Pre-stimulus phase and amplitude regulation of phase-locked responses are maximized in the critical state

Abstract

Understanding why identical stimuli give differing neuronal responses and percepts is a central challenge in research on attention and consciousness. Ongoing oscillations reflect functional states that bias processing of incoming signals through amplitude and phase. It is not known, however, whether the effect of phase or amplitude on stimulus processing depends on the long-term global dynamics of the networks generating the oscillations. Here, we show, using a computational model, that the ability of networks to regulate stimulus response based on pre-stimulus activity requires near-critical dynamics—a dynamical state that emerges from networks with balanced excitation and inhibition, and that is characterized by scale-free fluctuations. We also find that networks exhibiting critical oscillations produce differing responses to the largest range of stimulus intensities. Thus, the brain may bring its dynamics close to the critical state whenever such network versatility is required.

Dynamic relationships between spontaneous and evoked electrophysiological activity

“…These results show that for a variety of neurophysiological parameters, trial-by-trial fluctuations in the pre-stimulus period influence variation in post-stimulus neural responses to stimuli in predictable ways. Our results extend recent findings relating prestimulus spectral power to ERP components 27 , 52 – 54 , 58 – 61 , and complement cellular and modeling research investigating this question 36 , 62 – 64 . While negative correlation between spontaneous and evoked alpha band power has been suggested by 52 – 54 , our study is the first to provide robust evidence of this phenomenon using (a) statistics which avoid circular analysis, (b) multiple imaging modalities, and (c) a very large sample size.…”

“…In EEG investigations, the power of cortical oscillations, in particular the alpha band, are thought to reflect modulations of cortical excitability, and as such have been investigated for their role in shaping stimulus processing 27 – 32 . Other work has investigated the influence of more general physiological variables such as desynchronization and arousal on poststimulus activity, operationalizing these in various ways 33 – 35 , or has conducted modeling work on the question 36 , 37 . While this work has revealed useful insights into the relationship between ongoing brain states and stimulus processing, the specific electrophysiological variables which exhibit relationships between their ongoing and evoked dynamics are not known, nor are the form of these relationships (e.g., positive versus negative correlation) clear.…”

Neural excitability and sensory input determine intensity perception with opposing directions in initial cortical responses

“…However, it remains an open question whether the observed excitability changes reflect local or global neural dynamics. Although there is initial evidence that cortical excitability may be organized temporally in a scale-free manner (Stephani et al, 2020), which may reflect an embedding into global critical-state dynamics (Beggs & Plenz, 2003; Palva et al, 2013; Avramiea et al, 2020), future work has to examine the spatial organization of excitability more specifically across different somatotopic projections in primary sensory areas as well as across diverse brain regions.…”

Amplitude and phase coupling optimize information transfer between brain networks that function at criticality

“…Interestingly, at the same balance we find scale-free distributions of neuronal avalanches—another hallmark of critical brain dynamics 23 . Both neuronal avalanches 28–30 and critical oscillations 26 have been associated with the widest dynamic range to stimuli. This suggests that at the critical point, networks might be most responsive to inputs coming from distant brain areas.…”