The brain dynamics of visuospatial perspective-taking captured by intracranial EEG.

Visuospatial perspective-taking (VPT) is the ability to imagine a scene from a position different from the one used in self-perspective judgments (SPJ). We typically use VPT to understand how others see the environment. VPT requires overcoming the self-perspective, and impairments in this process are implicated in various brain disorders, such as schizophrenia and autism. However, the underlying brain areas of VPT are not well distinguished from SPJ-related ones and from domain-general responses to both perspectives. In addition, hierarchical processing theory suggests that domain-specific processes emerge over time from domain-general ones. It mainly focuses on the sensory system, but outside of it, support for this hypothesis is lacking. Therefore, we aimed to spatiotemporally distinguish brain responses domain-specific to VPT from the specific ones to self-perspective, and domain-general responses to both perspectives. In particular, we intended to test whether VPT- and SPJ specific responses begin later than the general ones. We recorded intracranial EEG data from 30 patients with epilepsy who performed a task requiring laterality judgments during VPT and SPJ, and analyzed the spatiotemporal features of responses in the broad gamma band (50-150 Hz). We found VPT-specific processing in a more extensive brain network than SPJ-specific processing. Their dynamics were similar, but both differed from the general responses, which began earlier and lasted longer. Our results anatomically distinguish VPT-specific from SPJ-specific processing. Furthermore, we temporally differentiate between domain-specific and domain-general processes both inside and outside the sensory system, which serves as a novel example of hierarchical processing.

Electrical Source Imaging of Somatosensory Evoked Potentials from Intracranial EEG Signals.

Stereoelectroencephalography (SEEG) records electrical brain activity with intracerebral electrodes. However, it has an inherently limited spatial coverage. Electrical source imaging (ESI) infers the position of the neural generators from the recorded electric potentials, and thus, could overcome this spatial undersampling problem. Here, we aimed to quantify the accuracy of SEEG ESI under clinical conditions. We measured the somatosensory evoked potential (SEP) in SEEG and in high-density EEG (HD-EEG) in 20 epilepsy surgery patients. To localize the source of the SEP, we employed standardized low resolution brain electromagnetic tomography (sLORETA) and equivalent current dipole (ECD) algorithms. Both sLORETA and ECD converged to similar solutions. Reflecting the large differences in the SEEG implantations, the localization error also varied in a wide range from 0.4 to 10 cm. The SEEG ESI localization error was linearly correlated with the distance from the putative neural source to the most activated contact. We show that it is possible to obtain reliable source reconstructions from SEEG under realistic clinical conditions, provided that the high signal fidelity recording contacts are sufficiently close to the source of the brain activity.

Timing of Allocentric and Egocentric Spatial Processing in Human Intracranial EEG.

Spatial reference frames (RFs) play a key role in spatial cognition, especially in perception, spatial memory, and navigation. There are two main types of RFs: egocentric (self-centered) and allocentric (object-centered). Although many fMRI studies examined the neural correlates of egocentric and allocentric RFs, they could not sample the fast temporal dynamics of the underlying cognitive processes. Therefore, the interaction and timing between these two RFs remain unclear. Taking advantage of the high temporal resolution of intracranial EEG (iEEG), we aimed to determine the timing of egocentric and allocentric information processing and describe the brain areas involved. We recorded iEEG and analyzed broad gamma activity (50-150 Hz) in 37 epilepsy patients performing a spatial judgment task in a three-dimensional circular virtual arena. We found overlapping activation for egocentric and allocentric RFs in many brain regions, with several additional egocentric- and allocentric-selective areas. In contrast to the egocentric responses, the allocentric responses peaked later than the control ones in frontal regions with overlapping selectivity. Also, across several egocentric or allocentric selective areas, the egocentric selectivity appeared earlier than the allocentric one. We identified the maximum number of egocentric-selective channels in the medial occipito-temporal region and allocentric-selective channels around the intraparietal sulcus in the parietal cortex. Our findings favor the hypothesis that egocentric spatial coding is a more primary process, and allocentric representations may be derived from egocentric ones. They also broaden the dominant view of the dorsal and ventral streams supporting egocentric and allocentric space coding, respectively.

Tackling the challenges of group network inference from intracranial EEG data.

Introduction: Intracranial EEG (iEEG) data is a powerful way to map brain function, characterized by high temporal and spatial resolution, allowing the study of interactions among neuronal populations that orchestrate cognitive processing. However, the statistical inference and analysis of brain networks using iEEG data faces many challenges related to its sparse brain coverage, and its inhomogeneity across patients. Methods: We review these challenges and develop a methodological pipeline for estimation of network structure not obtainable from any single patient, illustrated on the inference of the interaction among visual streams using a dataset of 27 human iEEG recordings from a visual experiment employing visual scene stimuli. 100 ms sliding window and multiple band-pass filtered signals are used to provide temporal and spectral resolution. For the connectivity analysis we showcase two connectivity measures reflecting different types of interaction between regions of interest (ROI): Phase Locking Value as a symmetric measure of synchrony, and Directed Transfer Function-asymmetric measure describing causal interaction. For each two channels, initial uncorrected significance testing at p < 0.05 for every time-frequency point is carried out by comparison of the data-derived connectivity to a baseline surrogate-based null distribution, providing a binary time-frequency connectivity map. For each ROI pair, a connectivity density map is obtained by averaging across all pairs of channels spanning them, effectively agglomerating data across relevant channels and subjects. Finally, the difference of the mean map value after and before the stimulation is compared to the same statistic in surrogate data to assess link significance. Results: The analysis confirmed the function of the parieto-medial temporal pathway, mediating visuospatial information between dorsal and ventral visual streams during visual scene analysis. Moreover, we observed the anterior hippocampal connectivity with more posterior areas in the medial temporal lobe, and found the reciprocal information flow between early processing areas and medial place area. Discussion: To summarize, we developed an approach for estimating network connectivity, dealing with the challenge of sparse individual coverage of intracranial EEG electrodes. Its application provided new insights into the interaction between the dorsal and ventral visual streams, one of the iconic dualities in human cognition.

Intracerebral mechanisms explaining the impact of incidental feedback on mood state and risky choice.

Identifying factors whose fluctuations are associated with choice inconsistency is a major issue for rational decision theory. Here, we investigated the neuro-computational mechanisms through which mood fluctuations may bias human choice behavior. Intracerebral EEG data were collected in a large group of subjects (n=30) while they were performing interleaved quiz and choice tasks that were designed to examine how a series of unrelated feedbacks affect decisions between safe and risky options. Neural baseline activity preceding choice onset was confronted first to mood level, estimated by a computational model integrating the feedbacks received in the quiz task, and then to the weighting of option attributes, in a computational model predicting risk attitude in the choice task. Results showed that (1) elevated broadband gamma activity (BGA) in the ventromedial prefrontal cortex (vmPFC) and dorsal anterior insula (daIns) was respectively signaling periods of high and low mood, (2) increased vmPFC and daIns BGA respectively promoted and tempered risk taking by overweighting gain vs. loss prospects. Thus, incidental feedbacks induce brain states that correspond to different moods and bias the evaluation of risky options. More generally, these findings might explain why people experiencing positive (or negative) outcome in some part of their life tend to expect success (or failure) in any other.

Elevated D-dimer as an immediate response to alemtuzumab treatment.

Alemtuzumab as a treatment of highly active multiple sclerosis causes a rapid decrease in inflammatory activity due the lysis of immune cells. Subsequent cytokine release determines the infusion-associated reaction that is a frequent adverse event of alemtuzumab treatment. Recently, serious cardiovascular and thrombotic adverse reactions following alemtuzumab infusion have been described. In our study, the dynamics of coagulation parameters were analyzed in 13 multiple sclerosis patients treated with alemtuzumab. An immediate, significant increase in the level of D-dimer was observed after the first administration of alemtuzumab. This observation provides evidence of coagulation activation and the potential risk of thrombotic complications with this therapy. Prophylactic low molecular weight heparin pretreatment maybe considered in patients receiving alemtuzumab.

Mapping the Scene and Object Processing Networks by Intracranial EEG.

Human perception and cognition are based predominantly on visual information processing. Much of the information regarding neuronal correlates of visual processing has been derived from functional imaging studies, which have identified a variety of brain areas contributing to visual analysis, recognition, and processing of objects and scenes. However, only two of these areas, namely the parahippocampal place area (PPA) and the lateral occipital complex (LOC), were verified and further characterized by intracranial electroencephalogram (iEEG). iEEG is a unique measurement technique that samples a local neuronal population with high temporal and anatomical resolution. In the present study, we aimed to expand on previous reports and examine brain activity for selectivity of scenes and objects in the broadband high-gamma frequency range (50-150 Hz). We collected iEEG data from 27 epileptic patients while they watched a series of images, containing objects and scenes, and we identified 375 bipolar channels responding to at least one of these two categories. Using K-means clustering, we delineated their brain localization. In addition to the two areas described previously, we detected significant responses in two other scene-selective areas, not yet reported by any electrophysiological studies; namely the occipital place area (OPA) and the retrosplenial complex. Moreover, using iEEG we revealed a much broader network underlying visual processing than that described to date, using specialized functional imaging experimental designs. Here, we report the selective brain areas for scene processing include the posterior collateral sulcus and the anterior temporal region, which were already shown to be related to scene novelty and landmark naming. The object-selective responses appeared in the parietal, frontal, and temporal regions connected with tool use and object recognition. The temporal analyses specified the time course of the category selectivity through the dorsal and ventral visual streams. The receiver operating characteristic analyses identified the PPA and the fusiform portion of the LOC as being the most selective for scenes and objects, respectively. Our findings represent a valuable overview of visual processing selectivity for scenes and objects based on iEEG analyses and thus, contribute to a better understanding of visual processing in the human brain.

The dynamics of error processing in the human brain as reflected by high-gamma activity in noninvasive and intracranial EEG.

Error detection in motor behavior is a fundamental cognitive function heavily relying on local cortical information processing. Neural activity in the high-gamma frequency band (HGB) closely reflects such local cortical processing, but little is known about its role in error processing, particularly in the healthy human brain. Here we characterize the error-related response of the human brain based on data obtained with noninvasive EEG optimized for HGB mapping in 31 healthy subjects (15 females, 16 males), and additional intracranial EEG data from 9 epilepsy patients (4 females, 5 males). Our findings reveal a multiscale picture of the global and local dynamics of error-related HGB activity in the human brain. On the global level as reflected in the noninvasive EEG, the error-related response started with an early component dominated by anterior brain regions, followed by a shift to parietal regions, and a subsequent phase characterized by sustained parietal HGB activity. This phase lasted for more than 1 s after the error onset. On the local level reflected in the intracranial EEG, a cascade of both transient and sustained error-related responses involved an even more extended network, spanning beyond frontal and parietal regions to the insula and the hippocampus. HGB mapping appeared especially well suited to investigate late, sustained components of the error response, possibly linked to downstream functional stages such as error-related learning and behavioral adaptation. Our findings establish the basic spatio-temporal properties of HGB activity as a neural correlate of error processing, complementing traditional error-related potential studies.

Predominance of Movement Speed Over Direction in Neuronal Population Signals of Motor Cortex: Intracranial EEG Data and A Simple Explanatory Model.

How neuronal activity of motor cortex is related to movement is a central topic in motor neuroscience. Motor-cortical single neurons are more closely related to hand movement velocity than speed, that is, the magnitude of the (directional) velocity vector. Recently, there is also increasing interest in the representation of movement parameters in neuronal population activity, such as reflected in the intracranial EEG (iEEG). We show that in iEEG, contrasting to what has been previously found on the single neuron level, speed predominates over velocity. The predominant speed representation was present in nearly all iEEG signal features, up to the 600-1000 Hz range. Using a model of motor-cortical signals arising from neuronal populations with realistic single neuron tuning properties, we show how this reversal can be understood as a consequence of increasing population size. Our findings demonstrate that the information profile in large population signals may systematically differ from the single neuron level, a principle that may be helpful in the interpretation of neuronal population signals in general, including, for example, EEG and functional magnetic resonance imaging. Taking advantage of the robust speed population signal may help in developing brain-machine interfaces exploiting population signals.

The role of ECoG magnitude and phase in decoding position, velocity, and acceleration during continuous motor behavior.

In neuronal population signals, including the electroencephalogram (EEG) and electrocorticogram (ECoG), the low-frequency component (LFC) is particularly informative about motor behavior and can be used for decoding movement parameters for brain-machine interface (BMI) applications. An idea previously expressed, but as of yet not quantitatively tested, is that it is the LFC phase that is the main source of decodable information. To test this issue, we analyzed human ECoG recorded during a game-like, one-dimensional, continuous motor task with a novel decoding method suitable for unfolding magnitude and phase explicitly into a complex-valued, time-frequency signal representation, enabling quantification of the decodable information within the temporal, spatial and frequency domains and allowing disambiguation of the phase contribution from that of the spectral magnitude. The decoding accuracy based only on phase information was substantially (at least 2 fold) and significantly higher than that based only on magnitudes for position, velocity and acceleration. The frequency profile of movement-related information in the ECoG data matched well with the frequency profile expected when assuming a close time-domain correlate of movement velocity in the ECoG, e.g., a (noisy) "copy" of hand velocity. No such match was observed with the frequency profiles expected when assuming a copy of either hand position or acceleration. There was also no indication of additional magnitude-based mechanisms encoding movement information in the LFC range. Thus, our study contributes to elucidating the nature of the informative LFC of motor cortical population activity and may hence contribute to improve decoding strategies and BMI performance.