Top

Published in:

Open Access 20-04-2022 | Original Article

Morphological and hemispheric and sex differences of the anterior ascending ramus and the horizontal ascending ramus of the lateral sulcus

Authors: Yu Wang, Feifei Xu, Wenjuan Zhou, Lanwei Hou, Yuchun Tang, Shuwei Liu

Published in: Brain Structure and Function | Issue 6/2022

Abstract

Broca’s area is composed of the pars opercularis (PO) and the pars triangularis (PTR) of the inferior frontal gyrus; the anterior ascending ramus of the lateral sulcus (aals) separates the PO from the PTR, and the horizontal ascending ramus of the lateral sulcus (hals) separates the PTR from the pars orbitalis. The morphometry of these two sulci maybe has potential effects on the various functions of Broca’s area. Exploring the morphological variations, hemispheric differences and sex differences of these two sulci contributed to a better localization of Broca's area. BrainVISA was used to reconstruct and parameterize these two sulci based on data from 3D MR images of 90 healthy right-handed subjects. The 3D anatomic morphologies of these two sulci were investigated using 4 sulcal parameters: average depth (AD), average width (AW), outer length (OL) and inner length (IL). The aals and hals could be identified in 98.89% and 98.33%, respectively, of the hemispheres evaluated. The morphological patterns of these two sulci were categorized into four typical types. There were no statistically significant interhemispheric or sex differences in the frequency of the morphological patterns. There was statistically significant interhemispheric difference in the IL of the aals. Significant sex differences were found in the AD and the IL of the aals and OL of the hals. Our results not only provide a structural basis for functional studies related to Broca’s area but also are helpful in determining the precise position of Broca’s area in neurosurgery.

Alexander MP, Naeser MA, Palumbo C (1990) Broca’s area aphasias: aphasia after lesions including the frontal operculum. Neurology 40(2):353–362. https://doi.org/10.1212/wnl.40.2.353CrossRefPubMed

Amunts K, Weiss PH, Mohlberg H, Pieperhoff P, Eickhoff S, Gurd JM, Marshall JC, Shah NJ, Fink GR, Zilles K (2004) Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space–the roles of Brodmann areas 44 and 45. Neuroimage 22(1):42–56. https://doi.org/10.1016/j.neuroimage.2003.12.031CrossRefPubMed

Aylward EH, Richards TL, Berninger VW, Nagy WE, Field KM, Grimme AC, Richards AL, Thomson JB, Cramer SC (2003) Instructional treatment associated with changes in brain activation in children with dyslexia. Neurology 61(2):212–219. https://doi.org/10.1212/01.wnl.0000068363.05974.64CrossRefPubMed

Bastos Leite AJ, Scheltens P, Barkhof F (2004) Pathological aging of the brain: an overview. Top Magn Reson Imaging 15(6):369–389. https://doi.org/10.1097/01.rmr.0000168070.90113.dcCrossRefPubMed

Broca (1861) Nouvelle observation d’aphémie produite par une lésion de la moitié postérieure des deuxième et troisième circonvolutions frontales. 36:398–407

Clos M, Amunts K, Laird AR, Fox PT, Eickhoff SB (2013) Tackling the multifunctional nature of Broca’s region meta-analytically: co-activation-based parcellation of area 44. Neuroimage 83:174–188. https://doi.org/10.1016/j.neuroimage.2013.06.041CrossRefPubMed

Cosgrove KP, Mazure CM, Staley JK (2007) Evolving knowledge of sex differences in brain structure, function, and chemistry. Biol Psychiatry 62(8):847–855. https://doi.org/10.1016/j.biopsych.2007.03.001CrossRefPubMedPubMedCentral

Eser Ocak P, Kocaeli H (2017) Investigation of topographical anatomy of Broca’s area: an anatomic cadaveric study. Surg Radiol Anat 39(4):357–365. https://doi.org/10.1007/s00276-016-1748-0CrossRefPubMed

Frere PB, Vetter NC, Artiges E, Filippi I, Miranda R, Vulser H, Paillere-Martinot ML, Ziesch V, Conrod P, Cattrell A, Walter H, Gallinat J, Bromberg U, Jurk S, Menningen E, Frouin V, Papadopoulos Orfanos D, Stringaris A, Penttila J, van Noort B, Grimmer Y, Schumann G, Smolka MN, Martinot JL, Lemaitre H, Imagen c (2020) Sex effects on structural maturation of the limbic system and outcomes on emotional regulation during adolescence. Neuroimage 210:116441. doi:https://doi.org/10.1016/j.neuroimage.2019.116441

Ge J, Peng G, Lyu B, Wang Y, Zhuo Y, Niu Z, Tan LH, Leff AP, Gao JH (2015) Cross-language differences in the brain network subserving intelligible speech. Proc Natl Acad Sci USA 112(10):2972–2977. https://doi.org/10.1073/pnas.1416000112CrossRefPubMedPubMedCentral

Goucha T, Friederici AD (2015) The language skeleton after dissecting meaning: a functional segregation within Broca’s Area. Neuroimage 114:294–302. https://doi.org/10.1016/j.neuroimage.2015.04.011CrossRefPubMed

Hamelin L, Bertoux M, Bottlaender M, Corne H, Lagarde J, Hahn V, Mangin JF, Dubois B, Chupin M, de Souza LC, Colliot O, Sarazin M (2015) Sulcal morphology as a new imaging marker for the diagnosis of early onset Alzheimer’s disease. Neurobiol Aging 36(11):2932–2939. https://doi.org/10.1016/j.neurobiolaging.2015.04.019CrossRefPubMed

Han S, Ma Y (2014) Cultural differences in human brain activity: a quantitative meta-analysis. Neuroimage 99:293–300. https://doi.org/10.1016/j.neuroimage.2014.05.062CrossRefPubMed

Havas V, Gabarros A, Juncadella M, Rifa-Ros X, Plans G, Acebes JJ, de Diego BR, Rodriguez-Fornells A (2015) Electrical stimulation mapping of nouns and verbs in Broca’s area. Brain Lang 145–146:53–63. https://doi.org/10.1016/j.bandl.2015.04.005CrossRefPubMed

Heim S, Eickhoff SB, Amunts K (2008) Specialisation in Broca’s region for semantic, phonological, and syntactic fluency? Neuroimage 40(3):1362–1368. https://doi.org/10.1016/j.neuroimage.2008.01.009CrossRefPubMed

Johansson BB (2006) Cultural and linguistic influence on brain organization for language and possible consequences for dyslexia: a review. Ann Dyslexia 56(1):13–50. https://doi.org/10.1007/s11881-006-0002-6CrossRefPubMed

Keller SS, Highley JR, Garcia-Finana M, Sluming V, Rezaie R, Roberts N (2007) Sulcal variability, stereological measurement and asymmetry of Broca’s area on MR images. J Anat 211(4):534–555. https://doi.org/10.1111/j.1469-7580.2007.00793.xCrossRefPubMedPubMedCentral

Keller SS, Crow T, Foundas A, Amunts K, Roberts N (2009) Broca’s area: nomenclature, anatomy, typology and asymmetry. Brain Lang 109(1):29–48. https://doi.org/10.1016/j.bandl.2008.11.005CrossRefPubMed

Kochunov P, Mangin JF, Coyle T, Lancaster J, Thompson P, Riviere D, Cointepas Y, Regis J, Schlosser A, Royall DR, Zilles K, Mazziotta J, Toga A, Fox PT (2005) Age-related morphology trends of cortical sulci. Hum Brain Mapp 26(3):210–220. https://doi.org/10.1002/hbm.20198CrossRefPubMedPubMedCentral

Kochunov P, Thompson PM, Coyle TR, Lancaster JL, Kochunov V, Royall D, Mangin JF, Riviere D, Fox PT (2008) Relationship among neuroimaging indices of cerebral health during normal aging. Hum Brain Mapp 29(1):36–45. https://doi.org/10.1002/hbm.20369CrossRefPubMed

Kurth F, Jancke L, Luders E (2017) Sexual dimorphism of Broca’s region: More gray matter in female brains in Brodmann areas 44 and 45. J Neurosci Res 95(1–2):626–632. https://doi.org/10.1002/jnr.23898CrossRefPubMedPubMedCentral

Liu T, Wen W, Zhu W, Trollor J, Reppermund S, Crawford J, Jin JS, Luo S, Brodaty H, Sachdev P (2010) The effects of age and sex on cortical sulci in the elderly. Neuroimage 51(1):19–27. https://doi.org/10.1016/j.neuroimage.2010.02.016CrossRefPubMed

Lou Y, Zhao L, Yu S, Sun B, Hou Z, Zhang Z, Tang Y, Liu S (2019) Brain asymmetry differences between Chinese and Caucasian populations: a surface-based morphometric comparison study. Brain Imaging Behav. https://doi.org/10.1007/s11682-019-00184-7CrossRef

Luders E, Gaser C, Jancke L, Schlaug G (2004) A voxel-based approach to gray matter asymmetries. Neuroimage 22(2):656–664. https://doi.org/10.1016/j.neuroimage.2004.01.032CrossRefPubMed

Luders E, Kurth F, Toga AW, Narr KL, Gaser C (2013) Meditation effects within the hippocampal complex revealed by voxel-based morphometry and cytoarchitectonic probabilistic mapping. Front Psychol 4:398. https://doi.org/10.3389/fpsyg.2013.00398CrossRefPubMedPubMedCentral

Mohammadi H, Joghataei MT, Rahimi Z, Faghihi F, Khazaie H, Farhangdoost H, Mehrpour M (2017) Sex steroid hormones and sex hormone binding globulin levels, CYP17 MSP AI (-34T:C) and CYP19 codon 39 (Trp:Arg) variants in children with developmental stuttering. Brain Lang 175:47–56. https://doi.org/10.1016/j.bandl.2017.09.004CrossRefPubMed

Petrides M (2014) Neuroanatomy of language regions of the human brain. Academic Press

Petrides M, Pandya DN (2002) Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci 16(2):291–310. https://doi.org/10.1046/j.1460-9568.2001.02090.xCrossRefPubMed

Petrides M, Alivisatos B, Meyer E, Evans AC (1993) Functional activation of the human frontal cortex during the performance of verbal working memory tasks. Proc Natl Acad Sci USA 90(3):878–882. https://doi.org/10.1073/pnas.90.3.878CrossRefPubMedPubMedCentral

Petrides M (2016) The ventrolateral frontal region. In: Neurobiology of Language. Elsevier, pp 25–33

Powell JL, Kemp GJ, Roberts N, Garcia-Finana M (2012) Sulcal morphology and volume of Broca’s area linked to handedness and sex. Brain Lang 121(3):206–218. https://doi.org/10.1016/j.bandl.2012.03.003CrossRefPubMed

Schaffler L, Luders HO, Dinner DS, Lesser RP, Chelune GJ (1993) Comprehension deficits elicited by electrical stimulation of Broca’s area. Brain 116(Pt 3):695–715. https://doi.org/10.1093/brain/116.3.695CrossRefPubMed

Siok WT, Perfetti CA, Jin Z, Tan LH (2004) Biological abnormality of impaired reading is constrained by culture. Nature 431(7004):71–76. https://doi.org/10.1038/nature02865CrossRefPubMed

Siok WT, Niu Z, Jin Z, Perfetti CA, Tan LH (2008) A structural-functional basis for dyslexia in the cortex of Chinese readers. Proc Natl Acad Sci USA 105(14):5561–5566. https://doi.org/10.1073/pnas.0801750105CrossRefPubMedPubMedCentral

Sprung-Much T, Petrides M (2020) Morphology and spatial probability maps of the horizontal ascending ramus of the lateral fissure. Cereb Cortex 30(3):1586–1602. https://doi.org/10.1093/cercor/bhz189CrossRefPubMed

Sun YF, Lee JS, Kirby R (2010) Brain imaging findings in dyslexia. Pediatr Neonatol 51(2):89–96. https://doi.org/10.1016/S1875-9572(10)60017-4CrossRefPubMed

Tang Y, Zhao L, Lou Y, Shi Y, Fang R, Lin X, Liu S, Toga A (2018) Brain structure differences between Chinese and Caucasian cohorts: a comprehensive morphometry study. Hum Brain Mapp 39(5):2147–2155. https://doi.org/10.1002/hbm.23994CrossRefPubMedPubMedCentral

Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385(6614):313–318. https://doi.org/10.1038/385313a0CrossRefPubMed

Westphal AJ, Reggente N, Ito KL, Rissman J (2016) Shared and distinct contributions of rostrolateral prefrontal cortex to analogical reasoning and episodic memory retrieval. Hum Brain Mapp 37(3):896–912. https://doi.org/10.1002/hbm.23074CrossRefPubMed

Wu CY, Ho MH, Chen SH (2012) A meta-analysis of fMRI studies on Chinese orthographic, phonological, and semantic processing. Neuroimage 63(1):381–391. https://doi.org/10.1016/j.neuroimage.2012.06.047CrossRefPubMed

Xu J, Kobayashi S, Yamaguchi S, Iijima K, Okada K, Yamashita K (2000) Gender effects on age-related changes in brain structure. AJNR Am J Neuroradiol 21(1):112–118PubMedPubMedCentral

Xu M, Baldauf D, Chang CQ, Desimone R, Tan LH (2017) Distinct distributed patterns of neural activity are associated with two languages in the bilingual brain. Sci Adv 3(7):e1603309. https://doi.org/10.1126/sciadv.1603309CrossRefPubMedPubMedCentral

Xu M, Liang X, Ou J, Li H, Luo YJ, Tan LH (2020) Sex Differences in functional brain networks for language. Cereb Cortex 30(3):1528–1537. https://doi.org/10.1093/cercor/bhz184CrossRefPubMed

Title: Morphological and hemispheric and sex differences of the anterior ascending ramus and the horizontal ascending ramus of the lateral sulcus
Authors: Yu Wang
Feifei Xu
Wenjuan Zhou
Lanwei Hou
Yuchun Tang
Shuwei Liu
Publication date: 20-04-2022
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 6/2022
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-022-02482-1

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Morphological and hemispheric and sex differences of the anterior ascending ramus and the horizontal ascending ramus of the lateral sulcus

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 6/2022

Myelin water fraction in relation to fractional anisotropy and reading in 10-year-old children

Aberrant topological organization and age-related differences in the human connectome in subjective cognitive decline by using regional morphology from magnetic resonance imaging

Comparative anatomical analysis of dopamine systems in Mus musculus and Peromyscus californicus

Cortico-amygdalar connectivity and externalizing/internalizing behavior in children with neurodevelopmental disorders

Cortical thickness of primary motor and vestibular brain regions predicts recovery from fall and balance directly after spaceflight

Meditation-induced effects on whole-brain structural and effective connectivity