Background: The Perturbational Complexity Index (PCI) was recently introduced to assess the capacity of thalamocortical circuits to engage in complex patterns of causal interactions. While showing high accuracy in detecting consciousness in brain-injured patients, PCI depends on elaborate experimental setups and offline processing, and has restricted applicability to other types of brain signals beyond transcranial magnetic stimulation and high-density EEG (TMS/hd-EEG) recordings. Objective: We aim to address these limitations by introducing PCI ST , a fast method for estimating perturbational complexity of any given brain response signal. Methods: PCI ST is based on dimensionality reduction and state transitions (ST) quantification of evoked potentials. The index was validated on a large dataset of TMS/hd-EEG recordings obtained from 108 healthy subjects and 108 brain-injured patients, and tested on sparse intracranial recordings (SEEG) of 9 patients undergoing intracranial single-pulse electrical stimulation (SPES) during wakefulness and sleep. Results: When calculated on TMS/hd-EEG potentials, PCI ST performed with the same accuracy as the original PCI, while improving on the previous method by being computed in less than a second and requiring a simpler setup. In SPES/SEEG signals, the index was able to quantify a systematic reduction of intracranial complexity during sleep, confirming the occurrence of state-dependent changes in the effective connectivity of thalamocortical circuits, as originally assessed through TMS/hd-EEG. Conclusions: PCI ST represents a fundamental advancement towards the implementation of a reliable and fast clinical tool for the bedside assessment of consciousness as well as a general measure to explore the neuronal mechanisms of loss/recovery of brain complexity across scales and models.
We would like to thank Per M. Knutsen for help in preparation of the experimental set-up and Charlotte Boccara for advice regarding the writing. We are especially grateful to Marcello Massimini, Andrea Pigorini, Matteo Fecchio and Simone Russo for their valuable comments, suggestions, and support along the way. Renzo Comolatti's current affiliation: Department of Biomedical and Clinical Sciences "L.
Background:The Perturbational Complexity Index (PCI) was recently introduced to assess the capacity of thalamocortical circuits to engage in complex patterns of causal interactions. While showing high accuracy in detecting consciousness in brain injured patients, PCI depends on elaborate experimental setups and offline processing and has restricted applicability to other types of brain signals beyond transcranial magnetic stimulation and high-density EEG (TMS/hd-EEG) recordings. Objective:We aim to address these limitations by introducing PCI ST , a fast method for estimating perturbational complexity of any given brain response signal.Methods: PCI ST is based on dimensionality reduction and state transitions (ST) quantification of evoked potentials. The index was validated on a large dataset of TMS/hd-EEG recordings obtained from 108 healthy subjects and 108 brain injured patients, and tested on sparse intracranial recordings (SEEG) of 9 patients undergoing intra-cerebral single-pulse electrical stimulation (SPES). Results:When calculated on TMS/hd-EEG potentials, PCI ST performed with the same accuracy as the original PCI, while improving on the previous method by being computed in less than a second and requiring a simpler set-up. In SPES/SEEG signals, the index was able to quantify a systematic reduction of intracerebral complexity during sleep, confirming the occurrence of state-dependent changes in the effective connectivity of thalamocortical circuits, as originally assessed through TMS/hd-EEG.Conclusions: PCI ST represents a fundamental advancement towards the implementation of a reliable and fast clinical tool for the bedside assessment of consciousness as well as a general measure to explore the neuronal mechanisms of loss/recovery of brain complexity across scales and models.
The capacity of the human brain to sustain complex dynamics consistently drops when consciousness fades. Several recent studies in humans found a remarkable reduction of the complexity of cortical responses to local stimulation during dreamless sleep, general anaesthesia, and coma. So far, this perturbational complexity has never been estimated in non-human animals in vivo. Here, we quantify the complexity of electroencephalographic responses to intracranial electrical stimulation in rats, comparing wakefulness to propofol, sevoflurane, and ketamine anaesthesia. We confirm the changes previously observed in humans: from highly complex evoked activity during wakefulness, to simpler responses, suppression of high frequencies, and reduced phase-locking with propofol and sevoflurane.We then deepen our mechanistic understanding by analyzing functional connectivity, and by showing how these parameters dissociate with ketamine, and depend on intensity and site of stimulation. This approach opens the way for further direct investigations of the mechanisms underlying brain complexity and consciousness. hypothesis that neuronal hyperpolarization might prevent cortical neurons from engaging in durable, complex interactions 12,13,14,15 . RESULTS Single pulse electrical stimulation triggered complex ERPs during wakefulness, but not during propofol anaesthesiaWe recorded epidural EEG activity from 16 screw electrodes chronically implanted through the skull in head-and body-restrained male, adult rats. Recording electrodes were in contact with the dura and organized in a symmetric grid, covering most of the cortex in both hemispheres (M2, secondary motor cortex; M1, primary motor cortex; S1, primary somatosensory cortex; RS, retrosplenial cortex; PA, parietal associative cortex; V1, primary visual cortex; V2, secondary visual cortex; GND, ground electrode over cerebellum). We stimulated right M2 by single monophasic, electrical current pulses (typically: 1 ms duration, 50 µA amplitude, at 0.1 Hz) via a chronically implanted bipolar electrode, located 4.38 ± 0.26 mm rostral from bregma, 0.47 ± 0.09 mm below the cortical surface, mainly corresponding to layer II/III (based on histology after recording, 8 rats; Fig. 1a; all values are reported as mean ± SEM). Pulse trains delivered at similar coordinates triggered coordinated whisker deflections 16 , whereas EEG responses following single stimuli were not measurably contaminated by movements ( Supplementary Fig. 1, Video 1-2) and were reproducible throughout recording sessions and across days (Supplementary Fig. 2). No correlation between the stimulating electrode locations and ERP amplitude or duration was found (Supplementary Fig. 3).We performed electrophysiological recordings in 9 rats during wakefulness and propofol anaesthesia (∼1.1 mg/kg/min, i.v.) at a depth that produced spontaneous, slow, high-amplitude EEG oscillations and was sufficient to abolish any detectable motor response to pain stimuli. The redistribution of EEG power from high to low frequencies was confirmed ...
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