Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-19T13:23:04.623Z Has data issue: false hasContentIssue false
  • English
  • Français

Abnormal brain oscillations persist after recovery from bipolar depression

Published online by Cambridge University Press:  03 February 2017

P. Canali ,
S. Casarotto ,
M. Rosanova ,
G. Sferrazza-Papa ,
A.G. Casali ,
O. Gosseries ,
M. Massimini ,
E. Smeraldi ,
C. Colombo  and
F. Benedetti
P. Canali*
Affiliation:
Department of clinical neurosciences, scientific institute Ospedale San Raffaele, university Vita-Salute San Raffaele, San Raffaele Turro, 20, via Stamira d’Ancona, 20127Milano, Italy
S. Casarotto
Affiliation:
Department of biomedical and clinical sciences “L. Sacco”, università degli Studi di Milano, Milano, Italy
M. Rosanova
Affiliation:
Department of biomedical and clinical sciences “L. Sacco”, università degli Studi di Milano, Milano, Italy Fondazione Europea di Ricerca Biomedica, FERB Onlus, Milan, Italy
G. Sferrazza-Papa
Affiliation:
Department of clinical neurosciences, scientific institute Ospedale San Raffaele, university Vita-Salute San Raffaele, San Raffaele Turro, 20, via Stamira d’Ancona, 20127Milano, Italy
A.G. Casali
Affiliation:
Institute of science and technology, Federal university of São Paulo, 330, Rua Talim, São José dos Campos, Brazil
O. Gosseries
Affiliation:
Coma science group, GIGA research & neurology department, university hospital of Liège, Liège, Belgium Center for sleep and consciousness, Postle laboratory, department of psychology and psychiatry, university of Wisconsin, Madison, WI, USA
M. Massimini
Affiliation:
Department of biomedical and clinical sciences “L. Sacco”, università degli Studi di Milano, Milano, Italy
E. Smeraldi
Affiliation:
Department of clinical neurosciences, scientific institute Ospedale San Raffaele, university Vita-Salute San Raffaele, San Raffaele Turro, 20, via Stamira d’Ancona, 20127Milano, Italy
C. Colombo
Affiliation:
Department of clinical neurosciences, scientific institute Ospedale San Raffaele, university Vita-Salute San Raffaele, San Raffaele Turro, 20, via Stamira d’Ancona, 20127Milano, Italy
F. Benedetti
Affiliation:
Department of clinical neurosciences, scientific institute Ospedale San Raffaele, university Vita-Salute San Raffaele, San Raffaele Turro, 20, via Stamira d’Ancona, 20127Milano, Italy
*
⁎Corresponding author. Tel.: +39 02 26433156; fax: +39 02 26433265. E-mail address: [email protected] (P. Canali).
Get access

Abstract

When directly perturbed in healthy subjects, premotor cortical areas generate electrical oscillations in the beta range (20–40 Hz). In schizophrenia, major depressive disorder and bipolar disorder (BD), these oscillations are markedly reduced, in terms of amplitude and frequency. However, it still remains unclear whether these abnormalities can be modulated over time, or if they can be still observed after treatment. Here, we employed transcranial magnetic stimulation (TMS) combined with EEG to assess the frontal oscillatory activity in eighteen BD patients before/after antidepressant treatments (sleep deprivation and light therapy), relative to nine healthy controls. In order to detect dominant frequencies, event related spectral perturbations (ERSP) were computed for each TMS/EEG session in all participants, using wavelet decomposition. The natural frequency at which the cortical circuit oscillates was calculated as the frequency value with the largest power across 300 ms post-stimulus time interval. Severity of depression markedly decreased after treatment with 12 patients achieving response and nine patients achieving remission. TMS/EEG resulted in a significant activation of the beta/gamma band response (21–50 Hz) in healthy controls. In patients, the main frequencies of premotor EEG responses to TMS did not significantly change before/after treatment and were always significantly lower than those of controls (11–27 Hz) and comparable in patients achieving remission and in those not responding to treatment. These results suggest that the reduction of natural frequencies is a trait marker of BD, independent from the clinical status of the patients. The present findings shed light on the neurobiological underpinning of severe psychiatric disorders and demonstrate that TMS/EEG represents a unique tool to develop biomarkers in psychiatry.

Keywords

TMS/EEGGamma oscillationsBiomarkersBipolar disorderGABAergic circuits
Type
Original article
Information
European Psychiatry , Volume 41 , Issue 1 , March 2017 , pp. 10 - 15
Copyright
Copyright © European Psychiatric Association 2017

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bauer, M.S.Kirk, G.F.Gavin, C.Williford, W.O.Determinants of functional outcome and healthcare costs in bipolar disorder: a high-intensity follow-up study. J Affect Disord. 2001;65:231–241.CrossRefGoogle ScholarPubMed
Murray, C.J.Lopez, A.D.Evidence-based health policy – lessons from the Global burden of disease study. Science. 1996;274:740–743.CrossRefGoogle ScholarPubMed
Ketter, T.A.Nosology, diagnostic challenges, and unmet needs in managing bipolar disorder. J Clin Psychiatry. 2010;71:e27.10.4088/JCP.8125tx12cCrossRefGoogle ScholarPubMed
Poletti, S.Sferrazza Papa, G.Locatelli, C.Colombo, C.Benedetti, F.Neuropsychological deficits in bipolar depression persist after successful antidepressant treatment. J Affect Disord. 2014;156:144–149.10.1016/j.jad.2013.11.023CrossRefGoogle ScholarPubMed
Poletti, S.Bollettini, I.Mazza, E.Locatelli, C.Radaelli, D.Vai, B.et al.Cognitive performances associate with measures of white matter integrity in bipolar disorder. J Affect Disord. 2015;174:342–352.CrossRefGoogle ScholarPubMed
Biomarkers Definitions Working G, Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther. 2001;69:89–95.10.1067/mcp.2001.113989CrossRefGoogle Scholar
Buzsaki, G.Draguhn, A.Neuronal oscillations in cortical networks. Science. 2004;304:1926–1929.CrossRefGoogle ScholarPubMed
Nikolic, D.Fries, P.Singer, W.Gamma oscillations: precise temporal coordination without a metronome. Trends Cogn Sci. 2013;17:54–55.10.1016/j.tics.2012.12.003CrossRefGoogle ScholarPubMed
Başar, E.Brain oscillations in neuropsychiatric disease. Dialogues Clin Neurosci. 2013;15:291–300.Google ScholarPubMed
Ozerdem, A.Kocaaslan, S.Tunca, Z.Basar, E.Event related oscillations in euthymic patients with bipolar disorder. Neurosci Lett. 2008;444:5–10.10.1016/j.neulet.2008.07.081CrossRefGoogle ScholarPubMed
Ozerdem, A.Guntekin, B.Atagun, I.Turp, B.Basar, E.Reduced long distance gamma (28-48 Hz) coherence in euthymic patients with bipolar disorder. J Affect Disord. 2011;132:325–332.10.1016/j.jad.2011.02.028CrossRefGoogle ScholarPubMed
Shaw, A.Brealy, J.Richardson, H.Muthukumaraswamy, S.D.Edden, R.A.John Evans, C.et al.Marked reductions in visual evoked responses but not gamma-aminobutyric acid concentrations or gamma-band measures in remitted depression. Biol Psychiatry. 2013;73:691–698.CrossRefGoogle ScholarPubMed
Chen, S.S.Tu, P.C.Su, T.P.Hsieh, J.C.Lin, Y.C.Chen, L.F.Impaired frontal synchronization of spontaneous magnetoencephalographic activity in patients with bipolar disorder. Neurosci Lett. 2008;445:174–178.CrossRefGoogle ScholarPubMed
Buzsaki, G.Watson, B.O.Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease. Dialogues Clin Neurosci. 2012;14:345–367.Google ScholarPubMed
Canali, P.A role for TMS/EEG in neuropsychiatric disorders. Neurol Psychiatry Brain Res 2014;20:37–40.CrossRefGoogle Scholar
Rosanova, M.Casarotto, S.Pigorini, A.Canali, P.Casali, A.G.Massimini, M.Combining transcranial magnetic stimulation with electroencephalography to study human cortical excitability and effective connectivity. In: Fellin, T.Halassa, M.Neuronal network analysis concepts and experimental approaches New York, Heidelberg: Springer; 2012. p. 435–457.Google Scholar
Rosanova, M.Casali, A.Bellina, V.Resta, F.Mariotti, M.Massimini, M.Natural frequencies of human corticothalamic circuits. J Neurosci. 2009;29:7679–7685.10.1523/JNEUROSCI.0445-09.2009CrossRefGoogle ScholarPubMed
Canali, P.Sarasso, S.Rosanova, M.Casarotto, S.Sferrazza-Papa, G.Gosseries, O.et al.Shared reduction of oscillatory natural frequencies in bipolar disorder, major depressive disorder and schizophrenia. J Affect Disord. 2015;184:111–115.10.1016/j.jad.2015.05.043CrossRefGoogle Scholar
Benedetti, F.Bernasconi, A.Blasi, V.Cadioli, M.Colombo, C.Falini, A.et al.Neural and genetic correlates of antidepressant response to sleep deprivation – A functional magnetic resonance imaging study of moral valence decision, in bipolar depression. Arch Gen Psychiatry. 2007;64:179–187.CrossRefGoogle ScholarPubMed
Canali, P.Sferrazza Papa, G.Casali, A.G.Fecchio, M.Pigorini, A.Schiena, G.et al.Changes of cortical excitability as biomarkers of antidepressant response in bipolar depression. Bipolar Disord. 2014;16:809–819.CrossRefGoogle Scholar
Benedetti, F.Poletti, S.Hoogenboezem, T.A.Locatelli, C.Ambree, O.de Wit, H.et al.Stem cell factor (SCF) is a putative biomarker of antidepressant response. J Neuroimmune Pharmacol 2016.CrossRefGoogle ScholarPubMed
Benedetti, F.Riccaboni, R.Locatelli, C.Poletti, S.Dallaspezia, S.Colombo, C.Rapid treatment response of suicidal symptoms to lithium, sleep deprivation, and light therapy (chronotherapeutics) in drug-resistant bipolar depression. J Clin Psychiatry. 2014;75:133–140.CrossRefGoogle Scholar
Virtanen, J.Ruohonen, J.Naatanen, R.Ilmoniemi, R.J.Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med Biol Eng Comput. 1999;37:322–326.CrossRefGoogle ScholarPubMed
Casali, A.G.Casarotto, S.Rosanova, M.Mariotti, M.Massimini, M.General indices to characterize the electrical response of the cerebral cortex to TMS. Neuroimage. 2010;49:1459–1468.CrossRefGoogle ScholarPubMed
Horne, J.A.Human sleep, sleep loss and behaviour. Implications for the prefrontal cortex and psychiatric disorder. Br J Psychiatry. 1993;162:413–419.10.1192/bjp.162.3.413CrossRefGoogle ScholarPubMed
Casarotto, S.Romero Lauro, L.J.Bellina, V.Casali, A.G.Rosanova, M.Pigorini, A.et al.EEG responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time. Plos One. 2010;5:e10281.CrossRefGoogle ScholarPubMed
Massimini, M.Ferrarelli, F.Huber, R.Esser, S.K.Singh, H.Tononi, G.Breakdown of cortical effective connectivity during sleep. Science. 2005;309:2228–2232.CrossRefGoogle ScholarPubMed
Delorme, A.Makeig, S.EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004;134:9–21.CrossRefGoogle ScholarPubMed
McCulloch, C.E.Searle, S.R.Neuhaus, J.M.Generalized, linear, and mixed models. 2nd ed. New York: John Wiley & Sons; 2008.Google Scholar
Timm, N.Kim, K.Univariate and multivariate general linear models: theory and applications with SAS. 2nd ed. Berlin: Heidelberg Springer; 2006.Google Scholar
Hill, TLewicki, P. Statistics: methods and applications. A comprehensive reference for science, industry, and data mining. General Linear Models, StatSoft, Tulsa (OK). 2006; Chapter 18:245–76.Google Scholar
Bartos, M.Vida, I.Jonas, P.Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci. 2007;8:45–56.10.1038/nrn2044CrossRefGoogle ScholarPubMed
Uhlhaas, P.J.Haenschel, C.Nikolic, D.Singer, W.The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophr Bull. 2008;34:927–943.CrossRefGoogle ScholarPubMed
Sohal, V.S.Zhang, F.Yizhar, O.Deisseroth, K.Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature. 2009;459:698–702.CrossRefGoogle ScholarPubMed
Benes, F.M.Berretta, S.Gabaergic interneurons. implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology. 2001;25:1–27.CrossRefGoogle ScholarPubMed
Whittington, M.A.Cunningham, M.O.LeBeau, F.E.Racca, C.Traub, R.D.Multiple origins of the cortical gamma rhythm. Dev Neurobiol. 2011;71:92–106.10.1002/dneu.20814CrossRefGoogle ScholarPubMed
Gray, C.M.McCormick, D.A.Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science. 1996;274:109–113.CrossRefGoogle ScholarPubMed
Traub, R.D.Bibbig, A.LeBeau, F.E.Cunningham, M.O.Whittington, M.A.Persistent gamma oscillations in superficial layers of rat auditory neocortex: experiment and model. J Physiol. 2005;562:3–8.CrossRefGoogle ScholarPubMed
Gonzalez-Burgos, G.Lewis, D.A.GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia. Schizophr Bull. 2008;34:944–961.10.1093/schbul/sbn070CrossRefGoogle Scholar
Brenner, C.A.Kieffaber, P.D.Clementz, B.A.Johannesen, J.K.Shekhar, A.O’Donnell, B.F.et al.Event-related potential abnormalities in schizophrenia: a failure to “gate in” salient information?. Schizophr Res. 2009;113:332–338.10.1016/j.schres.2009.06.012CrossRefGoogle Scholar
Wang, A.Y.Lohmann, K.M.Yang, C.K.Zimmerman, E.I.Pantazopoulos, H.Herring, N.et al.Bipolar disorder type 1 and schizophrenia are accompanied by decreased density of parvalbumin- and somatostatin-positive interneurons in the parahippocampal region. Acta Neuropathol. 2011;122:615–626.CrossRefGoogle ScholarPubMed
Sibille, E.Morris, H.M.Kota, R.S.Lewis, D.A.GABA-related transcripts in the dorsolateral prefrontal cortex in mood disorders. Int J Neuropsychopharmacol. 2011;14:721–734.CrossRefGoogle ScholarPubMed
Bhagwagar, Z.Wylezinska, M.Jezzard, P.Evans, J.Ashworth, F.Sule, A.et al.Reduction in occipital cortex gamma-aminobutyric acid concentrations in medication-free recovered unipolar depressed and bipolar subjects. Biol Psychiatry. 2007;61:806–812.CrossRefGoogle ScholarPubMed
Uhlhaas, P.J.Singer, W.High-frequency oscillations and the neurobiology of schizophrenia. Dialogues Clin Neurosci. 2013;15:301–313.Google ScholarPubMed
Chitty, K.M.Lagopoulos, J.Lee, R.S.Hickie, I.B.Hermens, D.F.A systematic review and meta-analysis of proton magnetic resonance spectroscopy and mismatch negativity in bipolar disorder. Eur Neuropsychopharmacol. 2013;23:1348–1363.CrossRefGoogle ScholarPubMed
Lan, M.J.McLoughlin, G.A.Griffin, J.L.Tsang, T.M.Huang, J.T.Yuan, P.et al.Metabonomic analysis identifies molecular changes associated with the pathophysiology and drug treatment of bipolar disorder. Mol Psychiatry. 2009;14:269–279.CrossRefGoogle ScholarPubMed
Korotkova, T.Fuchs, E.C.Ponomarenko, A.von Engelhardt, J.Monyer, H.NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron. 2010;68:557–569.CrossRefGoogle ScholarPubMed
Hong, L.E.Summerfelt, A.Buchanan, R.W.O’Donnell, P.Thaker, G.K.Weiler, M.A.et al.Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine. Neuropsychopharmacology. 2010;35:632–640.10.1038/npp.2009.168CrossRefGoogle ScholarPubMed
Hakami, T.Jones, N.C.Tolmacheva, E.A.Gaudias, J.Chaumont, J.Salzberg, M.et al.NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness. Plos One 2009;4:e6755.CrossRefGoogle ScholarPubMed
Homayoun, H.Moghaddam, B.NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci. 2007;27:11496–11500.10.1523/JNEUROSCI.2213-07.2007CrossRefGoogle ScholarPubMed
Spencer, K.M.The functional consequences of cortical circuit abnormalities on gamma oscillations in schizophrenia: insights from computational modeling. Front Hum Neurosci. 2009;3:33.10.3389/neuro.09.033.2009CrossRefGoogle ScholarPubMed
Yizhar, O.Fenno, L.E.Davidson, T.J.Mogri, M.Deisseroth, K.Optogenetics in neural systems. Neuron. 2011;71:9–34.CrossRefGoogle ScholarPubMed
Zarate, C.A. Jr.Brutsche, N.E.Ibrahim, L.Franco-Chaves, J.Diazgranados, N.Cravchik, A.et al.Replication of ketamine's antidepressant efficacy in bipolar depression: a randomized controlled add-on trial. Biol Psychiatry. 2012;71:939–946.CrossRefGoogle ScholarPubMed
Ozerdema, A.Guntekind, B.Atagune, M.I.Basar, E.Brain oscillations in bipolar disorder in search of new biomarkers. Suppl Clin Neurophysiol. 2013;62:207–221.CrossRefGoogle ScholarPubMed
Whittington, M.A.Faulkner, H.J.Doheny, H.C.Traub, R.D.Neuronal fast oscillations as a target site for psychoactive drugs. Pharmacol Ther. 2000;86:171–190.CrossRefGoogle ScholarPubMed
O’Gorman, R.L.Poil, S.S.Brandeis, D.Klaver, P.Bollmann, S.Ghisleni, C.et al.Coupling between resting cerebral perfusion and EEG. Brain Topogr. 2013;26:442–457.CrossRefGoogle ScholarPubMed
Varela, F.Lachaux, J.P.Rodriguez, E.Martinerie, J.The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci. 2001;2:229–239.CrossRefGoogle ScholarPubMed
Lewis, A.G.Wang, L.Bastiaansen, M.Fast oscillatory dynamics during language comprehension: unification versus maintenance and prediction?. Brain Lang. 2015;148:51–63.CrossRefGoogle ScholarPubMed
Benasich, A.A.Gou, Z.Choudhury, N.Harris, K.D.Early cognitive and language skills are linked to resting frontal gamma power across the first 3 years. Behav Brain Res 2008;195:215–222.CrossRefGoogle ScholarPubMed
Kucewicz, M.T.Cimbalnik, J.Matsumoto, J.Y.Brinkmann, B.H.Bower, M.R.Vasoli, V.et al.High frequency oscillations are associated with cognitive processing in human recognition memory. Brain. 2014;137:2231–2244.10.1093/brain/awu149CrossRefGoogle ScholarPubMed
Benedetti, F.Bollettini, I.Recent findings on the role of white matter pathology in bipolar disorder. Harv Rev Psychiatry. 2014;22:338–341.CrossRefGoogle ScholarPubMed
Basar, E.Schurmann, M.Basar-Eroglu, C.Demiralp, T.Selectively distributed gamma band system of the brain. Int J Psychophysiol. 2001;39:129–135.CrossRefGoogle ScholarPubMed
Submit a response

Comments

No Comments have been published for this article.