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The analysis of EEG microstates for investigating rapid whole-brain network dynamics during rest and tasks has become a standard practice in the EEG research community, leading to a substantial increase in publications across various affective, cognitive, social and clinical neuroscience domains. Recognizing the growing significance of this analytical method, the authors aim to provide the microstate research community with a comprehensive discussion on methodological standards, unresolved questions, and the functional relevance of EEG microstates. In August 2022, a conference was hosted in Bern, Switzerland, which brought together many researchers from 19 countries. During the conference, researchers gave scientific presentations and engaged in roundtable discussions aiming at establishing steps toward standardizing EEG microstate analysis methods. Encouraged by the conference's success, a special issue was launched in Brain Topography to compile the current state-of-the-art in EEG microstate research, encompassing methodological advancements, experimental findings, and clinical applications. The call for submissions for the special issue garnered 48 contributions from researchers worldwide, spanning reviews, meta-analyses, tutorials, and experimental studies. Following a rigorous peer-review process, 33 papers were accepted whose findings we will comprehensively discuss in this Editorial.
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Mapeo Encefálico , Encéfalo , Humanos , Mapeo Encefálico/métodos , Electroencefalografía/métodos , DescansoRESUMEN
Over the last decade, EEG resting-state microstate analysis has evolved from a niche existence to a widely used and well-accepted methodology. The rapidly increasing body of empirical findings started to yield overarching patterns of associations of biological and psychological states and traits with specific microstate classes. However, currently, this cross-referencing among apparently similar microstate classes of different studies is typically done by "eyeballing" of printed template maps by the individual authors, lacking a systematic procedure. To improve the reliability and validity of future findings, we present a tool to systematically collect the actual data of template maps from as many published studies as possible and present them in their entirety as a matrix of spatial similarity. The tool also allows importing novel template maps and systematically extracting the findings associated with specific microstate maps from ongoing or published studies. The tool also allows importing novel template maps and systematically extracting the findings associated with specific microstate maps in the literature. The analysis of 40 included sets of template maps indicated that: (i) there is a high degree of similarity of template maps across studies, (ii) similar template maps were associated with converging empirical findings, and (iii) representative meta-microstates can be extracted from the individual studies. We hope that this tool will be useful in coming to a more comprehensive, objective, and overarching representation of microstate findings.
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Encéfalo , Electroencefalografía , Humanos , Reproducibilidad de los Resultados , OjoRESUMEN
OBJECTIVE: This study aimed to assess whether non-invasive brain stimulation with transcranial alternating current stimulation at gamma-frequency (γ-tACS) applied over the precuneus can improve episodic memory and modulate cholinergic transmission by modulating cerebral rhythms in early Alzheimer's disease (AD). METHODS: In this randomized, double-blind, sham controlled, crossover study, 60 AD patients underwent a clinical and neurophysiological evaluation including assessment of episodic memory and cholinergic transmission pre and post 60 minutes treatment with γ-tACS targeting the precuneus or sham tACS. In a subset of 10 patients, EEG analysis and individualized modelling of electric field distribution were carried out. Predictors to γ-tACS efficacy were evaluated. RESULTS: We observed a significant improvement in the Rey Auditory Verbal Learning (RAVL) test immediate recall (p < 0.001) and delayed recall scores (p < 0.001) after γ-tACS but not after sham tACS. Face-name associations scores improved with γ-tACS (p < 0.001) but not after sham tACS. Short latency afferent inhibition, an indirect measure of cholinergic transmission, increased only after γ-tACS (p < 0.001). ApoE genotype and baseline cognitive impairment were the best predictors of response to γ-tACS. Clinical improvement correlated with the increase in gamma frequencies in posterior regions and with the amount of predicted electric field distribution in the precuneus. INTERPRETATION: Precuneus γ-tACS, able to increase γ-power activity on the posterior brain regions, showed a significant improvement of episodic memory performances, along with restoration of intracortical excitability measures of cholinergic transmission. Response to γ-tACS was dependent on genetic factors and disease stage. ANN NEUROL 2022;92:322-334.
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Enfermedad de Alzheimer , Memoria Episódica , Estimulación Transcraneal de Corriente Directa , Enfermedad de Alzheimer/terapia , Encéfalo , Colinérgicos , Estudios Cruzados , HumanosRESUMEN
Evidence suggests that the stream of consciousness is parsed into transient brain states manifesting themselves as discrete spatiotemporal patterns of global neuronal activity. Electroencephalographical (EEG) microstates are proposed as the neurophysiological correlates of these transiently stable brain states that last for fractions of seconds. To further understand the link between EEG microstate dynamics and consciousness, we continuously recorded high-density EEG in 23 surgical patients from their awake state to unconsciousness, induced by step-wise increasing concentrations of the intravenous anesthetic propofol. Besides the conventional parameters of microstate dynamics, we introduce a new implementation of a method to estimate the complexity of microstate sequences. The brain activity under the surgical anesthesia showed a decreased sequence complexity of the stereotypical microstates, which became sparser and longer-lasting. However, we observed an initial increase in microstates' temporal dynamics and complexity with increasing depth of sedation leading to a distinctive "U-shape" that may be linked to the paradoxical excitation induced by moderate levels of propofol. Our results support the idea that the brain is in a metastable state under normal conditions, balancing between order and chaos in order to flexibly switch from one state to another. The temporal dynamics of EEG microstates indicate changes of this critical balance between stability and transition that lead to altered states of consciousness.
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Estado de Conciencia , Propofol , Encéfalo/fisiología , Estado de Conciencia/fisiología , Electroencefalografía/métodos , Humanos , Propofol/farmacología , Inconsciencia/inducido químicamenteRESUMEN
Episodic autobiographical memory (EAM) is a complex cognitive function that emerges from the coordination of specific and distant brain regions. Specific brain rhythms, namely theta and gamma oscillations and their synchronization, are thought of as putative mechanisms enabling EAM. Yet, the mechanisms of inter-regional interaction in the EAM network remain unclear in humans at the whole brain level. To investigate this, we analyzed EEG recordings of participants instructed to retrieve autobiographical episodes. EEG recordings were projected in the source space, and time-courses of atlas-based brain regions-of-interest (ROIs) were derived. Directed phase synchrony in high theta (7-10 Hz) and gamma (30-80 Hz) bands and high theta-gamma phase-amplitude coupling were computed between each pair of ROIs. Using network-based statistics, a graph-theory method, we found statistically significant networks for each investigated mechanism. In the gamma band, two sub-networks were found, one between the posterior cingulate cortex (PCC) and the medial temporal lobe (MTL) and another within the medial frontal areas. In the high theta band, we found a PCC to ventromedial prefrontal cortex (vmPFC) network. In phase-amplitude coupling, we found the high theta phase of the left MTL biasing the gamma amplitude of posterior regions and the vmPFC. Other regions of the temporal lobe and the insula were also phase biasing the vmPFC. These findings suggest that EAM, rather than emerging from a single mechanism at a single frequency, involves precise spatio-temporal signatures mapping on distinct memory processes. We propose that the MTL orchestrates activity in vmPFC and PCC via precise phase-amplitude coupling, with vmPFC and PCC interaction via high theta phase synchrony and gamma synchronization contributing to bind information within the PCC-MTL sub-network or valuate the candidate memory within the medial frontal sub-network.
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Memoria Episódica , Encéfalo , Mapeo Encefálico , Humanos , Recuerdo Mental , Corteza Prefrontal , Lóbulo Temporal , Ritmo TetaRESUMEN
Re-activations of task-dependent patterns of neural activity take place during post-encoding periods of wakeful rest and sleep. However, it is still unclear how the temporal dynamics of brain states change during these periods, which are shaped by prior conscious experiences. Here, we examined the very brief periods of wakeful rest immediately after encoding and recognition of auditory and visual stimuli, by applying the EEG microstate analysis, in which the global variance of the EEG is explained by only a few prototypical topographies. We identified the dominant brain states of sub-second duration during the tasks-dependent periods of rest, finding that the temporal dynamics-represented here by two temporal parameters: the frequency of occurrence and the fraction of time coverage-of three task-related microstate classes changed compared to wakeful rest. This study provides evidence of experience-dependent temporal changes in post-encoding periods of resting brain activity, which can be captured using the EEG microstates approach.
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Mapeo Encefálico , Electroencefalografía , Encéfalo , Humanos , Descanso , VigiliaRESUMEN
Episodic memory (EM) is classically conceived as a memory for events, localized in space and time, and characterized by autonoetic consciousness (ANC) allowing to mentally travel back in time and subjectively relive an event. Building on recent evidence that the first-person visual co-perception of one's own body during encoding impacts EM, we used a scene recognition task in immersive virtual reality (VR) and measured how first-person body view would modulate peri-encoding resting-state fMRI, EM performance, and ANC. Specifically, we investigated the impact of body view on post-encoding functional connectivity in an a priori network of regions related either to EM or multisensory bodily processing and used these regions in a seed-to-whole brain analysis. Post-encoding connectivity between right hippocampus (rHC) and right parahippocampus (rPHC) was enhanced when participants encoded scenes while seeing their body. Moreover, the strength of connectivity between the rHC, rPHC and the neocortex displayed two main patterns with respect to body view. The connectivity with a sensorimotor fronto-parietal network, comprising primary somatosensory and primary motor cortices, correlated with ANC after - but not before - encoding, depending on body view. The opposite change of connectivity was found between rHC, rPHC and the medial parietal cortex (from being correlated with ANC before encoding to an absence of correlation after encoding), but irrespective of body view. Linking immersive VR and fMRI for the study of EM and ANC, these findings suggest that seeing one's own body during encoding impacts the brain activity related to EM formation by modulating the connectivity between the right hippocampal formation and the neocortical regions involved in the processing of multisensory bodily signals and self-consciousness.
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Imagen Corporal , Encéfalo/fisiología , Memoria Episódica , Adulto , Mapeo Encefálico , Femenino , Hipocampo/fisiología , Humanos , Imagen por Resonancia Magnética , Masculino , Vías Nerviosas/fisiología , Realidad Virtual , Adulto JovenRESUMEN
Electroencephalography (EEG) recordings performed in magnetic resonance imaging (MRI) scanners are affected by complex artifacts caused by heart function, often termed pulse artifacts (PAs). PAs can strongly compromise EEG data quality, and remain an open problem for EEG-fMRI. This study investigated the properties and mechanisms of PA variability across heartbeats, which has remained largely unaddressed to date, and evaluated its impact on PA correction approaches. Simultaneous EEG-fMRI was performed at 7T on healthy participants at rest or under visual stimulation, with concurrent recordings of breathing and cardiac activity. PA variability was found to contribute to EEG variance with more than 500 µV2 at 7T, which extrapolates to 92 µV2 at 3T. Clustering analyses revealed that PA variability not only is linked to variations in head position/orientation, as previously hypothesized, but also, and more importantly, to the respiratory cycle and to heart rate fluctuations. The latter mechanisms are associated to short-timescale variability (even across consecutive heartbeats), and their importance varied across EEG channels. In light of this PA variability, three PA correction techniques were compared: average artifact subtraction (AAS), optimal basis sets (OBS), and an approach based on K-means clustering. All methods allowed the recovery of visual evoked potentials from the EEG data; nonetheless, OBS and K-means tended to outperform AAS, likely due to the inability of the latter in modeling short-timescale variability. Altogether, these results offer novel insights into the dynamics and underlying mechanisms of the pulse artifact, with important consequences for its correction, relevant to most EEG-fMRI applications.
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Artefactos , Electroencefalografía , Procesamiento de Imagen Asistido por Computador/métodos , Imagen por Resonancia Magnética , Pulso Arterial , Adulto , Femenino , Humanos , Masculino , Adulto JovenRESUMEN
The temporal structure of self-generated cognition is a key attribute to the formation of a meaningful stream of consciousness. When at rest, our mind wanders from thought to thought in distinct mental states. Despite the marked importance of ongoing mental processes, it is challenging to capture and relate these states to specific cognitive contents. In this work, we employed ultra-high field functional magnetic resonance imaging (fMRI) and high-density electroencephalography (EEG) to study the ongoing thoughts of participants instructed to retrieve self-relevant past episodes for periods of 22sec. These task-initiated, participant-driven activity patterns were compared to a distinct condition where participants performed serial mental arithmetic operations, thereby shifting from self-related to self-unrelated thoughts. BOLD activity mapping revealed selective enhanced activity in temporal, parietal and occipital areas during the memory compared to the mental arithmetic condition, evincing their role in integrating the re-experienced past events into conscious representations during memory retrieval. Functional connectivity analysis showed that these regions were organized in two major subparts, previously associated to "scene-reconstruction" and "self-experience" subsystems. EEG microstate analysis allowed studying these participant-driven thoughts in the millisecond range by determining the temporal dynamics of brief periods of stable scalp potential fields. This analysis revealed selective modulation of occurrence and duration of specific microstates in the memory and in the mental arithmetic condition, respectively. EEG source analysis revealed similar spatial distributions of the sources of these microstates and the regions identified with fMRI. These findings imply a functional link between BOLD activity changes in regions related to a certain mental activity and the temporal dynamics of mentation, and support growing evidence that specific fMRI networks can be captured with EEG as repeatedly occurring brief periods of integrated coherent neuronal activity, lasting only fractions of seconds.
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Mapeo Encefálico/métodos , Encéfalo/fisiología , Pensamiento/fisiología , Adulto , Electroencefalografía/métodos , Femenino , Humanos , Imagen por Resonancia Magnética/métodos , MasculinoRESUMEN
How do our bodies influence who we are? Recent research in cognitive neuroscience has examined consciousness associated with the self and related multisensory processing of bodily signals, the so-called bodily self-consciousness. A parallel line of research has highlighted the concept of the autobiographical self and the associated autonoetic consciousness, which enables us to mentally travel in time. The subjective re-experiencing of past episodes is described as re-living them from within or outside one's body. In this brief perspective, I aim to explore the underlying characteristics of self-consciousness and its relation to bodily signals and episodic memory. I will outline some recent behavioral and neuroimaging evidence indicating that bodily cues play a fundamental role in autobiographical memory. Finally, I will discuss these emerging concepts regarding the current understanding of bodily-self, autobiographical-self, their links to self-consciousness, and suggest directions for future research.
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Conscious experiences unify distinct phenomenological experiences that seem to be continuously evolving. Yet, empirical evidence shows that conscious mental activity is discontinuous and can be parsed into a series of states of thoughts that manifest as discrete spatiotemporal patterns of global neuronal activity lasting for fractions of seconds. EEG measures the brain's electrical activity with high temporal resolution on the scale of milliseconds and, therefore, might be used to investigate the fast spatiotemporal structure of conscious mental states. Such analyses revealed that the global scalp electric fields during spontaneous mental activity are parceled into blocks of stable topographies that last around 60-120 ms, the so-called EEG microstates. These brain states may be representing the basic building blocks of consciousness, the "atoms of thought." Altered states of consciousness, such as sleep, anesthesia, meditation, or psychiatric diseases, influence the spatiotemporal dynamics of microstates. In this brief perspective, we suggest that it is possible to examine the underlying characteristics of self-consciousness using this EEG microstates approach. Specifically, we will summarize recent results on EEG microstate alterations in mind-wandering, meditation, sleep and anesthesia, and discuss the functional significance of microstates in altered states of consciousness.
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The ultrafast spatiotemporal dynamics of large-scale neural networks can be examined using resting-state electroencephalography (EEG) microstates, representing transient periods of synchronized neural activity that evolve dynamically over time. In adults, four canonical microstates have been shown to explain most topographic variance in resting-state EEG. Their temporal structures are age-, sex- and state-dependent, and are susceptible to pathological brain states. However, no studies have assessed the spatial and temporal properties of EEG microstates exclusively during early childhood, a critical period of rapid brain development. Here we sought to investigate EEG microstates recorded with high-density EEG in a large sample of 103, 4-8-year-old children. Using data-driven k-means cluster analysis, we show that the four canonical microstates reported in adult populations already exist in early childhood. Using multiple linear regressions, we demonstrate that the temporal dynamics of two microstates are associated with age and sex. Source localization suggests that attention- and cognitive control-related networks govern the topographies of the age- and sex-dependent microstates. These novel findings provide unique insights into functional brain development in children captured with EEG microstates.
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We review the latest evidence from animal models, studies in humans using electrophysiology, experimental memory paradigms, and non-invasive brain stimulation (NIBS), in the form of transcranial alternating current stimulation (tACS), suggesting that the altered activity in networks that contribute to the autobiographical memory (ABM) deficits may be modifiable. ABM involves a specific brain network of interacting regions that store and retrieve life experiences. Deficits in ABM are early symptoms in patients with Alzheimer's disease (AD), and serve as relevant predictors of disease progression. The possibility to modify the neural substrates of ABM opens exciting avenues for the development of therapeutic approaches. Beyond a summary of the causal role of brain oscillations in ABM, we propose a new approach of modulating brain oscillations using personalized tACS with the possibility of reducing ABM deficits. We suggest that human experimental studies using cognitive tasks, EEG, and tACS can have future translational clinical implications.
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Sustained attention and working memory were improved in young adults after they engaged in a recently developed, closed-loop, digital meditation practice. Whether this type of meditation also has a sustained effect on dominant resting-state networks is currently unknown. In this study, we examined the resting brain states before and after a period of breath-focused, digital meditation training versus placebo using an electroencephalography (EEG) microstate approach. We found topographical changes in postmeditation rest, compared with baseline rest, selectively for participants who were actively involved in the meditation training and not in participants who engaged with an active, expectancy-match, placebo control paradigm. Our results suggest a reorganization of brain network connectivity after 6 weeks of intensive meditation training in brain areas, mainly including the right insula, the superior temporal gyrus, the superior parietal lobule, and the superior frontal gyrus bilaterally. These findings provide an opening for the development of a novel noninvasive treatment of neuropathological states by low-cost, breath-focused, digital meditation practice, which can be monitored by the EEG microstate approach.
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Meditación , Encéfalo , Mapeo Encefálico , Electroencefalografía , Humanos , Imagen por Resonancia Magnética , Descanso , Adulto JovenRESUMEN
Alzheimer's disease (AD) is an irreversible, progressive brain disorder that can cause dementia (Alzheimer's disease-related dementia, ADRD) with growing cognitive disability and vast physical, emotional, and financial pressures not only on the patients but also on caregivers and families. Loss of memory is an early and very debilitating symptom in AD patients and a relevant predictor of disease progression. Data from rodents, as well as human studies, suggest that dysregulation of specific brain oscillations, particularly in the hippocampus, is linked to memory deficits. Animal and human studies demonstrate that non-invasive brain stimulation (NIBS) in the form of transcranial alternating current stimulation (tACS) allows to reliably and safely interact with ongoing oscillatory patterns in the brain in specific frequencies. We developed a protocol for patient-tailored home-based tACS with an instruction program to train a caregiver to deliver daily sessions of tACS that can be remotely monitored by the study team. We provide a discussion of the neurobiological rationale to modulate oscillations and a description of the study protocol. Data of two patients with ADRD who have completed this protocol illustrate the feasibility of the approach and provide pilot evidence on the safety of the remotely-monitored, caregiver-administered, home-based tACS intervention. These findings encourage the pursuit of a large, adequately powered, randomized controlled trial of home-based tACS for memory dysfunction in ADRD.
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Why do people sometimes report that they remember dreams, while at other times they recall no experience? Despite the interest in dreams that may happen during the night, it has remained unclear which brain states determine whether these conscious experiences will occur and what prevents us from waking up during these episodes. Here we address this issue by comparing the EEG activity preceding awakenings with recalled vs. no recall of dreams using the EEG microstate approach. This approach characterizes transiently stable brain states of sub-second duration that involve neural networks with nearly synchronous dynamics. We found that two microstates (3 and 4) dominated during NREM sleep compared to resting wake. Further, within NREM sleep, microstate 3 was more expressed during periods followed by dream recall, whereas microstate 4 was less expressed. Source localization showed that microstate 3 encompassed the medial frontal lobe, whereas microstate 4 involved the occipital cortex, as well as thalamic and brainstem structures. Since NREM sleep is characterized by low-frequency synchronization, indicative of neuronal bistability, we interpret the increased presence of the "frontal" microstate 3 as a sign of deeper local deactivation, and the reduced presence of the "occipital" microstate 4 as a sign of local activation. The latter may account for the occurrence of dreaming with rich perceptual content, while the former may account for why the dreaming brain may undergo executive disconnection and remain asleep. This study demonstrates that NREM sleep consists of alternating brain states whose temporal dynamics determine whether conscious experience arises.
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Sueños/fisiología , Electroencefalografía/métodos , Adulto , Anciano , Encéfalo/diagnóstico por imagen , Encéfalo/fisiología , Mapeo Encefálico , Sueños/psicología , Femenino , Humanos , Masculino , Recuerdo Mental/fisiología , Persona de Mediana Edad , Red Nerviosa/fisiología , Polisomnografía , Descanso/fisiología , Sueño de Onda Lenta/fisiología , Vigilia/fisiología , Adulto JovenRESUMEN
INTRODUCTION: Personally meaningful past episodes, defined as episodic memories (EM), are subjectively re-experienced from the natural perspective and location of one's own body, as described by bodily self-consciousness (BSC). Neurobiological mechanisms of memory consolidation suggest how initially irrelevant episodes may be remembered, if related information makes them gain importance later in time, leading for instance, to a retroactive memory strengthening in humans. METHODS: Using an immersive virtual reality system, we were able to directly manipulate the presence or absence of one's body, which seems to prevent a loss of initially irrelevant, self-unrelated past events. RESULTS AND CONCLUSION: Our findings provide an evidence that personally meaningful memories of our past are not fixed, but may be strengthened by later events, and that body-related integration is important for the successful recall of episodic memories.
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Memoria Episódica , Realidad Virtual , Emociones , Humanos , Recuerdo Mental , Interfaz Usuario-ComputadorRESUMEN
Episodic memories (EMs) are recollections of contextually rich and personally relevant past events. EM has been linked to the sense of self, allowing one to mentally travel back in subjective time and re-experience past events. However, the sense of self has recently been linked to online multisensory processing and bodily self-consciousness (BSC). It is currently unknown whether EM depends on BSC mechanisms. Here, we used a new immersive virtual reality (VR) system that maintained the perceptual richness of life episodes and fully controlled the experimental stimuli during encoding and retrieval, including the participant's body. Our data reveal a classical EM finding, which shows that memory for complex real-life like scenes decays over time. However, here we also report a novel finding that delayed retrieval performance can be enhanced when participants view their body as part of the virtual scene during encoding. This body effect was not observed when no virtual body or a moving control object was shown, thereby linking the sense of self, and BSC in particular, to EMs. The present VR methodology and the present behavioral findings will enable to study key aspects of EM in healthy participants and may be especially beneficial for the restoration of self-relevant memories in future experiments.
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Imagen Corporal/psicología , Memoria Episódica , Realidad Virtual , Adulto , Emociones , Femenino , Humanos , Masculino , Recuerdo Mental , Modelos Neurológicos , Modelos Psicológicos , Estimulación Luminosa , Autoimagen , Interfaz Usuario-Computador , Percepción Visual , Adulto JovenRESUMEN
Parietal cortex and adjacent parts of the temporal cortex have recently been associated with bodily self-consciousness (BSC). Similarly, growing evidence suggests that the lateral parietal cortex is crucial for the subjective aspects of episodic autobiographical memory (EAM), which is based on the conscious experience of reliving past events. However, the neuroanatomical relationship between both fundamental aspects remains currently unexplored. Moreover, despite the wealth of neuroimaging data on EAM, only few neuroimaging studies have examined BSC and even fewer examined those aspects of BSC that are most closely related to EAM. Here, we investigated whether regions in the inferior parietal lobule (IPL) that have been involved in spatial aspects of BSC (self-location and first-person perspective), as described by Ionta et al. (2011) are also active in studies investigating autobiographical memory. To examine this relation, we thus compared the regions indicated in the study by Ionta et al. (2011) based on data in healthy participants and neurological patients, with the results from a meta-analytical study we performed based on functional neuroimaging studies on EAM and semantic autobiographical memory (SAM). We report an anatomical overlap bilaterally in the angular gyrus (AG), but not in other parietal or temporal lobe structures between BSC and EAM. Moreover, there was no overlap between BSC and SAM. These preliminary data suggest that the bilateral AG may be a key structure for the conscious re-experiencing of past life episodes (EAM) and the conscious on-line experience of being located and experiencing the world in first-person (BSC).