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Nozais, V., Forkel, S. J., Petit, L., Talozzi, L., Corbetta, M., Thiebaut de Schotten, M., & Joliot, M. (2023). Atlasing white matter and grey matter joint contributions to resting-state networks in the human brain. Communications Biology, 6: 726. doi:10.1038/s42003-023-05107-3.
Abstract
Over the past two decades, the study of resting-state functional magnetic resonance imaging has revealed that functional connectivity within and between networks is linked to cognitive states and pathologies. However, the white matter connections supporting this connectivity remain only partially described. We developed a method to jointly map the white and grey matter contributing to each resting-state network (RSN). Using the Human Connectome Project, we generated an atlas of 30 RSNs. The method also highlighted the overlap between networks, which revealed that most of the brain’s white matter (89%) is shared between multiple RSNs, with 16% shared by at least 7 RSNs. These overlaps, especially the existence of regions shared by numerous networks, suggest that white matter lesions in these areas might strongly impact the communication within networks. We provide an atlas and an open-source software to explore the joint contribution of white and grey matter to RSNs and facilitate the study of the impact of white matter damage to these networks. In a first application of the software with clinical data, we were able to link stroke patients and impacted RSNs, showing that their symptoms aligned well with the estimated functions of the networks. -
Parlatini, V., Itahashi, T., Lee, Y., Liu, S., Nguyen, T. T., Aoki, Y. Y., Forkel, S. J., Catani, M., Rubia, K., Zhou, J. H., Murphy, D. G., & Cortese, S. (2023). White matter alterations in Attention-Deficit/Hyperactivity Disorder (ADHD): a systematic review of 129 diffusion imaging studies with meta-analysis. Molecular Psychiatry, 28, 4098-4123. doi:10.1038/s41380-023-02173-1.
Abstract
Aberrant anatomical brain connections in attention-deficit/hyperactivity disorder (ADHD) are reported inconsistently across
diffusion weighted imaging (DWI) studies. Based on a pre-registered protocol (Prospero: CRD42021259192), we searched PubMed,
Ovid, and Web of Knowledge until 26/03/2022 to conduct a systematic review of DWI studies. We performed a quality assessment
based on imaging acquisition, preprocessing, and analysis. Using signed differential mapping, we meta-analyzed a subset of the
retrieved studies amenable to quantitative evidence synthesis, i.e., tract-based spatial statistics (TBSS) studies, in individuals of any
age and, separately, in children, adults, and high-quality datasets. Finally, we conducted meta-regressions to test the effect of age,
sex, and medication-naïvety. We included 129 studies (6739 ADHD participants and 6476 controls), of which 25 TBSS studies
provided peak coordinates for case-control differences in fractional anisotropy (FA)(32 datasets) and 18 in mean diffusivity (MD)(23
datasets). The systematic review highlighted white matter alterations (especially reduced FA) in projection, commissural and
association pathways of individuals with ADHD, which were associated with symptom severity and cognitive deficits. The meta-
analysis showed a consistent reduced FA in the splenium and body of the corpus callosum, extending to the cingulum. Lower FA
was related to older age, and case-control differences did not survive in the pediatric meta-analysis. About 68% of studies were of
low quality, mainly due to acquisitions with non-isotropic voxels or lack of motion correction; and the sensitivity analysis in high-
quality datasets yielded no significant results. Findings suggest prominent alterations in posterior interhemispheric connections
subserving cognitive and motor functions affected in ADHD, although these might be influenced by non-optimal acquisition
parameters/preprocessing. Absence of findings in children may be related to the late development of callosal fibers, which may
enhance case-control differences in adulthood. Clinicodemographic and methodological differences were major barriers to
consistency and comparability among studies, and should be addressed in future investigations.Additional information
supplementary information prisma checklist peak coordinates 1 peak coordinates 2 -
Barrett, R. L. C., Dawson, M., Dyrby, T. B., Krug, K., Ptito, M., D'Arceuil, H., Croxson, P. L., Johnson, P. J., Howells, H., Forkel, S. J., Dell'Acqua, F., & Catani, M. (2020). Differences in Frontal Network Anatomy Across Primate Species. The Journal of Neuroscience, 40(10), 2094-2107. doi:10.1523/JNEUROSCI.1650-18.2019.
Abstract
The frontal lobe is central to distinctive aspects of human cognition and behavior. Some comparative studies link this to a larger frontal cortex and even larger frontal white matter in humans compared with other primates, yet others dispute these findings. The discrepancies between studies could be explained by limitations of the methods used to quantify volume differences across species, especially when applied to white matter connections. In this study, we used a novel tractography approach to demonstrate that frontal lobe networks, extending within and beyond the frontal lobes, occupy 66% of total brain white matter in humans and 48% in three monkey species: vervets (Chlorocebus aethiops), rhesus macaque (Macaca mulatta) and cynomolgus macaque (Macaca fascicularis), all male. The simian–human differences in proportional frontal tract volume were significant for projection, commissural, and both intralobar and interlobar association tracts. Among the long association tracts, the greatest difference was found for tracts involved in motor planning, auditory memory, top-down control of sensory information, and visuospatial attention, with no significant differences in frontal limbic tracts important for emotional processing and social behaviour. In addition, we found that a nonfrontal tract, the anterior commissure, had a smaller volume fraction in humans, suggesting that the disproportionally large volume of human frontal lobe connections is accompanied by a reduction in the proportion of some nonfrontal connections. These findings support a hypothesis of an overall rearrangement of brain connections during human evolution. -
Forkel, S. J., Rogalski, E., Drossinos Sancho, N., D'Anna, L., Luque Laguna, P., Sridhar, J., Dell'Acqua, F., Weintraub, S., Thompson, C., Mesulam, M.-M., & Catani, M. (2020). Anatomical evidence of an indirect pathway for word repetition. Neurology, 94, e594-e606. doi:10.1212/WNL.0000000000008746.
Abstract
Objective: To combine MRI-based cortical morphometry and diffusion white matter tractography to describe the anatomical correlates of repetition deficits in patients with primary progressive aphasia (PPA).
Methods: The traditional anatomical model of language identifies a network for word repetition that includes Wernicke and Broca regions directly connected via the arcuate fasciculus. Recent tractography findings of an indirect pathway between Wernicke and Broca regions suggest a critical role of the inferior parietal lobe for repetition. To test whether repetition deficits are associated with damage to the direct or indirect pathway between both regions, tractography analysis was performed in 30 patients with PPA (64.27 ± 8.51 years) and 22 healthy controls. Cortical volume measurements were also extracted from 8 perisylvian language areas connected by the direct and indirect pathways.
Results: Compared to healthy controls, patients with PPA presented with reduced performance in repetition tasks and increased damage to most of the perisylvian cortical regions and their connections through the indirect pathway. Repetition deficits were prominent in patients with cortical atrophy of the temporo-parietal region with volumetric reductions of the indirect pathway.
Conclusions: The results suggest that in PPA, deficits in repetition are due to damage to the temporo-parietal cortex and its connections to Wernicke and Broca regions. We therefore propose a revised language model that also includes an indirect pathway for repetition, which has important clinical implications for the functional mapping and treatment of neurologic patients. -
Forkel, S. J., & Thiebaut de Schotten, M. (2020). Towards metabolic disconnection – symptom mapping. Brain, 143(3), 718-721. doi:10.1093/brain/awaa060.
Abstract
This scientific commentary refers to ‘Metabolic lesion-deficit mapping of human cognition’ by Jha etal. -
Friedrich, P., Forkel, S. J., & Thiebaut de Schotten, M. (2020). Mapping the principal gradient onto the corpus callosum. NeuroImage, 223: 117317. doi:10.1016/j.neuroimage.2020.117317.
Abstract
Gradients capture some of the variance of the resting-state functional magnetic resonance imaging (rsfMRI) signal. Amongst these, the principal gradient depicts a functional processing hierarchy that spans from sensory-motor cortices to regions of the default-mode network. While the cortex has been well characterised in terms of gradients little is known about its underlying white matter. For instance, comprehensive mapping of the principal gradient on the largest white matter tract, the corpus callosum, is still missing. Here, we mapped the principal gradient onto the midsection of the corpus callosum using the 7T human connectome project dataset. We further explored how quantitative measures and variability in callosal midsection connectivity relate to the principal gradient values. In so doing, we demonstrated that the extreme values of the principal gradient are located within the callosal genu and the posterior body, have lower connectivity variability but a larger spatial extent along the midsection of the corpus callosum than mid-range values. Our results shed light on the relationship between the brain's functional hierarchy and the corpus callosum. We further speculate about how these results may bridge the gap between functional hierarchy, brain asymmetries, and evolution.Additional information
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Friedrich, P., Thiebaut de Schotten, M., Forkel, S. J., Stacho, M., & Howells, H. (2020). An ancestral anatomical and spatial bias for visually guided behavior. Proceedings of the National Academy of Sciences of the United States of America, 117(5), 2251-2252. doi:10.1073/pnas.1918402117.
Abstract
Human behavioral asymmetries are commonly studied in the context of structural cortical and connectional asymmetries. Within this framework, Sreenivasan and Sridharan (1) provide intriguing evidence of a relationship between visual asymmetries and the lateralization of superior colliculi connections—a phylogenetically older mesencephalic structure. Specifically, response facilitation for cued locations (i.e., choice bias) in the contralateral hemifield was associated with differences in the connectivity of the superior colliculus. Given that the superior colliculus has a structural homolog—the optic tectum—which can be traced across all Vertebrata, these results may have meaningful evolutionary ramifications. -
Howells, H., Puglisi, G., Leonetti, A., Vigano, L., Fornia, L., Simone, L., Forkel, S. J., Rossi, M., Riva, M., Cerri, G., & Bello, L. (2020). The role of left fronto-parietal tracts in hand selection: Evidence from neurosurgery. Cortex, 128, 297-311. doi:10.1016/j.cortex.2020.03.018.
Abstract
Strong right-hand preference on the population level is a uniquely human feature, although its neural basis is still not clearly defined. Recent behavioural and neuroimaging literature suggests that hand preference may be related to the orchestrated function and size of fronto-parietal white matter tracts bilaterally. Lesions to these tracts induced during tumour resection may provide an opportunity to test this hypothesis. In the present study, a cohort of seventeen neurosurgical patients with left hemisphere brain tumours were recruited to investigate whether resection of certain white matter tracts affects the choice of hand selected for the execution of a goal-directed task (assembly of jigsaw puzzles). Patients performed the puzzles, but also tests for basic motor ability, selective attention and visuo-constructional ability, preoperatively and one month after surgery. An atlas-based disconnectome analysis was conducted to evaluate whether resection of tracts was significantly associated with changes in hand selection. Diffusion tractography was also used to dissect fronto-parietal tracts (the superior longitudinal fasciculus) and the corticospinal tract. Results showed a shift in hand selection despite the absence of any motor or cognitive deficits, which was significantly associated with frontal and parietal resections rather than other lobes. In particular, the shift in hand selection was significantly associated with the resection of dorsal rather than ventral fronto-parietal white matter connections. Dorsal white matter pathways contribute bilaterally to control of goal-directed hand movements. We show that unilateral lesions, that may unbalance the cooperation of the two hemispheres, can alter the choice of hand selected to accomplish movements. -
Milham, M., Petkov, C. I., Margulies, D. S., Schroeder, C. E., Basso, M. A., Belin, P., Fair, D. A., Fox, A., Kastner, S., Mars, R. B., Messinger, A., Poirier, C., Vanduffel, W., Van Essen, D. C., Alvand, A., Becker, Y., Ben Hamed, S., Benn, A., Bodin, C., Boretius, S. Milham, M., Petkov, C. I., Margulies, D. S., Schroeder, C. E., Basso, M. A., Belin, P., Fair, D. A., Fox, A., Kastner, S., Mars, R. B., Messinger, A., Poirier, C., Vanduffel, W., Van Essen, D. C., Alvand, A., Becker, Y., Ben Hamed, S., Benn, A., Bodin, C., Boretius, S., Cagna, B., Coulon, O., El-Gohary, S. H., Evrard, H., Forkel, S. J., Friedrich, P., Froudist-Walsh, S., Garza-Villarreal, E. A., Gao, Y., Gozzi, A., Grigis, A., Hartig, R., Hayashi, T., Heuer, K., Howells, H., Ardesch, D. J., Jarraya, B., Jarrett, W., Jedema, H. P., Kagan, I., Kelly, C., Kennedy, H., Klink, P. C., Kwok, S. C., Leech, R., Liu, X., Madan, C., Madushanka, W., Majka, P., Mallon, A.-M., Marche, K., Meguerditchian, A., Menon, R. S., Merchant, H., Mitchell, A., Nenning, K.-H., Nikolaidis, A., Ortiz-Rios, M., Pagani, M., Pareek, V., Prescott, M., Procyk, E., Rajimehr, R., Rautu, I.-S., Raz, A., Roe, A. W., Rossi-Pool, R., Roumazeilles, L., Sakai, T., Sallet, J., García-Saldivar, P., Sato, C., Sawiak, S., Schiffer, M., Schwiedrzik, C. M., Seidlitz, J., Sein, J., Shen, Z.-m., Shmuel, A., Silva, A. C., Simone, L., Sirmpilatze, N., Sliwa, J., Smallwood, J., Tasserie, J., Thiebaut de Schotten, M., Toro, R., Trapeau, R., Uhrig, L., Vezoli, J., Wang, Z., Wells, S., Williams, B., Xu, T., Xu, A. G., Yacoub, E., Zhan, M., Ai, L., Amiez, C., Balezeau, F., Baxter, M. G., Blezer, E. L., Brochier, T., Chen, A., Croxson, P. L., Damatac, C. G., Dehaene, S., Everling, S., Fleysher, L., Freiwald, W., Griffiths, T. D., Guedj, C., Hadj-Bouziane, F., Harel, N., Hiba, B., Jung, B., Koo, B., Laland, K. N., Leopold, D. A., Lindenfors, P., Meunier, M., Mok, K., Morrison, J. H., Nacef, J., Nagy, J., Pinsk, M., Reader, S. M., Roelfsema, P. R., Rudko, D. A., Rushworth, M. F., Russ, B. E., Schmid, M. C., Sullivan, E. L., Thiele, A., Todorov, O. S., Tsao, D., Ungerleider, L., Wilson, C. R., Ye, F. Q., Zarco, W., & Zhou, Y.-d. (2020). Accelerating the Evolution of Nonhuman Primate Neuroimaging. Neuron, 105(4), 600-603. doi:10.1016/j.neuron.2019.12.023.
Abstract
Nonhuman primate neuroimaging is on the cusp of a transformation, much in the same way its human counterpart was in 2010, when the Human Connectome Project was launched to accelerate progress. Inspired by an open data-sharing initiative, the global community recently met and, in this article, breaks through obstacles to define its ambitions.Additional information
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Waymel, A., Friedrich, P., Bastian, P.-A., Forkel, S. J., & Thiebaut de Schotten, M. (2020). Anchoring the human olfactory system within a functional gradient. NeuroImage, 216: 116863. doi:10.1016/j.neuroimage.2020.116863.
Abstract
Margulies et al. (2016) demonstrated the existence of at least five independent functional connectivity gradients in the human brain. However, it is unclear how these functional gradients might link to anatomy. The dual origin theory proposes that differences in cortical cytoarchitecture originate from two trends of progressive differentiation between the different layers of the cortex, referred to as the hippocampocentric and olfactocentric systems. When conceptualising the functional connectivity gradients within the evolutionary framework of the Dual Origin theory, the first gradient likely represents the hippocampocentric system anatomically. Here we expand on this concept and demonstrate that the fifth gradient likely links to the olfactocentric system. We describe the anatomy of the latter as well as the evidence to support this hypothesis. Together, the first and fifth gradients might help to model the Dual Origin theory of the human brain and inform brain models and pathologies. -
Catani, M., Dell'Acqua, F., Bizzi, A., Forkel, S. J., Williams, S. C., Simmons, A., Murphy, D. G., & Thiebaut de Schotten, M. (2012). Beyond cortical localization in clinico-anatomical correlation. Cortex, 48(10), 1262-1287. doi:10.1016/j.cortex.2012.07.001.
Abstract
Last year was the 150th anniversary of Paul Broca's landmark case report on speech disorder that paved the way for subsequent studies of cortical localization of higher cognitive functions. However, many complex functions rely on the activity of distributed networks rather than single cortical areas. Hence, it is important to understand how brain regions are linked within large-scale networks and to map lesions onto connecting white matter tracts. To facilitate this network approach we provide a synopsis of classical neurological syndromes associated with frontal, parietal, occipital, temporal and limbic lesions. A review of tractography studies in a variety of neuropsychiatric disorders is also included. The synopsis is accompanied by a new atlas of the human white matter connections based on diffusion tensor tractography freely downloadable on http://www.natbrainlab.com. Clinicians can use the maps to accurately identify the tract affected by lesions visible on conventional CT or MRI. The atlas will also assist researchers to interpret their group analysis results. We hope that the synopsis and the atlas by allowing a precise localization of white matter lesions and associated symptoms will facilitate future work on the functional correlates of human neural networks as derived from the study of clinical populations. Our goal is to stimulate clinicians to develop a critical approach to clinico-anatomical correlative studies and broaden their view of clinical anatomy beyond the cortical surface in order to encompass the dysfunction related to connecting pathways.Additional information
supplementary file
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