Population-based tract-to-region connectome of the human brain and its hierarchical topology

Yeh, Fang‐Cheng

doi:10.1038/s41467-022-32595-4

Cited by 41 publications

(36 citation statements)

References 67 publications

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“…The IFOF, which has been attributed to the ventral pathway of the human brain, 128 mainly connects the frontal (IFG, MFG, dlPFC 129 ) with the occipital lobe. 59 However, the anatomic dissection of the IFOF 130 and probabilistic tract-to-region connectome matrices 131 further identified terminations in the IPL and the posterior part of the temporo-basal area. The IFOF has also been shown to contribute to visuospatial attention, 132–134 as well as inhibition 135 and alertness.…”

Section: Discussionmentioning

confidence: 99%

Joint impact on attention, alertness and inhibition of lesions at a frontal white matter crossroad

Kaufmann

Cazzoli

Vanbellingen

et al. 2022

Brain

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In everyday life, information from different cognitive domains - such as visuospatial attention, alertness, and inhibition - needs to be integrated between different brain regions. Early models suggested that completely segregated brain networks control these three cognitive domains. However, more recent accounts, mainly based on neuroimaging data in healthy participants, indicate that different tasks lead to specific patterns of activation within the same, higher-order and “multiple-demand” network. If so, then a lesion to critical substrates of this common network should determine a concomitant impairment in all three cognitive domains. The aim of the present study was to critically investigate this hypothesis, i.e., to identify focal stroke lesions within the network that can concomitantly impact visuospatial attention, alertness and inhibition. We studied an unselected sample of 60 first-ever right-hemispheric, subacute stroke patients using a data-driven, bottom-up approach. Patients performed 12 standardized neuropsychological and oculomotor tests, four per cognitive domain. Principal component analyses revealed a strong relationship between all three cognitive domains: 10 of 12 tests loaded on a first, Common Component. Analysis of the neuroanatomical lesion correlates using different approaches (i.e., Voxel-Based and Tractwise Lesion-Symptom Mapping, Disconnectome maps) provided convergent evidence on the association between severe impairment of this Common Component and lesions at the intersection of Superior Longitudinal Fasciculus II and III, Frontal Aslant Tract and, to a lesser extent, the Putamen and Inferior Fronto-Occipital Fasciculus. Moreover, patients with a lesion involving this region were significantly more impaired in daily living cognition, which provides an ecological validation of our results. A probabilistic functional atlas of the multiple-demand network was performed to confirm the potential relationship between patients’ lesion substrates and observed cognitive impairments as a function of the MD-network connectivity disruption. These findings show, for the first time, that a lesion to a specific white matter crossroad can determine a concurrent breakdown in all three considered cognitive domains. Our results support the multiple-demand network model, proposing that different cognitive operations depend on specific collaborators and their interaction, within the same underlying neural network. Our findings also extend this hypothesis by showing (1) the contribution of SLF and FAT to the multiple-demand network, and (2) a critical neuroanatomical intersection, crossed by a vast amount of long-range white matter tracts, many of which interconnect cortical areas of the multiple-demand network. The vulnerability of this crossroad to stroke has specific cognitive and clinical consequences; this has the potential to influence future rehabilitative approaches.

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Section: Discussionmentioning

confidence: 99%

Joint impact on attention, alertness and inhibition of lesions at a frontal white matter crossroad

Kaufmann

Cazzoli

Vanbellingen

et al. 2022

Brain

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“…We focus on these connections, and exclude connections to regions without sufficient electrode coverage for across-subject correlations, such as the occipital lobe. Each of these tracts was defined based on the population-averaged tractography atlases HCP1065 (AF, SLF, TPAT) 23 and HCP842 (U-fibers) 50 . The SLF was split into two sections connecting frontal and parietal and frontal and central brain regions, because merging these sections would lead to inaccurate estimates of the length of the SLF and bias transmission speed estimates described in the next section.…”

Section: Methodsmentioning

confidence: 99%

“…The SLF was split into two sections connecting frontal and parietal and frontal and central brain regions, because merging these sections would lead to inaccurate estimates of the length of the SLF and bias transmission speed estimates described in the next section. We subsequently matched the ECoG electrodes, located on the gray matter surface, to the tractography atlas using the gray matter endpoint probability estimates of the tracts 23 . In this way, we were able to investigate the CCEP based connectivity for different fiber tracts.…”

Section: Methodsmentioning

confidence: 99%

“…To quantify age-related changes in conduction delays across some well described association fiber bundles, we use a white matter atlas to extract CCEPs across the arcuate fasciculus (AF), two sections of superior longitudinal fasciculus (SLF) and the temporo-parietal aslant tract (TPAT) in each subject 23 (Fig. 1a ).…”

Section: Mainmentioning

confidence: 99%

“…The data that support the findings of this study are being made available in BIDS format on OpenNeuro: https://openneuro.org/datasets/ds004080 . Atlases of white matter tracts were defined based on the population-averaged tractography atlases HCP1065 (AF, SLF, TPAT) 23 and HCP842 (U-fibers) 50 : https://brain.labsolver.org/hcp_trk_atlas .…”

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confidence: 99%

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Developmental trajectory of transmission speed in the human brain

et al. 2023

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The structure of the human connectome develops from childhood throughout adolescence to middle age, but how these structural changes affect the speed of neuronal signaling is not well described. In 74 subjects, we measured the latency of cortico-cortical evoked responses across association and U-fibers and calculated their corresponding transmission speeds. Decreases in conduction delays until at least 30 years show that the speed of neuronal communication develops well into adulthood.

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Outcomes and Mechanisms Associated With Selective Thalamic Neuronal Loss in Chronic Traumatic Brain Injury

Woodrow,

Grossac,

Hong

et al. 2024

JAMA Netw Open

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ImportanceThe chronic neuronal burden of traumatic brain injury (TBI) is not fully characterized by routine imaging, limiting understanding of the role of neuronal substrates in adverse outcomes.ObjectiveTo determine whether tissues that appear healthy on routine imaging can be investigated for selective neuronal loss using [11C]flumazenil (FMZ) positron emission tomography (PET) and to examine whether this neuronal loss is associated with long-term outcomes.Design, Setting, and ParticipantsIn this cross-sectional study, data were collected prospectively from 2 centers (University of Cambridge in the UK and Weill Cornell Medicine in the US) between September 1, 2004, and May 31, 2021. Patients with TBI (&gt;6 months postinjury) were compared with healthy control participants (all aged &gt;18 years). Individuals with neurological disease, benzodiazepine use, or contraindication to magnetic resonance imaging were excluded. Data were retrospectively collated with nonconsecutive recruitment, owing to convenience and scanner or PET ligand availability. Data were analyzed between February 1 and September 30, 2023.ExposureFlumazenil voxelwise binding potential relative to nondisplaceable binding potential (BPND).Main Outcomes and MeasuresSelective neuronal loss identified with FMZ PET was compared between groups on voxelwise and regional scales, and its association with functional, cognitive, and psychological outcomes was examined using Glasgow Outcome Scale (GOS) scores, measures of sustained executive attention (animal and sustained fluency), and 36-Item Short Form Health Survey (SF-36) scores. Diffusion tensor imaging was used to assess structural connectivity of regions of cortical damage, and its association with thalamic selective neuronal loss.ResultsIn this study, 24 patients with chronic TBI (mean [SD] age, 39.2 [12.3] years; 18 men [75.0%]) and 33 healthy control participants (mean [SD] age, 47.6 [20.5] years; 23 men [69.7%]) underwent FMZ PET. Patients with TBI had a median time of 29 (range, 7-95) months from injury to scan. They displayed selective neuronal loss in thalamic nuclei, over and above gross volume loss in the left thalamus, and bilateral central, mediodorsal, ventral-lateral dorsal, anterior, and ventral anterior thalamic nuclei, across a wide range of injury severities. Neuronal loss was associated with worse functional outcome using GOS scores (left thalamus, left ventral anterior, and bilateral central, mediodorsal, and anterior nuclei), worse cognitive outcome on measures of sustained executive attention (left thalamus, bilateral central, and right mediodorsal nuclei), and worse emotional outcome using SF-36 scores (right central thalamic nucleus). Chronic thalamic neuronal loss partially mirrored the location of primary cortical contusions, which may indicate secondary injury mechanisms of transneuronal degeneration.Conclusions and RelevanceThe findings of this study suggest that selective thalamic vulnerability may have chronic neuronal consequences with relevance to long-term outcome, suggesting the evolving and potentially lifelong thalamic neuronal consequences of TBI. FMZ PET is a more sensitive marker of the burden of neuronal injury than routine imaging; therefore, it could inform outcome prognostication and may lead to the development of individualized precision medicine approaches.

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Population-based tract-to-region connectome of the human brain and its hierarchical topology

Cited by 41 publications

References 67 publications

Joint impact on attention, alertness and inhibition of lesions at a frontal white matter crossroad

Joint impact on attention, alertness and inhibition of lesions at a frontal white matter crossroad

Developmental trajectory of transmission speed in the human brain

Outcomes and Mechanisms Associated With Selective Thalamic Neuronal Loss in Chronic Traumatic Brain Injury

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