W. Dale Stevens

Intrinsic architecture underlying the relations among the default, dorsal attention, and frontoparietal control networks of the human brain

Human cognition is increasingly characterized as an emergent property of interactions among distributed, functionally specialized brain networks. We recently demonstrated that the antagonistic “default” and “dorsal attention” networks—subserving internally and externally directed cognition, respectively—are modulated by a third “frontoparietal control” network that flexibly couples with either network depending on task domain. However, little is known about the intrinsic functional architecture underlying this relationship. We used graph theory to analyze network properties of intrinsic functional connectivity within and between these three large-scale networks. Task-based activation from three independent studies were used to identify reliable brain regions (“nodes”) of each network. We then examined pairwise connections (“edges”) between nodes, as defined by resting-state functional connectivity MRI. Importantly, we used a novel bootstrap resampling procedure to determine the reliability of graph edges. Furthermore, we examined both full and partial correlations. As predicted, there was a higher degree of integration within each network than between networks. Critically, whereas the default and dorsal attention networks shared little positive connectivity with one another, the frontoparietal control network showed a high degree of between-network interconnectivity with each of these networks. Furthermore, we identified nodes within the frontoparietal control network of three different types—default-aligned, dorsal attention-aligned, and dual-aligned—that we propose play dissociable roles in mediating internetwork communication. The results provide evidence consistent with the idea that the frontoparietal control network plays a pivotal gate-keeping role in goal-directed cognition, mediating the dynamic balance between default and dorsal attention networks.

Reductions in cortical activity during priming

Priming is a nonconscious form of memory in which an encounter with a stimulus influences the subsequent identification, production or classification of the same or a related stimulus. Neuroimaging studies have revealed that behavioral priming is typically accompanied by reduced activity in several cortical regions. We review recent studies that have concerned two key issues. First, specificity effects produced by changes between study and test in either the physical features of stimuli or the behavioral response reveal cortical sensitivity to the perceptual, conceptual and stimulus-to-decision mapping properties of primed items. Second, correlations between behavioral priming and activity reductions are robust across a range of tasks and procedures in prefrontal regions but not in posterior regions. On the basis of these recent studies, we suggest that the reduction in cortical activity during priming involves at least two different mechanisms.

Correlated Low-Frequency BOLD Fluctuations in the Resting Human Brain Are Modulated by Recent Experience in Category-Preferential Visual Regions

The resting brain is associated with significant intrinsic activity fluctuations, such as the correlated low-frequency (LF) blood oxygen level-dependent (BOLD) fluctuations measured by functional magnetic resonance imaging. Despite a recent expansion of studies investigating resting-state LF-BOLD correlations, their nature and function are poorly understood. A major constraint on LF-BOLD correlations appears to be stable properties of anatomic connectivity. There is also evidence that coupling can be modulated by recent or ongoing task performance, suggesting that certain components of correlated dynamics are malleable on short timescales. Here, we compared activity during extended periods of rest following performance of 2 distinct cognitive tasks using different categories of visual stimuli-faces and complex scenes. Prolonged exposure to these distinct categories of visual information caused frontal networks to couple differentially with posterior category-preferential visual regions during subsequent periods of rest. In addition, we report preliminary evidence suggesting that conditions exist in which the degree of modulation of LF-BOLD correlations predicts subsequent memory. The finding that resting-state LF-BOLD correlations are modulated by recent experience in functionally specific brain regions engaged during prior task performance clarifies their role as a dynamic phenomenon which may be involved in mnemonic processes.

A Neural Mechanism Underlying Memory Failure in Older Adults

Older adults have reduced memory, primarily for recall, but also for recognition (Craik and McDowd, 1987), particularly for unfamiliar faces (Bartlett et al., 1989). Behavioral studies have shown that age-related memory declines are due in part to distraction from impaired inhibition of task-irrelevant input during encoding (Healey et al., 2008). Functional magnetic resonance imaging (fMRI) has been used to uncover the sources of memory deficits associated with aging. To date, this work has focused on successful encoding, while the neural correlates of unsuccessful encoding are unknown. Here, we provide novel evidence of a neural mechanism underlying memory failures exclusively affecting older adults. Whereas both younger and older adults showed reduced activation of brain regions important for encoding (e.g., hippocampus) during unsuccessful encoding, only older adults showed increased activity in brain regions mediating distraction (e.g., auditory cortex) and in left prefrontal cortex. Further, these regions were functionally connected with medial parietal areas, previously identified as default mode regions (Raichle and Snyder, 2007), which may reflect environmental monitoring. Our results suggest that increased distraction from task-irrelevant input (auditory in this case), associated with the unfamiliar and noisy fMRI environment, may increase environmental monitoring. This in turn could hinder suppression of default mode processing, resulting in memory failures in older adults. These findings provide novel evidence of a brain mechanism underlying the behavioral evidence that impaired inhibition of extraneous input during encoding leads to memory failure in older adults and may have implications for the ubiquitous use of fMRI for investigating neurocognitive aging.

Functional connectivity constrains the category-related organization of human ventral occipitotemporal cortex

One of the most robust and oft‐replicated findings in cognitive neuroscience is that several spatially distinct, functionally dissociable ventral occipitotemporal cortex (VOTC) regions respond preferentially to different categories of concrete entities. However, the determinants of this category‐related organization remain to be fully determined. One recent proposal is that privileged connectivity of these VOTC regions with other regions that store and/or process category‐relevant properties may be a major contributing factor. To test this hypothesis, we used a multicategory functional magnetic resonance imaging (MRI) localizer to individually define category‐related brain regions of interest (ROIs) in a large group of subjects (n = 33). We then used these ROIs in resting‐state functional connectivity MRI analyses to explore spontaneous functional connectivity among these regions. We demonstrate that during rest, distinct category‐preferential VOTC regions show differentially stronger functional connectivity with other regions that have congruent category‐preference, as defined by the functional localizer. Importantly, a “tool”‐preferential region in the left medial fusiform gyrus showed differentially stronger functional connectivity with other left lateralized cortical regions associated with perceiving and knowing about common tools—posterior middle temporal gyrus (involved in perception of nonbiological motion), lateral parietal cortex (critical for reaching, grasping, manipulating), and ventral premotor cortex (involved in storing/executing motor programs)—relative to other category‐related regions in VOTC of both the right and left hemisphere. Our findings support the claim that privileged connectivity with other cortical regions that store and/or process category‐relevant properties constrains the category‐related organization of VOTC. Hum Brain Mapp 36:2187–2206, 2015.

Resting‐state functional connectivity MRI reveals active processes central to cognition

Analysis of spontaneously correlated low-frequency activity fluctuations across the brain using functional magnetic resonance imaging (MRI)-commonly referred to as resting-state functional connectivity (RSFC) MRI-was initially seen as a useful tool for mapping functional-anatomic networks in the living human brain, characterizing brain changes and differences in clinical populations, and studying comparative anatomy across species. However, little was known about the potential relevance of RSFC to cognitive processes. Indeed, there has been considerable controversy and debate as to the utility of studying the resting-state in cognitive neuroscience. However, recent work has shown that RSFC, rather than merely reflecting passive or epiphenomenal activity within underlying functional-anatomic networks, reveals important dynamic processes that play an active role in cognition. RSFC has been associated with individual differences in a number of behavioral and cognitive domains, including perception, language, learning and memory, and the organization of conceptual knowledge. In this article, we review and integrate the latest research demonstrating that RSFC is functionally relevant to human behavior and higher-level cognition, and propose a hypothesis regarding its mechanism of action on functional network dynamics and cognition. We conclude that RSFC MRI will be an invaluable tool for future discovery of the fundamental neurocognitive interactions that underlie cognition. WIREs Cogn Sci 2014, 5:233-245. doi: 10.1002/wcs.1275 CONFLICT OF INTEREST: The authors have declared no conflicts of interest for this article. For further resources related to this article, please visit the WIREs website.

Hemispheric Asymmetry of Visual Scene Processing in the Human Brain: Evidence from Repetition Priming and Intrinsic Activity

Asymmetrical specialization of cognitive processes across the cerebral hemispheres is a hallmark of healthy brain development and an important evolutionary trait underlying higher cognition in humans. While previous research, including studies of priming, divided visual field presentation, and split-brain patients, demonstrates a general pattern of right/left asymmetry of form-specific versus form-abstract visual processing, little is known about brain organization underlying this dissociation. Here, using repetition priming of complex visual scenes and high-resolution functional magnetic resonance imaging (MRI), we demonstrate asymmetrical form specificity of visual processing between the right and left hemispheres within a region known to be critical for processing of visual spatial scenes (parahippocampal place area [PPA]). Next, we use resting-state functional connectivity MRI analyses to demonstrate that this functional asymmetry is associated with differential intrinsic activity correlations of the right versus left PPA with regions critically involved in perceptual versus conceptual processing, respectively. Our results demonstrate that the PPA comprises lateralized subregions across the cerebral hemispheres that are engaged in functionally dissociable yet complementary components of visual scene analysis. Furthermore, this functional asymmetry is associated with differential intrinsic functional connectivity of the PPA with distinct brain areas known to mediate dissociable cognitive processes.

Spontaneous neural activity predicts individual differences in performance

We each have particular strengths—some of us are good at math and others are good at language—that vary from one person to another. Less appreciated is the fact that individual differences also extend to performing what appear on the surface to be simple perceptual tasks, like learning to detect one visual form among an array of visually similar forms (1, 2). Neurophysiological studies in awake monkeys and functional MRI (fMRI) studies in humans have provided considerable information about the neural changes that accompany visual perceptual learning—including that learning is highly specific to the retinotopic location of the trained stimulus—making it an ideal model system for studying cortical plasticity (3). Typically, there is also a large amount of intersubject performance variability, making it an ideal model for exploring the neural correlates of individual differences. However, other than good learners showing greater neural activity during the first learning trials than poor learners (2), little is known about the neural underpinnings of individual differences in perceptual learning. In PNAS, Baldassarre et al. (4) present a unique approach to this topic by evaluating the relationship between visual perceptual learning and slowly (<0.1 Hz) fluctuating, spontaneous neural activity recorded during an fMRI resting-state scan 1–2 days before learning.

Privileged Functional Connectivity between the Visual Word Form Area and the Language System

The visual word form area (VWFA) is a region in the left occipitotemporal sulcus of literate individuals that is purportedly specialized for visual word recognition. However, there is considerable controversy about its functional specificity and connectivity, with some arguing that it serves as a domain-general, rather than word-specific, visual processor. The VWFA is a critical region for testing hypotheses about the nature of cortical organization, because it is known to develop only through experience (i.e., reading acquisition), and widespread literacy is too recent to have influenced genetic determinants of brain organization. Using a combination of advanced fMRI analysis techniques, including individual functional localization, multivoxel pattern analysis, and high-resolution resting-state functional connectivity (RSFC) analyses, with data from 33 healthy adult human participants, we demonstrate that (1) the VWFA can discriminate words from nonword letter strings (pseudowords); (2) the VWFA has preferential RSFC with Wernickes area and other core regions of the language system; and (3) the strength of the RSFC between the VWFA and Wernickes area predicts performance on a semantic classification task with words but not other categories of visual stimuli. Our results are consistent with the hypothesis that the VWFA is specialized for lexical processing of real words because of its functional connectivity with Wernickes area. SIGNIFICANCE STATEMENT The visual word form area (VWFA) is critical for determining the nature of category-related organization of the ventral visual system. However, its functional specificity and connectivity are fiercely debated. Recent work concluded that the VWFA is a domain-general, rather than word-specific, visual processor with no preferential functional connectivity with the language system. Using more advanced techniques, our results stand in stark contrast to these earlier findings. We demonstrate that the VWFA is highly specialized for lexical processing of real words, and that a fundamental factor driving this specialization is its preferential intrinsic functional connectivity with core regions of the language system. Our results support the hypothesis that intrinsic functional connectivity contributes to category-related specialization within the human ventral visual system.