Brain connectivity analysis from EEG signals using stable phase-synchronized states during face perception tasks

This is the author accepted manuscript. The final version is available from Elsevier via the DOI in this recordDegree of phase synchronization between different Electroencephalogram (EEG) channels is known to be the manifestation of the underlying mechanism of information coupling between different brain regions. In this paper, we apply a continuous wavelet transform (CWT) based analysis technique on EEG data, captured during face perception tasks, to explore the temporal evolution of phase synchronization, from the onset of a stimulus. Our explorations show that there exists a small set (typically 3-5) of unique synchronized patterns or synchrostates, each of which are stable of the order of milliseconds. Particularly, in the beta (β) band, which has been reported to be associated with visual processing task, the number of such stable states has been found to be three consistently. During processing of the stimulus, the switching between these states occurs abruptly but the switching characteristic follows a well-behaved and repeatable sequence. This is observed in a single subject analysis as well as a multiple-subject group-analysis in adults during face perception. We also show that although these patterns remain topographically similar for the general category of face perception task, the sequence of their occurrence and their temporal stability varies markedly between different face perception scenarios (stimuli) indicating toward different dynamical characteristics for information processing, which is stimulus-specific in nature. Subsequently, we translated these stable states into brain complex networks and derived informative network measures for characterizing the degree of segregated processing and information integration in those synchrostates, leading to a new methodology for characterizing information processing in human brain. The proposed methodology of modeling the functional brain connectivity through the synchrostates may be viewed as a new way of quantitative characterization of the cognitive ability of the subject, stimuli and information integration/segregation capability.The work presented in this paper was supported by FP7 EU funded MICHELANGELO project, Grant Agreement #288241. Website: www.michelangelo-project.eu/

Prediction of Synchrostate Transitions in EEG Signals Using Markov Chain Models

This is the author accepted manuscript. The final version is available from IEEE via the DOI in this record.This paper proposes a stochastic model using the concept of Markov chains for the inter-state transitions of the millisecond order quasi-stable phase synchronized patterns or synchrostates, found in multi-channel Electroencephalogram (EEG) signals. First and second order transition probability matrices are estimated for Markov chain modelling from 100 trials of 128-channel EEG signals during two different face perception tasks. Prediction accuracies with such finite Markov chain models for synchrostate transition are also compared, under a data-partitioning based cross-validation scheme.The work presented in this paper was supported by FP7 EU funded MICHELANGELO project, Grant Agreement #288241

EEG source-space synchrostate transitions and Markov modeling in the math-gifted brain during a long-chain reasoning task

To reveal transition dynamics of global neuronal networks of math‐gifted adolescents in handling long‐chain reasoning, this study explores momentary phase‐synchronized patterns, that is, electroencephalogram (EEG) synchrostates, of intracerebral sources sustained in successive 50 ms time windows during a reasoning task and non‐task idle process. Through agglomerative hierarchical clustering for functional connectivity graphs and nested iterative cosine similarity tests, this study identifies seven general and one reasoning‐specific prototypical functional connectivity patterns from all synchrostates. Markov modeling is performed for the time‐sequential synchrostates of each trial to characterize the interstate transitions. The analysis reveals that default mode network, central executive network (CEN), dorsal attention network, cingulo‐opercular network, left/right ventral frontoparietal network, and ventral visual network aperiodically recur over non‐task or reasoning process, exhibiting high predictability in interactively reachable transitions. Compared to non‐gifted subjects, math‐gifted adolescents show higher fractional occupancy and mean duration in CEN and reasoning‐triggered transient right frontotemporal network (rFTN) in the time course of the reasoning process. Statistical modeling of Markov chains reveals that there are more self‐loops in CEN and rFTN of the math‐gifted brain, suggesting robust state durability in temporally maintaining the topological structures. Besides, math‐gifted subjects show higher probabilities in switching from the other types of synchrostates to CEN and rFTN, which represents more adaptive reconfiguration of connectivity pattern in the large‐scale cortical network for focused task‐related information processing, which underlies superior executive functions in controlling goal‐directed persistence and high predictability of implementing imagination and creative thinking during long‐chain reasoning

Classification of autism spectrum disorder using supervised learning of brain connectivity measures extracted from synchrostates

This is the author accepted manuscript. The final version is available from IOP Publishing via the DOI in this record.OBJECTIVE: The paper investigates the presence of autism using the functional brain connectivity measures derived from electro-encephalogram (EEG) of children during face perception tasks. APPROACH: Phase synchronized patterns from 128-channel EEG signals are obtained for typical children and children with autism spectrum disorder (ASD). The phase synchronized states or synchrostates temporally switch amongst themselves as an underlying process for the completion of a particular cognitive task. We used 12 subjects in each group (ASD and typical) for analyzing their EEG while processing fearful, happy and neutral faces. The minimal and maximally occurring synchrostates for each subject are chosen for extraction of brain connectivity features, which are used for classification between these two groups of subjects. Among different supervised learning techniques, we here explored the discriminant analysis and support vector machine both with polynomial kernels for the classification task. MAIN RESULTS: The leave one out cross-validation of the classification algorithm gives 94.7% accuracy as the best performance with corresponding sensitivity and specificity values as 85.7% and 100% respectively. SIGNIFICANCE: The proposed method gives high classification accuracies and outperforms other contemporary research results. The effectiveness of the proposed method for classification of autistic and typical children suggests the possibility of using it on a larger population to validate it for clinical practice.The work presented in this paper was supported by FP7 EU funded MICHELANGELO project, Grant Agreement #288241. URL: www.michelangelo-project.eu/

Using large-scale neural models to interpret connectivity measures of cortico-cortical dynamics at millisecond temporal resolution

Over the last two decades numerous functional imaging studies have shown that higher order cognitive functions are crucially dependent on the formation of distributed, large-scale neuronal assemblies (neurocognitive networks), often for very short durations. This has fueled the development of a vast number of functional connectivity measures that attempt to capture the spatiotemporal evolution of neurocognitive networks. Unfortunately, interpreting the neural basis of goal directed behavior using connectivity measures on neuroimaging data are highly dependent on the assumptions underlying the development of the measure, the nature of the task, and the modality of the neuroimaging technique that was used. This paper has two main purposes. The first is to provide an overview of some of the different measures of functional/effective connectivity that deal with high temporal resolution neuroimaging data. We will include some results that come from a recent approach that we have developed to identify the formation and extinction of task-specific, large-scale neuronal assemblies from electrophysiological recordings at a ms-by-ms temporal resolution. The second purpose of this paper is to indicate how to partially validate the interpretations drawn from this (or any other) connectivity technique by using simulated data from large-scale, neurobiologically realistic models. Specifically, we applied our recently developed method to realistic simulations of MEG data during a delayed match-to-sample (DMS) task condition and a passive viewing of stimuli condition using a large-scale neural model of the ventral visual processing pathway. Simulated MEG data using simple head models were generated from sources placed in V1, V4, IT, and prefrontal cortex (PFC) for the passive viewing condition. The results show how closely the conclusions obtained from the functional connectivity method match with what actually occurred at the neuronal network level

Using Brain Connectivity Measure of EEG Synchrostates for Discriminating Typical and Autism Spectrum Disorder

This is the author accepted manuscript. The final version is available from IEEE via the DOI in this record.In this paper we utilized the concept of stable phase synchronization topography - synchrostates - over the scalp derived from EEG recording for formulating brain connectivity network in Autism Spectrum Disorder (ASD) and typically-growing children. A synchronization index is adapted for forming the edges of the connectivity graph capturing the stability of each of the synchrostates. Such network is formed for 11 ASD and 12 control group children. Comparative analyses of these networks using graph theoretic measures show that children with autism have a different modularity of such networks from typical children. This result could pave the way to a new modality for possible identification of ASD from non-invasively recorded EEG data

Functional connectivity signatures of visual-motor coordination using spectral dynamical analysis

Visual-motor coordination is an essential function of human motion control, which requires interactions of multiple brain regions. Visual tracking is a behavioural task that requires intensive visual-motor coordination, which makes it a good paradigm to study the underlying mechanism of visual-motor coordination. In this research, tracking paradigm was used to study the visual-motor coordination, and both behaviour and electroencephalography (EEG) functional connectivity were analysed. The behavioural analysis explored the anticipatory characteristic of human motion control. In the tracking paradigm, participants were asked to trace a target moving with constant speed along a circular trajectory. Two different types of tracking paradigm were applied in the research. Firstly, the full visibility tracking trials were performed, in which participants had the full visibility of the target movement. Participants showed weak anticipatory behaviour in the full visibility tracking trials. In order to observe stronger anticipatory behaviour, the intermittent tracking trials were then performed, in which two target-invisible zones were added. It was found that participants applied two distinctive control modes of visual-motor coordination in the target-visible zone and target-invisible zone, respectively. The result showed that the target-invisible zone made participants perform anticipatory control of visual tracking. In order to identify the brain activities related to visual processing and motion control separately in the visual-motor feedback loops, two reference conditions were designed and compared with the tracking trials. The functional connectivity was defined using phase-locking synchrony, and both static and dynamical features of the network were investigated. For static analysis, the time-averaged graphical properties of functional connectivity were investigated. To investigate dynamical properties, a new dynamical network analysis method was developed based on eigenvector representation of functional connectivity. Both static and dynamic analyses demonstrated significant differences between cortical functional connectivity networks of open and closed visual-motor loop. Additionally, the dynamical network analysis also revealed that the EEG network related to visualmotor coordination undergoes a meta-stable state dynamics in the prime eigenvector space. This method can also potentially be applied to other network system to reveal the meta-stable states structure

Neuronal oscillations: from single-unit activity to emergent dynamics and back

L’objectiu principal d’aquesta tesi és avançar en la comprensió del processament d’informació en xarxes neuronals en presència d’oscil lacions subumbrals. La majoria de neurones propaguen la seva activitat elèctrica a través de sinapsis químiques que són activades, exclusivament, quan el corrent elèctric que les travessa supera un cert llindar. És per aquest motiu que les descàrregues ràpides i intenses produïdes al soma neuronal, els anomenats potencials d’acció, són considerades la unitat bàsica d’informació neuronal, és a dir, el senyal mínim i necessari per a iniciar la comunicació entre dues neurones. El codi neuronal és entès, doncs, com un llenguatge binari que expressa qualsevol missatge (estímul sensorial, memòries, etc.) en un tren de potencials d’acció. Tanmateix, cap funció cognitiva rau en la dinàmica d’una única neurona. Circuits de milers de neurones connectades entre sí donen lloc a determinats ritmes, palesos en registres d’activitat colectiva com els electroencefalogrames (EEG) o els potencials de camp local (LFP). Si els potencials d’acció de cada cèl lula, desencadenats per fluctuacions estocàstiques de les corrents sinàptiques, no assolissin un cert grau de sincronia, no apareixeria aquesta periodicitat a nivell de xarxa. Per tal de poder entendre si aquests ritmes intervenen en el codi neuronal hem estudiat tres situacions. Primer, en el Capítol 2, hem mostrat com una cadena oberta de neurones amb un potencial de membrana intrínsecament oscil latori filtra un senyal periòdic arribant per un dels extrems. La resposta de cada neurona (pulsar o no pulsar) depèn de la seva fase, de forma que cada una d’elles rep un missatge filtrat per la precedent. A més, cada potencial d’acció presinàptic provoca un canvi de fase en la neurona postsinàptica que depèn de la seva posició en l’espai de fases. Els períodes d’entrada capaços de sincronitzar les oscil lacions subumbrals són aquells que mantenen la fase d’arribada dels potencials d’acció fixa al llarg de la cadena. Per tal de què el missatge arribi intacte a la darrera neurona cal, a més a més, que aquesta fase permeti la descàrrega del voltatge transmembrana. En segon cas, hem estudiat una xarxa neuronal amb connexions tant a veïns propers com de llarg abast, on les oscil lacions subumbrals emergeixen de l’activitat col lectiva reflectida en els corrents sinàptics (o equivalentment en el LFP). Les neurones inhibidores aporten un ritme a l’excitabilitat de la xarxa, és a dir, que els episodis en què la inhibició és baixa, la probabilitat d’una descàrrega global de la població neuronal és alta. En el Capítol 3 mostrem com aquest ritme implica l’aparició d’una bretxa en la freqüència de descàrrega de les neurones: o bé polsen espaiadament en el temps o bé en ràfegues d’elevada intensitat. La fase del LFP determina l’estat de la xarxa neuronal codificant l’activitat de la població: els mínims indiquen la descàrrega simultània de moltes neurones que, ocasionalment, han superat el llindar d’excitabilitat degut a un decreixement global de la inhibició, mentre que els màxims indiquen la coexistència de ràfegues en diferents punts de la xarxa degut a decreixements locals de la inhibició en estats globals d’excitació. Aquesta dinàmica és possible gràcies al domini de la inhibició sobre l’excitació. En el Capítol 4 considerem acoblament entre dues xarxes neuronals per tal d’estudiar la interacció entre ritmes diferents. Les oscil lacions indiquen recurrència en la sincronització de l’activitat col lectiva, de manera que durant aquestes finestres temporals una població optimitza el seu impacte en una xarxa diana. Quan el ritme de la població receptora i el de l’emissora difereixen significativament, l’eficiència en la comunicació decreix, ja que les fases de màxima resposta de cada senyal LFP no mantenen una diferència constant entre elles. Finalment, en el Capítol 5 hem estudiat com les oscil lacions col lectives pròpies de l’estat de son donen lloc al fenomen de coherència estocàstica. Per a una intensitat òptima del soroll, modulat per l’excitabilitat de la xarxa, el LFP assoleix una regularitat màxima donant lloc a un període refractari de la població neuronal. En resum, aquesta Tesi mostra escenaris d’interacció entre els potencials d’acció, característics de la dinàmica de neurones individuals, i les oscil lacions subumbrals, fruit de l’acoblament entre les cèl lules i ubiqües en la dinàmica de poblacions neuronals. Els resultats obtinguts aporten funcionalitat a aquests ritmes emergents, agents sincronitzadors i moduladors de les descàrregues neuronals i reguladors de la comunicació entre xarxes neuronals.The main objective of this thesis is to better understand information processing in neuronal networks in the presence of subthreshold oscillations. Most neurons propagate their electrical activity via chemical synapses, which are only activated when the electric current that passes through them surpasses a certain threshold. Therefore, fast and intense discharges produced at the neuronal soma (the action potentials or spikes) are considered the basic unit of neuronal information. The neuronal code is understood, then, as a binary language that expresses any message (sensory stimulus, memories, etc.) in a train of action potentials. Circuits of thousands of interconnected neurons give rise to certain rhythms, revealed in collective activity measures such as electroencephalograms (EEG) and local field potentials (LFP). Synchronization of action potentials of each cell, triggered by stochastic fluctuations of the synaptic currents, cause this periodicity at the network level.To understand whether these rhythms are involved in the neuronal code we studied three situations. First, in Chapter 2, we showed how an open chain of neurons with an intrinsically oscillatory membrane potential filters a periodic signal coming from one of its ends. The response of each neuron (to spike or not) depends on its phase, so that each cell receives a message filtered by the preceding one. Each presynaptic action potential causes a phase change in the postsynaptic neuron, which depends on its position in the phase space. Those incoming periods that are able to synchronize the subthreshold oscillations, keep the phase of arrival of action potentials fixed along the chain. The original message reaches intact the last neuron provided that this phase allows the discharge of the transmembrane voltage.I the second case, we studied a neuronal network with connections to both long range and close neighbors, in which the subthreshold oscillations emerge from the collective activity apparent in the synaptic currents. The inhibitory neurons provide a rhythm to the excitability of the network. When inhibition is low, the likelihood of a global discharge of the neuronal population is high. In Chapter 3 we show how this rhythm causes a gap in the discharge frequency of neurons: either they pulse single spikes or they fire bursts of high intensity. The LFP phase determines the state of the neuronal network, coding the activity of the population: its minima indicate the simultaneous discharge of many neurons, while its maxima indicate the coexistence of bursts due to local decreases of inhibition at global states of excitation. In Chapter 4 we consider coupling between two neural networks in order to study the interaction between different rhythms. The oscillations indicate recurrence in the synchronization of collective activity, so that during these time windows a population optimizes its impact on a target network. When the rhythm of the emitter and receiver population differ significantly, the communication efficiency decreases as the phases of maximum response of each LFP signal do not maintain a constant difference between them.Finally, in Chapter 5 we studied how oscillations typical of the collective sleep state give rise to stochastic coherence. For an optimal noise intensity, modulated by the excitability of the network, the LFP reaches a maximal regularity leading to a refractory period of the neuronal population.In summary, this Thesis shows scenarios of interaction between action potentials, characteristics of the dynamics of individual neurons, and the subthreshold oscillations, outcome of the coupling between the cells and ubiquitous in the dynamics of neuronal populations . The results obtained provide functionality to these emerging rhythms, triggers of synchronization and modulator agents of the neuronal discharges and regulators of the communication between neuronal networks

Anatomical Connectivity Influences both Intra- and Inter-Brain Synchronizations

Recent development in diffusion spectrum brain imaging combined to functional simulation has the potential to further our understanding of how structure and dynamics are intertwined in the human brain. At the intra-individual scale, neurocomputational models have already started to uncover how the human connectome constrains the coordination of brain activity across distributed brain regions. In parallel, at the inter-individual scale, nascent social neuroscience provides a new dynamical vista of the coupling between two embodied cognitive agents. Using EEG hyperscanning to record simultaneously the brain activities of subjects during their ongoing interaction, we have previously demonstrated that behavioral synchrony correlates with the emergence of inter-brain synchronization. However, the functional meaning of such synchronization remains to be specified. Here, we use a biophysical model to quantify to what extent inter-brain synchronizations are related to the anatomical and functional similarity of the two brains in interaction. Pairs of interacting brains were numerically simulated and compared to real data. Results show a potential dynamical property of the human connectome to facilitate inter-individual synchronizations and thus may partly account for our propensity to generate dynamical couplings with others