Brain Topography

, Volume 29, Issue 2, pp 308–321 | Cite as

Towards Using Microstate-Neurofeedback for the Treatment of Psychotic Symptoms in Schizophrenia. A Feasibility Study in Healthy Participants

  • Laura Diaz Hernandez
  • Kathryn Rieger
  • Anja Baenninger
  • Daniel Brandeis
  • Thomas Koenig
Original Paper

Abstract

Spontaneous EEG signal can be parsed into sub-second periods of stable functional states (microstates) that assumingly correspond to brief large scale synchronization events. In schizophrenia, a specific class of microstate (class “D”) has been found to be shorter than in healthy controls and to be correlated with positive symptoms. To explore potential new treatment options in schizophrenia, we tested in healthy controls if neurofeedback training to self-regulate microstate D presence is feasible and what learning patterns are observed. Twenty subjects underwent EEG-neurofeedback training to up-regulate microstate D presence. The protocol included 20 training sessions, consisting of baseline trials (resting state), regulation trials with auditory feedback contingent on microstate D presence, and a transfer trial. Response to neurofeedback was assessed with mixed effects modelling. All participants increased the percentage of time spent producing microstate D in at least one of the three conditions (p < 0.05). Significant between-subjects across-sessions results showed an increase of 0.42 % of time spent producing microstate D in baseline (reflecting a sustained change in the resting state), 1.93 % of increase during regulation and 1.83 % during transfer. Within-session analysis (performed in baseline and regulation trials only) showed a significant 1.65 % increase in baseline and 0.53 % increase in regulation. These values are in a range that is expected to have an impact upon psychotic experiences. Additionally, we found a negative correlation between alpha power and microstate D contribution during neurofeedback training. Given that microstate D has been related to attentional processes, this result provides further evidence that the training was to some degree specific for the attentional network. We conclude that microstate-neurofeedback training proved feasible in healthy subjects. The implementation of the same protocol in schizophrenia patients may promote skills useful to reduce positive symptoms by means of EEG-neurofeedback.

Keywords

EEG Neurofeedback Resting state Microstates Modelling Schizophrenia 

References

  1. Andreasen NC, Paradiso S, O’Leary DS (1998) Cognitive dysmetria as an integrative theory of schizophrenia: a dysfunction in cortical-subcortical-cerebellar circuitry? Schizophr Bull 24:203–218CrossRefPubMedGoogle Scholar
  2. Arns M, Heinrich H, Strehl U (2014) Evaluation of neurofeedback in ADHD: the long and winding road. Biol Psychol 95:108–115CrossRefPubMedGoogle Scholar
  3. Bates D, Maechler M, Bolker B and Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–7. http://CRAN.R-project.org/package=lme4
  4. Bolea AS (2010) Neurofeedback treatment of chronic inpatient schizophrenia. J Neurother 14(1):47–54CrossRefGoogle Scholar
  5. Borkenau P, Ostendorf F (1993) NEO-Fünf-Faktoren Inventar (NEO-FFI) nach Costa und McCrae [NEO Five-Factor Personality Inventory (NEO-FFI) according Costa and McCrae]. Hogrefe, GöttingenGoogle Scholar
  6. Boutros NN, Arfken C, Galderisi S, Warrick J, Pratt G, Iacono W (2008) The status of spectral EEG abnormality as a diagnostic test for schizophrenia. Schizophr Res 99:225–237PubMedCentralCrossRefPubMedGoogle Scholar
  7. Britz J, Van De Ville D, Michel CM (2010) BOLD correlates of EEG topography reveal rapid resting-state network dynamics. NeuroImage 52:1162–1170CrossRefPubMedGoogle Scholar
  8. Cho MK, Jang HS, Jeong S-H, Jang I-S, Choi B-J, Lee M-GT (2008) Alpha neurofeedback improves the maintaining ability of alpha activity. NeuroReport 19:315–317CrossRefPubMedGoogle Scholar
  9. Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215CrossRefPubMedGoogle Scholar
  10. Delorme A, Sejnowski T, Makeig S (2007) Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis. Neuroimage 34:1443–1449PubMedCentralCrossRefPubMedGoogle Scholar
  11. Derogatis LR, Melisaratos N (1983) The Brief Symptom Inventory: an introductory report. Psychol Med 13:595–605CrossRefPubMedGoogle Scholar
  12. Fahrenberg J, Myrtek M, Schumacher J, Brähler E (2000) Fragebogen zür Lebenszufriedenheit (FLZ). Handanweisung, GermanyGoogle Scholar
  13. Gevensleben H, Kleemeyer M, Rothenberger LG, Studer P, Flaig-Rohr A et al (2014) Neurofeedback in ADHD: further pieces of the puzzle. Brain Topogr 27:20–32CrossRefPubMedGoogle Scholar
  14. Gruzelier J (2013). EEG-neurofeedback for optimising performance I: A review of cognitive and affective outcome in healthy participants. Neurosci Biobehav RevGoogle Scholar
  15. Gruzelier J (2014) EEG-neurofeedback for optimising performance III: A review of methodological and theoretical considerations. Neurosci Biobehav Rev 1–24Google Scholar
  16. Gruzelier J, Hardman E, Wild J, Zaman R (1999) Learned control of slow potential interhemispheric asymmetry in schizophrenia. Int J Psychophysiol 34:341–348CrossRefPubMedGoogle Scholar
  17. Hartmann T, Lorenz I, Muller N, Langguth B, Weisz N (2014) The effects of neurofeedback on oscillatory processes related to tinnitus. Brain Topogr 27:149–157CrossRefPubMedGoogle Scholar
  18. Holtforth MG, Grawe K. 2003. The incongruence questionnaire (ink). An instrument for the analysis of motivational incongruence. Zeitschrift fur Klinische Psychologie und Psychotherapie Forschung und PraxisGoogle Scholar
  19. Kikuchi M, Koenig T, Wada Y, Higashima M, Koshino Y et al (2007) Native EEG and treatment effects in neuroleptic-naïve schizophrenic patients: time and frequency domain approaches. Schizophr Res 97:163–172CrossRefPubMedGoogle Scholar
  20. Kindler J, Hubl D, Strik WK, Dierks T, Koenig T (2011) Resting-state EEG in schizophrenia: auditory verbal hallucinations are related to shortening of specific microstates. Clin Neurophysiol 122:1179–1182CrossRefPubMedGoogle Scholar
  21. Knoblauch A, Hauser F, Gewaltig MO, Korner E, Palm G (2012) Does spike-timing-dependent synaptic plasticity couple or decouple neurons firing in synchrony? Front Comput Neurosci 6:55PubMedCentralCrossRefPubMedGoogle Scholar
  22. Koenig T, Kochi K, Lehmann D (1998) Event-related electric microstates of the brain differ between words with visual and abstract meaning. Electroencephalogr Clin Neurophysiol 106:535–546CrossRefPubMedGoogle Scholar
  23. Koenig T, Lehmann D, Merlo MC, Kochi K, Hell D, Koukkou M (1999) A deviant EEG brain microstate in acute, neuroleptic-naive schizophrenics at rest. Eur Arch Psychiatry Clin Neurosci 249:205–211CrossRefPubMedGoogle Scholar
  24. Koenig T, Prichep L, Lehmann D, Sosa PV, Braeker E et al (2002) Millisecond by millisecond, year by year: normative EEG microstates and developmental stages. NeuroImage 16:41–48CrossRefPubMedGoogle Scholar
  25. Laufs H, Kleinschmidt A, Beyerle A, Eger E, Salek-Haddadi A et al (2003a) EEG-correlated fMRI of human alpha activity. Neuroimage 19:1463–1476CrossRefPubMedGoogle Scholar
  26. Laufs H, Krakow K, Sterzer P, Eger E, Beyerle A et al (2003b) Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest. Proc Natl Acad Sci USA 100:11053–11058PubMedCentralCrossRefPubMedGoogle Scholar
  27. Lehmann D (1987) In: Gevins AS, Remond A (eds) Principles of spatial analysis, Elsevier, Amsterdam, pp 309–54Google Scholar
  28. Lehmann D, Strik WK, Henggeler B, Koenig T, Koukkou M (1998) Brain electric microstates and momentary conscious mind states as building blocks of spontaneous thinking: I. Visual imagery and abstract thoughts. Int J Psychophysiol 29:1–11CrossRefPubMedGoogle Scholar
  29. Lehmann D, Faber PL, Galderisi S, Herrmann WM, Kinoshita T et al (2005) EEG microstate duration and syntax in acute, medication-naive, first-episode schizophrenia: a multi-center study. Psychiatry Res 138:141–156CrossRefPubMedGoogle Scholar
  30. Lehrl S, Triebig G, Fischer B (1995) Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence. Acta Neurol Scand 91:335–345CrossRefPubMedGoogle Scholar
  31. Liechti MD, Maurizio S, Heinrich H, Jäncke L, Meier L et al (2012) First clinical trial of tomographic neurofeedback in attention-deficit/hyperactivity disorder: evaluation of voluntary cortical control. Clinical Neurophysiology 123(10):1989–2005CrossRefPubMedGoogle Scholar
  32. Littow H, Huossa V, Karjalainen S, Jaaskelainen E, Haapea M et al (2015) Aberrant functional connectivity in the default mode and central executive networks in subjects with schizophrenia - a whole-brain Resting-state ICA study. Front Psychiatry 6:26PubMedCentralCrossRefPubMedGoogle Scholar
  33. Menon V (2011) Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci 15:483–506CrossRefPubMedGoogle Scholar
  34. Mottaz A, Solcà M, Magnin C, Corbet T, Schnider A, Guggisberg AG (2014) Clinical Neurophysiology Neurofeedback training of alpha-band coherence enhances motor performance. Clin NeurophysiolGoogle Scholar
  35. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  36. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  37. Ritsner MS (2010) Pregnenolone, dehydroepiandrosterone, and schizophrenia: alterations and clinical trials. CNS Neurosci Ther 16:32–44CrossRefPubMedGoogle Scholar
  38. Ros T, Moseley MJ, Pa Bloom, Benjamin L, La Parkinson, Gruzelier JH (2009) Optimizing microsurgical skills with EEG neurofeedback. BMC Neurosci 10:87PubMedCentralCrossRefPubMedGoogle Scholar
  39. Ros T, Théberge J, Pa Frewen, Kluetsch R, Densmore M et al (2013) Mind over chatter: plastic up-regulation of the fMRI salience network directly after EEG neurofeedback. NeuroImage 65:324–335CrossRefPubMedGoogle Scholar
  40. Ros T, Bernard JB, Lanius RA, Vuilleumier P (2014) Tuning pathological brain oscillations with neurofeedback: a systems neuroscience framework. Front Hum Neurosci 8:1008PubMedCentralCrossRefPubMedGoogle Scholar
  41. Ruiz S, Lee S, Soekadar SR, Caria A, Veit R et al (2011) Acquired self-control of insula cortex modulates emotion recognition and brain network connectivity in schizophrenia. Hum Brain Mapp 34:200–212CrossRefPubMedGoogle Scholar
  42. Saletu B, Itil TM, Saletu M (1971) Auditory evoked response, EEG, and thought process in schizophrenics. Am J Psychiatry 128:336–344CrossRefPubMedGoogle Scholar
  43. Schneider F, Elbert T, Heimann H, Welker A, Stetter F et al (1992a) Self-regulation of slow cortical potentials in psychiatric patients: alcohol dependency. Biofeedback self Regul 18:23–32CrossRefGoogle Scholar
  44. Schneider F, Rockstroh B, Heimann H, Lutzenberger W, Mattes R et al (1992b) Self-regulation of slow cortical potentials in psychiatric patients: schizophrenia. Biofeedback self Regul 17:277–292CrossRefPubMedGoogle Scholar
  45. Shergill SS, Murray RM, McGuire PK (1998) Auditory hallucinations: a review of psychological treatments. Schizophr Res 32:137–150CrossRefPubMedGoogle Scholar
  46. Shields SA, Mallory ME, Simon A (1989) The body awareness questionnaire: Reliability and validity. J Personal Assess 53(4):802–815CrossRefGoogle Scholar
  47. Shutara Y, Koga Y, Fujita K, Takeuchi H, Mochida M, Takemasa K (1996) An event-related potential study on the impairment of automatic processing of auditory input in schizophrenia. Brain Topogr 8:285–289CrossRefPubMedGoogle Scholar
  48. Spielberger CD (2010) State-Trait Anxiety Inventory. The Corsini Encyclopedia of Psychology. Wiley, HobokenGoogle Scholar
  49. Sterman MB, Egner T (2006) Foundation and practice of neurofeedback for the treatment of epilepsy. Appl Psychophysiol Biofeedback 31:21–35CrossRefPubMedGoogle Scholar
  50. Strelets V, Faber PL, Golikova J, Novototsky-Vlasov V, Koenig T et al (2003) Chronic schizophrenics with positive symptomatology have shortened EEG microstate durations. Clin Neurophysiol 114:2043–2051CrossRefPubMedGoogle Scholar
  51. Surmeli T, Ertem A, Eralp E, Kos IH (2012) Schizophrenia and the efficacy of qEEG-guided neurofeedback treatment: a clinical case series. Clin EEG Neurosci 43:133–144CrossRefPubMedGoogle Scholar
  52. Tomescu MI, Ta Rihs, Becker R, Britz J, Custo A et al (2014) Deviant dynamics of EEG resting state pattern in 22q11.2 deletion syndrome adolescents: a vulnerability marker of schizophrenia? Schizophr Res 157:175–181CrossRefPubMedGoogle Scholar
  53. Watson D, Clark LA, Tellegen A (1988) Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol 54:1063–1070CrossRefPubMedGoogle Scholar
  54. Woodward ND, Rogers B, Heckers S (2011) Functional resting-state networks are differentially affected in schizophrenia. Schizophr Res 130:86–93PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Laura Diaz Hernandez
    • 1
  • Kathryn Rieger
    • 1
    • 2
  • Anja Baenninger
    • 1
  • Daniel Brandeis
    • 3
    • 4
    • 5
    • 6
  • Thomas Koenig
    • 1
    • 2
  1. 1.Translational Research Center, University Hospital of PsychiatryUniversity of BernBern 60Switzerland
  2. 2.Center for Cognition, Learning and MemoryUniversity of BernBernSwitzerland
  3. 3.Department of Child and Adolescent PsychiatryUniversity of ZürichZurichSwitzerland
  4. 4.Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty MannheimHeidelberg UniversityMannheimGermany
  5. 5.Zurich Center for Integrative Human PhysiologyUniversity of ZürichZurichSwitzerland
  6. 6.Neuroscience Center ZurichUniversity and ETH ZürichZurichSwitzerland

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