Brain Structure and Function

, Volume 221, Issue 4, pp 1877–1897 | Cite as

Cytoarchitecture of the human lateral occipital cortex: mapping of two extrastriate areas hOc4la and hOc4lp

  • Aleksandar Malikovic
  • Katrin Amunts
  • Axel Schleicher
  • Hartmut Mohlberg
  • Milenko Kujovic
  • Nicola Palomero-Gallagher
  • Simon B. Eickhoff
  • Karl Zilles
Original Article

Abstract

The microstructural correlates of the functional segregation of the human lateral occipital cortex are largely unknown. Therefore, we analyzed the cytoarchitecture of this region in ten human post-mortem brains using an observer-independent and statistically testable parcellation method to define the position and extent of areas in the lateral occipital cortex. Two new cytoarchitectonic areas were found: an anterior area hOc4la and a posterior area hOc4lp. hOc4la was located behind the anterior occipital sulcus in rostral and ventral portions of this region where it occupies the anterior third of the middle and inferior lateral occipital gyri. hOc4lp was found in caudal and dorsal portions of this region where it extends along the superior and middle lateral occipital gyri. The cytoarchitectonic areas were registered to 3D reconstructions of the corresponding brains, which were subsequently spatially normalized to the Montreal Neurological Institute reference space. Continuous probabilistic maps of both areas based on the analysis of ten brains were generated to characterize their inter-subject variability in location and size. The maps of hOc4la and hOc4lp were then used as seeds for meta-analytic connectivity modeling and quantitative functional decoding to identify their co-activation patterns and assignment to functional domains. Convergent evidence from their location, topography, size, functional domains and connectivity indicates that hOc4la and hOc4lp are the potential anatomical correlates of the functionally defined lateral occipital areas LO-1 and LO-2.

Keywords

Human visual cortex Cytoarchitecture Lateral occipital cortex Probabilistic maps Brain mapping Functional meta-analysis LO-1 LO-2 

References

  1. Abdollahi RO, Kolster H, Glasser MF, Robinson EC, Coalson TS, Dierker D, Jenkinson M, van Essen DC, Orban GA (2014) Correspondences between retinotopic areas and myelin maps in human visual cortex. Neuroimage 99:509–524CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amunts K, Zilles K (2001) Advances in cytoarchitectonic mapping of the human cerebral cortex. Neuroimaging Clin N Am 11:151–169PubMedGoogle Scholar
  3. Amunts K, Malikovic A, Mohlberg H, Schormann T, Zilles K (2000) Brodmann’s areas 17 and 18 brought into stereotaxic space—where and how variable? Neuroimage 11:66–84CrossRefPubMedGoogle Scholar
  4. Amunts K, Weis PH, Mohlberg H, Pieperhoff P, Gurd J, Shah JN, Marshall CJ, Fink GR, Zilles K (2004) Analysis of the neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—the role of Brodmann’s areas 44 and 45. Neuroimage 22:42–56CrossRefPubMedGoogle Scholar
  5. Amunts K, Kedo O, Kindler M, Pieperhoff P, Schneider F, Mohlberg H, Habel U, Shah JN, Zilles K (2005) Cytoarchitectonic mapping of the human amygdale, hippocampal region and entorhinal cortex. Anat Embryol 210:343–352CrossRefPubMedGoogle Scholar
  6. Amunts K, Armstrong E, Malikovic A, Hömke L, Mohlberg H, Schleicher A, Zilles K (2007) Gender-specific left-right asymmetries in human visual cortex. J Neurosci 27(6):1356–1364CrossRefPubMedGoogle Scholar
  7. Bartels P (1979) Numerical evaluation of cytologic data. II. Comparison of profiles. Anal Quant Cytol 1:77–83PubMedGoogle Scholar
  8. Caspers S, Geyer S, Schleicher A, Mohlberg H, Amunts K, Zilles K (2006) The human inferior parietal cortex: cytoarchitectonic parcellation and interindividual variability. Neuroimage 33:430–448CrossRefPubMedGoogle Scholar
  9. Caspers J, Zilles K, Eickhoff SB, Schleicher A, Mohlberg H, Amunts K (2013) Cytoarchitectonical analysis and probabilistic mapping of two extrastriate areas of the human posterior fusiform gyrus. Brain Struct Funct 218(2):511–526CrossRefPubMedPubMedCentralGoogle Scholar
  10. Choi H-J, Zilles K, Mohlberg H, Schleicher A, Fink G, Armstrong E, Amunts K (2006) Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus. J Comp Neurol 495(1):53–69CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cieslik EC, Zilles K, Caspers S, Roski C, Kellermann TS, Jakobs O, Langner R, Laird AR, Fox PT, Eickhoff S (2013) Is there “One” DLPFC in cognitive action control? Evidence for heterogeneity from co-activation-based parcellation. Cereb Cortex 23(11):2677–2689CrossRefPubMedPubMedCentralGoogle 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 18:192–205CrossRefPubMedGoogle Scholar
  13. Dupont P, De Bruyn B, Vandenberghe R, Rosier AM, Michiels J, Marchal G, Mortelmans L, Orban GA (1997) The kinetic occipital region in human visual cortex. Cereb Cortex 7:283–292CrossRefPubMedGoogle Scholar
  14. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335CrossRefPubMedGoogle Scholar
  15. Eickhoff SB, Paus T, Caspers S, Grosbras MH, Evans AC, Zilles K, Amunts K (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36:511–521CrossRefPubMedGoogle Scholar
  16. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30(9):2907–2926CrossRefPubMedPubMedCentralGoogle Scholar
  17. Eickhoff SB, Bzdok D, Laird AR, Caspers S, Zilles K, Fox PT (2011) Co-activation patterns distinguish cortical modules their connectivity and functional differentiation. Neuroimage 57(3):938–949CrossRefPubMedPubMedCentralGoogle Scholar
  18. Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT (2012) Activation likelihood estimation meta-analysis revisited. Neuroimage 59(3):2349–2361CrossRefPubMedPubMedCentralGoogle Scholar
  19. Evans AC, Collins DL, Mills SR, Brown ED, Kelly RL, Peters TM (1993) 3D statistical neuroanatomical models from 305 MRI volumes. In: Proceeding of the IEEE-NSS-MI Symposium London. MTP press, UK, pp 1813–1817Google Scholar
  20. Glasser MF, van Essen DC (2011) Mapping human cortical areas in vivo based on myelin content as revealed by T1- and T2-weighted MRI. J Neurosci 31:11597–11616CrossRefPubMedPubMedCentralGoogle Scholar
  21. Glasser MF, Goyal MS, Preuss TM, Raichle ME, van Essen DC (2014) Trends and properties of human cerebral cortex: correlations with cortical myelin content. Neuroimage 93:165–175CrossRefPubMedGoogle Scholar
  22. Goldman PS, Nauta WJH (1977) Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey. Brain Res 122:393–413CrossRefPubMedGoogle Scholar
  23. Goldman-Rakic PS (1984) Modular organization of prefrontal cortex. TINS 7:419–429Google Scholar
  24. Goldman-Rakic PS (1995) Anatomical and functional circuits in prefrontal cortex of nonhuman primates. In: Jasper HH, Riggio S, Goldman-Rakic PS (eds) Epilepsy and the Functional Anatomy of the Frontal Lobe. Raven Press, New York, pp 51–65Google Scholar
  25. Goldman-Rakic PS, Schwartz ML (1982) Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. Science 216:755–757CrossRefPubMedGoogle Scholar
  26. Grill-Spector K (2003) The neural basis of object perception. Curr Opin Neurobiol 13(2):159–166CrossRefPubMedGoogle Scholar
  27. Grill-Spector K, Kushnir T, Edelman S, Avidan G, Itzchak J, Malach R (1999) Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24:187–203CrossRefPubMedGoogle Scholar
  28. Grill-Spector K, Kourtzi Z, Kanwisher N (2001) The lateral occipital complex and its role in object recognition. Vision Res 41:1409–1422CrossRefPubMedGoogle Scholar
  29. Grossman E, Donnelly M, Price R, Pickens D, Morgan V, Neighbor G, Blake R (2000) Brain areas involved in perception of biological motion. J Cogn Neurosci 12(5):711–720CrossRefPubMedGoogle Scholar
  30. Henn S, Schormann T, Engler K, Zilles K, Witsch K (1997) Elastische Anpassung in der digitalen Bildverarbeitung auf mehreren Auflösungsstufen mit Hilfe von Mehrgitterverfahren. In: Paulus E, Wahl FM (eds) Mustererkennung 1997. Springer, Berlin, pp 392–399CrossRefGoogle Scholar
  31. Henriksson L, Karvonen J, Salminen-Vaparanta N, Railo H, Vanni S (2012) Retinotopic maps, spatial tuning, and locations of human visual areas in surface coordinates characterized with multifocal and blocked fMRI designs. PLoS One 7(5):e36859CrossRefPubMedPubMedCentralGoogle Scholar
  32. Holmes CJ, Hoge R, Collins L, Woods R, Toga AW, Evans AC (1998) Enhancement of MR images using registration for signal averaging. J Comput Assisted Tomogr 22:324–333CrossRefGoogle Scholar
  33. Hömke L (2006) A multigrid method for anisotropic PDE’s in elastic image registration. Numer Linear Algebra Appl 13:215–229CrossRefGoogle Scholar
  34. Jones SE, Buchbinder BR, Aharon I (2000) Three-dimensional mapping of cortical thickness using laplace’s equation. Hum Brain Mapp 11:12–32CrossRefPubMedGoogle Scholar
  35. Kellermann TS, Caspers S, Fox PT, Zilles K, Roski C, Laird AR, Turetsky BI, Eickhoff SB (2013) Task- and resting-state functional connectivity of brain regions related to affection and susceptible to concurrent cognitive demand. Neuroimage 72:69–82CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kolster H, Peeters R, Orban GA (2010) The retinotopic organization of the human middle temporal area MT/V5 and its cortical neighbors. J Neurosci 30(29):9801–9820CrossRefPubMedGoogle Scholar
  37. Kononen M, Paakkonen A, Pihlajamaki M, Partanen K, Karjalainen PA, Soimakallio S, Aronen HJ (2003) Visual processing of coherent rotation in the central visual field: an fMRI study. Perception 32(10):1247–1257CrossRefPubMedGoogle Scholar
  38. Kourtzi Z, Kanwisher N (2001) Representation of perceived object shape by the human lateral occipital complex. Science 293:1506–1509CrossRefPubMedGoogle Scholar
  39. Kourtzi Z, Erb M, Grodd W, Bülthoff H (2003) Representation of the perceived 3-D object shape in the human lateral occipital complex. Cereb Cortex 13(9):911–920CrossRefPubMedGoogle Scholar
  40. Kujovic M, Zilles K, Malikovic A, Schleicher A, Rottschy C, Mohlberg H, Eickhoff S, Amunts K (2013) Cytoarchitectonic mapping of the dorsal extrastriate human visual cortex. Brain Struct Funct 2018(1):157–172CrossRefGoogle Scholar
  41. Laird AR, Eickhoff SB, Kurth F, Fox PM, Uecker AM, Turner JA, Robinson JL, Lancaster JL, Fox PT (2009) ALE meta-analysis workflows via the BrainMap database: progress towards a probabilistic functional brain atlas. Front Neuroinform 3:23CrossRefPubMedPubMedCentralGoogle Scholar
  42. Laird AR, Eickhoff SB, Fox PM, Uecker AM, Ray KL, Saenz JJ Jr, McKay DR, Bzdok D, Laird RW, Robinson JL, Turner JA, Turkeltaub PE, Lancaster JL, Fox PT (2011) The BrainMap strategy for standardization, sharing, and meta-analysis of neuroimaging data. BMC Res Notes 4(349):349CrossRefPubMedPubMedCentralGoogle Scholar
  43. Larsson J, Heeger DJ (2006) Two retinotopic visual areas in human lateral occipital cortex. J Neurosci 26(51):13128–13142CrossRefPubMedPubMedCentralGoogle Scholar
  44. Larsson J, Heeger DJ, Landy MS (2010) Orientation selectivity of motion-boundary responses in human visual cortex. J Neurophysiol 104(6):2940–2950CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mahalanobis PC, Majumda DN, Rao DC (1949) Anthropometric survey of the united provinces. A statistical study. Sankhya 9:89–324Google Scholar
  46. Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RBH (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci 92:8135–8139CrossRefPubMedPubMedCentralGoogle Scholar
  47. Malikovic A, Amunts K, Schleicher A, Mohlberg H, Eickhoff SB, Wilms M, Palomero-Gallagher N, Armstrong E, Zilles K (2007) Cytoarchitectonic analysis of the human extrastriate cortex in the region V5/MT+: a probabilistic, stereotaxic map of area hOc5. Cereb Cortex 17(3):562–574CrossRefPubMedGoogle Scholar
  48. Malikovic A, Vucetic B, Milisavljevic M, Tosevski J, Sazdanovic P, Milojevic B, Malobabic S (2012) Occipital sulci of the human brain: variability and morphometry. Anat Sci Int 87(2):61–70CrossRefPubMedGoogle Scholar
  49. Merker B (1983) Silver staining of cell bodies means of physical development. J Neurosci Methods 9:235–241CrossRefPubMedGoogle Scholar
  50. Murray SO, Olshausen BA, Woods DL (2003) Processing shape, motion and three-dimensional shape-from-motion in the human cortex. Cereb Cortex 13(5):508–516CrossRefPubMedGoogle Scholar
  51. Press WA, Brewer AA, Dougherty RF, Wade AR, Wandell BA (2001) Visual areas and spatial summation in human visual cortex. Vision Res 41:1321–1332CrossRefPubMedGoogle Scholar
  52. Reetz K, Dogan I, Rolfs A, Binkofski F, Schulz JB, Laird AR, Fox PT, Eickhoff SB (2012) Investigating function and connectivity of morphometric findings-exemplified on cerebellar atrophy in spinocerebellar ataxia 17 (SCA17). Neuroimage 62(3):1354–1366CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rottschy C, Eickhoff SB, Schleicher A, Mohlberg H, Kujovic M, Zilles K, Amunts K (2007) Ventral visual cortex in humans: cytoarchitectonic mapping of two extrastriate areas. Hum Brain Mapp 28:1045–1059CrossRefPubMedGoogle Scholar
  54. Rottschy C, Caspers S, Roski C, Reetz K, Dogan I, Schulz JB, Zilles K, Laird AR, Fox PT, Eickhoff SB (2012) Differentiated parietal connectivity of frontal regions for “what” and “where” memory. Brain Struct Funct 218(6):1551–1567CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sarkheil P, Vuong QC, Bülthoff HH, Noppeney U (2008) The integration of higher order form and motion by the human brain. Neuroimage 42:1529–1536CrossRefPubMedGoogle Scholar
  56. Sarkisov SA, Filimonoff IN, Preobrashenskaya NS (1949) Cytoarchitecture of the human cortex cerebri. Medgiz, Moscow, Russia (in Russian)Google Scholar
  57. Sawamura H, Georgieva S, Vogels R, Vanduffel W, Orban GA (2005) Using functional magnetic resonance imaging to assess adaptation and size invariance of shape processing by humans and monkeys. J Neurosci 25(17):4294–4306CrossRefPubMedGoogle Scholar
  58. Sayres R, Grill-Spector K (2008) Relating retinotopic and object-selective responses in human lateral occipital cortex. J Neurophysiol 100:249–267CrossRefPubMedPubMedCentralGoogle Scholar
  59. Scheperjans F, Eickhoff SB, Hömke L, Mohlberg H, Hermann K, Amunts K, Zilles K (2008) Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in human superior parietal cortex. Cereb Cortex 18(9):2141–2157CrossRefPubMedPubMedCentralGoogle Scholar
  60. Schleicher A, Zilles K (1990) A quantitative approach to cytoarchitectonics: analysis of structural inhomogeneities in nervous tissue using an image analyser. J Microsc 157:367–381CrossRefPubMedGoogle Scholar
  61. Schleicher A, Palomero-Gallagher N, Morosan P, Zilles K (1999) Observer-independent method for microstructural parcellation of cerebral cortex: a quantitative approach to cytoarchitectonics. Neuroimage 9:165–177CrossRefPubMedGoogle Scholar
  62. Schleicher A, Amunts K, Geyer S, Kowalski T, Schormann T, Palomero-Gallagher N, Zilles K (2000) A stereological approach to human cortical architecture: identification and delineation of cortical areas. J Chem Neuroanat 20:31–47CrossRefPubMedGoogle Scholar
  63. Schleicher A, Palomero-Gallagher N, Morosan P, Eickhoff SB, Kowalski T, de Vos K, Amunts K, Zilles K (2005) Quantitative architectural analysis: a new approach to cortical mapping. Anat Embriol 210(5–6):373–386CrossRefGoogle Scholar
  64. Schmitt O, Böhme M (2002) A robust transcortical profile scanner for generating 2-d traverses in histological sections of richly curved cortical courses. Neuroimage 16:1103–1119CrossRefPubMedGoogle Scholar
  65. Seiffert AE, Somers DC, Dale AM, Tootell RBH (2003) Functional MRI studies of human visual motion perception: texture, luminance, attention and after-effects. Cereb Cortex 13(4):340–349CrossRefPubMedGoogle Scholar
  66. Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889–893CrossRefPubMedGoogle Scholar
  67. Smith AT, Greenlee MW, Singh KD, Kraemer FM, Hennig J (1998) The processing of first- and second-order motion in human visual cortex assessed by functional magnetic resonance imaging (fMRI). J Neurosci 18:3816–3830PubMedGoogle Scholar
  68. Stanley D, Rubin N (2005) Rapid detection of salient regions: evidence from apparent motion. J Vis 5:690–701CrossRefPubMedGoogle Scholar
  69. Swisher JD, Halko MA, Merabet LB, McMains SA, Somers DC (2007) Visual topography of human intraparietal sulcus. J Neurosci 27(20):5326–5337CrossRefPubMedGoogle Scholar
  70. Talairach J, Tournoux P (1988) Coplanar stereotaxic atlas of the human brain. Thieme, StuttgartGoogle Scholar
  71. Tootell RB, Hadjikhani N (2001) Where is ‘dorsal V4’ in human visual cortex? Retinotopic, topographic and functional evidence. Cereb Cortex 11:298–311CrossRefPubMedGoogle Scholar
  72. Van Oostende S, Sunaert S, Van Hecke P, Marchal G, Orban GA (1997) The kinetic occipital (KO) region in man: an fMRI study. Cereb Cortex 7(7):690–701CrossRefPubMedGoogle Scholar
  73. Vinberg J, Grill-Spector K (2008) Representation of shapes, edges and surfaces across multiple cues in the human visual cortex. J Neurophysiol 99:1380–1393CrossRefPubMedGoogle Scholar
  74. Wandell BA, Dumoulin SO, Brewer AA (2007) Visual field maps in human cortex. Neuron 56:366–383CrossRefPubMedGoogle Scholar
  75. Weiner KS, Grill-Spector K (2011) Not one extrastriate body area: using anatomical landmarks, hMT+, and visual field maps to parcellate limb-selective activations in human lateral occipitotemporal cortex. NeuroImage 56:2183–2199CrossRefPubMedPubMedCentralGoogle Scholar
  76. Wree A, Schleicher A, Zilles K (1982) Estimation of volume fractions in nervous tissue with an image analyzer. J Neurosci Methods 6:29–43CrossRefPubMedGoogle Scholar
  77. Zeki S, Perry RJ, Bartels A (2003) The processing of kinetic contours in the brain. Cereb Cortex 13(2):189–202CrossRefPubMedGoogle Scholar
  78. Zilles K, Schleicher A, Palomero-Gallagher N, Amunts K (2002) Quantitative analysis of cyto- and receptor architecture of the human brain. In: Mazziota J, Toga A (eds) Brain Mapping: the methods, 2nd edn. Academic Press, New York, pp 573–602CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Aleksandar Malikovic
    • 1
    • 2
    • 3
  • Katrin Amunts
    • 1
    • 2
  • Axel Schleicher
    • 1
  • Hartmut Mohlberg
    • 2
  • Milenko Kujovic
    • 1
  • Nicola Palomero-Gallagher
    • 2
  • Simon B. Eickhoff
    • 2
    • 4
  • Karl Zilles
    • 2
    • 5
    • 6
  1. 1.C. and O. Vogt Institute for Brain ResearchHeinrich Heine UniversityDüsseldorfGermany
  2. 2.Institute of Neuroscience and Medicine (INM-1), Research Centre JülichJülichGermany
  3. 3.Institute of Anatomy, Faculty of MedicineUniversity of BelgradeBelgradeRepublic of Serbia
  4. 4.Institute of Clinical Neuroscience and Medical PsychologyHeinrich Heine UniversityDüsseldorfGermany
  5. 5.Department of Psychiatry, Psychotherapy and PsychosomaticsRWTH Aachen UniversityAachenGermany
  6. 6.JARA-Brain, Jülich-Aachen Research AllianceJülichGermany

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