Gamma oscillations as a biomarker for major depression: an emerging topic

Paul J Fitzgerald, Brendon O Watson, Paul J Fitzgerald, Brendon O Watson

Abstract

Identifying biomarkers for major depression is of high importance for improving diagnosis and treatment of this common and debilitating neuropsychiatric disorder, as the field seeks to move toward both personalized and more effective treatments. Here we focus on electroencephalography (EEG) or direct scalp voltage recordings as such a biomarker, with an emphasis on gamma and high gamma oscillations (or "rhythms"). In the last several decades, alpha and theta band rhythms have been found to provide information on depressive state as well as recovery, but the gamma band is less well characterized with respect to depression. We summarize some key findings on gamma rhythms (especially their amplitude) as a biomarker or endophenotype for major depression. These studies suggest: (1) under certain conditions gamma rhythms can distinguish subjects with major depression from healthy controls, (2) gamma may distinguish bipolar disorder from unipolar depression, (3) various pharmacological and non-pharmacological treatments that counteract depression also alter gamma, (4) animal models of depression-like behavior show gamma abnormalities, with changes in gamma associated with therapeutic recovery. The most informative approaches in the future may combine profiles of gamma band power across the brain to assess ratios of activity across regions. Overall we have good evidence to suggest that gamma rhythms may provide objective information on major depressive disease status, but we will need further work to better define the precise measures to follow.

Conflict of interest statement

The authors declare that they have no conflict of interest.

References

    1. Miller, K. J., et al. Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations. NeuroImage10.1016/j.neuroimage.2013.08.070 (2014).
    1. Nir, Y., et al. Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat. Neurosci.10.1038/nn.2177 (2008).
    1. Ray, S., Crone, N. E., Niebur, E., Franaszczuk, P. J. & Hsiao, S. S.. Neural correlates of high-gamma oscillations (60-200 Hz) in macaque local field potentials and their potential implications in electrocorticography. J. Neurosci.10.1523/JNEUROSCI.2848-08.2008 (2008).
    1. Watson, B. O., Ding, M. & Buzsaki, G. Temporal coupling of field potentials and action potentials in the neocortex. Eur. J. Neurosci.10.1111/ejn.13807 (2018).
    1. Buzsáki, G. & Wang, X.-J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci.10.1146/annurev-neuro-062111-150444(2012).
    1. Gonzalez-Burgos, G., Cho, R. Y. & Lewis, D. A. Alterations in cortical network oscillations and parvalbumin neurons in schizophrenia. Biol. Psychiatr.10.1016/j.biopsych.2015.03.010 (2015).
    1. Iosifescu, D. V. Electroencephalography-derived biomarkers of antidepressant response. Harvard Rev. Psychiatr.10.3109/10673229.2011.586549 (2011).
    1. Nystrom, C., Matousek, M. & Hallstrom, T. Relationships between EEG and clinical characteristics in major depressive disorder. Acta Psychiatr. Scand.10.1111/j.1600-0447.1986.tb02700.x (1986).
    1. Baskaran, A., Milev, R. & McIntyre, R. S. The neurobiology of the EEG biomarker as a predictor of treatment response in depression. Neuropharmacology10.1016/j.neuropharm.2012.04.021 (2012).
    1. Sohal, V. S. How close are we to understanding what (if anything) oscillations do in cortical circuits? J. Neurosci. 10.1523/JNEUROSCI.0990-16.2016 (2016).
    1. Buzsáki, G. Neural syntax: cell assemblies, synapsembles, and readers. Neuron10.1016/j.neuron.2010.09.023 (2010).
    1. Nir, Y., et al. Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr. Biol. 10.1016/j.cub.2007.06.066 (2007).
    1. Fries P, Reynolds J, Rorie A, Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science. 2001;291:1560–1563. doi: 10.1126/science.1055465.
    1. Kim, H., Ährlund-Richter, S., Wang, X., Deisseroth, K. & Carlén, M. Prefrontal parvalbumin neurons in control of attention. Cell10.1016/j.cell.2015.11.038 (2016).
    1. Colgin, L. L., et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature. 10.1038/nature08573 (2009).
    1. Fernandez-Ruiz, et al. Entorhinal-CA3 dual-input control of spike timing in the hippocampus by theta-gamma coupling. Neuron. 2017;93:1213–1226. doi: 10.1016/j.neuron.2017.02.017.
    1. Spellman, T., et al. Hippocampal-prefrontal input supports spatial encoding in working memory. Nature. 10.1038/nature14445 (2015).
    1. Siegle, G. J., Condray, R., Thase, M. E., Keshavan, M. & Steinhauer, S. R. Sustained gamma-band EEG following negative words in depression and schizophrenia. Int. J. Psychophysiol. 10.1016/j.ijpsycho.2008.04.008 (2010).
    1. Strelets VB, Garakh ZV, Novototskii-Vlasov VY. Comparative study of the gamma rhythm in normal conditions, during examination stress, and in patients with first depressive episode. Neurosci. Behav. Physiol. 2007;37:387–394. doi: 10.1007/s11055-007-0025-4.
    1. Akdemir Akar S, Kara S, Agambayev S, bilgic vedat. Nonlinear analysis of EEG in major depression with fractal dimensions. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2015;2015:7410–7413.
    1. Liao, S.-C., Wu, C.-T., Huang, H.-C., Cheng, W.-T. & Liu, Y.-H. Major depression detection from EEG signals using Kernel Eigen-filter-bank common spatial patterns. Sensors. 10.3390/s17061385 (2017).
    1. Pizzagalli, D. A., Peccoralo, L. A., Davidson, R. J. & Cohen, J. D. Resting anterior cingulate activity and abnormal responses to errors in subjects with elevated depressive symptoms: a 128-channel study. Human Brain Mapp. 10.1002/hbm.20172 (2006).
    1. Lee, P. S., Chen, Y. S., Hsieh, J. C., Su, T. P. & Chen, L. F. Distinct neuronal oscillatory responses between patients with bipolar and unipolar disorders: a magnetoencephalographic study. J. Affect Disord. 10.1016/j.jad.2009.08.020 (2010).
    1. Liu, T. Y., Chen, Y. S., Su, T. P., Hsieh, J. C. & Chen, L. F. Abnormal early gamma responses to emotional faces differentiate unipolar from bipolar disorder patients. BioMed Res. Int. 10.1155/2014/906104 (2014).
    1. Isomura, S., et al. Differentiation between major depressive disorder and bipolar disorder by auditory steady-state responses. J. Affect. Disord. 10.1016/j.jad.2015.11.034 (2016).
    1. Liu, T. Y., et al. Different patterns of abnormal gamma oscillatory activity in unipolar and bipolar disorder patients during an implicit emotion task. Neuropsychologia. 10.1016/j.neuropsychologia.2012.03.004 (2012).
    1. Oda, Y., et al. Gamma band neural synchronization deficits for auditory steady state responses in bipolar disorder patients. PLoS ONE10.1371/journal.pone.0039955 (2012).
    1. Akhmetshina, D., et al. The serotonin reuptake inhibitor citalopram suppresses activity in the neonatal rat barrel cortex in vivo. Brain Res. Bull. 10.1016/j.brainresbull.2016.03.011 (2016).
    1. Mendez, P., Pazienti, A., Szabo, G. & Bacci, A. Direct alteration of a specific inhibitory circuit of the hippocampus by antidepressants. J. Neurosci. 10.1523/JNEUROSCI.1720-12.2012 (2012).
    1. Puig, M. V., Watakabe, A., Ushimaru, M., Yamamori, T. & Kawaguchi, Y. Serotonin modulates fast-spiking interneuron and synchronous activity in the rat prefrontal cortex through 5-HT1A and 5-HT2A receptors. J. Neurosci. 10.1523/JNEUROSCI.3335-09.2010 (2010).
    1. Hajós M, Hoffmann WE, Robinson DD, Yu JH. Norepinephrine but not serotonin reuptake inhibitors enhance theta and gamma activity of the septo-hippocampal system. Neuropsychopharmacology. 2003;28:857–864. doi: 10.1038/sj.npp.1300116.
    1. Nugent, A. C., et al. Ketamine has distinct electrophysiological and behavioral effects in depressed and healthy subjects. Mol. Psychiatr. 10.1038/s41380-018-0028-2 (2018).
    1. Berman RM, et al. Antidepressant effects of ketamine in depressed patients. Biol. Psychiatry. 2000;47:351–354. doi: 10.1016/S0006-3223(99)00230-9.
    1. Hakami, T., et al. NMDA receptor hypofunction leads to generalized and persistent aberrant γ oscillations independent of hyperlocomotion and the state of consciousness. PLoS ONE10.1371/journal.pone.0006755 (2009).
    1. Hunt, M. J., Raynaud, B. & Garcia, R. Ketamine dose-dependently induces high-frequency oscillations in the nucleus accumbens in freely moving rats. Biol. Psychiatry10.1016/j.biopsych.2006.01.020 (2006).
    1. Hong, L. E., et al. Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine. Neuropsychopharmacology10.1038/npp.2009.168 (2010).
    1. Muthukumaraswamy, S. D., et al. Evidence that subanesthetic doses of ketamine cause sustained disruptions of NMDA and AMPA-mediated frontoparietal connectivity in humans. J. Neurosci.10.1523/JNEUROSCI.0903-15.2015 (2015).
    1. Shaw, A. D., et al. Ketamine amplifies induced gamma frequency oscillations in the human cerebral cortex. Eur. Neuropsychopharmacol. 10.1016/j.euroneuro.2015.04.012 (2015).
    1. Noda, Y., et al. Resting-state EEG gamma power and theta–gamma coupling enhancement following high-frequency left dorsolateral prefrontal rTMS in patients with depression. Clin. Neurophysiol. 10.1016/j.clinph.2016.12.023 (2017).
    1. Bailey, N. W., et al. Responders to rTMS for depression show increased fronto-midline theta and theta connectivity compared to non-responders. Brain Stimulation. 10.1016/j.brs.2017.10.015 (2018).
    1. Pathak, Y., Salami, O., Baillet, S., Li, Z. & Butson, C. R. Longitudinal changes in depressive circuitry in response to neuromodulation therapy. Front. Neural Circuits10.3389/fncir.2016.00050 (2016).
    1. Canali, P., et al. Abnormal brain oscillations persist after recovery from bipolar depression. Eur. Psychiatry10.1016/j.eurpsy.2016.10.005 (2017).
    1. Kazemi, R., et al. Electrophysiological correlates of bilateral and unilateral repetitive transcranial magnetic stimulation in patients with bipolar depression. Psychiatry Res. 10.1016/j.psychres.2016.04.061 (2016).
    1. Sun, Y. et al. Deep brain stimulation modulates gamma oscillations and theta-gamma coupling in treatment resistant depression. Brain Stimul.10.1016/j.brs.2015.06.010 (2015).
    1. Schoenberg, P. L. A. & Speckens, A. E. M. Multi-dimensional modulations of α and γ cortical dynamics following mindfulness-based cognitive therapy in major depressive disorder. Cogn. Neurodyn. 10.1007/s11571-014-9308-oy (2015).
    1. Gazit, T., et al. Programmed deep brain stimulation synchronizes VTA gamma band field potential and alleviates depressive-like behavior in rats. Neuropharmacology. 10.1016/j.neuropharm.2014.12.003 (2015)
    1. Khalid, A., et al. Gamma oscillation in functional brain networks is involved in the spontaneous remission of depressive behavior induced by chronic restraint stress in mice. BMC Neurosci. 10.1186/s12868-016-0239-x (2016)
    1. Sauer, J. F., Strüber, M. & Bartos, M. Impaired fast-spiking interneuron function in a genetic mouse model of depression. eLife10.7554/eLife.04979 (2015).
    1. Voget, M., et al. Altered local field potential activity and serotonergic neurotransmission are further characteristics of the Flinders sensitive line rat model of depression. Behav. Brain Res. 10.1016/j.bbr.2015.05.027 (2015).
    1. Fee, C., Banasr, M. & Sibille, E. Somatostatin-positive gamma-aminobutyric acid interneuron deficits in depression: cortical microcircuit and therapeutic perspectives. Biol. Psychiatry10.1016/j.biopsych.2017.05.024 (2017).
    1. Devalle, F., Roxin, A. & Montbrió, E. Firing rate equations require a spike synchrony mechanism to correctly describe fast oscillations in inhibitory networks. PLoS Computat. Biol. 10.1371/journal.pcbi.1005881 (2017).
    1. Watson, B. O., Levenstein, D., Greene, J. P., Gelinas, J. N. & Buzsáki, G. Network homeostasis and state dynamics of neocortical sleep. Neuron10.1016/j.neuron.2016.03.036 (2016).
    1. Tekell JL, et al. High frequency EEG activity during sleep: characteristics in schizophrenia and depression. Clin. Eeg. Neurosci. 2005;36:25–35. doi: 10.1177/155005940503600107.
    1. Ossandon, T., et al. Transient suppression of broadband gamma power in the default-mode network is correlated with task complexity and subject performance. J. Neurosci. 10.1523/JNEUROSCI.2483-11.2011 (2011).
    1. Mathalon, D. H. & Sohal, V. S. Neural oscillations and synchrony in brain dysfunction and neuropsychiatric disorders it’s about time. JAMA Psychiatry10.1001/jamapsychiatry.2015.0483 (2015).
    1. Lachaux, J. P., et al. Relationship between task-related gamma oscillations and BOLD signal: new insights from combined fMRI and intracranial EEG. Human Brain Mapp. 10.1002/hbm.20352 (2007).
    1. Muthukumaraswamy, S. D. & Singh, K. D. Functional decoupling of BOLD and gamma-band amplitudes in human primary visual cortex. Human Brain Mapping. 10.1002/hbm.20644 (2009).
    1. Marzbani, H., Marateb, H. R. & Mansourian, M. Methodological note: neurofeedback: a comprehensive review on system design, methodology and clinical applications. Basic Clin. Neurosci. 10.15412/J.BCN.03070208 (2016).
    1. Al-Kaysi, A. M., et al. Predicting tDCS treatment outcomes of patients with major depressive disorder using automated EEG classification. J. Affect. Disord. 10.1016/j.jad.2016.10.021 (2017).
    1. Saleem, A. B., et al. Subcortical source and modulation of the narrowband gamma oscillation in mouse visual cortex. Neuron10.1016/j.neuron.2016.12.028 (2017).
    1. Bessaih, T., Higley, M. J. & Contreras, D. Millisecond precision temporal encoding of stimulus features during cortically generated gamma oscillations in the rat somatosensory cortex. J. Physiol. 10.1113/JP275245 (2018).
    1. Hopf J, et al. Localizing visual discrimination processes in time and space. J. Neurophysiol. 2002;88:2088–2095. doi: 10.1152/jn.2002.88.4.2088.
    1. Mideksa, K. G., et al. Impact of head modeling and sensor types in localizing human gamma-band oscillations. In 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, EMBC (2014) 10.1109/EMBC.2014.6944059
    1. Aronson, J. K. Biomarkers and surrogate endpoints. Br. J. Clin. Pharmacol. 10.1111/j.1365-2125.2005.02435.x (2005).
    1. Uhlhaas, P. J. & Singer, W. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 10.1038/nrn2774 (2010).
    1. Gandal, M. J., et al. Shared molecular neuropathology across major psychiatric disorders parallels polygenic overlap. Science10.1126/science.aad6469 (2018)
    1. Rojas, D. C. & Wilson, L. B. γ-band abnormalities as markers of autism spectrum disorders. Biomarkers Med. 10.2217/bmm.14.15 (2014).
    1. Hermes, D., Kasteleijn-Nolst Trenité, D. G. A. & Winawer, J. Gamma oscillations and photosensitive epilepsy. Curr. Biol. 10.1016/j.cub.2017.03.076 (2017).
    1. Cukier, H. N., et al. Exome sequencing of extended families with autism reveals genes shared across neurodevelopmental and neuropsychiatric disorders. Mol. Autism. 10.1186/2040-2392-5-1 (2014).
    1. Kanner, A. M., et al. Epilepsy as a network disorder (1): what can we learn from other network disorders such as autistic spectrum disorder and mood disorders? Epilepsy Behav. 10.1016/j.yebeh.2017.09.014 (2017).
    1. Scharfman, H. E., et al. Epilepsy as a network disorder (2): what can we learn from other network disorders such as dementia and schizophrenia, and what are the implications for translational research? Epilepsy Behav. 10.1016/j.yebeh.2017.09.016 (2018).
    1. Dienel, S. J. & Lewis, D. A. Alterations in cortical interneurons and cognitive function in schizophrenia. Neurobiol. Dis.10.1016/j.nbd.2018.06.020 (2018).
    1. Rive MM, et al. Neural correlates of dysfunctional emotion regulation in major depressive disorder. A systematic review of neuroimaging studies. Neurosci. Biobehav. Rev. 2013;37:2529–2553. doi: 10.1016/j.neubiorev.2013.07.018.
    1. Voytek, B. & Knight, R. T. Dynamic network communication as a unifying neural basis for cognition, development, aging, and disease. Biol. Psychiatry10.1016/j.biopsych.2015.04.016 (2015).

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