Temporo-basal sulcal connections: a manual annotation protocol and an investigation of sexual dimorphism and heritability.
Collateral sulcus
Occipito-temporal sulcus
Rhinal sulcus
Sulcal variability
Temporal lobe
Twin heritability
Journal
Brain structure & function
ISSN: 1863-2661
Titre abrégé: Brain Struct Funct
Pays: Germany
ID NLM: 101282001
Informations de publication
Date de publication:
Jul 2023
Jul 2023
Historique:
received:
31
01
2023
accepted:
07
06
2023
medline:
13
7
2023
pubmed:
26
6
2023
entrez:
26
6
2023
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 37358662
doi: 10.1007/s00429-023-02663-6
pii: 10.1007/s00429-023-02663-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1459-1478Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-19-P3IA-0001
Organisme : National Health and Medical Research Council
ID : APP1161356
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Auzias G, Viellard M, Takerkart S, Villeneuve N, Poinso F, Da Fonséca D, Girard N, Deruelle C (2014) Atypical sulcal anatomy in young children with autism spectrum disorder. NeuroImage Clin 4:593–603. https://doi.org/10.1016/j.nicl.2014.03.008
doi: 10.1016/j.nicl.2014.03.008
pubmed: 24936410
pmcid: 4053636
Bajic D, Kumlien E, Mattsson P, Lundberg S, Wang C, Raininko R (2009) Incomplete hippocampal inversion—is there a relation to epilepsy? Eur Radiol 19(10):2544–2550. https://doi.org/10.1007/s00330-009-1438-y
doi: 10.1007/s00330-009-1438-y
pubmed: 19440714
Bates TC, Maes H, Neale MC (2019) Umx: twin and path-based structural equation modeling in R. Twin Res Hum Genet 22(1):27–41. https://doi.org/10.1017/thg.2019.2
doi: 10.1017/thg.2019.2
pubmed: 30944056
Baulac M, De Grissac N, Hasboun D, Oppenheim C, Adam C, Arzimanoglou A, Semah F, Lehéricy S, Clémenceau S, Berger B (1998) Hippocampal developmental changes in patients with partial epilepsy: magnetic resonance imaging and clinical aspects: hippocampal developmental changes and epilepsy. Ann Neurol 44(2):223–233. https://doi.org/10.1002/ana.410440213
doi: 10.1002/ana.410440213
pubmed: 9708545
Bernasconi N, Kinay D, Andermann F, Antel S, Bernasconi A (2005) Analysis of shape and positioning of the hippocampal formation: an MRI study in patients with partial epilepsy and healthy controls. Brain 128(10):2442–2452. https://doi.org/10.1093/brain/awh599
doi: 10.1093/brain/awh599
pubmed: 16014649
Borrell V (2018) How cells fold the cerebral cortex. J Neurosci 38(4):776–783. https://doi.org/10.1523/JNEUROSCI.1106-17.2017
doi: 10.1523/JNEUROSCI.1106-17.2017
pubmed: 29367288
pmcid: 6596235
Cachia A, Paillère-Martinot M-L, Galinowski A, Januel D, de Beaurepaire R, Bellivier F, Artiges E et al (2008) Cortical folding abnormalities in schizophrenia patients with resistant auditory hallucinations. Neuroimage 39(3):927–935. https://doi.org/10.1016/j.neuroimage.2007.08.049
doi: 10.1016/j.neuroimage.2007.08.049
pubmed: 17988891
Chi JG, Dooling EC, Gilles FH (1977) Gyral development of the human brain. Ann Neurol 1(1):86–93. https://doi.org/10.1002/ana.410010109
doi: 10.1002/ana.410010109
pubmed: 560818
Cikla U, Menekse G, Quraishi A, Neves G, Keles A, Liu C, Salamat SM, Baskaya MK (2016) The sulci of the inferior surface of the temporal lobe: an anatomical study: inferior surface of the temporal lobe. Clin Anat 29(7):932–942. https://doi.org/10.1002/ca.22767
doi: 10.1002/ca.22767
pubmed: 27521775
Cury C, Toro R, Cohen F, Fischer C, Mhaya A, Samper-González J, Hasboun D et al (2015) Incomplete hippocampal inversion: a comprehensive MRI study of over 2000 subjects. Front Neuroanat 9:160. https://doi.org/10.3389/fnana.2015.00160
doi: 10.3389/fnana.2015.00160
pubmed: 26733822
pmcid: 4686650
De Zubicaray GI, Chiang MC, McMahon KL, Shattuck DW, Toga AW, Martin NG, Wright MJ, Thompson PM (2008) Meeting the challenges of neuroimaging genetics. Brain Imaging Behav 2(4):258–263. https://doi.org/10.1007/s11682-008-9029-0
doi: 10.1007/s11682-008-9029-0
pubmed: 20016769
pmcid: 2794202
Ecker C, Andrews D, Dell’Acqua F, Daly E, Murphy C, Catani M, Thiebaut de Schotten M et al (2016) Relationship between cortical gyrification, white matter connectivity, and autism spectrum disorder. Cereb Cortex 26(7):3297–3309. https://doi.org/10.1093/cercor/bhw098
doi: 10.1093/cercor/bhw098
pubmed: 27130663
pmcid: 4898679
Gebre RK, Senjem ML, Raghavan S, Schwarz CG, Gunter JL, Hofrenning EI, Reid RI et al (2023) Cross-scanner harmonization methods for structural MRI may need further work: a comparison study. Neuroimage 269:119912. https://doi.org/10.1016/j.neuroimage.2023.119912
doi: 10.1016/j.neuroimage.2023.119912
pubmed: 36731814
Guadalupe T, Mathias SR, vanErp TGM, Whelan CD, Zwiers MP, Abe Y, Abramovic L et al (2017) Human subcortical brain asymmetries in 15,847 people worldwide reveal effects of age and sex. Brain Imaging Behav 11(5):1497–1514. https://doi.org/10.1007/s11682-016-9629-z
doi: 10.1007/s11682-016-9629-z
pubmed: 27738994
Guen Le, Yann GA, Leroy F, Noulhiane M, Dehaene-Lambertz G, Duchesnay E, Mangin J-F, Coulon O, Frouin V (2018) Genetic influence on the sulcal pits: on the origin of the first cortical folds. Cereb Cortex 28(6):1922–1933. https://doi.org/10.1093/cercor/bhx098
doi: 10.1093/cercor/bhx098
pubmed: 28444225
Huntgeburth SC, Petrides M (2012) Morphological patterns of the collateral sulcus in the human brain: morphology of the collateral sulcus. Eur J Neurosci 35(8):1295–1311. https://doi.org/10.1111/j.1460-9568.2012.08031.x
doi: 10.1111/j.1460-9568.2012.08031.x
pubmed: 22512258
Im K, Lee J-M, Seo SW, Kim SH, Kim SI, Duk LN (2008) Sulcal morphology changes and their relationship with cortical thickness and gyral white matter volume in mild cognitive impairment and Alzheimer’s disease. Neuroimage 43(1):103–113. https://doi.org/10.1016/j.neuroimage.2008.07.016
doi: 10.1016/j.neuroimage.2008.07.016
pubmed: 18691657
Im K, Pienaar R, Lee J-M, Joon-Kyung Seong Yu, Choi Y, Lee KH, Ellen Grant P (2011) Quantitative comparison and analysis of sulcal patterns using sulcal graph matching: a twin study. Neuroimage 57(3):1077–1086. https://doi.org/10.1016/j.neuroimage.2011.04.062
doi: 10.1016/j.neuroimage.2011.04.062
pubmed: 21596139
Im K, Raschle NM, Smith SA, Ellen Grant P, Gaab N (2016) Atypical sulcal pattern in children with developmental dyslexia and at-risk kindergarteners. Cereb Cortex 26(3):1138–1148. https://doi.org/10.1093/cercor/bhu305
doi: 10.1093/cercor/bhu305
pubmed: 25576531
Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5(2):143–156. https://doi.org/10.1016/S1361-8415(01)00036-6
doi: 10.1016/S1361-8415(01)00036-6
pubmed: 11516708
Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17(2):825–841. https://doi.org/10.1006/nimg.2002.1132
doi: 10.1006/nimg.2002.1132
pubmed: 12377157
Kim H, Bernasconi N, Bernhardt B, Colliot O, Bernasconi A (2008) Basal temporal sulcal morphology in healthy controls and patients with temporal lobe epilepsy. Neurology 70(22):2159–2165. https://doi.org/10.1212/01.wnl.0000313150.62832.79
doi: 10.1212/01.wnl.0000313150.62832.79
pubmed: 18505994
Kippenhan JS (2005) Genetic contributions to human gyrification: sulcal morphometry in Williams syndrome. J Neurosci 25(34):7840–7846. https://doi.org/10.1523/JNEUROSCI.1722-05.2005
doi: 10.1523/JNEUROSCI.1722-05.2005
pubmed: 16120786
pmcid: 6725255
Kong XZ, Mathias SR, Guadalupe T, ENIGMA Laterality Working Group, Glahn DC, Franke B, Crivello F et al (2018) Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA consortium. Proc Natl Acad Sci 115(22):E5154–E5163. https://doi.org/10.1073/pnas.1718418115
doi: 10.1073/pnas.1718418115
pubmed: 29764998
pmcid: 5984496
Kong X-Z, Postema MC, Guadalupe T, Kovel C, Boedhoe PSW, Hoogman M, Mathias SR et al (2022) Mapping brain asymmetry in health and disease through the ENIGMA consortium. Hum Brain Mapp 43(1):167–181. https://doi.org/10.1002/hbm.25033
doi: 10.1002/hbm.25033
pubmed: 32420672
Kroenke CD, Bayly PV (2018) How forces fold the cerebral cortex. J Neurosci 38(4):767–775. https://doi.org/10.1523/JNEUROSCI.1105-17.2017
doi: 10.1523/JNEUROSCI.1105-17.2017
pubmed: 29367287
pmcid: 5783962
Kruggel F, Solodkin A (2020) Heritability of structural patterning in the human cerebral cortex. Neuroimage 221:117169. https://doi.org/10.1016/j.neuroimage.2020.117169
doi: 10.1016/j.neuroimage.2020.117169
pubmed: 32693166
Libero LE, Schaer M, Li DD, Amaral DG, Nordahl CW (2019) A longitudinal study of local gyrification index in young boys with autism spectrum disorder. Cereb Cortex 29(6):2575–2587. https://doi.org/10.1093/cercor/bhy126
doi: 10.1093/cercor/bhy126
pubmed: 29850803
Lohmann G (1999) Sulcal variability of twins. Cereb Cortex 9(7):754–763. https://doi.org/10.1093/cercor/9.7.754
doi: 10.1093/cercor/9.7.754
pubmed: 10554998
Mohr A, Weisbrod M, Schellinger P, Knauth M (2004) The similarity of brain morphology in healthy monozygotic twins. Cogn Brain Res 20(1):106–110. https://doi.org/10.1016/j.cogbrainres.2004.02.001
doi: 10.1016/j.cogbrainres.2004.02.001
Neale B (2014) Liability threshold models. In: Balakrishnan N, Colton T, Everitt B, Piegorsch W, Ruggeri F, Teugels JL (eds) Wiley StatsRef: statistics reference online, 1st edn. Wiley, New York. https://doi.org/10.1002/9781118445112.stat06439
doi: 10.1002/9781118445112.stat06439
Neale MC, Cardon LR (2011) Methodology for genetic studies of twins and families. Springer, Dordrecht
Neale MC, Hunter MD, Pritikin JN, Zahery M, Brick TR, Kirkpatrick RM, Estabrook R, Bates TC, Maes HH, Boker SM (2016) OpenMx 2.0: extended structural equation and statistical modeling. Psychometrika 81(2):535–549. https://doi.org/10.1007/s11336-014-9435-8
doi: 10.1007/s11336-014-9435-8
pubmed: 25622929
Nordahl CW, Dierker D, Mostafavi I, Schumann CM, Rivera SM, Amaral DG, Van Essen DC (2007) Cortical folding abnormalities in autism revealed by surface-based morphometry. J Neurosci 27(43):11725–11735. https://doi.org/10.1523/JNEUROSCI.0777-07.2007
doi: 10.1523/JNEUROSCI.0777-07.2007
pubmed: 17959814
pmcid: 6673212
Novak K, Czech T, Prayer D, Dietrich W, Serles W, Lehr S, Baumgartner C (2002) Individual variations in the sulcal anatomy of the basal temporal lobe and its relevance for epilepsy surgery: an anatomical study performed using magnetic resonance imaging. J Neurosurg 96(3):464–473. https://doi.org/10.3171/jns.2002.96.3.0464
doi: 10.3171/jns.2002.96.3.0464
pubmed: 11883830
Ovalioglu AO, Ovalioglu TC, Canaz G, Emel E (2018) Morphologic variations of the collateral sulcus on the Mediobasal region of the temporal lobe: an anatomical study. World Neurosurg 118:e212–e216. https://doi.org/10.1016/j.wneu.2018.06.156
doi: 10.1016/j.wneu.2018.06.156
pubmed: 29966775
Penttilä J, Paillére-Martinot M-L, Martinot J-L, Mangin J-F, Burke L, Corrigall R, Frangou S, Cachia A (2008) Global and temporal cortical folding in patients with early-onset schizophrenia. J Am Acad Child Adolesc Psychiatry 47(10):1125–1132. https://doi.org/10.1097/CHI.0b013e3181825aa7
doi: 10.1097/CHI.0b013e3181825aa7
pubmed: 18725863
Penttilä J, Paillère-Martinot M-L, Martinot J-L, Ringuenet D, Wessa M, Houenou J, Gallarda T et al (2009) Cortical folding in patients with bipolar disorder or unipolar depression. J Psychiatry Neurosci 34(2):127–135
pubmed: 19270763
pmcid: 2647564
Pereira JB, Ibarretxe-Bilbao N, Marti M-J, Compta Y, Junqué C, Bargallo N, Tolosa E (2012) Assessment of cortical degeneration in patients with Parkinson’s disease by voxel-based morphometry, cortical folding, and cortical thickness. Hum Brain Mapp 33(11):2521–2534. https://doi.org/10.1002/hbm.21378
doi: 10.1002/hbm.21378
pubmed: 21898679
Pizzagalli F, Auzias G, Yang Q, Mathias SR, Faskowitz J, Boyd JD, Amini A et al (2020) The reliability and heritability of cortical folds and their genetic correlations across hemispheres. Commun Biol 3(1):510. https://doi.org/10.1038/s42003-020-01163-1
doi: 10.1038/s42003-020-01163-1
pubmed: 32934300
pmcid: 7493906
Revelle W (2022) psychTools: tools to accompany the ’psych; package for psychological research. https://CRAN.R-project.org/package=psychTools
Ritchie SJ, Cox SR, Shen X, Lombardo MV, Reus LM, Alloza C, Harris MA et al (2018) Sex differences in the adult human brain: evidence from 5216 UK Biobank participants. Cereb Cortex 28(8):2959–2975. https://doi.org/10.1093/cercor/bhy109
doi: 10.1093/cercor/bhy109
pubmed: 29771288
pmcid: 6041980
Ronan L, Fletcher PC (2015) From genes to folds: a review of cortical gyrification theory. Brain Struct Funct 220(5):2475–2483. https://doi.org/10.1007/s00429-014-0961-z
doi: 10.1007/s00429-014-0961-z
pubmed: 25511709
Routier A, Burgos N, Díaz M, Bacci M, Bottani S, El-Rifai O, Fontanella S et al (2021) Clinica: an open-source software platform for reproducible clinical neuroscience studies. Front Neuroinform 15:689675. https://doi.org/10.3389/fninf.2021.689675
doi: 10.3389/fninf.2021.689675
pubmed: 34483871
pmcid: 8415107
Ruigrok AN, Salimi-Khorshidi G, Lai MC, Baron-Cohen S, Lombardo MV, Tait RJ, Suckling J (2014) A meta-analysis of sex differences in human brain structure. Neurosci Biobehav Rev 39:34–50. https://doi.org/10.1016/j.neubiorev.2013.12.004
doi: 10.1016/j.neubiorev.2013.12.004
pubmed: 24374381
pmcid: 3969295
Strike LT, Hansell NK, Couvy-Duchesne B, Thompson PM, De Zubicaray GI, McMahon KL, Wright MJ (2019) Genetic complexity of cortical structure: differences in genetic and environmental factors influencing cortical surface area and thickness. Cereb Cortex 29(3):952–962. https://doi.org/10.1093/cercor/bhy002
doi: 10.1093/cercor/bhy002
pubmed: 29377989
Strike LT, Blokland GAM, Hansell NK, Martin NG, Toga AW, Thompson PM, De Zubicaray GI, McMahon KL, Wright MJ (2022a) Queensland twin IMaging (QTIM). Openneuro. https://doi.org/10.18112/OPENNEURO.DS004169.V1.0.6
Strike LT, Hansell NK, Chuang KH, Miller JL, de Zubicaray GI, Thompson PM, McMahon KL, Wright MJ (2022b) The Queensland twin adolescent brain project, a longitudinal study of adolescent brain development. Preprint. Neuroscience. https://doi.org/10.1101/2022.05.19.492753
doi: 10.1101/2022.05.19.492753
Strike LT, Hansell NK, Miller JL, Chuang K-H, Thompson PM, De Zubicaray GI, McMahon KL, Wright MJ (2022c) Queensland twin adolescent brain (QTAB). Openneuro. https://doi.org/10.18112/OPENNEURO.DS004146.V1.0.3
The IMAGEN consortium, Schumann G, Loth E, Banaschewski T, Barbot A, Barker G, Büchel C et al (2010) The IMAGEN study: reinforcement-related behaviour in normal brain function and psychopathology. Mol Psychiatry 15(12):1128–1139. https://doi.org/10.1038/mp.2010.4
doi: 10.1038/mp.2010.4
Troiani V, Snyder W, Kozick S, Patti MA, Beiler D (2022) Variability and concordance of sulcal patterns in the orbitofrontal cortex: a twin study. Psychiatry Rese Neuroimaging 324:111492. https://doi.org/10.1016/j.pscychresns.2022.111492
doi: 10.1016/j.pscychresns.2022.111492
Verweij KJ, Mosing MA, Zietsch BP, Medland SE (2012) Estimating heritability from twin studies. In: Elston RC, Satagopan JM, Sun S (eds) Statistical human genetics, vol 850. Methods in molecular biology. Humana Press, Totowa, pp 151–170. https://doi.org/10.1007/978-1-61779-555-8_9
doi: 10.1007/978-1-61779-555-8_9
Wen J, Thibeau-Sutre E, Diaz-Melo M, Samper-González J, Routier A, Bottani S, Dormont D, Durrleman S, Burgos N, Colliot O (2020) Convolutional neural networks for classification of Alzheimer’s disease: overview and reproducible evaluation. Med Image Anal 63:101694. https://doi.org/10.1016/j.media.2020.101694
doi: 10.1016/j.media.2020.101694
pubmed: 32417716
Yang G, Bozek J, Han M, Gao J-H (2020) Constructing and evaluating a cortical surface atlas and analyzing cortical sex differences in young Chinese adults. Hum Brain Mapp 41(9):2495–2513. https://doi.org/10.1002/hbm.24960
doi: 10.1002/hbm.24960
pubmed: 32141680
pmcid: 7267952
Yun HJ, Perez JDR, Patricia Sosa J, Valdés A, Madan N, Kitano R, Akiyama S et al (2021) Regional alterations in cortical sulcal depth in living fetuses with down syndrome. Cereb Cortex 31(2):757–767. https://doi.org/10.1093/cercor/bhaa255
doi: 10.1093/cercor/bhaa255
pubmed: 32940649
Zilles K, Armstrong E, Schleicher A, Kretschmann H-J (1988) The human pattern of gyrification in the cerebral cortex. Anat Embryol 179(2):173–179. https://doi.org/10.1007/BF00304699
doi: 10.1007/BF00304699