The time-course of perceptual decision-making: temporal and spatial dynamics of scalp-recorded oscillatory phase and amplitude

Thesis (Ph.D.) - Indiana University, Psychological & Brain Sciences, 2014In natural conditions the brain has to actively integrate information about the current percept with information about past/present behavioral demands and cognitive states of the observer along with future outcomes related to a decision. Despite of somewhat extensive research, we still know little about the neuro-cognitive mechanisms and temporal dynamics allowing an observer to perceive an object and rapidly make a decision about it. This dissertation is based on previous research suggesting that there must be at least two cognitive processes underlying a task such as perceptual decision-making. An early mechanism related to the perception of information and a later one related to the subsequent decision-making process. Evidence has led to the proposal of the match-and-utilization model, stating that early synchronization in the gamma band is the result of a match between the current percept and memory/attentional processes. In contrast, later synchronization would reflect the utilization/readout of the early matching process; updating or influencing future processes. Evidence for this two-stage process, comes mainly from the classic event-related potential literature and, in lesser degree, from newer measures such as oscillatory amplitude. Moreover, the exploration of multivariate nonlinear techniques derived from the study of synchronization between and within neural systems, has been largely neglected in the literature. Thus, explorations of a more complete electrophysiological picture than the one provided by ERP or ERSP analyses alone, can provide us more information about the relation between neural oscillations and ERP components as electrophysiological markers of cognitive events. This is important because differential roles for frequency, phase, and amplitude as different information coding strategies in neural systems have been theoretically suggested and empirically shown. The present work presents for the first time, concomitant analyses of phase and amplitude dynamics in the context of perceptual decision-making. In this dissertation I present a parametrical task that can effectively separate the visual properties of the stimuli from the decision regarding the task at hand. Results indicate that the experimental design effectively separated stimulus properties from task demands. Additionally, I suggest distinct roles for the temporal dynamics of gamma-band oscillations. Finally, a central role for alpha oscillations is suggested

Complex network modelling of EEG band coupling in dyslexia: An exploratory analysis of auditory processing and diagnosis

Complex network analysis has an increasing relevance in the study of neurological disorders, enhancing the knowledge of brain’s structural and functional organization. Network structure and efficiency reveal different brain states along with different ways of processing the informa- tion. This work is structured around the exploratory analysis of the brain processes involved in low-level auditory processing. A complex network analysis was performed on the basis of brain coupling obtained from electroencephalography (EEG) data, while different auditory stim- uli were presented to the subjects. This coupling is inferred from the Phase-Amplitude coupling (PAC) from different EEG electrodes to explore differences between control and dyslexic sub- jects. Coupling data allows the construction of a graph, and then, graph theory is used to study the characteristics of the complex networks throughout time for control and dyslexic subjects. This results in a set of metrics including clustering coefficient, path length and small-worldness. From this, different characteristics linked to the temporal evolution of networks and coupling are pointed out for dyslexics. Our study revealed patterns related to Dyslexia as losing the small- world topology. Finally, these graph-based features are used to classify between control and dyslexic subjects by means of a Support Vector Machine (SVM).This work was supported by projects PGC2018-098813-B-C32 (Spanish “Ministerio de Cien- cia, Innovación y Universidades”), UMA20-FEDERJA-086 (Consejería de econnomía y conocimiento, Junta de Andalucía) and by European Regional Development Funds (ERDF). We gratefully ac- knowledge the support of NVIDIA Corporation with the donation of one of the GPUs used for this research. Work by F.J.M.M. was supported by the MICINN “Juan de la Cierva - Incorpo- ración” Fellowship. We also thank the Leeduca research group and Junta de Andalucía for the data supplied and the support. Funding for open access charge: Universidad de Málaga / CBU

Individual differences in LPP amplitude and theta power predict cue-induced eating during a cued food delivery task

Due to individual differences in the brain’s reward system, some individuals are more vulnerable than others to maladaptive, reward-seeking behaviors, such as substance use or compulsive eating. A body of research has demonstrated that individuals who attribute higher levels of incentive salience to reward-associated cues than to pleasant images (termed “C\u3eP group” throughout) are more vulnerable to compulsive eating than those who attribute higher incentive salience to pleasant images than reward- associated cues (P\u3eC group). Meanwhile, a separate body of research has demonstrated that cognitive control also regulates eating by enabling top-down attentional control. This dissertation aims to identify how both cognitive control and incentive salience act in tandem to regulate cue-induced eating. A central question of this research is: do individuals in the C\u3eP group also show attenuated cognitive control? Because the animal literature indicates that individuals who attribute high incentive salience to reward-associated cues also show attenuated top-down attentional control, I hypothesized that C\u3eP individuals would also show attenuated cognitive control relative to P\u3eC individuals. To test this hypothesis, I analyzed electroencephalogram (EEG) data collected during a controlled cued food delivery task, in which participants viewed images and were dispensed food rewards (candy) that they could choose to eat or discard, and non-food objects (beads, control condition). From the EEG recordings, I calculated the amplitude of the late positive potential (LPP) and power (µV2) in the theta (θ, 4-8 Hz) frequency band as metrics of affective and cognitive processing, respectively. To identify individual differences in both affective and cognitive processing, I then conducted two separate K-means (k = 2) cluster analyses using LPP and theta power data. The LPP-based cluster analysis replicated previous findings: C\u3eP individuals ate significantly more candies during the experiment than P\u3eC individuals. However, I found no significant differences in theta power between the P\u3eC and C\u3eP groups. Meanwhile, the theta-based cluster analysis found that some individuals show higher theta during the candy condition than the bead condition (θCA\u3eθBE), while others show higher theta power during the bead condition than the candy condition (θBE\u3eθCA). Furthermore, the θCA\u3eθBE group ate significantly more during the experiment than the θBE\u3eθCA group. Finally, I crossed group assignments from both the LPP- and theta-based cluster analyses to create four groups based on LPP- and theta-based risk factors: those with no risk factors (P\u3eC & θBE\u3eθCA group), those with only an LPP risk factor (C\u3eP & θCA\u3eθBE), those with only a theta risk factor (P\u3eC & θCA\u3eθBE), and finally those with both risk factors (C\u3eP & θCA\u3eθBE). I found that individuals with no risk factors ate the least of all four groups, and the other three groups showed significantly higher levels of eating behavior on average. From these results, I can conclude that both cognitive and affective brain systems are involved in regulating cue-induced eating. However, the finding that P\u3eC and C\u3eP individuals do not show significant differences in theta power suggests that cognitive and affective mechanisms may act independently in humans. Because an individual with an affective vulnerability to cue-induced eating may not also have a cognitive vulnerability, this underscores the need for targeted, individualized treatments for maladaptive behaviors. For example, these research findings could be applied to the use of transcranial magnetic stimulation (TMS) to ameliorate addictive disorders: individuals with higher theta power during food-related decision-making may be selected for excitatory stimulation of brain regions associated with cognitive control, such as dorsolateral prefrontal cortex (dlPFC), whereas individuals who attribute high incentive salience to reward-related cues may benefit from inhibitory stimulation of reward-associated areas, such as medial prefrontal cortex (mPFC)

Transient Global Amnesia Deteriorates the Network Efficiency of the Theta Band

Acute perturbation of the hippocampus, one of the connector hubs in the brain, is a key step in the pathophysiological cascade of transient global amnesia (TGA). We tested the hypothesis that network efficiency, meaning the efficiency of information exchange over a network, is impaired during the acute stage of TGA. Graph theoretical analysis was applied to resting-state EEG data collected from 21 patients with TGA. The EEG data were obtained twice, once during the acute stage (�� 24 hours after symptom onset) and once during the resolved stage (�� 2 months after symptom onset) of TGA. Characteristic path lengths and clustering coefficients of functional networks constructed using phase-locking values were computed and normalized as a function of the degree in the delta, theta, alpha, beta 1, beta 2 and gamma frequency bands of the EEG. We investigated whether the normalized characteristic path length (nCPL) and normalized clustering coefficients (nCC) differed significantly between the acute and resolved stages of TGA at each frequency band using the Wilcoxon signed-rank test. For networks where the nCPL or nCC differed significantly between the two stages, we also evaluated changes in the connections of the brain networks. During the acute stage of TGA, the nCPL of the theta band networks with mean degrees of 8, 8.5, 9 and 9.5 significantly increased (P �� 0.05). During the acute stage, the lost edges for these networks were mostly found between the anterior (frontal and anterior temporal) and posterior (parieto-occipital and posterior temporal) brain regions, whereas newly developed edges were primarily found between the left and right frontotemporal regions. The nCC of the theta band with a mean degree of 5.5 significantly decreased during the acute stage (P �� 0.05). Our results indicate that TGA deteriorates the network efficiency of the theta frequency band. This effect might be related to the desynchronization between the anterior and posterior brain areas

Hyperedge bundling : A practical solution to spurious interactions in MEG/EEG source connectivity analyses

Inter-areal functional connectivity (FC), neuronal synchronization in particular, is thought to constitute a key systems-level mechanism for coordination of neuronal processing and communication between brain regions. Evidence to support this hypothesis has been gained largely using invasive electrophysiological approaches. In humans, neuronal activity can be non-invasively recorded only with magneto-and electroencephalography (MEG/EEG), which have been used to assess FC networks with high temporal resolution and whole-scalp coverage. However, even in source-reconstructed MEG/EEG data, signal mixing, or "source leakage", is a significant confounder for FC analyses and network localization. Signal mixing leads to two distinct kinds of false-positive observations: artificial interactions (AI) caused directly by mixing and spurious interactions (SI) arising indirectly from the spread of signals from true interacting sources to nearby false loci. To date, several interaction metrics have been developed to solve the AI problem, but the SI problem has remained largely intractable in MEG/EEG all-to-all source connectivity studies. Here, we advance a novel approach for correcting SIs in FC analyses using source-reconstructed MEG/EEG data. Our approach is to bundle observed FC connections into hyperedges by their adjacency in signal mixing. Using realistic simulations, we show here that bundling yields hyperedges with good separability of true positives and little loss in the true positive rate. Hyperedge bundling thus significantly decreases graph noise by minimizing the false-positive to true-positive ratio. Finally, we demonstrate the advantage of edge bundling in the visualization of large-scale cortical networks with real MEG data. We propose that hypergraphs yielded by bundling represent well the set of true cortical interactions that are detectable and dissociable in MEG/EEG connectivity analysis.Peer reviewe

The Aha! Experience of Spatial Reorientation

The experience of spatial re-orientation is investigated as an instance of the wellknown phenomenon of the Aha! moment. The research question is: What are the visuospatial conditions that are most likely to trigger the spatial Aha! experience? The literature suggests that spatial re-orientation relies mainly on the geometry of the environment and a visibility graph analysis is used to quantify the visuospatial information. Theories from environmental psychology point towards two hypotheses. The Aha! experience may be triggered by a change in the amount of visual information, described by the isovist properties of area and revelation, or by a change in the complexity of the visual information associated with the isovist properties of clustering coefficient and visual control. Data from participants’ exploratory behaviour and EEG recordings are collected during wayfinding in virtual reality urban environments. Two types of events are of interest here: (a) sudden changes of the visuospatial information preceding subjects' response to investigate changes in EEG power; and (b) participants brain dynamics (Aha! effect) just before the response to examine differences in isovist values at this location. Research on insights, time-frequency analysis of the P3 component and findings from navigation and orientation studies suggest that the spatial Aha! experience may be reflected by: a parietal alpha power decrease associated with the switch of the representation and a frontocentral theta increase indexing spatial processing during decision-making. Single-trial time-frequency analysis is used to classify trials into two conditions based on the alpha/theta power differences between a 3s time-period before participants’ response and a time-period of equal duration before that. Behavioural results show that participants are more likely to respond at locations with low values of clustering coefficient and high values of visual control. The EEG analysis suggests that the alpha decrease/theta increase condition occurs at locations with significantly lower values of clustering coefficient and higher values of visual control. Small and large decreases in clustering coefficient, just before the response, are associated with significant differences in delta/theta power. The values of area and revelation do not show significant differences. Both behavioural and EEG results suggest that the Aha! experience of re-orientation is more likely to be triggered by a change in the complexity of the visual-spatial environment rather than a change in the amount, as measured by the relevant isovist properties

Spatial encoding in primate hippocampus during free navigation.

The hippocampus comprises two neural signals-place cells and θ oscillations-that contribute to facets of spatial navigation. Although their complementary relationship has been well established in rodents, their respective contributions in the primate brain during free navigation remains unclear. Here, we recorded neural activity in the hippocampus of freely moving marmosets as they naturally explored a spatial environment to more explicitly investigate this issue. We report place cells in marmoset hippocampus during free navigation that exhibit remarkable parallels to analogous neurons in other mammalian species. Although θ oscillations were prevalent in the marmoset hippocampus, the patterns of activity were notably different than in other taxa. This local field potential oscillation occurred in short bouts (approximately .4 s)-rather than continuously-and was neither significantly modulated by locomotion nor consistently coupled to place-cell activity. These findings suggest that the relationship between place-cell activity and θ oscillations in primate hippocampus during free navigation differs substantially from rodents and paint an intriguing comparative picture regarding the neural basis of spatial navigation across mammals

Evaluation and implementation of functional cerebral biomarkers in Alzheimer’s disease

The aim of this thesis was to evaluate and implement functional cerebral biomarkers in Alzheimer’s disease (AD) with respect to pathophysiology, disease severity, prognosis and treatment effect in medical trials. We focused on functional cerebral biomarkers that assess synaptic activity and functional connectivity using electroencephalography (EEG), magnetoencephalography (MEG) and 18 F-fluorodeoxyglucose (FDG) positron emission tomography (PET). In the different chapters a broad range of challenges associated with this topic was covered. We started by using FDG- PET to observe the effects of the experimental treatment of AD patients with the medical food Souvenaid, followed by EEG as treatment outcome measure in a trial with the drug PQ912. Next to the primary outcomes, the results of these studies revealed that more research was needed to observe which markers could observe reliable, reproducible and valid results and what the factors were that could influence their ability to do this. The EEG markers, rather than the FDG- PET markers, showed promising results. Therefore, we aimed to investigate the effects of sensitivity, reproducibility, heterogeneity of the population and treatment efficacy, while maintaining a well-defined study population and study design, on EEG biomarkers. We first investigated the reproducibility of AD related changes in functional connectivity captured by different measures in electroencephalography (EEG) and magnetoencephalography (MEG). Second, we evaluated the influence of subtypes of AD on various EEG measures and, on the other hand, we used EEG to find heterogeneity and to predict clinical progression

An investigation into the mechanisms of inter-brain synchrony during early social interactions

Over the last 20 years there has been a growing increase in the amount of research investigating how and why two or more individual’s brain activity can synchronise during social interaction. What we know so far from this research is that inter-brain synchrony (defined through temporally coordinated patterns of brain activity between two interacting individuals, Holroyd 2022) tends to associate with moments of behavioural coordination (i.e., when two individuals are doing or attending to the same thing at the same time) and task cooperation (i.e., the action or process of two individuals working together to the same end). These observations have led many researchers to theorise over whether and how behavioural coordination mechanistically drives inter-brain synchrony (Wass et al., 2020; Hamilton, 2021). There is also some very recent evidence to suggest that increased inter-brain synchrony actually facilitates/ supports aspects of social interaction. For example, inter-brain synchrony has been shown to predict team performance (Reinero et al., 2021), although this research is primarily based on correlational study designs. Taken together however the field of inter-brain synchrony shares one fundamental limitation; that is that it does not account (although see recent animal research e.g., Kingsbury et al., 2019; Zhang et al., 2019), empirically for the mechanisms that give rise to inter-brain synchrony, which would help to falsify claims that inter-brain synchrony is a core mechanism facilitating social interaction. This is because of two main reasons; Firstly, the study of inter-brain synchrony has primarily been investigated as a time-invariant property, almost no studies have explored how inter-brain synchrony varies over time relative to individual moments of behavioural coordination. Secondly, little attention has been paid to the changes in the underlying signal properties (i.e., increases in power, changes in frequency) that must take place for two unsynchronised signals to become synchronised (e.g., Haresign et al., 2022). Using two-person naturalistic biobehavioural recording techniques, coupled with state of the art, EEG pre-processing and analyses procedures (see chapters 5 and 6), the present thesis examines the mechanisms that give rise to inter-brain synchrony during parent-infant social interactions. Evidence is presented showing how inter-brain synchrony does not arise around individual moments of gaze coordination. This is despite previous investigations suggesting that increased inter-brain synchrony (averaged over all moments of eye contact) associates with gaze synchrony. Evidence also shows the contribution of behavioural coordination across multiple modalities to inter-brain synchrony during parent-infant social interaction. Discussion is focused on the contribution of these findings to our understanding of the mechanisms that give rise to inter-brain synchrony

Analysis of infant cortical synchrony is constrained by the number of recording electrodes and the recording montage

Objective: To assess how the recording montage in the neonatal EEG influences the detection of cortical source signals and their phase interactions. Methods: Scalp EEG was simulated by forward modeling 20-200 simultaneously active sources covering the cortical surface of a realistic neonatal head model. We assessed systematically how the number of scalp electrodes (11-85), analysis montage, or the size of cortical sources affect the detection of cortical phase synchrony. Statistical metrics were developed for quantifying the resolution and reliability of the montages. Results: The findings converge to show that an increase in the number of recording electrodes leads to a systematic improvement in the detection of true cortical phase synchrony. While there is always a ceiling effect with respect to discernible cortical details, we show that the average and Laplacian montages exhibit superior specificity and sensitivity as compared to other conventional montages. Conclusions: Reliability in assessing true neonatal cortical synchrony is directly related to the choice of EEG recording and analysis configurations. Because of the high conductivity of the neonatal skull, the conventional neonatal EEG recordings are spatially far too sparse for pertinent studies, and this loss of information cannot be recovered by re-montaging during analysis. Significance: Future neonatal EEG studies will need prospective planning of recording configuration to allow analysis of spatial details required by each study question. Our findings also advice about the level of details in brain synchrony that can be studied with existing datasets or by using conventional EEG recordings. (C) 2015 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.Peer reviewe