Epidural electrocorticography for monitoring of arousal in locked-in state

Abstract

Electroencephalography (EEG) often fails to assess both the level (i.e., arousal) and the content (i.e., awareness) of pathologically altered consciousness in patients without motor responsiveness. This might be related to a decline of awareness, to episodes of low arousal and disturbed sleep patterns, and/or to distorting and attenuating effects of the skull and intermediate tissue on the recorded brain signals. Novel approaches are required to overcome these limitations. We introduced epidural electrocorticography (ECoG) for monitoring of cortical physiology in a late-stage amytrophic lateral sclerosis patient in completely locked-in state (CLIS). Despite long-term application for a period of six months, no implant-related complications occurred. Recordings from the left frontal cortex were sufficient to identify three arousal states. Spectral analysis of the intrinsic oscillatory activity enabled us to extract state-dependent dominant frequencies at <4, ~7 and ~20 Hz, representing sleep-like periods, and phases of low and elevated arousal, respectively. In the absence of other biomarkers, ECoG proved to be a reliable tool for monitoring circadian rhythmicity, i.e., avoiding interference with the patient when he was sleeping and exploiting time windows of responsiveness. Moreover, the effects of interventions addressing the patient’s arousal, e.g., amantadine medication, could be evaluated objectively on the basis of physiological markers, even in the absence of behavioral parameters. Epidural ECoG constitutes a feasible trade-off between surgical risk and quality of recorded brain signals to gain information on the patient’s present level of arousal. This approach enables us to optimize the timing of interactions and medical interventions, all of which should take place when the patient is in a phase of high arousal. Furthermore, avoiding low-responsiveness periods will facilitate measures to implement alternative communication pathways involving brain-computer interfaces (BCI).

Nine decades of electrocorticography: A comparison between epidural and subdural recordings

“…Other human studies aimed to identify cortical states over the course of the progression of amyotrophic lateral sclerosis, using low frequencies recorded with epidural grids. Among other results, they described three state‐dependent frequency domains (<4 Hz for sleep‐like periods, ~7 Hz for low arousal and ~20 Hz for elevated arousal) (e.g., Martens et al, 2014), showing for the first time the usability of epidural ECoG to detect cortical states in individuals with complete paralysis.…”

“…On the other hand, subdural NHP studies reported that movement‐related subdural signals remained well detectable over 2 years of implantation (Degenhart et al, 2016; Ryapolova‐Webb et al, 2014), despite the initial signal amplitude decrease during the first 300 days (Degenhart et al, 2016). In humans, Martens et al (2014) were able to identify three levels of arousal as an individual with locked‐in syndrome transitioned into complete locked‐in syndrome over the course of 6 months, whereas Benabid et al (2019) presented stable exoskeleton control using epidural ECoG in a tetraplegic patient for 2 years. Similarly, click‐based decoding performance in an individual with locked‐in syndrome implanted with subdural ECoG remained stable over 3 years (Pels et al, 2019).…”

“…With respect to human epidural chronic studies, no complications arose during the studies by the groups of Benabid (one patient) (Benabid et al, 2019) and Gharabhaghi (one patient) (Martens et al, 2014). A risk factor related to epidural recordings seems to relate to the application of cortical stimulation (Tsubokawa et al, 1993).…”

“…Most current ECoG‐based chronic recording research is based on subdural recordings. However, it has often been suggested that epidural placement of ECoG may be associated with fewer infections and complications (e.g., Bundy et al, 2014; Fischer et al, 2019; Martens et al, 2014; Moran, 2010), which is conceptually attractive for the novel chronic applications of ECoG, including BCI. Yet, it is currently unclear if that is really the case and whether epidural recordings offer similar signal quality and precision as subdural ECoG electrodes.…”

Visual epidural field potentials possess high functional specificity in single trials

“…Epidural arrays, however, offer a less traumatic access to intracranial brain signals, and commercially available arrays have recently been used for e.g. diagnosis of the cognitive state in locked-in syndrome (Martens et al, 2014;Bensch et al, 2014) and rehabilitation of patients after stroke (Gharabaghi et al, 2014a;2014b). In the motor system, recent studies in non-human primates showed that EFPs allow well decoding of hand and finger gestures (Choi et al, 2018).…”