Scale-free fluctuations are ubiquitous in behavioral performance and neuronal activity. In time scales from seconds to hundreds of seconds, psychophysical dynamics and the amplitude fluctuations of neuronal oscillations are governed by power-law-form longrange temporal correlations (LRTCs). In millisecond time scales, neuronal activity comprises cascade-like neuronal avalanches that exhibit power-law size and lifetime distributions. However, it remains unknown whether these neuronal scaling laws are correlated with those characterizing behavioral performance or whether neuronal LRTCs and avalanches are related. Here, we show that the neuronal scaling laws are strongly correlated both with each other and with behavioral scaling laws. We used source reconstructed magneto-and electroencephalographic recordings to characterize the dynamics of ongoing cortical activity. We found robust power-law scaling in neuronal LRTCs and avalanches in resting-state data and during the performance of audiovisual threshold stimulus detection tasks. The LRTC scaling exponents of the behavioral performance fluctuations were correlated with those of concurrent neuronal avalanches and LRTCs in anatomically identified brain systems. The behavioral exponents also were correlated with neuronal scaling laws derived from a resting-state condition and with a similar anatomical topography. Finally, despite the difference in time scales, the scaling exponents of neuronal LRTCs and avalanches were strongly correlated during both rest and task performance. Thus, long and short time-scale neuronal dynamics are related and functionally significant at the behavioral level. These data suggest that the temporal structures of human cognitive fluctuations and behavioral variability stem from the scaling laws of individual and intrinsic brain dynamics.spontaneous activity | threshold detection | criticality H uman cognitive and behavioral performance is highly variable and exhibits slow fluctuations that are salient in continuous performance tasks (CPTs) (1). Psychophysical time series have been known since the early 1950s to be nonrandomly clustered (2), and later studies have shown that hit-rate and/or reaction-time fluctuations in CPT data are fractal and power-law autocorrelated across hundreds of seconds (3-9). The biological origins and relevance of these dynamic, however, remain unclear (10, 11).Similar to those in behavioral performance, the fluctuations of collective neuronal activity at many levels of the nervous system are scale-free and governed by power-law scaling laws. On short time scales (10 −3 −10 −1 s), negative deflections in local field potentials form spatiotemporal cascades of activity, "neuronal avalanches" (32-34), the size and lifetime distributions of which are power laws akin to those of a critical branching process (33). Neuronal avalanches characterize spontaneous neuronal network activity in organotypic cultures (32), brain slices in vitro (35), and monkey (34) and human cortex (36) in vivo. In monkey cortex, the avalanche...
When combined with source modeling, magneto- (MEG) and electroencephalography (EEG) can be used to study long-range interactions among cortical processes non-invasively. Estimation of such inter-areal connectivity is nevertheless hindered by instantaneous field spread and volume conduction, which artificially introduce linear correlations and impair source separability in cortical current estimates. To overcome the inflating effects of linear source mixing inherent to standard interaction measures, alternative phase- and amplitude-correlation based connectivity measures, such as imaginary coherence and orthogonalized amplitude correlation have been proposed. Being by definition insensitive to zero-lag correlations, these techniques have become increasingly popular in the identification of correlations that cannot be attributed to field spread or volume conduction. We show here, however, that while these measures are immune to the direct effects of linear mixing, they may still reveal large numbers of spurious false positive connections through field spread in the vicinity of true interactions. This fundamental problem affects both region-of-interest-based analyses and all-to-all connectome mappings. Most importantly, beyond defining and illustrating the problem of spurious, or "ghost" interactions, we provide a rigorous quantification of this effect through extensive simulations. Additionally, we further show that signal mixing also significantly limits the separability of neuronal phase and amplitude correlations. We conclude that spurious correlations must be carefully considered in connectivity analyses in MEG/EEG source space even when using measures that are immune to zero-lag correlations.
Frequency tagging has been widely used to study the role of visual selective attention. Presenting a visual stimulus flickering at a specific frequency generates so-called steady-state visually evoked responses. However, frequency tagging is mostly done at lower frequencies (<30 Hz). This produces a visible flicker, potentially interfering with both perception and neuronal oscillations in the theta, alpha and beta band. To overcome these problems, we used a newly developed projector with a 1440 Hz refresh rate allowing for frequency tagging at higher frequencies. We asked participants to perform a cued spatial attention task in which imperative pictorial stimuli were presented at 63 Hz or 78 Hz while measuring whole-head magnetoencephalography (MEG). We found posterior sensors to show a strong response at the tagged frequency. Importantly, this response was enhanced by spatial attention. Furthermore, we reproduced the typical modulations of alpha band oscillations, i.e., decrease in the alpha power contralateral to the attentional cue. The decrease in alpha power and increase in frequency tagged signal with attention correlated over subjects. We hereby provide proof-of-principle for the use of high-frequency tagging to study sensory processing and neuronal excitability associated with attention.
A growing body of evidence suggests that the neuronal dynamics are poised at criticality. Neuronal avalanches and long-range temporal correlations (LRTCs) are hallmarks of such critical dynamics in neuronal activity and occur at fast (subsecond) and slow (seconds to hours) timescales, respectively. The critical dynamics at different timescales can be characterized by their power-law scaling exponents. However, insight into the avalanche dynamics and LRTCs in the human brain has been largely obtained with sensor-level MEG and EEG recordings, which yield only limited anatomical insight and results confounded by signal mixing. We investigated here the relationship between the human neuronal dynamics at fast and slow timescales using both source-reconstructed MEG and intracranial stereotactical electroencephalography (SEEG). Both MEG and SEEG revealed avalanche dynamics that were characterized parameter-dependently by power-law or truncated-power-law size distributions. Both methods also revealed robust LRTCs throughout the neocortex with distinct scaling exponents in different functional brain systems and frequency bands. The exponents of power-law regimen neuronal avalanches and LRTCs were strongly correlated across subjects. Qualitatively similar power-law correlations were also observed in surrogate data without spatial correlations but with scaling exponents distinct from those of original data. Furthermore, we found that LRTCs in the autonomous nervous system, as indexed by heart-rate variability, were correlated in a complex manner with cortical neuronal avalanches and LRTCs in MEG but not SEEG. These scalp and intracranial data hence show that power-law scaling behavior is a pervasive but neuroanatomically inhomogeneous property of neuronal dynamics in central and autonomous nervous systems.
Fluctuations with power-law scaling and long-range temporal correlations (LRTCs) are characteristic to human psychophysical performance. Systems operating in a critical state exhibit such LRTCs, but phenomenologically similar fluctuations and LRTCs may also be caused by slow decay of the system’s memory without the system being critical. Theoretically, criticality endows the system with the greatest representational capacity and flexibility in state transitions. Without criticality, however, slowly decaying system memory would predict inflexibility. We addressed these contrasting predictions of the ‘criticality’ and ‘long-memory’ candidate mechanisms of human behavioral LRTCs by using a Go/NoGo task wherein the commission errors constitute a measure of cognitive flexibility. Response time (RT) fluctuations in this task exhibited power-law frequency scaling, autocorrelations, and LRTCs. We show here that the LRTC scaling exponents, quantifying the strength of long-range correlations, were negatively correlated with the commission error rates. Strong LRTCs hence parallel optimal cognitive flexibility and, in line with the criticality hypothesis, indicate a functionally advantageous state. This conclusion was corroborated by a positive correlation between the LRTC scaling exponents and executive functions measured with the Rey-Osterrieth Complex Figure test. Our results hence support the notion that LRTCs arise from critical dynamics that is functionally significant for human cognitive performance.
Inter-areal synchronization of neuronal oscillations at frequencies below ~100 Hz is a pervasive feature of neuronal activity and is thought to regulate communication in neuronal circuits. In contrast, faster activities and oscillations have been considered to be largely local-circuit-level phenomena without large-scale synchronization between brain regions. We show, using human intracerebral recordings, that 100–400 Hz high-frequency oscillations (HFOs) may be synchronized between widely distributed brain regions. HFO synchronization expresses individual frequency peaks and exhibits reliable connectivity patterns that show stable community structuring. HFO synchronization is also characterized by a laminar profile opposite to that of lower frequencies. Importantly, HFO synchronization is both transiently enhanced and suppressed in separate frequency bands during a response-inhibition task. These findings show that HFO synchronization constitutes a functionally significant form of neuronal spike-timing relationships in brain activity and thus a mesoscopic indication of neuronal communication per se.
Scale-free neuronal dynamics and interareal correlations are emergent characteristics of spontaneous brain activity. How such dynamics and the anatomical patterns of neuronal connectivity are mutually related in brain networks has, however, remained unclear. We addressed this relationship by quantifying the network colocalization of scale-free neuronal activity—both neuronal avalanches and long-range temporal correlations (LRTCs)—and functional connectivity (FC) by means of intracranial and noninvasive human resting-state electrophysiological recordings. We found frequency-specific colocalization of scale-free dynamics and FC so that the interareal couplings of LRTCs and the propagation of neuronal avalanches were most pronounced in the predominant pathways of FC. Several control analyses and the frequency specificity of network colocalization showed that the results were not trivial by-products of either brain dynamics or our analysis approach. Crucially, scale-free neuronal dynamics and connectivity also had colocalized modular structures at multiple levels of network organization, suggesting that modules of FC would be endowed with partially independent dynamic states. These findings thus suggest that FC and scale-free dynamics—hence, putatively, neuronal criticality as well—coemerge in a hierarchically modular structure in which the modules are characterized by dense connectivity, avalanche propagation, and shared dynamic states.
Spatial attention provides a mechanism for, respectively, enhancing relevant and suppressing irrelevant information. While it is well established that attention modulates oscillations in the alpha band, it remains unclear if alpha oscillations are involved in directly modulating the neuronal excitability associated with the allocation of spatial attention. In this study, in humans, we utilized a novel broadband frequency (60-70 Hz) tagging paradigm to quantify neuronal excitability in relation to alpha oscillations in a spatial attention paradigm. We used magnetoencephalography to characterize ongoing brain activity as it allows for localizing the sources of both the alpha and frequency tagging responses. We found that attentional modulation of alpha power and the frequency tagging response are uncorrelated over trials. Importantly, the neuronal sources of the tagging response were localized in early visual cortex (V1) whereas the sources of the alpha activity were identified around parietooccipital sulcus. Moreover, we found that attention did not modulate the latency of the frequency tagged responses. Our findings point to alpha band oscillations serving a downstream gating role rather than implementing gain control of excitability in early visual regions.
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