Functional and structural architecture of the human dorsal frontoparietal attention network

Abstract

The dorsal frontoparietal attention network has been subdivided into at least eight areas in humans. However, the circuitry linking these areas and the functions of different circuit paths remain unclear. Using a combination of neuroimaging techniques to map spatial representations in frontoparietal areas, their functional interactions, and structural connections, we demonstrate different pathways across human dorsal frontoparietal cortex for the control of spatial attention. Our results are consistent with these pathways computing object-centered and/or viewer-centered representations of attentional priorities depending on task requirements. Our findings provide an organizing principle for the frontoparietal attention network, where distinct pathways between frontal and parietal regions contribute to multiple spatial representations, enabling flexible selection of behaviorally relevant information.parietal cortex | frontal cortex | DTI | fMRI | connectivity V isual scenes usually contain many different objects, which cannot all be processed simultaneously because of the limited capacity of the visual system. Attention mechanisms are thus needed to select the most behaviorally relevant information for further processing. Previous studies have demonstrated activations over large portions of dorsal frontoparietal cortex during a variety of selective attention tasks (1, 2). In humans, these regions include intraparietal sulcus areas 1-5 (IPS1-IPS5) and superior parietal lobule area 1 (SPL1) in posterior parietal cortex (PPC), defined by spatial topographic mapping (3, 4), as well as the frontal eye field (FEF) and the putative human supplementary eye field (SEF) in frontal cortex (Fig. S1). Although these areas are commonly conceptualized as a frontoparietal attention network, the circuitry linking areas, the functions of different circuit paths, and the different roles of individual areas in representing attentional priorities remain unclear.Because everyday actions rely on representations of attentional priorities in egocentric (gaze-centered, body-centered) and allocentric (object-centered, world-centered) spatial reference frames (5-9)-for example, to pick up a coffee cup, we must know where the cup is relative to our body, as well as where the handle is relative to the cup-we need to flexibly specify and read out attentional priorities in different reference frames. However, human neuroimaging studies have largely focused on gaze-centered representations and have been relatively unsuccessful in finding representations in other spatial reference frames, perhaps because they have focused on visual cortex (e.g., refs. 10 and 11). In frontoparietal cortex, the topographic organization of IPS1-5, SPL1, and FEF suggests that they contain spatial representations at least in egocentric reference frames (3,12,13). In contrast, human SEF lacks a clear topography ( Fig. S1; refs. 14-16). Macaque SEF also lacks a clear topography (17,18), although macaque SEF neurons have been shown to represent space in gaze-centered as...

Trial History Effects in the Ventral Attentional Network

“…This prioritization is widely believed to reflect the biasing of perceptual processing systems to favor material that will support current processing goals at the expense of material that will not; these biases have their source in a broadly distributed network of frontal and parietal regions (Desimone & Duncan, 1995). A dorsal attentional network that includes the frontal eye-fields (FEF) and the superior aspect of the intra-parietal sulcus (IPS) maintains attentional biases towards information that supports current task goals (Kincade et al, 2005;Szczepanski et al, 2010Szczepanski et al, , 2013Kastner et al, 2007). Successful attentional function, however, requires not only that biases towards task-relevant material be generally maintained across task conditions; but also they will interact with the specific context of the current stimulus environment.…”

“…Attentional biases in favor of task-relevant information are generally thought to be instantiated and maintained by the dorsal attentional system (Kincade et al, 2005;Szczepanski et al, 2010Szczepanski et al, , 2013Kastner et al, 2007;Zhou & Desimone, 2011). Trial history effects have been found within the dorsal attentional systems of both human and non-human primates (Kristjansson et al, 2007;Bichot & Schall, 1999;2002); this system is generally more challenged (or less efficient) if the specific stimulus characteristics consistent with task goals vary from trial to trial.…”

Variation in functional connectivity along anterior-to-posterior intraparietal sulcus, and relationship with age across late childhood and adolescence

“…In these studies, structural connectivity is defined using probabilistic tractography to determine the likelihood that two regions are joined by a direct white matter pathway. With regards to the IPS, posterior regions show preferential connectivity with dorsal and ventral visual regions (Bray et al, 2013b;Greenberg et al, 2012), while anterior regions show more probable connections to prefrontal and pre-motor regions (Bray et al, 2013b;Mars et al, 2011;Szczepanski et al, 2013). Lesion studies (Vandenberghe et al, 2012) and task activation and connectivity studies (Hutchinson et al, 2015) further support functional sub-divisions along the IPS.…”

“…These regions show differences in functional responses across tasks (Bray et al, 2013a;Sheremata et al, 2010;Silver and Kastner, 2009;Swisher et al, 2007;Szczepanski et al, 2013), and differential white matter structural connectivity to visual regions and parts of the dorsal attention network (Bray et al, 2013b;Greenberg et al, 2012;Szczepanski et al, 2013). In these studies, structural connectivity is defined using probabilistic tractography to determine the likelihood that two regions are joined by a direct white matter pathway.…”

Using the Force: STEM Knowledge and Experience Construct Shared Neural Representations of Engineering Concepts

“…Specifically, we find that as participants develop a more categorical representational space (as indicated by behavioral DSMs), a dorsal-to-ventral shift occurs in the neural informational networks representing those conceptual categories. This shift may be NEURAL REPRESENTATIONS OF ENGINEERING CONCEPTS 34 indicative of a transition in attention from the visuospatial configuration of features within a given image, processed by the dorsal stream (Haxby et al, 1991;Szczepanski, Pinsk, Douglas, Kastner, & Saalmann, 2013), toward a focus on higher-level categorization across the image set (Chi et al, 1981), which is associated with processing in the ventral stream (Kravitz et al, 2011;McGugin, Newton, Gore, & Gauthier, 2014;Tarr & Gauthier, 2000). Additionally, within the ventral stream, more anterior informational networks more strongly reflect the learned categorical structure for both groups of participants.…”