Patients with epilepsy are characterized by a dysregulation of excitation/inhibition balance (E/I). The assessment of E/I may inform clinicians during the diagnosis and therapy management, even though it is rarely performed. An accessible measure of the E/I of the brain represents a clinically relevant feature. Here, we exploited the exponent of the aperiodic component of the power spectrum of the electroencephalography (EEG) signal, as a non-invasive and cost-effective proxy of the E/I balance. We recorded resting-state activity with high-density EEG from 67 patients with temporal lobe epilepsy and 35 controls. We extracted the exponent of the aperiodic fit of the power spectrum from source-reconstructed EEG and tested differences between patients with epilepsy and controls. Spearman’s correlation was performed between the exponent and clinical variables (age of onset, epilepsy duration and neuropsychology) and cortical expression of epilepsy-related genes derived from the Allen Human Brain Atlas. Patients with temporal lobe epilepsy showed a significantly larger exponent, corresponding to inhibition-directed E/I balance, in bilateral frontal and temporal regions. Lower E/I in the left entorhinal and bilateral dorsolateral prefrontal cortices corresponded to a lower performance of short-term verbal memory. Limited to patients with temporal lobe epilepsy, we detected a significant correlation between the exponent and the cortical expression of GABRA1, GRIN2A, GABRD, GABRG2, KCNA2 and PDYN genes. EEG aperiodic exponent maps the E/I balance non-invasively in patients with epilepsy and reveals a close relationship between altered E/I patterns, cognition and genetics.
Objective: Large aperiodic bursts of activations named neuronal avalanches have been used to characterize whole‐brain activity, as their presence typically relates to optimal dynamics. Epilepsy is characterized by alterations in large‐scale brain network dynamics. Here we exploited neuronal avalanches to characterize differences in electroencephalography (EEG) basal activity, free from seizures and/or interictal spikes, between patients with temporal lobe epilepsy (TLE) and matched controls.Method: We defined neuronal avalanches as starting when the z‐scored source‐reconstructed EEG signals crossed a specific threshold in any region and ending when all regions returned to baseline. This technique avoids data manipulation or assumptions of signal stationarity, focusing on the aperiodic, scale‐free components of the signals. We computed individual avalanche transition matrices to track the probability of avalanche spreading across any two regions, compared them between patients and controls, and related them to memory performance in patients.Results: We observed a robust topography of significant edges clustering in regions functionally and structurally relevant for the TLE, such as the entorhinal cortex, the inferior parietal and fusiform area, the inferior temporal gyrus, and the anterior cingulate cortex. We detected a significant correlation between the centrality of the entorhinal cortex in the transition matrix and the long‐term memory performance (delay recall Rey–Osterrieth Complex Figure Test).Significance: Our results show that the propagation patterns of large‐scale neuronal avalanches are altered in TLE during the resting state, suggesting a potential diagnostic application in epilepsy. Furthermore, the relationship between specific patterns of propagation and memory performance support the neurophysiological relevance of neuronal avalanches.
There is an increasing interest in applying artificial intelligence techniques to forecast epileptic seizures. In particular, machine learning algorithms could extract nonlinear statistical regularities from electroencephalographic (EEG) time series that can anticipate abnormal brain activity. The recent literature reports promising results in seizure detection and prediction tasks using machine and deep learning methods. However, performance evaluation is often based on questionable randomized cross-validation schemes, which can introduce correlated signals (e.g., EEG data recorded from the same patient during nearby periods of the day) into the partitioning of training and test sets. The present study demonstrates that the use of more stringent evaluation strategies, such as those based on leave-one-patient-out partitioning, leads to a drop in accuracy from about 80% to 50% for a standard eXtreme Gradient Boosting (XGBoost) classifier on two different data sets. Our findings suggest that the definition of rigorous evaluation protocols is crucial to ensure the generalizability of predictive models before proceeding to clinical trials.
The study of neural pre-stimulus or “anticipatory” activity opened a new window for understanding how the brain actively constructs the forthcoming reality. Usually, experimental paradigms designed to study anticipatory activity make use of stimuli. The purpose of the present study is to expand the study of neural anticipatory activity upon the temporal occurrence of dichotomic, statistically unpredictable (random) stimuli within an ecological experimental paradigm. To this purpose, we used a simplified driving simulation including two possible, randomly-presented trial types: a car crash end trial and a no car crash end trial. Event Related Potentials (ERP) were extracted -3,000 ms before stimulus onset. We identified a fronto-central negativity starting around 1,000 ms before car crash presentation. By contrast, a whole-scalp distributed positivity characterized the anticipatory activity observed before the end of the trial in the no car crash end condition. The present data are in line with the hypothesis that the brain may also anticipate dichotomic, statistically unpredictable stimuli, relaying onto different pre-stimulus ERP activity. Possible integration with car-smart-systems is also suggested.
In this study, we investigated the effect of global temporal prediction on the brain capability to implicitly adjust proactive motor control. We used the Dynamic Temporal Prediction (DTP), in which local and global predictions of an imperative stimulus were manipulated by using different stimulus-onset asynchronies (SOAs), presented with several distribution probabilities. At a behavioural level, the results show a performance adjustment (reaction time decrease) depending on the implicit use of global prediction. At a neurophysiological level, three separate computational steps underlying motor control were investigated. First, the expectancy implementation was associated with global probability-dependent contingent negative variation (CNV) modulation supported by the recruitment of a frontoparietal network involving the anterior cingulate, the left intraparietal sulcus, the occipital, and the premotor areas. Second, the response implementation was modulated by the global prediction fostering stimulus processing (P3 increase) at the motor response level, as suggested by both oscillatory (beta desynchronization), as well as source analysis (frontal cortical network). Third, the expectancy violation lead to a negativity increase (omission-detection potential) time locked to the global rule violation and additionally, to delta and theta power increase interpreted as inhibitory control and rule violation detection, respectively. The expectancy violation further engaged a left lateralized network including the temporal parietal junction (TPJ) and the motor cortex, suggesting involvement of attentional reorienting and a motor adjustment. Finally, these findings provide new insights on the neurocognitive mechanisms underlying proactive motor control, suggesting an overlapping between implicit and explicit processes.