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Neural synchrony during perceptual organization in schizophrenia [Elektronische Ressource] / von Christine Grützner

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Neural Synchrony during PerceptualOrganization in SchizophreniaDissertationzur Erlangung des Doktorgradesder Naturwissenschaftenvorgelegt beim Fachbereich Psychologie und Sportwissenschaftender Johann Wolfgang Goethe - Universit atin Frankfurt am MainvonChristine Grutzneraus DusseldorfFrankfurt am Main 2010D30vom Fachbereich Psychologie und Sportwissenschaften der Johann WolfgangGoethe - Universit at in Frankfurt am Main als Dissertation angenommen.Dekan:Prof. Dr. Winfried BanzerGutachter:Prof. Dr. Monika Knopf, Johann Wolfgang Goethe - Universit at, FrankfurtProf. Dr. Wolf Singer, Max-Planck-Institut fur Hirnforschung, FrankfurtDatum der Disputation:AcknowledgmentsThe research presented in this thesis was carried out at the Max-Planck-Institute for Brain Research in the Department of Neurophysiology. I wouldlike to thank PD Dr. Peter Uhlhaas, the supervisor of this dissertation, andProf. Dr. Wolf Singer for giving me the opportunity to work in this excel-lent scienti c environment, present my work at conferences, and take part invarious workshops.I am deeply grateful to Dr. Michael Wibral, the head of the MEG unit at theBrain Imaging Center in Frankfurt, for his guidance and support during mythesis. This project would not have been possible without your help, expertiseand patience to answer all my questions.

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Published 01 January 2010
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Neural Synchrony during Perceptual
Organization in Schizophrenia
Dissertation
zur Erlangung des Doktorgrades
der Naturwissenschaften
vorgelegt beim Fachbereich Psychologie und Sportwissenschaften
der Johann Wolfgang Goethe - Universit at
in Frankfurt am Main
von
Christine Grutzner
aus Dusseldorf
Frankfurt am Main 2010
D30vom Fachbereich Psychologie und Sportwissenschaften der Johann Wolfgang
Goethe - Universit at in Frankfurt am Main als Dissertation angenommen.
Dekan:
Prof. Dr. Winfried Banzer
Gutachter:
Prof. Dr. Monika Knopf, Johann Wolfgang Goethe - Universit at, Frankfurt
Prof. Dr. Wolf Singer, Max-Planck-Institut fur Hirnforschung, Frankfurt
Datum der Disputation:Acknowledgments
The research presented in this thesis was carried out at the Max-Planck-
Institute for Brain Research in the Department of Neurophysiology. I would
like to thank PD Dr. Peter Uhlhaas, the supervisor of this dissertation, and
Prof. Dr. Wolf Singer for giving me the opportunity to work in this excel-
lent scienti c environment, present my work at conferences, and take part in
various workshops.
I am deeply grateful to Dr. Michael Wibral, the head of the MEG unit at the
Brain Imaging Center in Frankfurt, for his guidance and support during my
thesis. This project would not have been possible without your help, expertise
and patience to answer all my questions.
Thank you to all colleagues at the Max-Planck-Institute, Brain Imaging Cen-
ter, the MEG lab and the Laboratory of Neurophysiology and Neuroimag-
ing. I especially thank Sandra Anti, Corinna Haenschel, Michael Lindner,
Jutta Mayer, Viola Oertel-Kn ochel, Viola Priesemann, Frederic Roux, Anna
Rotarska-Jagiela, Anne Schmidt, Brigitte Sinke, Cerisa Stawowski, and Sarah
Weigelt for their friendship and advice, and for helping me through di cult
times.
I would like to thank Tahmine Tozman for help with MEG data acquisition,
and Sandra Anti, Erhan Genc and Axel Kohler for help with fMRI data acquisi-
tion and analysis. Thank you also to our colleagues at the Clinic for Psychiatry
and Psychotherapy in Cologne who recruited the rst-episode schizophrenia
patients and accompanied them to Frankfurt for our measurements. My grat-
iitude also goes to PD Dr. Sabine Heim for her guidance at the beginning of
the writing process, and to Prof. Dr. Monika Knopf for supervising me during
the nal stage of the dissertation.
I am very grateful to my family, especially my parents Julia and Friedrich Till-
mann, and my sister and brothers Marietta, Matthias and Alexander Tillmann,
for all their support on my way during the last years.
Finally, I want to thank my husband, Immanuel Grutzner, for helping me keep
my spirits up and giving me the strength to keep going { without your support,
I would have never been able to complete this work. Thank you for everything.
iiAbstract
Current theories of schizophrenia suggest that the pathophysiology of the dis-
order may be the result of a de cit in the coordination of neural activity
within and between areas of the brain, which may lead to impairments in basic
cognitive functions such as contextual disambiguation and dynamic grouping
(Phillips and Silverstein, 2003). This notion has been supported by recent
studies showing that patients with schizophrenia are characterized by reduced
synchronous, oscillatory activity in the gamma-frequency band during sensory
processing (e.g., Spencer et al., 2003; Green et al., 2003; Wynn et al., 2005).
However, it is currently unclear to what extent high-frequency gamma-band
oscillations (> 60 Hz) contribute to impaired neural synchronization as re-
search has so far focussed on gamma-band oscillations between 30 and 60 Hz.
In addition, it is not known whether de cits in high-frequency oscillations are
already present at the onset of the disorder and to what extent reductions
may be related to the confounding in uence of antipsychotic medication. Fi-
nally, the neural generators underlying impairments in synchronous oscillatory
activity in schizophrenia have not been investigated yet.
To address these questions, we recorded MEG activity during a visual closure
task (Mooney faces task) in medicated chronic schizophrenia patients, drug-
na ve rst-episode schizophrenia patients and healthy controls. MEG data
were analysed for spectral power between 25 and 150 Hz, and beamforming
techniques were used to localize the sources of oscillatory gamma-band activity.
In healthy controls, we observed that the processing of Mooney faces was as-
iiisociated with sustained high-frequency gamma-band activity (> 60 Hz). A
time-resolved analysis of the neural generators underlying perceptual closure
revealed a network of distributed sources in occipito-temporal, parietal and
frontal regions, which were di erentially activated during speci c time inter-
vals. In chronic schizophrenia patients, we found a pronounced reduction of
high-frequency gamma-band oscillatory activity that was accompanied by an
impairment in perceptual organization and involved reduced source power in
various brain regions associated with perceptual closure. First-episode patients
were also characterized by a de cit in high-frequency gamma-band activity and
reductions of source power in multiple areas; these impairments, however, were
less pronounced than in chronic patients. Regarding behavioral performance,
rst-episode patients were not impaired in their ability to detect Mooney faces,
but exhibited a loss in speci city of face detection.
In conclusion, our results suggest that schizophrenia is associated with a
widespread reduction in high-frequency oscillations that indicate local net-
work abnormalities. These dysfunctions are independent of medication status
and already present at illness onset, suggesting a possible progressive de cit
during the course of the disorder.
ivContents
1 Introduction 1
1.1 Gestalt Theory of Visual Perception . . . . . . . . . . . . . . . . 4
1.1.1 Origins of Gestalt Theory . . . . . . . . . . . . . . . . . 4
1.1.2 Gestalt Principles of Perceptual Organization . . . . . . 5
1.2 Perceptual Organization and Neural Synchrony . . . . . . . . . 7
1.2.1 Theories of Visual Feature Binding . . . . . . . . . . . . 7
1.2.2 Gamma-Band Oscillations and Visual Binding . . . . . . 13
1.2.3 Mechanisms of Gamma-Band Oscillations . . . . . . . . 19
1.3 Cognitive and Neural Coordination in Schizophrenia . . . . . . . 21
1.3.1 Clinical Features of Schizophrenia . . . . . . . . . . . . . 21
1.3.2 Perceptual Organization in Schizophrenia . . . . . . . . . 28
1.3.3 Neural Synchrony in Schizophrenia . . . . . . . . . . . . 37
1.3.4 Neurobiology of Schizophrenia . . . . . . . . . . . . . . . 42
1.4 Synopsis and Overview of Studies . . . . . . . . . . . . . . . . . 50
2 General Methods 55
2.1 Participants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
2.2 General Procedure . . . . . . . . . . . . . . . . . . . . . . . . . 56
vContents
2.3 Assessment of Psychopathology and Cognitive Function . . . . . 57
2.3.1 Psychopathology in Schizophrenia . . . . . . . . . . . . . 57
2.3.2 Assessment of Cognitive Function . . . . . . . . . . . . . 58
2.3.3 Assessment of General Intelligence . . . . . . . . . . . . 58
2.4 Visual Closure Task . . . . . . . . . . . . . . . . . . . . . . . . . 59
2.4.1 Mooney Faces Stimuli . . . . . . . . . . . . . . . . . . . 59
2.4.2 Stimulus Presentation . . . . . . . . . . . . . . . . . . . 62
2.4.3 Task . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64
2.5 MEG and FMRI Recordings . . . . . . . . . . . . . . . . . . . . 64
2.5.1 MEG Data Acquisition . . . . . . . . . . . . . . . . . . . 64
2.5.2 FMRI Data . . . . . . . . . . . . . . . . . . 65
3 Experimental Series 67
3.1 Neuroelectromagnetic Correlates of Perceptual Closure Processes 67
3.1.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 67
3.1.2 Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . 68
3.1.3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74
3.1.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . 83
3.2 High-Frequency Gamma Oscillations during Perceptual Organi-
zation in Chronic Schizophrenia Patients . . . . . . . . . . . . . 89
3.2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 89
3.2.2 Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
3.2.3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
3.2.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . 103
3.3 High-Frequency Gamma-Band Oscillations in Unmedicated
First-Episode Schizophrenia Patients . . . . . . . . . . . . . . . 108
3.3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 108
viContents
3.3.2 Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
3.3.3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . 114
3.3.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . 123
4 General Discussion 133
4.1 Gamma-Band Oscillations during Perceptual Organization in
Healthy Controls . . . . . . . . . . . . . . . . . . . . . . . . . . 133
4.2 Gamma-Band Activity in Schizophrenia . . . . . . . . . . . . . 137
4.3 Perceptual Organization in Sc . . . . . . . . . . . . . 141
4.4 Limitations and Future Directions . . . . . . . . . . . . . . . . . 143
4.5 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
References 149
Appendix 217
Zusammenfassung 233
viiContents
viii