The structural connectivity of higher order association cortices reflects human functional brain networks

Abstract

Human higher cognition arises from the main tertiary association cortices including the frontal, temporal and parietal lobes. Many studies have suggested that cortical functions must be shaped or emerge from the pattern of underlying physical (white matter) connectivity. Despite the importance of this hypothesis, there has not been a large-scale analysis of the white-matter connectivity within and between these associative cortices. Thus, we explored the pattern of intra- and inter-lobe white matter connectivity between multiple areas defined in each lobe. We defined 43 regions of interest on the lateral associative cortex cytoarchitectonically (6 regions of interest – ROIs in the frontal lobe and 17 ROIs in the parietal lobe) and anatomically (20 ROIs in the temporal lobe) on individuals' native space. The results demonstrated that intra-region connectivity for all 3 lobes was dense and graded generally. In contrary, the inter-lobe connectivity was relatively discrete and regionally specific such that only small sub-regions exhibited long-range connections to another lobe. The long-range connectivity was mediated by 6 major associative white matter tracts, consistent with the notion that these higher cognitive functions arises from brain-wide distributed connectivity. Using graph-theory network analysis we revealed five physically-connected sub-networks, which correspond directly to five known functional networks. This study provides strong and direct evidence that core functional brain networks mirror the brain's structural connectivity.

Establishing the cognitive signature of human brain networks derived from structural and functional connectivity

“…On a whole-brain scale, a recent study reported that resting-state networks were structurally connected by known white matter tracts (van den Heuvel et al 2009). Moreover, by utilizing graph-theory analysis, it has been demonstrated that brain areas with a higher degree of structural connectivity also showed a higher level of functional connectivity, supporting the proposal that functional connectivity is, at least in part, heavily constrained by the structural connectivity (Hagmann et al 2007; Honey et al 2009; Jung et al 2016). It should be noted, however, that the brain networks tested in these studies are often restricted to the primary sensory networks and/or default mode network (DMN); thus, it is important to extend the exploration to the higher cognitive networks commonly observed in task-active fMRI.…”

“…To characterize the task-independent networks, distortion-corrected DWI data [a detailed description of the tractography data has been previously published (Jung et al 2016)] and dual-echo rsfMRI data were used to define network formation within the lateral associative cortex (43 ROIs spanning frontal, lateral parietal, and temporal regions: Fig. S1; see Supplementary Information for further details).…”

“…Many studies have identified various brain networks using task-free datasets such as rsfMRI and diffusion imaging (Biswal et al 1995; Damoiseaux et al 2006; Beckmann et al 2005; Fox and Raichle 2007; van den Heuvel et al 2009; Hagmann et al 2007; Honey et al 2009; Jung et al 2016). Although these studies assert functional characteristics for the identified networks, the true cognitive functions of them are rarely probed directly.…”

“…Diffusion-weighted images were acquired in 24 healthy volunteers (11 females; mean age 25.9, range 19–47) without any record of neurological or psychiatric disorders, a dataset described previously and utilized for various tractography-related explorations (Cloutman et al 2012; Binney et al 2012; Jung et al 2016; Bajada et al 2015, 2017). All participants were right-handed, as assessed by the Edinburgh Handedness Inventory (Oldfield 1971).…”

The contribution of executive control to semantic cognition: Convergent evidence from semantic aphasia and executive dysfunction

“…Indeed, although the function of these regions appears to be at least partially distinct, recent network (path) analyses of white‐matter DTI and resting‐state fMRI data indicate that they form a ‘single functional module’ arising from their physical white‐matter connections (Jung, Cloutman, Binney, & Lambon Ralph, ). For example, although pMTG is not generally considered to be part of the multidemand network, it has strong white‐matter connectivity to lateral prefrontal regions and intraparietal sulcus (Binney, Parker, & Lambon Ralph, ; Jung et al ., ). Moreover, regions implicated in semantic control (pMTG; anterior IFG) lie between the multidemand network and the anterior temporal lobe implicated in the representation of heteromodal conceptual knowledge, in terms of both their location on the cortical surface and intrinsic functional connectivity (Davey et al ., ): If semantic control regions allow orthogonal representations of task context and conceptual knowledge to be integrated, these regions may not function normally in the face of significant disruption to the executive network.…”