Aperiodic brain activity and response to anesthesia vary in disorders of consciousness

Abstract

In the human electroencephalogram (EEG), oscillatory power peaks co-exist with non-oscillatory, aperiodic activity. Although EEG analysis has traditionally focused exclusively on oscillatory power, recent investigations have shown that the aperiodic EEG component can distinguish conscious wakefulness from sleep and anesthetic-induced unconsciousness (Lendner et al. 2020). This study investigates the aperiodic EEG component of individuals in a disorder of consciousness (DOC), and how it changes in response to exposure to anesthesia. High-density EEG was recorded from 43 individuals in a DOC. To measure the brain’s reaction to global perturbation, a subset of n = 16 were also exposed to a targeted infusion of propofol anesthesia. The aperiodic component was defined by the spectral slope and offset in the 1-45 Hz and 30-45 Hz range of the power spectral density. Brain network criticality and complexity were estimated using the pair correlation function (PCF) and Lempel-Ziv complexity, respectively. The level of responsiveness of all individuals in DOC was assessed using the Coma Recovery Scale-Revised (CRS-R). Recovery of consciousness was assessed three months post-EEG. At baseline, the EEG aperiodic component was more strongly correlated to the participants’ level of consciousness than the oscillatory component. Anesthesia caused a steepening of the spectral slope across participants. Importantly, the change in spectral slope positively correlated with the individual participant’s level of responsiveness. The spectral slope during exposure to anesthesia contained prognostic value for individuals with DOC. The anesthetic-induced change in aperiodic EEG was accompanied by loss of information-richness and a reduction in network criticality. The aperiodic EEG component in individuals with DOC has been historically neglected; this research highlights the importance of considering this measure for future research investigating brain mechanisms underlying consciousness.Significance StatementThe analysis of human EEG has traditionally focused on oscillatory power, which is characterized by peaks above a broadband, aperiodic component in the EEG power spectral density. This study is the first to demonstrate the value of the aperiodic EEG component and specifically, its reaction to propofol anesthesia for assessing individual’s level of, and capacity for, consciousness. Our results demonstrates that the pharmacological induced change in the aperiodic component accompanies the brain’s loss of network criticality and complexity. Most importantly, the magnitude of brain response to propofol anesthesia relies on an individual’s pre-anesthetic level of consciousness. Whereas the aperiodic EEG component has been historically neglected; this research highlights the necessity of considering this measure for future research that seeks to understand the neurophysiological underpinnings of consciousness.

The role of etiology in the identification of clinical markers of consciousness: comparing EEG alpha power, complexity, and spectral exponent

“…However, the spectral exponent significantly correlated with non-anoxic patients' CRS-R score (r(82)=0.33, p<0.05) (analysis 2). In line with previous research (Maschke, Duclos, Owen, et al 2022), a flatter exponent indicated a higher level of consciousness (see Figure 4 and 5). The correlation between the spectral exponent and non-anoxic patients' level of consciousness as well as its ability to distinguish responsive from unresponsive patients lost significance after p-value correction (see Figure 3 and 5).…”

“…Even though the EEG spectral exponent has been historically neglected, mounting evidence attributes changes in the spectral exponent as an index of altered states of consciousness (Colombo et al 2019;Lendner et al 2020;Colombo et al 2023). In addition, our group previously demonstrated that patients in a DOC are often characterized by a total absence of oscillatory peaks (Maschke, Duclos, Owen, et al 2022). In the current study, we validate the previously shown diagnostic value of the aperiodic component for non-anoxic patients (Maschke, Duclos, Owen, et al 2022;Colombo et al 2023).…”

“…Indeed, the electroencephalogram (EEG) spectral exponent (i.e., exponential decay of power over frequency) has gained increasing attention as a novel marker of consciousness (Colombo et al 2019;Lendner et al 2020;Maschke, Duclos, Owen, et al 2022;Colombo et al 2023;Leroy et al 2023). Especially in the absence of oscillatory peaks -which is a common phenomenon in disorders of consciousness (DOC) -our group has previously demonstrated diagnostic power of the spectral exponent above and beyond oscillatory power (Maschke, Duclos, Owen, et al 2022).…”

“…However, it remains unclear whether EEG complexity is an independent marker of level of consciousness, or epiphenomenal to changes in the spectral exponent. Although many studies have demonstrated a strong correlation between spectral exponent and spontaneous (Medel et al 2020;Alnes et al 2021;Maschke, Duclos, Owen, et al 2022) and evoked signal complexity (Colombo et al 2019;Maschke et al 2023), most studies of signal complexity do not concurrently analyze changes in the spectral exponent.…”

Individual trajectories for recovery of neocortical activity in disorders of consciousness

“…Recovery of consciousness is believed to co-occur with the emergence of a spectral peak in the lower frequency range (around 7 Hz), with a shift towards higher frequencies (first around 10 Hz and potentially around 20 Hz) during further recovery Edlow, Claassen, et al 2021. The relevance of EEG measurements in DoC is underscored by the notion that the re-emergence of physiological EEG features is associated with behavioral recovery Colombo et al 2023;Jørgensen and Holm 1998;Maschke et al 2023;Thibaut, Panda, et al 2021 and glucose uptake Annen et al 2023. Several hypotheses may explain the recovery of the EEG power spectrum in patients with DoC. One of these hypotheses, the meso-circuit hypothesis, states that the return of spectral peaks in the EEG power spectrum is a result of the restoration of excitation in the thalamocortical circuit and, more specifically, a more widespread cortico-striato-pallido-thalamic network N. D. Schiff 2010.…”