The human brain has the capacity to rapidly change state, and in epilepsy these state changes can be catastrophic, resulting in loss of consciousness, injury and even death. Theoretical interpretations considering the brain as a dynamical system suggest that prior to a seizure, recorded brain signals may exhibit critical slowing down, a warning signal preceding many critical transitions in dynamical systems. Using long-term intracranial electroencephalography (iEEG) recordings from fourteen patients with focal epilepsy, we monitored key signatures of critical slowing down prior to seizures. The metrics used to detect critical slowing down fluctuated over temporally long scales (hours to days), longer than would be detectable in standard clinical evaluation settings. Seizure risk was associated with a combination of these signals together with epileptiform discharges. These results provide strong validation of theoretical models and demonstrate that critical slowing down is a reliable indicator that could be used in seizure forecasting algorithms.

Critical dynamics are assumed to be an attractive mode for normal brain functioning as information processing and computational capabilities are found to be optimal in the critical state. Recent experimental observations of neuronal activity patterns following power-law distributions, a hallmark of systems at a critical state, have led to the hypothesis that human brain dynamics could be poised at a phase transition between ordered and disordered activity. A so far unresolved question concerns the medical significance of critical brain activity and how it relates to pathological conditions. Using data from invasive electroencephalogram recordings from humans we show that during epileptic seizure attacks neuronal activity patterns deviate from the normally observed power-law distribution characterizing critical dynamics. The comparison of these observations to results from a computational model exhibiting self-organized criticality (SOC) based on adaptive networks allows further insights into the underlying dynamics. Together these results suggest that brain dynamics deviates from criticality during seizures caused by the failure of adaptive SOC. Over the recent years it has become apparent that the concept of phase transitions is not only applicable to the systems classically considered in physics. It applies to a much wider class of complex systems exhibiting phases, characterized by qualitatively different types of long-term behavior. In the critical states, which are located directly at the transition, small changes can have a large effect on the system. This and other properties of critical states prove to be advantageous for computation and memory. It is therefore suspected that also cerebral neural networks operate close to criticality. This is supported by the in vitro and in vivo measurements of power-laws of certain scaling relationships that are the hallmarks of phase transitions. While critical dynamics is arguably an attractive mode of normal brain functioning, its relation to pathological brain conditions is still unresolved. Here we show that brain dynamics deviates from a critical state during epileptic seizure attacks in vivo. Furthermore, insights from a computational model suggest seizures to be caused by the failure of adaptive self-organized criticality, a mechanism of self-organization to criticality based on the interplay between network dynamics and topology.

Sleep encompasses approximately a third of our lifetime, yet its purpose and biological function are not well understood. Without sleep optimal brain functioning such as responsiveness to stimuli, information processing, or learning may be impaired. Such observations suggest that sleep plays a crucial role in organizing or reorganizing neuronal networks of the brain toward states where information processing is optimized.Increasing evidence suggests that cortical neuronal networks operate near a critical state characterized by balanced activity patterns, which supports optimal information processing. However, it remains unknown whether critical dynamics is affected in the course of wake and sleep, which would also impact information processing. Here, we show that signatures of criticality are progressively disturbed during wake and restored by sleep. We demonstrate that the precise power-laws governing the cascading activity of neuronal avalanches and the distribution of phase-lock intervals in human electroencephalographic recordings are increasingly disarranged during sustained wakefulness. These changes are accompanied by a decrease in variability of synchronization. Interpreted in the context of a critical branching process, these seemingly different findings indicate a decline of balanced activity and progressive distance from criticality toward states characterized by an imbalance toward excitation where larger events prevail dynamics. Conversely, sleep restores the critical state resulting in recovered power-law characteristics in activity and variability of synchronization. These findings support the intriguing hypothesis that sleep may be important to reorganize cortical network dynamics to a critical state thereby assuring optimal computational capabilities for the following time awake.

Information processing in complex systems is often found to be maximally efficient close to critical states associated with phase transitions. It is therefore conceivable that also neural information processing operates close to criticality. This is further supported by the observation of power-law distributions, which are a hallmark of phase transitions. An important open question is how neural networks could remain close to a critical point while undergoing a continual change in the course of development, adaptation, learning, and more. An influential contribution was made by Bornholdt and Rohlf, introducing a generic mechanism of robust self-organized criticality in adaptive networks. Here, we address the question whether this mechanism is relevant for real neural networks. We show in a realistic model that spike-time-dependent synaptic plasticity can self-organize neural networks robustly toward criticality. Our model reproduces several empirical observations and makes testable predictions on the distribution of synaptic strength, relating them to the critical state of the network. These results suggest that the interplay between dynamics and topology may be essential for neural information processing.

Significance: Dynamic changes of cortical excitability are relevant in both healthy and pathological network dynamics. In epilepsy, pathological changes in excitability commonly underlie the initiation and spread of seizures. Accordingly, the ability to monitor excitability and control its degree is important for adequate clinical care and treatment because classic EEG markers found in epilepsy such as interictal spikes do not reflect seizure propensity and thus excitability. Here, we identify excitability markers and test them on long-term electrocorticogram and EEG recordings. We show that they correlate with more direct excitability measures using external stimulation and allow for real-time excitability monitoring. Our results provide evidence that excitability of cortical networks is reduced by antiepileptic drugs and increases as a function of time awake.

Objective: Tracking seizures is crucial for epilepsy monitoring and treatment evaluation. Current epilepsy care relies on caretaker seizure diaries, but clinical seizure monitoring may miss seizures. Wearable devices may be better tolerated and more suitable for long‐term ambulatory monitoring. This study evaluates the seizure detection performance of custom‐developed machine learning (ML) algorithms across a broad spectrum of epileptic seizures utilizing wrist‐ and ankle‐worn multisignal biosensors.Methods: We enrolled patients admitted to the epilepsy monitoring unit and asked them to wear a wearable sensor on either their wrists or ankles. The sensor recorded body temperature, electrodermal activity, accelerometry (ACC), and photoplethysmography, which provides blood volume pulse (BVP). We used electroencephalographic seizure onset and offset as determined by a board‐certified epileptologist as a standard comparison. We trained and validated ML for two different algorithms: Algorithm 1, ML methods for developing seizure type‐specific detection models for nine individual seizure types; and Algorithm 2, ML methods for building general seizure type‐agnostic detection, lumping together all seizure types.Results: We included 94 patients (57.4% female, median age = 9.9 years) and 548 epileptic seizures (11 066 h of sensor data) for a total of 930 seizures and nine seizure types. Algorithm 1 detected eight of nine seizure types better than chance (area under the receiver operating characteristic curve [AUC‐ROC] = .648–.976). Algorithm 2 detected all nine seizure types better than chance (AUC‐ROC = .642–.995); a fusion of ACC and BVP modalities achieved the best AUC‐ROC (.752) when combining all seizure types together.Significance: Automatic seizure detection using ML from multimodal wearable sensor data is feasible across a broad spectrum of epileptic seizures. Preliminary results show better than chance seizure detection. The next steps include validation of our results in larger datasets, evaluation of the detection utility tool for additional clinical seizure types, and integration of additional clinical information.