Power spectrum slope is related to motor function after focal cerebral ischemia in the rat

Abstract

Electroencephalography (EEG) changes across vigilance states have been observed after ischemic stroke in patients and experimental stroke models, but their relation to functional recovery remains unclear. Here, we evaluate motor function, as measured by single pellet reaching (SPR), as well as local EEG changes in nonrapid eye movement (NREM), rapid eye movement (REM), and wakefulness during a 30 day recovery period after middle cerebral artery occlusion or sham surgery in rats. Small cortical infarcts resulted in poor SPR performance and induced widespread changes in EEG spectra in the ipsilesional hemisphere in all vigilance states, without causing major changes in sleep-wake architecture. Ipsilesional 1-4 Hz power was increased after stroke, whereas power in higher frequencies was reduced, resulting in a steeper slope of the power spectrum. Microelectrode array analysis of ipsilesional M1 showed that these spectral changes were present on the microelectrode level throughout M1 and were not related to increased synchronization between electrodes. Spectrum slope was significantly correlated with poststroke motor function and may thus be a useful readout of recovery-related plasticity.

An electrophysiological marker of arousal level in humans

“…1/f dynamics are observed across a variety of tasks ( He et al, 2010 ; Miller et al, 2009a ; Miller et al, 2009b ; Voytek et al, 2015 ), change with lifespan ( Voytek et al, 2015 ), and exhibit state-dependent variations during sleep ( Freeman and Zhai, 2009 ; Leemburg et al, 2018 ; Miskovic et al, 2019 ; Robinson et al, 2011 ) and anesthesia ( Colombo et al, 2019 ; Gao et al, 2017 ). Critically, these dynamics can be observed irrespective of the employed recording modality and species ( Colombo et al, 2019 ; Freeman and Zhai, 2009 ; Gao et al, 2017 ; He et al, 2010 ; Leemburg et al, 2018 ; Miskovic et al, 2019 ). However, to date, the underlying neural mechanisms giving rise to the prominent 1/f decay of the electrophysiological power spectrum are not well understood ( Buzsáki et al, 2012 ; He et al, 2010 ; Miller et al, 2009a ; Pesaran et al, 2018 ).…”

“…Future studies involving single neuron recordings and optogenetic manipulation will be needed to unravel the precise relationship between population firing statistics and changes in the spectral slope. Comparative studies in rodents ( Gao et al, 2017 ; Leemburg et al, 2018 ), non-human primates ( Gao et al, 2017 ) and humans ( Colombo et al, 2019 ; He et al, 2010 ; Miller et al, 2009a ; Miller et al, 2009b ; Miskovic et al, 2019 ) combined with modeling work ( Chaudhuri et al, 2018 ; Robinson et al, 2011 ; Robinson et al, 2001 ) has the potential to integrate the divergent findings into a coherent framework, which is critical to further elucidate the neurophysiologic basis of 1/f dynamics and their relationship to arousal levels.…”

An Electrophysiological Marker of Arousal Level in Humans

“…Future studies involving single neuron recordings will be needed to unravel the precise relationship between population firing statistics and band-limited changes in the PSD slope. We believe that in particular comparative studies involving rodents(22, 45), primates(22) and humans combined with modeling work has the potential to integrate divergent findings into a coherent framework and to determine the neurophysiologic basis of the spectral slope. It will be of substantial interest to assess whether neurophysiological mechanisms are preserved across species, which greatly vary in anatomy, in particular in the prefrontal cortex(46, 47).…”

EEG spectral exponent as a synthetic index for the longitudinal assessment of stroke recovery

“…At both T0 and T1 neurological status was assessed using the National Institute of Health Stroke Scale (NIHSS) [34]. NIHSS is an 11 items scale used in the assessment of clinical impairment related with stroke, range 0-42, with higher values reflecting more severe damages.…”

“…Furthermore, the PSD decay in humans resulted to be steeper in conditions typically related with increased inhibition, such as NREM sleep [10,25,26] or general anesthesia [17], when compared to wakefulnessas indexed by more negative SE values [25,[27][28][29]. Therefore, the use of SE is gaining popularity also in the study of neurologic conditions [30][31][32][33] Interestingly, more negative SE values (paralleled by reduced E/I ratio) were found over the affected hemisphere in rat models of stroke [34]. Since the SE captures EEG slowing, and is sensitive to alterations in the E/I balance, we expect it to be a reliable measure of the neurophysiological alterations in stroke.…”