Local sleep-like cortical reactivity in the awake brain after focal injury

Abstract

One Sentence Summary: Focal cortical injuries are associated with local intrusion of sleep-like dynamics over the perilesional areas which disrupt local signal complexity and coexist with typical wakefulness cortical reactivity patterns within the same brain. AbstractThe functional consequences of brain injury are known to depend on neuronal alterations extending beyond the area of structural damage. Although a lateralized EEG slowing over the injured hemisphere was known since the early days of clinical neurophysiology, its electrophysiological mechanisms were not systematically investigated. In parallel, basic sleep research has thoroughly characterized the neuronal events underlying EEG slow waves in physiological conditions. These EEG events reflect brief interruptions of neuronal firing (OFF-periods) that can occur locally and have prominent consequences on network and behavioral functions. Notably, the EEG slow waves observed following focal brain injury have been never explicitly connected to local sleep-like neuronal events. In previous works, probing cortical circuits with transcranial magnetic stimulation coupled with EEG (TMS/EEG) proved as an effective way to reveal the tendency of cortical circuits to transiently plunge into silent OFF-periods. Here, using this approach, we show that the intact cortex surrounding focal brain injuries engages locally in pathological sleep-like dynamics. Specifically, we employed TMS/EEG in a cohort of thirty conscious awake patients with chronic focal and multifocal brain injuries of various etiologies. TMS systematically evoked prominent slow waves associated with sleep-like OFF-periods in the area surrounding focal cortico-subcortical lesions. These events were associated with a local disruption of signal complexity and were absent when stimulating the contralateral hemisphere. Perilesional sleep-like OFF-periods may represent a valid read-out of the electrophysiological state of discrete cortical circuits following brain injury as well as a potential target of interventions aimed at fostering functional recovery.

Recovery of consolidation after sleep following stroke—interaction of slow waves, spindles, and GABA

“…Recent work has shown that the balance between global SOs and local slow waves-delta waves (d)-determines whether there is an enhancement of skill or, instead, forgetting (Kim et al, 2019). Intriguingly, recordings in stroke patients (Poryazova et al, 2015;Sarasso et al, 2020;Tu-Chan et al, 2017;van Dellen et al, 2013) and in animal models of stroke (Burns, 1951;Burns and Webb, 1979;Carmichael and Chesselet, 2002;Gulati et al, 2015;Nita et al, 2007) have found a prevalence of local low-frequency power (<4 Hz) during awake periods; this also appears to be far more common after a cortical than a subcortical lesion (Macdonell et al, 1988).…”

Mechanisms Underlying Disorders of Consciousness: Bridging Gaps to Move Toward an Integrated Translational Science

“…Future approaches should seek relationships and convergence between metrics derived from information theory, graph theory, and dynamical systems theory and strive to connect them with structural measures. Contemporary examples include the recent link found between PCI and subcortical atrophy [76] and the recent association between focal cortical lesions and the generation of pathological slow waves, disconnection, and lost complexity [77,78].…”

“…This could be further enhanced through comparison with results from sleep and anesthesia research, in which microscopic mechanisms have been more comprehensively probed in preclinical work [87], producing mechanistic frameworks that span from whole-brain phenomena, such as individual susceptibility, to anesthetic-state transitions (neural inertia), all the way to genetic susceptibility factors for anesthesia [38,88,89]. Indeed, work in rodents and cortical slices alike has recently demonstrated that neuronal "off " periods determine a dramatic collapse of large-scale interactions and complexity during non-REM sleep and anesthesia [90][91][92], which can also be assessed by using EEG coupled with TMS in humans with brain damage [77,78].…”

Motor Cortical Network Excitability in Parkinson's Disease

“…Although our sham stimulation produced a tactile vibratory sensation, somatosensory co‐stimulation was not completely controlled for in sham blocks. However, somatosensory co‐stimulation does not contribute significantly to the early TEPs considered in the present study 48,71 . Because we did not use individual MRI neuronavigation, variability in pre‐SMA and SMA‐proper locations may have confounded TEP results due to distinctive functional changes occurring in the pre‐SMA and SMA‐proper in PD 64 .…”