Attention Networks and the Intrinsic Network Structure of the Human Brain

Abstract

Attention network theory states that attention is not a unified construct but consists of three independent systems that are supported by separable distributed networks: an alerting network to deploy attentional resources in anticipation of upcoming events, an orienting network to direct attention to a cued location, and a control network to select relevant information at the expense of concurrently available information. Ample behavioral and neuroimaging evidence supports the dissociation of the three attention domains. The strong assumption that each attentional system is realized through a separable network, however, raises the question how these networks relate to the intrinsic network structure of the brain. Our understanding of brain networks has advanced majorly in the past years due to the increasing focus on brain connectivity. It is well established that the brain is intrinsically organized into several large-scale networks whose modular structure persists across task states. Existing proposals on how the presumed attention networks relate to intrinsic networks rely mostly on anecdotal and partly contradictory arguments. We addressed this issue by mapping different attention networks with highest spatial precision at the level of cifti-grayordinates. Resulting group maps were compared to the group-level topology of 23 intrinsic networks which we reconstructed from the same participants' resting state fMRI data. We found that all attention domains recruited multiple and partly overlapping intrinsic networks and converged in the dorsal fronto-parietal and midcingulo-insular network. While we observed a preference of each attentional domain for its own set of intrinsic networks, implicated networks did not match well to those proposed in the literature. Our results indicate a necessary refinement of the attention network theory.

Systems-level decoding reveals the cognitive and behavioral profile of the human intraparietal sulcus

“…On the term-level, we also found associations that suggest an involvement of the IPS-centered attention system in both spatial orienting and selective executive attention. These findings support previous suggestions that the FPN interacts closely with the DAN during visuospatial attention (Spreng et al, 2010;Dixon et al, 2017Dixon et al, , 2018 and that different attention functions dissociate less across ICN than previously thought (Markett et al, 2022).…”

“…We used whole-brain seed-based resting-state functional connectivity (RSFC) in combination with a cortical parcellation (Huang et al, 2022) to identify cortical regions with functional coupling to the six IPS seed regions. We utilized resting-state data (∼11 min, TR = 800 ms, 2 mm cubic voxels) from a sample of N = 84 healthy young adults from a previous study (Markett et al, 2022), acquired with the HCP's pulse sequences (Harms et al, 2018) and preprocessed with HCP's minimal processing pipeline (Glasser et al, 2013) including noise-removal with ICA-Fix. Mean timeseries were extracted from each seed region's set of voxels and regressed against the time courses from all other voxels within the brain mask.…”

“…Cortical regions overlapping with any seed region were excluded from the lists. Full details on all acquisition and preprocessing steps are described in Markett et al (2022).…”

“…Both systems showed nearly identical patterns of overlaps with the frontoparietal DAN and the FPN across both hemispheres. While both ICNs feature the IPS as putative hub (Fox et al, 2005;Dosenbach et al, 2007;Power et al, 2011), previous work has rather focused on functional differences between the two networks (Vincent et al, 2008;Spreng et al, 2010;Fedorenko et al, 2013;Cole et al, 2014), for example in regard to attention (Corbetta and Shulman, 2002;Corbetta et al, 2008;Vossel et al, 2014;Markett et al, 2022), cognitive control (Cole and Schneider, 2007;Power et al, 2011;Marek and Dosenbach, 2018), cognitive flexibility (Cohen et al, 2014), but also to working memory and numeric cognition (Champod and Petrides, 2010;Fedorenko et al, 2013;Markett et al, 2018;Chang et al, 2019). In this light, the almost identical coactivations pattern of the IPS with both ICN during memory and numeric cognition suggests more similarity between the two ICN than previously thought.…”

“…This engagement extends to visuospatial processes including navigation and the perception of shapes and motions (Salillas et al, 2009;Tark and Curtis, 2013;Binkofski et al, 2016;Meier et al, 2018;Schultz and Bülthoff, 2019;Li and Shigemasu, 2021). Finally, the IPS plays an important role in the interplay of top-down and bottom-up guided pull of attentional processes (Corbetta et al, 1998(Corbetta et al, , 2008Corbetta and Shulman, 2002;Katsuki and Constantinidis, 2014;Connolly et al, 2016;Markett et al, 2022). Visuomotor coordination and visuospatial attentional processes are closely tied to saccade planning, in which the IPS is also involved (Corbetta et al, 1998;Grosbras et al, 2005;Morris et al, 2007;Baltaretu et al, 2020).…”