Abstract
The temporo-basal region of the human brain is composed of the collateral, the occipito-temporal, and the rhinal sulci. We manually rated (using a novel protocol) the connections between rhinal/collateral (RS-CS), collateral/occipito-temporal (CS-OTS) and rhinal/occipito-temporal (RS-OTS) sulci, using the MRI of nearly 3400 individuals including around 1000 twins. We reported both the associations between sulcal polymorphisms as well with a wide range of demographics (e.g. age, sex, handedness). Finally, we also estimated the heritability, and the genetic correlation between sulcal connections. We reported the frequency of the sulcal connections in the general population, which were hemisphere dependent. We found a sexual dimorphism of the connections, especially marked in the right hemisphere, with a CS-OTS connection more frequent in females (approximately 35–40% versus 20–25% in males) and an RS-CS connection more common in males (approximately 40–45% versus 25–30% in females). We confirmed associations between sulcal connections and characteristics of incomplete hippocampal inversion (IHI). We estimated the broad sense heritability to be 0.28–0.45 for RS-CS and CS-OTS connections, with hints of dominant contribution for the RS-CS connection. The connections appeared to share some of their genetic causing factors as indicated by strong genetic correlations. Heritability appeared much smaller for the (rarer) RS-OTS connection.
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Data availability
The QTIM and QTAB dataset are in open access and available online at https://openneuro.org/datasets/ds004169 and https://openneuro.org/datasets/ds004146. The IMAGEN dataset is available to interested researchers upon application to the IMAGEN Executive Committee (ponscentre@charite.de, https://imagen-project.org/?page_id=547).
Code availability
Code used to process the data and perform the analyses will be available upon publication as https://github.com/KevinDMR.
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Acknowledgements
The QTAB study acknowledges the Queensland Twin Registry Study (https://www.qimrberghofer.edu.au/study/queensland-twin-registry-study) for generously sharing database information for recruitment. The QTAB study was further facilitated through access to Twins Research Australia, a national resource supported by a Centre of Research Excellence Grant (ID: 1078102) from the National Health and Medical Research Council. We acknowledge access to the facilities and expertise of the CIBM Center for Biomedical Imaging, a Swiss research center of excellence founded and supported by Lausanne University Hospital (CHUV), University of Lausanne (UNIL), Ecole polytechnique fédérale de Lausanne (EPFL), University of Geneva (UNIGE) and Geneva University Hospitals (HUG).
Funding
The research leading to these results has received funding from the French government under management of Agence Nationale de la Recherche as part of the Investissements d'avenir program, reference ANR-19-P3IA-0001 (PRAIRIE 3IA Institute) and reference ANR-10-IAIHU-06 (Agence Nationale de la Recherche-10-IA Institut Hospitalo-Universitaire-6). BCD is supported by the NHMRC (CJ Martin Fellowship, APP1161356). The Imagen study is supported by the following sources. This work received support from the following sources: the European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (LSHM-CT-2007-037286), the Horizon 2020 funded ERC Advanced Grant ‘STRATIFY’ (Brain network based stratification of reinforcement-related disorders) (695313), Human Brain Project (HBP SGA 2, 785907, and HBP SGA 3, 945539), the Medical Research Council Grant 'c-VEDA’ (Consortium on Vulnerability to Externalizing Disorders and Addictions) (MR/N000390/1), the National Institute of Health (NIH) (R01DA049238, A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers), the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London, the Bundesministeriumfür Bildung und Forschung (BMBF grants 01GS08152; 01EV0711; Forschungsnetz AERIAL 01EE1406A, 01EE1406B; Forschungsnetz IMAC-Mind 01GL1745B), the Deutsche Forschungsgemeinschaft (DFG grants SM 80/7-2, SFB 940, TRR 265, NE 1383/14-1), the Medical Research Foundation and Medical Research Council (grants MR/R00465X/1 and MR/S020306/1), the National Institutes of Health (NIH) funded ENIGMA (grants 5U54EB020403-05 and 1R56AG058854-01), NSFC grant 82150710554 and European Union funded project ‘environMENTAL’, Grant No: 101057429. Further support was provided by grants from: the ANR (ANR-12-SAMA-0004, AAPG2019-GeBra), the Eranet Neuron (AF12-NEUR0008-01-WM2NA; and ANR-18-NEUR00002-01-ADORe), the Fondation de France (00081242), the Fondation pour la Recherche Médicale (DPA20140629802), the Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA), the Assistance-Publique-Hôpitaux-de-Paris and INSERM (interface grant), Paris Sud University IDEX 2012, the Fondation de l’Avenir (grant AP-RM-17-013), the Fédération pour la Recherche sur le Cerveau; the National Institutes of Health, Science Foundation Ireland (16/ERCD/3797), U.S.A. (Axon, Testosterone and Mental Health during Adolescence; RO1 MH085772-01A1) and by NIH Consortium grant U54 EB020403, supported by a cross-NIH alliance that funds Big Data to Knowledge Centres of Excellence. The QTIM study was supported by the National Institute of Child Health and Human Development (R01 HD050735), and the National Health and Medical Research Council (NHMRC 486682, 1009064), Australia. The QTAB study was funded by the National Health and Medical Research Council (NHMRC APP1078756), Australia.
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KDM had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concepts and study design: KDM, BCD, OC, CC. Acquisition, analysis or interpretation of data interpretation: all authors. Manuscript drafting or manuscript revision for important intellectual content: all authors Approval of final version of submitted manuscript: all authors. Literature research: KDM. Statistical analysis: KDM, BCD. Study supervision: BCD, OC, MBC, CC.
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Disclosure of interests related to the present article: none to disclose. Disclosure of interests unrelated to the present article: OC reports having received consulting fees from AskBio and Therapanacea, having received fees for writing a lay audience short paper from Expression Santé, and that his laboratory has received grants (paid to the institution) from Qynapse. Members from his laboratory have co-supervised a PhD. thesis with myBrainTechnologies and with Qynapse. OC’s spouse is an employee of myBrainTechnologies. OC holds a patent registered at the International Bureau of the World Intellectual Property Organization (PCT/IB2016/0526993, Schiratti J-B, Allassonniere S, Colliot O, Durrleman S, A method for determining the temporal progression of a biological phenomenon and associated methods and devices). Dr. Banaschewski served in an advisory or consultancy role for eye level, Infectopharm, Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Roche, and Takeda. He received conference support or speaker’s fee by Janssen, Medice and Takeda. He received royalties from Hogrefe, Kohlhammer, CIP Medien, Oxford University Press. The present work is unrelated to the above grants and relationships. Dr. Barker has received honoraria from General Electric Healthcare for teaching on scanner programming courses. Dr. Poustka served in an advisory or consultancy role for Roche and Viforpharm and received speaker’s fee by Shire. She received royalties from Hogrefe, Kohlhammer and Schattauer.
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de Matos, K., Cury, C., Chougar, L. et al. Temporo-basal sulcal connections: a manual annotation protocol and an investigation of sexual dimorphism and heritability. Brain Struct Funct 228, 1459–1478 (2023). https://doi.org/10.1007/s00429-023-02663-6
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DOI: https://doi.org/10.1007/s00429-023-02663-6