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Content-specific activity in frontoparietal and default-mode networks during prior-guided visual perception.

ABSTRACT: How prior knowledge shapes perceptual processing across the human brain, particularly in the frontoparietal (FPN) and default-mode (DMN) networks, remains unknown. Using ultra-high-field (7T) functional magnetic resonance imaging (fMRI), we elucidated the effects that the acquisition of prior knowledge has on perceptual processing across the brain. We observed that prior knowledge significantly impacted neural representations in the FPN and DMN, rendering responses to individual visual images more distinct from each other, and more similar to the image-specific prior. In addition, neural representations were structured in a hierarchy that remained stable across perceptual conditions, with early visual areas and DMN anchored at the two extremes. Two large-scale cortical gradients occur along this hierarchy: first, dimensionality of the neural representational space increased along the hierarchy; second, prior's impact on neural representations was greater in higher-order areas. These results reveal extensive and graded influences of prior knowledge on perceptual processing across the brain.

SUBMITTER: Gonzalez-Garcia C

PROVIDER: S-EPMC6067880 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Content-specific activity in frontoparietal and default-mode networks during prior-guided visual perception.

González-García Carlos C Flounders Matthew W MW Chang Raymond R Baria Alexis T AT He Biyu J BJ

eLife 20180731

How prior knowledge shapes perceptual processing across the human brain, particularly in the frontoparietal (FPN) and default-mode (DMN) networks, remains unknown. Using ultra-high-field (7T) functional magnetic resonance imaging (fMRI), we elucidated the effects that the acquisition of prior knowledge has on perceptual processing across the brain. We observed that prior knowledge significantly impacted neural representations in the FPN and DMN, rendering responses to individual visual images mo ...[more]

PMID: 30063006

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Project description:BackgroundFunctional abnormalities, mostly involving functionally specialized subsystems, have been associated with disorders of emotion regulation such as bipolar disorder (BD). Understanding how independent functional subsystems integrate globally and how they relate with anatomical cortical and subcortical networks is key to understanding how the human brain's architecture constrains functional interactions and underpins abnormalities of mood and emotion, particularly in BD.MethodsResting-state functional magnetic resonance time series were averaged to obtain individual functional connectivity matrices (using AFNI software); individual structural connectivity matrices were derived using deterministic non-tensor-based tractography (using ExploreDTI, version 4.8.6), weighted by streamline count and fractional anisotropy. Structural and functional nodes were defined using a subject-specific cortico-subcortical mapping (using Desikan-Killiany Atlas, FreeSurfer, version 5.3). Whole-brain connectivity alongside a permutation-based statistical approach and structure-function coupling were employed to investigate topological variance in individuals with predominantly euthymic BD relative to psychiatrically healthy control subjects.ResultsPatients with BD (n = 41) exhibited decreased (synchronous) connectivity in a subnetwork encompassing frontolimbic and posterior-occipital functional connections (T > 3, p = .048), alongside increased (antisynchronous) connectivity within a frontotemporal subnetwork (T > 3, p = .014); all relative to control subjects (n = 56). Preserved whole-brain functional connectivity and comparable structure-function coupling among whole-brain and edge-class connections were observed in patients with BD relative to control subjects.ConclusionsThis study presents a functional map of BD dysconnectivity that differentially involves communication within nodes belonging to functionally specialized subsystems-default mode, frontoparietal, and frontolimbic systems; these changes do not extend to be detected globally and may be necessary to maintain a remitted clinical state of BD. Preserved structure-function coupling in BD despite evidence of regional anatomical and functional deficits suggests a dynamic interplay between structural and functional subnetworks.

Project description:BackgroundMajor Depressive Disorder (MDD) is associated with alterations within the default mode (DMN) and frontoparietal (FPN) networks. However, it is unclear whether changes in these networks occur prior to onset in youth at high familial risk for MDD or are a consequence of MDD. Moreover, studies examining premorbid MDD vulnerability markers have focused on static rather than dynamic network properties, which could further elucidate DMN-FPN imbalances linked to MDD risk.MethodsEighty-nine unaffected 12-14-year-old adolescents both with (n = 27) and without (n = 62) a maternal history of MDD completed a resting state functional magnetic resonance imaging scan and self-report assessments of depressive symptoms and perceived stress at baseline and every three months across a two-year span. A coactivation pattern (CAP) analysis was conducted to examine functional network dynamic properties, including time spent in each CAP (total number of volumes), CAP persistence (number of consecutive volumes in each CAP), and number of transitions between posterior DMN-FPN and canonical DMN CAPs. Multilevel models estimated whether DMN-FPN dynamic properties predicted future depressive symptoms and stress sensitivity.ResultsHigh-risk adolescents spent more time and exhibited a longer persistence in a posterior DMN-FPN CAP. DMN-FPN CAP persistence predicted future perceived stress, but only among high-risk adolescents. High-risk adolescents characterized by high DMN-FPN persistence reported greater future perceived stress, whereas those showing low DMN-FPN persistence had reduced perceived stress over time. Unexpectedly, DMN-FPN dynamics did not predict future depressive symptoms.ConclusionsAltered DMN-FPN CAP properties among high-risk adolescents mirror alterations among individuals with MDD, suggesting that DMN-FPN dynamics may be a risk marker rather than consequence of MDD. Furthermore, longer DMN-FPN CAP persistence increases vulnerability in high-risk adolescents by predicting greater future stress sensitivity, a well-known catalyst for MDD. Replication in a larger sample is warranted.

Dataset Information

Content-specific activity in frontoparietal and default-mode networks during prior-guided visual perception.

Publications

Content-specific activity in frontoparietal and default-mode networks during prior-guided visual perception.

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