Self-Organized Criticality as a Neurodynamical Correlate of Consciousness: A neurophysiological approach to measure states of consciousness based on EEG-complexity features

Abstract

Background and Objectives This thesis was based on the hypothesis that the physics-derived theoretical framework of self-organized criticality can be applied to the neuronal dynamics of the human brain. From a consciousness science perspective, this is especially appealing as critical brain dynamics imply a vicinity a phase transition, which is associated with optimized information processing functions as well as the largest repertoire of configurations that a system explores throughout its temporal evolution. Hence, self-organised criticality could serve as a neurodynamical correlate for consciousness, which provides the possibility of deriving empirically testable neurophysiological indices suitable to characterise and quantify states of consciousness. The purpose of this work was to experimentally examine the feasibility of the self-organized criticality theory as a correlate for states of consciousness. Therefore, it was aimed at answering the following research questions based on the analysis of three 64 channel EEG datasets: (i) Can signatures of self-organized criticality be found on the level of the EEG in terms of scale-free distribution of neuronal avalanches and the presence of long-range temporal correlations (LRTC) in neuronal oscillations? (ii) Are criticality features suitable to differentiate state of consciousness in the spectrum of wakefulness? (iii) Can the neuronal dynamics be shifted towards the critical point of a phase transition associated with optimized information processing function by mind-body interventions? (iv) Can an explicit relationship to other nonlinear complexity features and power spectral density parameter be identified? (v) Do EEG-based criticality features reflect individual temperament traits? Material and Methods (1): Re-analysis: Thirty participants highly proficient in meditation (mean age 47 years, 11 females/19 males, meditation experience of at least 5 years practice or more than 1000 h of total meditation time) were measured with 64-channel EEG during one session consisting of a task-free baseline resting, a reading condition and three meditation conditions, namely thoughtless emptiness, presence monitoring and focused attention. (2): 64-channel EEG was recorded from 34 participants (mean age 36.0 ±13.4 years, 24 females/ 10 males) before, during and after a professional singing bowl massage. Further, psychometric data was assessed including absorption capacity defined as the individual’s capacity for engaging attentional resources in sensory and imaginative experiences measured by the Tellegen-Absorption Scale (TAS-D), subjective changes in in body sensation, emotional state, and mental state (CSP-14) as well as the phenomenology of consciousness (PCI-K). (3): Electrophysiological data (64 channels of EEG, EOG, ECG, skin conductance, and respiration) was recorded from 116 participants (mean age 40.0 ±13.4 years, 83 females/ 33 males) – in collaboration with the Institute of Psychology, Bundeswehr University Munich - during a task-free baseline resting state. The individual level of sensory processing sensitivity was assessed using the High Sensitive Person Scale (HSPS-G). The datasets were analysed applying analytical tools from self-organized criticality theory (detrended fluctuation analysis, neuronal avalanche analysis), nonlinear complexity algorithms (multiscale entropy, Higuchi’s fractal dimension) and power spectral density. In study 1 and 2, task conditions were contrasted, and effect sizes were compared using a paired two-tailed t-test calculated across participants, and features. T-values were corrected for multiple testing using false discovery rate. To calculate correlations between the EEG features, Spearman’s rank correlation was applied after determining that the distribution was not appropriate for parametric testing by the Shapiro-Wilk test. In addition, in study 1, a discrimination analysis was carried out to determine the classification performance of the EEG features. Here, partial least squares regression and receiver operating characteristics analysis was applied. To determine whether the EEG features reflect individual temperament traits, the individual level of absorption capacity (study 2) and sensory processing sensitivity (study 3) was correlated with the EEG features using Spearman’s rank correlation. Results Signatures of self-organized criticality in the form of scale-free distribution of neuronal avalanches and long-range temporal correlations (LRTCs) in the amplitude of neural oscillations were observed in three distinct EEG-datasets. EEG criticality as well as complexity features were suitable to characterise distinct states of consciousness. In study 1, compared to the task-free resting condition, all three meditative states revealed significantly reduced long-range temporal correlation with moderate effect sizes (presence monitoring: d= -0.49, p<.001; thoughtless emptiness: d= -0.37, p<.001; and focused attention: d= -0.28, p=.003). The critical exponent was suitable to differentiate between focused attention and presence monitoring (d= -0.32, p=.02). Further, in study 2, the criticality features significantly changed during the course of the experiment, whereby values indicated a shift towards the critical regime during the sound condition. Both analyses of the first and second dataset revealed that the critical exponent was significantly negatively correlated with the sample entropy, the scaling exponent resulting from the DFA denoting the amount of long-range temporal correlations as well as Higuchi’s fractal dimension in each condition, respectively. In addition, the critical scaling exponent was found to be significantly negatively correlated with the trait absorption (Spearman's ρ= -0.39, p= .007), whereas an association between critical dynamics and the level of sensory processing sensitivity could not be verified (study 3). Conclusion The findings of this thesis suggest that neuronal dynamics are governed by the phenomena of self-organized criticality. EEG-based criticality features were shown to be sensitive to detect experimentally induced alterations in the state of consciousness. Further, an explicit relationship with nonlinear measures determining the degree of neuronal complexity was identified. Thus, self-organized criticality seems feasible as a neurodynamical correlate for consciousness with the potential to quantify and characterize states of consciousness. Its agreement with the current most influencing theories in the field of consciousness research is discussed

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