Different Roles of Direct and Indirect Frontoparietal Pathways for Individual Working Memory Capacity

Abstract

The ability to temporarily store and manipulate information in working memory is a hallmark of human intelligence and differs considerably across individuals, but the structural brain correlates underlying these differences in working memory capacity (WMC) are only poorly understood. In two separate studies, diffusion MRI data and WMC scores were collected for 70 and 109 healthy individuals. Using a combination of probabilistic tractography and network analysis of the white matter tracts, we examined whether structural brain network properties were predictive of individual WMC. Converging evidence from both studies showed that lateral prefrontal cortex and posterior parietal cortex of high-capacity individuals are more densely connected compared with low-capacity individuals. Importantly, our network approach was further able to dissociate putative functional roles associated with two different pathways connecting frontal and parietal regions: a corticocortical pathway and a subcortical pathway. In Study 1, where participants were required to maintain and update working memory items, the connectivity of the direct and indirect pathway was predictive of WMC. In contrast, in Study 2, where participants were required to maintain working memory items without updating, only the connectivity of the direct pathway was predictive of individual WMC. Our results suggest an important dissociation in the circuitry connecting frontal and parietal regions, where direct frontoparietal connections might support storage and maintenance, whereas subcortically mediated connections support the flexible updating of working memory content.Key words: basal ganglia; diffusion MRI; network analysis; prefrontal cortex; working memory capacity IntroductionHumans and nonhuman primates have developed a remarkable capacity to store and manipulate information "online." This process, referred to as working memory, is fundamental for many perceptual and cognitive abilities (Fukuda et al., 2010;Johnson et al., 2013) and is closely linked to general intelligence (Conway et al., 2003). The capacity of working memory (WMC) varies substantially across individuals (Cowan, 2001;Luck and Vogel, 2013), but the neural correlates of individual differences in WMC are at present only poorly understood.Recent studies using fMRI and EEG suggest that differences in WMC can be partly attributed to differences in attentional processes involved in the selection of relevant and filtering of irrelevant information (Vogel and Machizawa, 2004;McNab and Klingberg, 2008;Luck and Vogel, 2013). Irrelevant information consumes unnecessary capacity, and it has been shown that lowcapacity individuals tend to encode irrelevant information to a greater extent than high-capacity individuals (Vogel et al., 2005;Luck and Vogel, 2013 Significance StatementUsing diffusion MRI and network analysis, we found that the capacity of healthy individuals to temporally maintain information in working memory was related to a cortical pathway connecting frontal and parietal regions. The up...

Assessing the Driver’s Current Level of Working Memory Load with High Density Functional Near-infrared Spectroscopy: A Realistic Driving Simulator Study

“…We also recorded task-related behavior, driving behavior, and peripheral physiology to simultaneously assess working memory load with measures other than fNIRS recordings. Our hypothesis is that neural activation patterns in the pre-frontal and parietal areas will be the relevant features for estimating the level of working memory load since previous laboratory studies have shown that these areas are known to be involved in working memory-related processing (LaBar et al, 1999; Wagner et al, 2005; Postle, 2006; Koenigs et al, 2009; Salazar et al, 2012; Lara and Wallis, 2015; Ekman et al, 2016). …”

Abnormal distraction and load‐specific connectivity during working memory in cognitively normal Parkinson's disease

“…Preserved connectivity within this circuit in the PD group contrasted with left middle frontal (BA 6)—right inferior parietal cortex connectivity, which was upregulated during distraction. Thus, opposite frontoparietal connectivity patterns were observed in homologous circuits that are pivotal for WM, which is compatible with compensation in PD when the demands on focused spatial attention are amplified (Ekman et al, ). Likewise, in both groups right putamen and bilateral precuneus couplings were stronger in the absence of distraction, possibly reflecting preserved updating (McNab & Klingberg, ) and storage (Galeano Weber et al, ) in PD when focusing attention is easier.…”

“…This loss in connectivity resembled PD patients' loss in coupling of a similar circuit (left putamen—BA 8) when encoding during distraction. Both findings suggest that frontostriatal dysfunction disrupts flexible updating of WM (Ekman et al, ; Hazy et al, ; McNab & Klingberg, ). Although load‐related putamen coupling in the control group was found with more distributed prefrontal regions (BA 8, DLPFC), this finding may reflect the higher demands of updating four relevant shapes in comparison to arrays of the same size that contain two relevant items and two distractors (Badre & Nee, ; Linden et al, ; Nee & Brown, ).…”

“…This result aligns with the basal ganglia's role in updating cognitive goals in concert with a region of the dorsal attention network (DAN) that supports top‐down visuospatial attention (Braga, Wilson, Sharp, Wise, & Leech, ; Corbetta, Patel, & Shulman, ). This frontostriatal circuit appears to set the system to selectively attend, thereby preventing undue interference from irrelevant stimuli (Ekman et al, ; Hazy et al, ; McNab & Klingberg, ). In contrast, PD participants failed to increase putamen—superior frontal cortex connectivity during distraction, despite advance cues signaling that an array would contain irrelevant shapes.…”

“…To identify sources of brain dysfunction, distraction and memory‐load modulated connectivity were studied for encoding and retrieval phases of the task. Owing to aberrant frontostriatal activation in PD during WM (Lewis et al, ; Marklund et al, ; Poston et al, ), we hypothesized that during encoding, context‐dependent connectivity of regions within the striatal‐thalamocortical circuit would be abnormal in PD during distraction (Ekman, Fiebach, Melzer, Tittgemeyer, & Derrfuss, ; McNab & Klingberg, ) and higher memory loads, which impose a greater burden on WM (Hazy et al, ; Nee & Brown, ). If dopamine depletion in PD disrupts the fidelity by which information is encoded into WM (Cools & D'Esposito, ), we predicted that during retrieval both distraction‐ and load‐dependent connectivity would be altered in the superior parietal cortex, which represents the contents of visual WM (Christophel, Cichy, Hebart, & Haynes, ; Galeano Weber, Peters, Hahn, Bledowski, & Fiebach, ).…”