Advertisement

Brain Structure and Function

, Volume 223, Issue 9, pp 4125–4152 | Cite as

Morphological patterns and spatial probability maps of two defining sulci of the posterior ventrolateral frontal cortex of the human brain: the sulcus diagonalis and the anterior ascending ramus of the lateral fissure

  • Trisanna Sprung-Much
  • Michael Petrides
Original Article
  • 353 Downloads

Abstract

The sulcus diagonalis (ds) and the anterior ascending ramus of the lateral fissure (aalf) are two defining sulci of the posterior ventrolateral frontal cortex, which is also known as the anterior language region in the language dominant hemisphere. The aalf extends dorsally from the lateral fissure, separating the pars opercularis from the pars triangularis of the inferior frontal gyrus. The ds, which is a relatively vertical sulcus, is found within the pars opercularis. Given the proximity and similar orientation of these two sulci, it can be difficult to identify them properly. The present study provides a means of differentiating these two sulci accurately using magnetic resonance imaging (MRI). Voxels within the ds and the aalf were labeled in 40 in vivo MRI volumes (1.5 T) that had been linearly registered to the Montreal Neurological Institute stereotaxic space to examine the morphological patterns of these two sulci and classify these patterns based on relations with neighboring sulci. The morphological variability and spatial extent of each sulcus was then quantified in the form of volumetric and surface spatial probability maps. The ds, a rather superficial sulcus, could be identified in 51.25% of hemispheres. The aalf, on the other hand, could be identified in 96.25% of hemispheres and was observed to extend medially, deep below the surface of the hemisphere, to reach the circular sulcus of the insula. Understanding the details of the sulcal morphology of this region, which, in the language dominant left hemisphere, constitutes Broca’s area, is crucial to functional and structural neuroimaging studies investigating language.

Keywords

Sulcus diagonalis Anterior ascending ramus of the lateral fissure Ventrolateral frontal cortex Magnetic resonance imaging Sulcal morphology Spatial probability map 

Notes

Acknowledgements

We thank Philip Novosad for technical assistance with Matlab and MINC Toolkit, as well for providing helpful feedback during manuscript revision. We also thank Guy Sprung and Dr. Sonja Huntgeburth for assistance in translating from German pertinent sections of Eberstaller’s manuscript, and Dr. Rhonda Amsel for statistical advice.

Funding

This research was supported by the Canadian Institutes of Health Research (CIHR) Foundation Grant FDN-143212 awarded to M. Petrides and a Fonds de Recherche du Québec - Santé scholarship awarded to T. Sprung-Much.

Compliance with ethical standards

Ethical standards

The authors declare that they have no competing financial or non-financial interests. All research was conducted in compliance with ethical standards.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

References

  1. Amiez C, Kostopoulos P, Champod A-S, Petrides M (2006) Local morphology predicts functional organization of the dorsal premotor region in the human brain. J Neurosci 26:2724–2731CrossRefGoogle Scholar
  2. Amiez C, Neveu R, Warrot D, Petrides M, Knoblauch K, Procyk E (2013) The location of feedback-related activity in the midcingulate cortex is predicted by local morphology. J Neurosci 33:2217–2228CrossRefGoogle Scholar
  3. Amunts K, Schleicher A, Bürgel U, Mohlberg H, Uylings H, Zilles K (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412:319–341CrossRefGoogle Scholar
  4. Amunts K et al (2004) Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—the roles of Brodmann areas 44 and 45. NeuroImage 22:42–56CrossRefGoogle Scholar
  5. Bailey P, Bonin G (1951) The isocortex of man. University of Illinois Press, UrbanaGoogle Scholar
  6. Betz W (1881) Ueber die feinere Structur der Gehirnrinde des Menschen. Zentralbl Med Wiss 19:193–195Google Scholar
  7. Broca P (1861) Remarques sur le siège de la faculté du langage articulé, suivies d’une observation d’aphémie (perte de la parole). Bulletin et Memoires de la Société Anatomique de Paris 6:330–357Google Scholar
  8. Brodmann K (1908) Beiträge zur histologischen Lokalisation der Grosshirnrinde. VI. Mitteilung: die Cortexgliederung des Menschen. Journal für Psychologie und Neurologie 10:231–246Google Scholar
  9. Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Barth, LeipzigGoogle Scholar
  10. Brodmann K (1910) Feinere Anatomie des Grosshirns. In: Lewandowsky M (ed) Handbuch der Neurologie. Springer, Berlin, pp 206–307CrossRefGoogle Scholar
  11. Campbell AW (1904) Histological studies on the localisation of cerebral function. Br J Psychiatry 50:651–662Google Scholar
  12. Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18:192–205CrossRefGoogle Scholar
  13. Corballis MC (2003) From mouth to hand: gesture, speech, and the evolution of right-handedness. Behav Brain Sci 26:199–208Google Scholar
  14. Cunningham DJ (1905) Textbook of anatomy. W. Wood and company, New YorkGoogle Scholar
  15. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9:179–194CrossRefGoogle Scholar
  16. Dejerine J (1914) Semiologie des affections du système nerveux. Masson, ParisGoogle Scholar
  17. Dronkers NF, Plaisant O, Iba-Zizen MT, Cabanis EA (2007) Paul Broca’s historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. Brain 130:1432–1441CrossRefGoogle Scholar
  18. Eberstaller O (1890) Das Stirnhirn: ein Beitrag zur Anatomie der Oberfläche des Grosshirns. Urban & Schwarzenberg, WeinGoogle Scholar
  19. Economo C, Koskinas GN (1925) Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. J. Springer, WeinGoogle Scholar
  20. Evans AC, Collins DL, Mills S, Brown E, Kelly R, Peters TM (1993) 3D statistical neuroanatomical models from 305 MRI volumes. In: IEEE conference record nuclear science symposium and medical imaging conference, San Francisco, CA, USA, pp 1813–1817Google Scholar
  21. Falzi G, Perrone P, Vignolo LA (1982) Right-left asymmetry in anterior speech region. Arch Neurol 39:239–240CrossRefGoogle Scholar
  22. Fischl B, Sereno MI, Dale AM (1999a) Cortical surface-based analysis. II. Inflation, flattening, and a surface-based coordinate system. NeuroImage 9:195–207CrossRefGoogle Scholar
  23. Fischl B, Sereno MI, Tootell RB, Dale AM (1999b) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272–284CrossRefGoogle Scholar
  24. Fischl B et al (2007) Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex 18:1973–1980CrossRefGoogle Scholar
  25. Fonov V, Evans AC, Botteron K, Almli CR, McKinstry RC, Collins DL, Brain Development Cooperative Group (2011) Unbiased average age-appropriate atlases for pediatric studies. NeuroImage 54:313–327CrossRefGoogle Scholar
  26. Foundas AL, Leonard CM, Gilmore RL, Fennell EB, Heilman KM (1996) Pars triangularis asymmetry and language dominance. Proc Natl Acad Sci USA 93:719–722CrossRefGoogle Scholar
  27. Foundas AL, Eure KF, Luevano LF, Weinberger DR (1998) MRI asymmetries of Broca’s area: the pars triangularis and pars opercularis. Brain Lang 64:282–296CrossRefGoogle Scholar
  28. Foundas AL, Bollich AM, Corey DM, Hurley M, Heilman KM (2001) Anomalous anatomy of speech–language areas in adults with persistent developmental stuttering. Neurology 57:207–215CrossRefGoogle Scholar
  29. Galaburda AM (1980) La région de Broca: observations anatomiques faites un siècle après la mort de son découvreur. Rev Neurol (Paris) 136:609–616Google Scholar
  30. Garey LJ (2006) Brodmann’s ‘localisation in the cerebral cortex’, 3rd edn. Springer, New YorkGoogle Scholar
  31. Germann J, Robbins S, Halsband U, Petrides M (2005) Precentral sulcal complex of the human brain: morphology and statistical probability maps. J Comp Neurol 493:334–356CrossRefGoogle Scholar
  32. Horwitz B, Amunts K, Bhattacharyya R, Patkin D, Jeffries K, Zilles K, Braun AR (2003) Activation of Broca’s area during the production of spoken and signed language: a combined cytoarchitectonic mapping and PET analysis. Neuropsychologia 41:1868–1876CrossRefGoogle Scholar
  33. Huntgeburth SC, Petrides M (2016) Three-dimensional probability maps of the rhinal and the collateral sulci in the human brain. Brain Struct Funct 221:4235–4255CrossRefGoogle Scholar
  34. Iaria G, Petrides M (2007) Occipital sulci of the human brain: variability and probability maps. J Comp Neurol 501:243–259CrossRefGoogle Scholar
  35. Klein D, Milner B, Zatorre RJ, Meyer E, Evans AC (1995) The neural substrates underlying word generation: a bilingual functional-imaging study. Proc Natl Acad Sci USA 92:2899–2903CrossRefGoogle Scholar
  36. Klein D, Zatorre RJ, Chen J-K, Milner B, Crane J, Belin P, Bouffard M (2006) Bilingual brain organization: a functional magnetic resonance adaptation study. NeuroImage 31:366–375CrossRefGoogle Scholar
  37. Knaus TA, Corey DM, Bollich AM, Lemen LC, Foundas AL (2007) Anatomical asymmetries of anterior perisylvian speech-language regions. Cortex 43:499–510CrossRefGoogle Scholar
  38. Kostopoulos P, Petrides M (2003) The mid-ventrolateral prefrontal cortex: insights into its role in memory retrieval. Eur J Neurosci 17:1489–1497CrossRefGoogle Scholar
  39. Kostopoulos P, Petrides M (2008) Left mid-ventrolateral prefrontal cortex: underlying principles of function. Eur J Neurosci 27:1037–1049CrossRefGoogle Scholar
  40. Kostopoulos P, Petrides M (2016) Selective memory retrieval of auditory what and auditory where involves the ventrolateral prefrontal cortex. Proc Natl Acad Sci USA 113:1919–1924CrossRefGoogle Scholar
  41. Lee YS, Turkeltaub P, Granger R, Raizada RD (2012) Categorical speech processing in Broca’s area: an fMRI study using multivariate pattern-based analysis. J Neurosci 32:3942–3948CrossRefGoogle Scholar
  42. LeMay M (1976) Morphological cerebral asymmetries of modern man, fossil man, and nonhuman primate. Ann N Y Acad Sci 280:349–366CrossRefGoogle Scholar
  43. Manjón JV, Coupé P, Martí-Bonmatí L, Collins DL, Robles M (2010) Adaptive non-local means denoising of MR images with spatially varying noise levels. J Magn Reson Imaging 31:192–203CrossRefGoogle Scholar
  44. Mazziotta JC, Toga AW, Evans AC, Fox PT, Lancaster JL (1995a) A probabilistic atlas of the human brain: theory and rationale for its development. The International Consortium for Brain Mapping (ICBM). NeuroImage 2:89–101CrossRefGoogle Scholar
  45. Mazziotta JC, Toga AW, Evans AC, Fox PT, Lancaster JL (1995b) Digital brain atlases. Trends Neurosci 18:210–211CrossRefGoogle Scholar
  46. Mazziotta J et al (2001) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356:1293–1322CrossRefGoogle Scholar
  47. Mock JR, Zadina JN, Corey DM, Cohen JD, Lemen LC, Foundas AL (2012) Atypical brain torque in boys with developmental stuttering. Dev Neuropsychol 37:434–452CrossRefGoogle Scholar
  48. Mohr JP (1976) Broca’s area and Broca’s aphasia. In: Whitaker H, Whitaker HA (eds) Studies in neurolinguistics, vol 1. Academic Press, New York, pp 201–233Google Scholar
  49. Mohr J et al (1978) The Harvard Cooperative Stroke Registry: a prospective registry. Neurology 28:754–762CrossRefGoogle Scholar
  50. Ono M, Kubik S, Abernathey CD (1990) Atlas of the cerebral sulci. Thieme, StuttgartGoogle Scholar
  51. Papoutsi M, de Zwart JA, Jansma JM, Pickering MJ, Bednar JA, Horwitz B (2009) From phonemes to articulatory codes: an fMRI study of the role of Broca’s area in speech production. Cereb Cortex 19:2156–2165CrossRefGoogle Scholar
  52. Paus T et al (1996) Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map. Cereb Cortex 6:207–214CrossRefGoogle Scholar
  53. Penfield W, Rasmussen T (1950) The cerebral cortex of man: a clinical study of localization of function. Macmillan, New YorkGoogle Scholar
  54. Penfield W, Roberts L (1959) Speech and brain mechanisms. Princeton University Press, New JerseyGoogle Scholar
  55. Petrides M (1994) Frontal lobes and working memory: evidence from investigations of the effects of cortical excision in nonhuman primates. In: Boller F, Grafman J (eds) Handbook of neuropsychology, vol 9. Elsevier, Amsterdam, pp 959–981Google Scholar
  56. Petrides M (1996) Specialized systems for the processing of mnemonic information within the primate frontal cortex. Philos Trans R Soc Lond B Biol Sci 351:1455–1462CrossRefGoogle Scholar
  57. Petrides M (2006) Broca’s area in the human and the non-human primate brain. In: Grodzinsky Y, Amunts K (eds) Broca’s region. Oxford University Press, Oxford, pp 31–48CrossRefGoogle Scholar
  58. Petrides M (2012) The human cerebral cortex: an MRI atlas of the sulci and gyri in MNI stereotaxic space. Academic Press, ChicagoGoogle Scholar
  59. Petrides M (2014) Neuroanatomy of language regions of the human brain. Academic Press, ChicagoGoogle Scholar
  60. Petrides M (2016) The ventrolateral frontal region. In: Hickok G, Small SL (eds) Neurobiology of language. Academic Press, London, pp 25–33CrossRefGoogle Scholar
  61. Petrides M, Pandya DN (1984) Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. J Comp Neurol 228:105–116CrossRefGoogle Scholar
  62. Petrides M, Pandya DN (1988) Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey. J Comp Neurol 273:52–66CrossRefGoogle Scholar
  63. Petrides M, Pandya DN (1994) Comparative cytoarchitectonic analysis of the human and the macaque frontal cortex. In: Boller F, Grafman J (eds) Handbook of neuropsychology, vol 9. Elsevier, Amsterdam, pp 17–58Google Scholar
  64. 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 16:291–310CrossRefGoogle Scholar
  65. 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 90:878–882CrossRefGoogle Scholar
  66. Petrides M, Alivisatos B, Evans AC (1995) Functional activation of the human ventrolateral frontal cortex during mnemonic retrieval of verbal information. Proc Natl Acad Sci USA 92:5803–5807CrossRefGoogle Scholar
  67. Rasmussen T, Milner B (1975) Clinical and surgical studies of the cerebral speech areas in man. In: Zülch KJ, Cretzfeldt O, Galbraith GC (eds) Cerebral localization. Springer, Berlin, pp 238–257CrossRefGoogle Scholar
  68. Sarkissov S, Filimonoff I, Kononowa E, Preobraschenskaja I, Kukuew L (1955) Atlas of the cytoarchitectonics of the human cerebral cortex. Medgiz, MoscowGoogle Scholar
  69. Segal E, Petrides M (2013) Functional activation during reading in relation to the sulci of the angular gyrus region. Eur J Neurosci 38:2793–2801CrossRefGoogle Scholar
  70. Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97CrossRefGoogle Scholar
  71. Smith GE (1907) A new topographical survey of the human cerebral cortex, being an account of the distribution of the anatomically distinct cortical areas and their relationship to the cerebral sulci. J Anat Physiol 41:237–254PubMedPubMedCentralGoogle Scholar
  72. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New YorkGoogle Scholar
  73. Toga AW, Thompson PM (2003) Mapping brain asymmetry. Nat Rev Neurosci 4:37–48CrossRefGoogle Scholar
  74. Tomaiuolo F, Giordano F (2016) Cerebal sulci and gyri are intrinsic landmarks for brain navigation in individual subjects: an instrument to assist neurosurgeons in preserving cognitive function in brain tumour surgery (Commentary on Zlatkina et al.). Eur J Neurosci 43:1266–1267CrossRefGoogle Scholar
  75. Tomaiuolo F, MacDonald J, Caramanos Z, Posner G, Chiavaras M, Evans AC, Petrides M (1999) Morphology, morphometry and probability mapping of the pars opercularis of the inferior frontal gyrus: an in vivo MRI analysis. Eur J Neurosci 11:3033–3046CrossRefGoogle Scholar
  76. Vincent RD, Buckthought A, MacDonald D (2016) Display 2.0: software for visualization and segmentation of surfaces and volumes. McConnell Brain Imaging Centre, Montreal Neurological Institute, Montreal, Quebec, CanadaGoogle Scholar
  77. Wada JA, Clarke R, Hamm A (1975) Cerebral hemispheric asymmetry in humans. Cortical speech zones in 100 adult and 100 infant brains. Arch Neurol 32:239–246CrossRefGoogle Scholar
  78. Wernicke C (1874) Der aphasische Symptomencomplex. Eine psychologische Studie auf anatomischer Basis. M. Cohn and Weigert, BreslauGoogle Scholar
  79. Zlatkina V, Petrides M (2014) Morphological patterns of the intraparietal sulcus and the anterior intermediate parietal sulcus of Jensen in the human brain. Proc Biol Sci 281:20141493CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Neurology and NeurosurgeryMontreal Neurological Institute and Hospital, McGill UniversityMontrealCanada
  2. 2.Department of PsychologyMcGill UniversityMontrealCanada

Personalised recommendations