Large-Scale Gradients in Human Cortical Organization Huntenburg, Julia M.; Bazin, Pierre-Louis; Margulies, Daniel S.
Trends in cognitive sciences,
January 2018, 2018-01-00, 20180101, 2018-01, Letnik:
22, Številka:
1
Journal Article
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Recent advances in mapping cortical areas in the human brain provide a basis for investigating the significance of their spatial arrangement. Here we describe a dominant gradient in cortical features ...that spans between sensorimotor and transmodal areas. We propose that this gradient constitutes a core organizing axis of the human cerebral cortex, and describe an intrinsic coordinate system on its basis. Studying the cortex with respect to these intrinsic dimensions can inform our understanding of how the spectrum of cortical function emerges from structural constraints.
Advances in neuroimaging technologies and analytics have enabled the discovery of gradients in microstructure, connectivity, gene expression, and function in the human cerebral cortex.
The notion that functional processing hierarchies are confined to sensorimotor systems is challenged by recent descriptions of global hierarchies, extending throughout transmodal association areas.
An innovative line of research has uncovered a cortical hierarchy in the temporal domain that accounts for spatially distributed functional specialization.
Research in the macaque monkey suggests that cortical areas with similar microstructure are more likely to be connected. Here, we examine this link in the human cerebral cortex using 2 magnetic ...resonance imaging (MRI) measures: quantitative T1 maps, which are sensitive to intracortical myelin content and provide an in vivo proxy for cortical microstructure, and resting-state functional connectivity. Using ultrahigh-resolution MRI at 7 T and dedicated image processing tools, we demonstrate a systematic relationship between T1-based intracortical myelin content and functional connectivity. This effect is independent of the proximity of areas. We employ nonlinear dimensionality reduction to characterize connectivity components and identify specific aspects of functional connectivity that are linked to myelin content. Our results reveal a consistent spatial pattern throughout different analytic approaches. While functional connectivity and myelin content are closely linked in unimodal areas, the correspondence is lower in transmodal areas, especially in posteromedial cortex and the angular gyrus. Our findings are in agreement with comprehensive reports linking histologically assessed microstructure and connectivity in different mammalian species and extend them to the human cerebral cortex in vivo.
Understanding how the structure of cognition arises from the topographical organization of the cortex is a primary goal in neuroscience. Previous work has described local functional gradients ...extending from perceptual and motor regions to cortical areas representing more abstract functions, but an overarching framework for the association between structure and function is still lacking. Here, we show that the principal gradient revealed by the decomposition of connectivity data in humans and the macaque monkey is anchored by, at one end, regions serving primary sensory/motor functions and at the other end, transmodal regions that, in humans, are known as the default-mode network (DMN). These DMN regions exhibit the greatest geodesic distance along the cortical surface—and are precisely equidistant—from primary sensory/motor morphological landmarks. The principal gradient also provides an organizing spatial framework for multiple large-scale networks and characterizes a spectrum from unimodal to heteromodal activity in a functional metaanalysis. Together, these observations provide a characterization of the topographical organization of cortex and indicate that the role of the DMN in cognition might arise from its position at one extreme of a hierarchy, allowing it to process transmodal information that is unrelated to immediate sensory input.
The disparity between the chronological age of an individual and their brain-age measured based on biological information has the potential to offer clinically relevant biomarkers of neurological ...syndromes that emerge late in the lifespan. While prior brain-age prediction studies have relied exclusively on either structural or functional brain data, here we investigate how multimodal brain-imaging data improves age prediction. Using cortical anatomy and whole-brain functional connectivity on a large adult lifespan sample (N=2354, age 19–82), we found that multimodal data improves brain-based age prediction, resulting in a mean absolute prediction error of 4.29 years. Furthermore, we found that the discrepancy between predicted age and chronological age captures cognitive impairment. Importantly, the brain-age measure was robust to confounding effects: head motion did not drive brain-based age prediction and our models generalized reasonably to an independent dataset acquired at a different site (N=475). Generalization performance was increased by training models on a larger and more heterogeneous dataset. The robustness of multimodal brain-age prediction to confounds, generalizability across sites, and sensitivity to clinically-relevant impairments, suggests promising future application to the early prediction of neurocognitive disorders.
•Brain-based age prediction is improved with multimodal neuroimaging data.•Participants with cognitive impairment show increased brain aging.•Age prediction models are robust to motion and generalize to independent datasets from other sites.
•The principal gradient of functional connectivity in the mouse cortex recapitulates an axis of neocortical evolution from archicortex and paleocortex.•Additional gradients highlight sensory ...specialization and reflect aspects of a sensory-to-transmodal hierarchy.•Functional connectivity gradients partly align with gene expression patterns.•Mouse cortical gradients are stable across data sets.
Understanding cortical organization is a fundamental goal of neuroscience that requires comparisons across species and modalities. Large-scale connectivity gradients have recently been introduced as a data-driven representation of the intrinsic organization of the cortex. We studied resting-state functional connectivity gradients in the mouse cortex and found robust spatial patterns across four data sets. The principal gradient of functional connectivity shows a striking overlap with an axis of neocortical evolution from two primordial origins. Additional gradients reflect sensory specialization and aspects of a sensory-to-transmodal hierarchy, and are associated with transcriptomic features. While some of these gradients strongly resemble observations in the human cortex, the overall pattern in the mouse cortex emphasizes the specialization of sensory areas over a global functional hierarchy.
Mind-wandering has a controversial relationship with cognitive control. Existing psychological evidence supports the hypothesis that episodes of mind-wandering reflect a failure to constrain thinking ...to task-relevant material, as well the apparently alternative view that control can facilitate the expression of self-generated mental content. We assessed whether this apparent contradiction arises because of a failure to consider differences in the types of thoughts that occur during mind-wandering, and in particular, the associated level of intentionality. Using multi-modal magnetic resonance imaging (MRI) analysis, we examined the cortical organisation that underlies inter-individual differences in descriptions of the spontaneous or deliberate nature of mind-wandering. Cortical thickness, as well as functional connectivity analyses, implicated regions relevant to cognitive control and regions of the default-mode network for individuals who reported high rates of deliberate mind-wandering. In contrast, higher reports of spontaneous mind-wandering were associated with cortical thinning in parietal and posterior temporal regions in the left hemisphere (which are important in the control of cognition and attention) as well as heightened connectivity between the intraparietal sulcus and a region that spanned limbic and default-mode regions in the ventral inferior frontal gyrus. Finally, we observed a dissociation in the thickness of the retrosplenial cortex/lingual gyrus, with higher reports of spontaneous mind-wandering being associated with thickening in the left hemisphere, and higher repots of deliberate mind-wandering with thinning in the right hemisphere. These results suggest that the intentionality of the mind-wandering state depends on integration between the control and default-mode networks, with more deliberation being associated with greater integration between these systems. We conclude that one reason why mind-wandering has a controversial relationship with control is because it depends on whether the thoughts emerge in a deliberate or spontaneous fashion.
•Deliberate and spontaneous mind-wandering have unique structural and functional correlates.•Reports of deliberate mind-wandering correlated with regions in both default-mode and fronto-parietal networks.•Spontaneous mind-wandering was linked to less integrity in parietal and temporal regions.•Intentionality during the mind-wandering state may depend upon integration between the default-mode and fronto-parietal networks.•These neurocognitive differences explain why mind-wandering has a complex relationship with cognitive control.
Connectivity between distant cortical areas is a valuable, yet costly feature of cortical organization and is predominantly found between regions of heteromodal association cortex. The recently ...proposed ‘tethering hypothesis’ describes the emergence of long-distance connections in association cortex as a function of their spatial separation from primary cortical regions. Here, we investigate this possibility by characterizing the distance between functionally connected areas along the cortical surface. We found a systematic relationship between an area’s characteristic connectivity distance and its distance from primary cortical areas. Specifically, the further a region is located from primary sensorimotor regions, the more distant are its functional connections with other areas of the cortex. The measure of connectivity distance also captured major functional subdivisions of the cerebral cortex: unimodal, attention, and higher-order association regions. Our findings provide evidence for the anchoring role of primary cortical regions in establishing the spatial distribution of cortical properties that are related to functional specialization and differentiation.
Mindfulness-based interventions for the prevention and treatment of depression are predicated on the idea that interoceptive awareness represents a crucial foundation for the cultivation of adaptive ...ways of responding to negative thoughts and mood states such as the ability to decenter. The current study used a multi-dimensional self-report assessment of interoceptive awareness, including regulatory and belief-related aspects of the construct, in order to characterize deficits in interoceptive awareness in depression, investigate whether brief mindfulness training could reduce these deficits, and to test whether the training unfolds its beneficial effects through the above-described pathway. Currently depressed patients (
n
= 67) were compared to healthy controls (
n
= 25) and then randomly allocated to receive either a brief training in mindfulness (per-protocol sample of
n
= 32) or an active control training (per-protocol sample of
n
= 28). Patients showed significant deficits across a range of regulatory and belief-related aspects of interoceptive awareness, mindfulness training significantly increased regulatory and belief-related aspects of interoceptive awareness, and reductions in depressive symptoms were mediated through a serial pathway in which training-related increases in aspects of interoceptive awareness were positively associated with the ability to decenter, which in turn was associated with reduced symptoms of depression. These results support the role of interoceptive awareness in facilitating adaptive responses to negative mood.
With recent improvements in human magnetic resonance imaging (MRI) at ultra-high fields, the amount of data collected per subject in a given MRI experiment has increased considerably. Standard image ...processing packages are often challenged by the size of these data. Dedicated methods are needed to leverage their extraordinary spatial resolution. Here, we introduce a flexible Python toolbox that implements a set of advanced techniques for high-resolution neuroimaging. With these tools, segmentation and laminar analysis of cortical MRI data can be performed at resolutions up to 500 μm in reasonable times. Comprehensive online documentation makes the toolbox easy to use and install. An extensive developer's guide encourages contributions from other researchers that will help to accelerate progress in the promising field of high-resolution neuroimaging.
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