Summary The ability to focus on and understand one talker in a noisy social environment is a critical social-cognitive capacity, whose underlying neuronal mechanisms are unclear. We investigated the manner in which speech streams are represented in brain activity and the way that selective attention governs the brain’s representation of speech using a ‘Cocktail Party’ Paradigm, coupled with direct recordings from the cortical surface in surgical epilepsy patients. We find that brain activity dynamically tracks speech streams using both low frequency phase and high frequency amplitude fluctuations, and that optimal encoding likely combines the two. In and near low level auditory cortices, attention ‘modulates’ the representation by enhancing cortical tracking of attended speech streams, but ignored speech remains represented. In higher order regions, the representation appears to become more ‘selective,’ in that there is no detectable tracking of ignored speech. This selectivity itself seems to sharpen as a sentence unfolds.
Analyses of intrinsic fMRI BOLD signal fluctuations reliably reveal correlated and anticorrelated functional networks in the brain. Since the BOLD signal is an indirect measure of neuronal activity, and anticorrelations can be introduced by preprocessing steps such as global signal regression (GSR), the neurophysiological significance of correlated and anticorrelated BOLD fluctuations is a source of debate. Here, we address this question by examining the correspondence between the spatial organization of correlated BOLD fluctuations and correlated fluctuations in electrophysiological high gamma power (HGP) signals recorded directly from the cortical surface of 5 patients. We demonstrate that both positive and negative BOLD correlations have neurophysiological correlates reflected in fluctuations of spontaneous neuronal activity. Although applying GSR to BOLD signals results in some BOLD anticorrelations that are not apparent in the ECoG data, it enhances the neuronal-hemodynamic correspondence overall. Together, these findings provide support for the neurophysiological fidelity of BOLD correlations and anticorrelations.
Electrophysiological mass potentials show complex spectral changes upon neuronal activation. However, it is unknown to what extent these complex band-limited changes are interrelated or, alternatively, reflect separate neuronal processes. To address this question, intracranial electrocorticograms (ECoG) responses were recorded in patients engaged in visuomotor tasks. We found that in the 10- to 100-Hz frequency range there was a significant reduction in the exponent χ of the 1/ fχ component of the spectrum associated with neuronal activation. In a minority of electrodes showing particularly high activations the exponent reduction was associated with specific band-limited power modulations: emergence of a high gamma (80–100 Hz) and a decrease in the alpha (9–12 Hz) peaks. Importantly, the peaks' height was correlated with the 1/ fχ exponent on activation. Control simulation ruled out the possibility that the change in 1/ fχ exponent was a consequence of the analysis procedure. These results reveal a new global, cross-frequency (10–100 Hz) neuronal process reflected in a significant reduction of the power spectrum slope of the ECoG signal.
Adaptive brain function is characterized by dynamic interactions within and between neuronal circuits, often occurring at the time scale of milliseconds. These complex interactions between adjacent and noncontiguous brain areas depend on a functional architecture that is maintained even in the absence of input. Functional MRI studies carried out during rest (R-fMRI) suggest that this architecture is represented in low-frequency (<0.1 Hz) spontaneous fluctuations in the blood oxygen level-dependent signal that are correlated within spatially distributed networks of brain areas. These networks, collectively referred to as the brain's intrinsic functional architecture, exhibit a remarkable correspondence with patterns of task-evoked coactivation as well as maps of anatomical connectivity. Despite this striking correspondence, there is no direct evidence that this intrinsic architecture forms the scaffold that gives rise to faster processes relevant to information processing and seizure spread. Here, we demonstrate that the spatial distribution and magnitude of temporally correlated low-frequency fluctuations observed with R-fMRI during rest predict the pattern and magnitude of corticocortical evoked potentials elicited within 500 ms after single-pulse electrical stimulation of the cerebral cortex with intracranial electrodes. Across individuals, this relationship was found to be independent of the specific regions and functional systems probed. Our findings bridge the immense divide between the temporal resolutions of these distinct measures of brain function and provide strong support for the idea that the low-frequency signal fluctuations observed with R-fMRI maintain and update the intrinsic architecture underlying the brain's repertoire of functional responses.
iELVis promises to speed the progress and enhance the robustness of intracranial electrode research. The software and extensive tutorial materials are freely available as part of the EpiSurg software project: https://github.com/episurg/episurg.
The cerebral cortex is composed of subregions whose functional specialization is largely determined by their incoming and outgoing connections with each other. In the present study, we asked which cortical regions can exert the greatest influence over other regions and the cortical network as a whole. Previous research on this question has relied on coarse anatomy (mapping large fiber pathways) or functional connectivity (mapping inter-regional statistical dependencies in ongoing activity). Here we combined direct electrical stimulation with recordings from the cortical surface to provide a novel insight into directed, inter-regional influence within the cerebral cortex of awake humans. These networks of directed interaction were reproducible across strength thresholds and across subjects. Directed network properties included (1) a decrease in the reciprocity of connections with distance; (2) major projector nodes (sources of influence) were found in peri-Rolandic cortex and posterior, basal and polar regions of the temporal lobe; and (3) major receiver nodes (receivers of influence) were found in anterolateral frontal, superior parietal, and superior temporal regions. Connectivity maps derived from electrical stimulation and from resting electrocorticography (ECoG) correlations showed similar spatial distributions for the same source node. However, higher-level network topology analysis revealed differences between electrical stimulation and ECoG that were partially related to the reciprocity of connections. Together, these findings inform our understanding of large-scale corticocortical influence as well as the interpretation of functional connectivity networks.
The brain’s spontaneous, intrinsic activity is increasingly being shown to reveal brain function, delineate large scale brain networks, and diagnose brain disorders. One of the most studied and clinically utilized types of intrinsic brain activity are oscillations in the electrocorticogram (ECoG), a relatively localized measure of cortical synaptic activity. Here we objectively characterize the types of ECoG oscillations commonly observed over particular cortical areas when an individual is awake and immobile with eyes closed, using a surface-based cortical atlas and cluster analysis. Both methods show that [1] there is generally substantial variability in the dominant frequencies of cortical regions and substantial overlap in dominant frequencies across the areas sampled (primarily lateral central, temporal, and frontal areas), [2] theta (4–8 Hz) is the most dominant type of oscillation in the areas sampled with a mode around 7 Hz, [3] alpha (8–13 Hz) is largely limited to parietal and occipital regions, and [4] beta (13–30 Hz) is prominent peri-Rolandically, over the middle frontal gyrus, and the pars opercularis. In addition, the cluster analysis revealed seven types of ECoG spectral power densities (SPDs). Six of these have peaks at 3, 5, 7 (narrow), 7 (broad), 10, and 17 Hz, while the remaining cluster is broadly distributed with less pronounced peaks at 8, 19, and 42 Hz. These categories largely corroborate conventional sub-gamma frequency band distinctions (delta, theta, alpha, and beta) and suggest multiple sub-types of theta. Finally, we note that gamma/high gamma activity (30+ Hz) was at times prominently observed, but was too infrequent and variable across individuals to be reliably characterized. These results should help identify abnormal patterns of ECoG oscillations, inform the interpretation of EEG/MEG intrinsic activity, and provide insight into the functions of these different oscillations and the networks that produce them. Specifically, our results support theories of the importance of theta oscillations in general cortical function, suggest that alpha activity is primarily related to sensory processing/attention, and demonstrate that beta networks extend far beyond primary sensorimotor regions.
Evidence for intrinsic functional connectivity (FC) within the human brain is largely from neuroimaging studies of hemodynamic activity. Data are lacking from anatomically precise electrophysiological recordings in the most widely studied nodes of human brain networks. Here we used a combination of fMRI and electrocorticography (ECoG) in five human neurosurgical patients with electrodes in the canonical "default" (medial prefrontal and posteromedial cortex), "dorsal attention" (frontal eye fields and superior parietal lobule), and "frontoparietal control" (inferior parietal lobule and dorsolateral prefrontal cortex) networks. In this unique cohort, simultaneous intracranial recordings within these networks were anatomically matched across different individuals. Within each network and for each individual, we found a positive, and reproducible, spatial correlation for FC measures obtained from resting-state fMRI and separately recorded ECoG in the same brains. This relationship was reliably identified for electrophysiological FC based on slow (<1 Hz) fluctuations of high-frequency broadband (70-170 Hz) power, both during wakeful rest and sleep. A similar FC organization was often recovered when using lower-frequency (1-70 Hz) power, but anatomical specificity and consistency were greatest for the high-frequency broadband range. An interfrequency comparison of fluctuations in FC revealed that high and low-frequency ranges often temporally diverged from one another, suggesting that multiple neurophysiological sources may underlie variations in FC. Together, our work offers a generalizable electrophysiological basis for intrinsic FC and its dynamics across individuals, brain networks, and behavioral states. The study of human brain networks during wakeful "rest", largely with fMRI, is now a major focus in both cognitive and clinical neuroscience. However, little is known about the neurophysiology of these networks and their dynamics. We studied neural activity during wakeful rest and sleep within neurosurgical patients with directly implanted electrodes. We found that network activity patterns showed striking similarities between fMRI and direct recordings in the same brains. With improved resolution of direct recordings, we also found that networks were best characterized with specific activity frequencies and that different frequencies show different profiles of within-network activity over time. Our work clarifies how networks spontaneously organize themselves across individuals, brain networks, and behavioral states.
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