Corticocortical Evoked Potentials Reveal Projectors and Integrators in Human Brain Networks

Abstract

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.

Structural and functional integration between dorsal and ventral language streams as revealed by blunt dissection and direct electrical stimulation

“…2 and 6). These anatomical and functional results also confirm previous evoked-potentials data, which demonstrated a strong functional link between the peri-rolandic cortex, the posterior, basal and polar regions of the temporal lobe (output nodes), and the anterolateral frontal, superior parietal, and superior temporal regions (input nodes) [Keller et al, 2014].…”

“…The primary implication of the frontal lobe in this circuitry has already been hypothesized by previous electrophysiological data based on cortico-cortical evoked potentials, showing that the stimulation of frontal language regions elicits stronger electrical responses in posterior language regions than vice versa [Keller et al, 2014;Matsumoto et al, 2004]. Moreover, we found a complete representation of all the main clusters of language components (i.e., semantic, phonological, articulatory, verbal planning, and execution) solely in the frontal lobe.…”

Mapping human brain networks with cortico-cortical evoked potentials

“…Group analysis suggests that regions in the lateral prefrontal and superior parietal-regions implicated in the default mode network [93,94]-demonstrate strong indegree with net inward flow, whereas the pre-central, post-central and posterior temporal regions demonstrate strong outdegree with net outward flow. Moreover, regions involved in motor or language function-defined clinically by behavioural disruption elicited by high-frequency stimulation at specific electrodes-demonstrated strong outdegree with net outward flow [95,96]. These results provide evidence of consistent directional information flow between regions of the neocortex.…”

“…10% for long-range connections) and the proportion of reciprocal connections in the brain decreases as separation distance increases. By comparing our data against a null model, we determined that the level of reciprocity in experimental data was higher than expected for short-range connections but no different than chance for long-range connections [95].…”

“…Here, functional connectivity was quantified by the temporal correlation of low-frequency (0.1-1 Hz) fluctuations of power within the high gamma (70-150 Hz) band, which, in turn, is thought to reflect aggregate spiking activity [104][105][106]. Regions exhibiting bidirectional CCEPs exhibited 40% stronger resting functional connectivity than those exhibiting unidirectional or no significant CCEP [95]. These data support the notion that the degree of reciprocal cortico-cortical connections predicts underlying functional connectivity.…”