Advertisement

Limbic Activity Modulation Guided by Functional Magnetic Resonance Imaging–Inspired Electroencephalography Improves Implicit Emotion Regulation

  • Author Footnotes
    1 JNK and YM-H contributed equally to this work.
    Jackob N. Keynan
    Footnotes
    1 JNK and YM-H contributed equally to this work.
    Affiliations
    Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel-Aviv University, Tel-Aviv, Israel

    The School of Psychological Sciences, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Author Footnotes
    1 JNK and YM-H contributed equally to this work.
    Yehudit Meir-Hasson
    Footnotes
    1 JNK and YM-H contributed equally to this work.
    Affiliations
    Blavatnik School of Computer Science, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Gadi Gilam
    Affiliations
    Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel-Aviv University, Tel-Aviv, Israel

    The School of Psychological Sciences, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Avihay Cohen
    Affiliations
    Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Gilan Jackont
    Affiliations
    Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel-Aviv University, Tel-Aviv, Israel

    The School of Psychological Sciences, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Sivan Kinreich
    Affiliations
    Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel-Aviv University, Tel-Aviv, Israel

    The School of Psychological Sciences, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Limor Ikar
    Affiliations
    Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Ayelet Or-Borichev
    Affiliations
    Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel-Aviv University, Tel-Aviv, Israel

    The School of Psychological Sciences, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Amit Etkin
    Affiliations
    Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford

    Sierra-Pacific Mental Illness Research, Education, and Clinical Center, Veterans Affairs Palo Alto Health Care System, Palo Alto, California
    Search for articles by this author
  • Anett Gyurak
    Affiliations
    Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford

    Sierra-Pacific Mental Illness Research, Education, and Clinical Center, Veterans Affairs Palo Alto Health Care System, Palo Alto, California
    Search for articles by this author
  • Ilana Klovatch
    Affiliations
    Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Nathan Intrator
    Affiliations
    Blavatnik School of Computer Science, Tel-Aviv University, Tel-Aviv, Israel

    Sagol School of Neuroscience, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Talma Hendler
    Correspondence
    Address correspondence to: Talma Hendler, M.D., Ph.D., Tel Aviv Sourasky Medical Center, Functional Brain Center, Wohl Institute for Advanced Imaging, 6 Weizman St, Tel Aviv, Israel.
    Affiliations
    Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel-Aviv University, Tel-Aviv, Israel

    The School of Psychological Sciences, Tel-Aviv University, Tel-Aviv, Israel

    Sagol School of Neuroscience, Tel-Aviv University, Tel-Aviv, Israel

    Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel
    Search for articles by this author
  • Author Footnotes
    1 JNK and YM-H contributed equally to this work.

      Abstract

      The amygdala has a pivotal role in processing traumatic stress; hence, gaining control over its activity could facilitate adaptive mechanism and recovery. To date, amygdala volitional regulation could be obtained only via real-time functional magnetic resonance imaging (fMRI), a highly inaccessible procedure. The current article presents high-impact neurobehavioral implications of a novel imaging approach that enables bedside monitoring of amygdala activity using fMRI-inspired electroencephalography (EEG), hereafter termed amygdala-electrical fingerprint (amyg-EFP). Simultaneous EEG/fMRI indicated that the amyg-EFP reliably predicts amygdala-blood oxygen level–dependent activity. Implementing the amyg-EFP in neurofeedback demonstrated that learned downregulation of the amyg-EFP facilitated volitional downregulation of amygdala-blood oxygen level–dependent activity via real-time fMRI and manifested as reduced amygdala reactivity to visual stimuli. Behavioral evidence further emphasized the therapeutic potential of this approach by showing improved implicit emotion regulation following amyg-EFP neurofeedback. Additional EFP models denoting different brain regions could provide a library of localized activity for low-cost and highly accessible brain-based diagnosis and treatment.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Johnston T.
        • van Reekum C.M.
        • Urry H.L.
        • Kalin N.H.
        • Davidson R.J.
        Failure to regulate: Counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression.
        J Neurosci. 2007; 27: 8877-8884
        • Ochsner K.N.
        • Bunge S.A.
        • Gross J.J.
        • Gabrieli J.D.
        Rethinking feelings: An fMRI study of the cognitive regulation of emotion.
        J Cogn Neurosci. 2002; 14: 1215-1229
        • Admon R.
        • Milad M.R.
        • Hendler T.
        A causal model of post-traumatic stress disorder: Disentangling predisposed from acquired neural abnormalities.
        Trends Cogn Sci. 2013; 17: 337-347
        • Weiskopf N.
        Real-time fMRI and its application to neurofeedback.
        Neuroimage. 2012; 62: 682-692
        • Gruzelier J.H.
        EEG-neurofeedback for optimising performance. I: A review of cognitive and affective outcome in healthy participants.
        Neurosci Biobehav Rev. 2013; 44: 124-141
        • Zotev V.
        • Krueger F.
        • Phillips R.
        • Alvarez R.P.
        • Simmons W.K.
        • Bellgowan P.
        • et al.
        Self-regulation of amygdala activation using real-time fMRI neurofeedback.
        PloS One. 2011; 6: e24522
        • Scheinost D.
        • Stoica T.
        • Saksa J.
        • Papademetris X.
        • Constable R.T.
        • Pittenger C.
        • Hampson M.
        Orbitofrontal cortex neurofeedback produces lasting changes in contamination anxiety and resting-state connectivity.
        Transl Psychiatry. 2013; 3: e250
        • Young K.D.
        • Zotev V.
        • Phillips R.
        • Misaki M.
        • Yuan H.
        • Drevets W.C.
        • Bodurka J.
        Real-time FMRI neurofeedback training of amygdala activity in patients with major depressive disorder.
        PloS One. 2014; 9: e88785
        • Birbaumer N.
        • Ruiz S.
        • Sitaram R.
        Learned regulation of brain metabolism.
        Trends Cogn Sci. 2013; 17: 295-302
        • Peniston E.G.
        • Kulkosky P.J.
        Alpha-theta brainwave neurofeedback for Vietnam veterans with combat related post-traumatic stress disorder.
        Med Psychother. 1991; 4: 47-60
        • Quaedflieg CWEM
        • Smulders F.T.Y.
        • Meyer T.
        • Peeters F.
        • Merckelbach H.
        • Smeets T.
        The validity of individual frontal alpha asymmetry EEG neurofeedback.
        Soc Cogn Affect Neurosci. 2016; 11: 33-43
        • Kinreich S.
        • Podlipsky I.
        • Intrator N.
        • Hendler T.
        Categorized EEG neurofeedback performance unveils simultaneous fMRI deep brain activation.
        in: Langs G. Rish I. Berthold M.R. Horvath T. Machine Learning and Interpretation in Neuroimaging. Springer-Verlag, Berlin2012: 108-115
        • Meir-Hasson Y.
        • Kinreich S.
        • Podlipsky I.
        • Hendler T.
        • Intrator N.
        An EEG finger-print of fMRI deep regional activation.
        Neuroimage. 2014; 102: 128-141
        • Kinreich S.
        • Podlipsky I.
        • Jamshy S.
        • Intrator N.
        • Hendler T.
        Neural dynamics necessary and sufficient for transition into pre-sleep induced by EEG NeuroFeedback.
        Neuroimage. 2014; 97: 19-28
        • Shibata K.
        • Watanabe T.
        • Sasaki Y.
        • Kawato M.
        Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.
        Science. 2011; 334: 1413-1415
        • Sulzer J.
        • Haller S.
        • Scharnowski F.
        • Weiskopf N.
        • Birbaumer N.
        • Blefari M.
        Real-time fMRI neurofeedback: Progress and challenges.
        Neuroimage. 2013; 76: 386-399
        • Admon R.
        • Lubin G.
        • Stern O.
        • Rosenberg K.
        • Sela L.
        • Ben-Ami H.
        • Hendler T.
        Human vulnerability to stress depends on amygdalaʼs predisposition and hippocampal plasticity.
        Proc Natl Acad Sci U S A. 2009; 106: 14120-14125
        • Etkin A.
        • Egner T.
        • Peraza D.M.
        • Kandel E.R.
        • Hirsch J.
        Resolving emotional conflict: A role for the rostral anterior cingulate cortex in modulating activity in the amygdala.
        Neuron. 2006; 51: 871-882
        • Rosenthal R.
        • Rosnow R.L.
        Contrast analysis: Focused comparisons in the analysis of variance.
        Cambridge University Press Archive, Cambridge, UK1985
        • Grech R.
        • Cassar T.
        • Muscat J.
        • Camilleri K.P.
        • Fabri S.G.
        • Zervakis M.
        • et al.
        Review on solving the inverse problem in EEG source analysis.
        J Neuroeng Rehabil. 2008; 5: 25
        • Pessoa L.
        • Adolphs R.
        Emotion processing and the amygdala: From a ‘low road’ to ‘many roads’ of evaluating biological significance.
        Nat Rev Neurosci. 2010; 11: 773-783
        • Seeley W.W.
        • Menon V.
        • Schatzberg A.F.
        • Keller J.
        • Glover G.H.
        • Kenna H.
        • et al.
        Dissociable intrinsic connectivity networks for salience processing and executive control.
        J Neurosci. 2007; 27: 2349-2356
        • Goldin P.R.
        • McRae K.
        • Ramel W.
        • Gross J.J.
        The neural bases of emotion regulation: Reappraisal and suppression of negative emotion.
        Biol Psychiatry. 2008; 63: 577-586
        • Ochsner K.N.
        • Gross J.J.
        Cognitive emotion regulation insights from social cognitive and affective neuroscience.
        Curr Dir Psychol Sci. 2008; 17: 153-158
        • Paret C.
        • Kluetsch R.
        • Ruf M.
        • Demirakca T.
        • Hoesterey S.
        • Ende G.
        • Schmahl C.
        Down-regulation of amygdala activation with real-time fMRI neurofeedback in a healthy female sample.
        Front Behav Neurosci. 2014; 8: 299
        • Brühl A.B.
        • Scherpiet S.
        • Sulzer J.
        • Stämpfli P.
        • Seifritz E.
        • Herwig U.
        Real-time neurofeedback using functional MRI could improve down-regulation of amygdala activity during emotional stimulation: A proof-of-concept study.
        Brain Topogr. 2014; 27: 138-148
        • Zotev V.
        • Phillips R.
        • Young K.D.
        • Drevets W.C.
        • Bodurka J.
        Prefrontal control of the amygdala during real-time fMRI neurofeedback training of emotion regulation.
        PLoS One. 2013; 8: e79184
        • Etkin A.
        • Schatzberg A.F.
        Common abnormalities and disorder-specific compensation during implicit regulation of emotional processing in generalized anxiety and major depressive disorders.
        Am J Psychiatry. 2011; 168: 968-978

      CHORUS Manuscript

      View Open Manuscript