuropsychopharmacology 35 2010 2590 2599
45. D. Nikolic, P. Fries, and W. Singer Gamma oscillations: precise temporal coordination without a metronome Trends Cogn. Sci. 17 2013 54 55
46. B.F. O'Donnell, W.P. Hetrick, J.L. Vohs, G.P. Krishnan, C.A. Carroll, and A. Shekhar Neural synchronization deficits to auditory stimulation in bipolar disorder NeuroReport 15 2004 1369 1372
47. B.F. O'Donnell, J.L. Vohs, W.P. Hetrick, C.A. Carroll, and A. Shekhar Auditory event-related potential abnormalities in bipolar disorder and schizophrenia Int. J. Psychophysiol. 53 2004 45 55
48. T. O'Donnell, S. Rotzinger, T.T. Nakashima, C.C. Hanstock, M. Ulrich, and P.H. Silverstone Chronic lithium and sodium valproate both decrease the concentration of myoinositol and increase the concentration of inositol monophosphates in rat brain Eur. Neuropsychopharmacol. 13 2003 199 207
49. A. Ozerdem, B. Guntekin, I. Atagun, B. Turp, and E. Basar Reduced long distance gamma (28-48 Hz) coherence in euthymic patients with bipolar disorder J. Affect. Disord. 132 2011 325 332
50. A. Ozerdem, B. Guntekin, E. Saatci, Z. Tunca, and E. Basar Disturbance in long distance gamma coherence in bipolar disorder Prog. Neuropsychopharmacol. Biol. Psychiatry 34 2010 861 865
51. M.O. Poulter, L. Du, V. Zhurov, M. Palkovits, G. Faludi, Z. Merali, and H. Anisman Altered organization of GABA(A) receptor mRNA expression in the depressed suicide brain Front. Mol. Neurosci. 3 2010 3
52. R.B. Price, D.C. Shungu, X. Mao, P. Nestadt, C. Kelly, K.A. Collins, J.W. Murrough, D.S. Charney, and S.J. Mathew Amino acid neurotransmitters assessed by proton magnetic resonance spectroscopy: relationship to treatment resistance in major depressive disorder Biol. Psychiatry 65 2009 792 800
53. G. Rajkowska, G. O'Dwyer, Z. Teleki, C.A. Stockmeier, and J.J. Miguel-Hidalgo GABAergic neurons immunoreactive for calcium binding proteins are reduced in the prefrontal cortex in major depression Neuropsychopharmacology 32 2007 471 482
54. E. Rodriguez, N. George, J.P. Lachaux, J. Martinerie, B. Renault, and F.J. Varela Perception shadow: long-distance synchronization of human brain activity Nature 397 1999 430 433
55. M. Rosanova, A. Casali, V. Bellina, F. Resta, M. Mariotti, and M. Massimini Natural frequencies of human corticothalamic circuits J. Neurosci. 29 2009 7679 7685
56. M. Rosanova, S. Casarotto, A. Pigorini, P. Canali, A.G. Casali, and M. Massimini Combining transcranial magnetic stimulation with electroencephalography to study human cortical excitability and effective connectivity T. Fellin, M. Halassa, Neuronal Network Analysis - Concepts and Experimental Approaches 2012 Springer New York/Heidelberg 435 457
57. A. Shaw, J. Brealy, H. Richardson, S.D. Muthukumaraswamy, R.A. Edden, C. John Evans, N.A. Puts, K.D. Singh, and P.A. Keedwell Marked reductions in visual evoked responses but not gamma-aminobutyric acid concentrations or gamma-band measures in remitted depression Biol. Psychiatry 73 2013 691 698
58. V.S. Sohal, F. Zhang, O. Yizhar, and K. Deisseroth Parvalbumin neurons and gamma rhythms enhance cortical circuit performance Nature 459 2009 698 702
59. K.M. Spencer The functional consequences of cortical circuit abnormalities on gamma oscillations in schizophrenia: insights from computational modeling Front. Hum. Neurosci. 3 2009 33
60. K.M. Spencer, D.F. Salisbury, M.E. Shenton, and R.W. McCarley Gamma-band auditory steady-state responses are impaired in first episode psychosis Biol. Psychiatry 64 2008 369 375
61. M.P. Symond, A.W. Harris, E. Gordon, and L.M. Williams "Gamma synchrony" in first-episode schizophrenia: a disorder of temporal connectivity? Am. J. Psychiatry 162 2005 459 465
62. R.D. Traub, A. Bibbig, F.E. LeBeau, M.O. Cunningham, and M.A. Whittington Persistent gamma oscillations in superficial layers of rat auditory neocortex: experiment and model J. Physiol. 562 2005 3 8
63. P.J. Uhlhaas, C. Haenschel, D. Nikolic, and W. Singer The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia Schizophr. Bull. 34 2008 927 943
64. P.J. Uhlhaas, and W. Singer Abnormal neural oscillations and synchrony in schizophrenia Nat. Rev. Neurosci. 11 2010 100 113
65. J. Virtanen, J. Ruohonen, R. Naatanen, and R.J. Ilmoniemi Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation Med. Biol. Eng. Comput. 37 1999 322 326
66. D.W. Volk, and D.A. Lewis Impaired prefrontal inhibition in schizophrenia: relevance for cognitive dysfunction Physiol. Behav. 77 2002 501 505
67. M.A. Whittington, M.O. Cunningham, F.E. LeBeau, C. Racca, and R.D. Traub Multiple origins of the cortical gamma rhythm Dev. Neurobiol. 71 2011 92 106
68. M.A. Whittington, H.J. Faulkner, H.C. Doheny, and R.D. Traub Neuronal fast oscillations as a target site for psychoactive drugs Pharmacol. Ther. 86 2000 171 190
69. M.A. Whittington, R.D. Traub, and J.G. Jefferys Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation Nature 373 1995 612 615
70. M.A. Whittington, R.D. Traub, N. Kopell, B. Ermentrout, and E.H. Buhl Inhibition-based rhythms: experimental and mathematical observations on network dynamics Int. J. Psychophysiol. 38 2000 315 336