Advertisement

Brain Structure and Function

, Volume 223, Issue 7, pp 3107–3119 | Cite as

A lateral-to-mesial organization of human ventral visual cortex at birth

  • P. Barttfeld
  • S. Abboud
  • H. Lagercrantz
  • U. Adén
  • N. Padilla
  • A. D. Edwards
  • L. Cohen
  • M. Sigman
  • S. Dehaene
  • G. Dehaene-Lambertz
Original Article
  • 305 Downloads

Abstract

In human adults, ventral extra-striate visual cortex contains a mosaic of functionally specialized areas, some responding preferentially to natural visual categories such as faces (fusiform face area) or places (parahippocampal place area) and others to cultural inventions such as written words and numbers (visual word form and number form areas). It has been hypothesized that this mosaic arises from innate biases in cortico-cortical connectivity. We tested this hypothesis by examining functional resting-state correlation at birth using fMRI data from full-term human newborns. The results revealed that ventral visual regions are functionally connected with their contra-lateral homologous regions and also exhibit distinct patterns of long-distance functional correlation with anterior associative regions. A mesial-to-lateral organization was observed, with the signal of the more lateral regions, including the sites of visual word and number form areas, exhibiting higher correlations with voxels of the prefrontal, inferior parietal and temporal cortices, including language areas. Finally, we observed hemispheric asymmetries in the functional correlation of key areas of the language network that may influence later adult hemispheric lateralization. We suggest that long-distance circuits present at birth constrain the subsequent functional differentiation of the ventral visual cortex.

Keywords

Neonates Brain Functional connectivity Language 

Notes

Acknowledgements

Authors would like to thank Elvis Dohmatob, Isabelle Denghien, François Leroy, Jessica Dubois and Parvaneh Adibpour for their constructive remarks during this work.

Supplementary material

429_2018_1676_MOESM1_ESM.pdf (2.7 mb)
Supplementary material 1 (PDF 2,686 KB)

References

  1. Alcauter S et al (2014) Development of thalamocortical connectivity during infancy and its cognitive correlations. J Neurosci 34:9067–9075CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amalric M, Dehaene S (2016) Origins of the brain networks for advanced mathematics in expert mathematicians. Proc Natl Acad Sci USA 113(18):4909–4917.  https://doi.org/10.1073/pnas.1603205113 CrossRefPubMedGoogle Scholar
  3. Arcaro MJ, Livingstone MS (2017) A hierarchical, retinotopic proto-organization of the primate visual system at birth. Elife.  https://doi.org/10.7554/eLife.26196 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Arichi T, Moraux A, Melendez A, Doria V, Groppo M, Merchant N, Edwards AD (2010) Somatosensory cortical activation identified by functional MRI in preterm and term infants. Neuroimage 49(3):2063–2071.  https://doi.org/10.1016/j.neuroimage.2009.10.038 CrossRefPubMedGoogle Scholar
  5. Bartocci M, Bergqvist LL, Lagercrantz H, Anand KJ (2006) Pain activates cortical areas in the preterm newborn brain. Pain 122(1–2):109–117CrossRefPubMedGoogle Scholar
  6. Bénézit A et al (2015) Organising white matter in a brain without corpus callosum fibres. Cortex.  https://doi.org/10.1016/j.cortex.2014.08.022 PubMedCrossRefGoogle Scholar
  7. Biagi L, Crespi SA, Tosetti M, Morrone MC (2015) BOLD response selective to flow-motion in very young infants. PLoS Biol 13(9):e1002260.  https://doi.org/10.1371/journal.pbio.1002260 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bristow D et al (2009) Hearing faces: how the infant brain matches the face it sees with the speech it hears. J Cogn Neurosci 21:905–921CrossRefPubMedGoogle Scholar
  9. Burnham D (1993) Visual recognition of mother by young infants: facilitation by speech. Perception 22:1133–1153CrossRefPubMedGoogle Scholar
  10. Cai Q, Paulignan Y, Brysbaert M, Ibarrola D, Nazir TA (2010) The left ventral occipito-temporal response to words depends on language lateralization but not on visual familiarity. Cereb Cortex 20(5):1153–1163.  https://doi.org/10.1093/cercor/bhp175 CrossRefPubMedGoogle Scholar
  11. Caspers J, Palomero-Gallagher N, Caspers S, Schleicher A, Amunts K, Zilles K (2015) Receptor architecture of visual areas in the face and word-form recognition region of the posterior fusiform gyrus. Brain Struct Funct 220(1):205–219.  https://doi.org/10.1007/s00429-013-0646-z CrossRefPubMedGoogle Scholar
  12. Chen X, Striano T, Rakoczy H (2004) Auditory-oral matching behavior in newborns. Dev Sci 7:42–47CrossRefPubMedGoogle Scholar
  13. Deen B, Richardson H, Dilks DD, Takahashi A, Keil B, Wald LL, Saxe R (2017) Organization of high-level visual cortex in human infants. Nat Commun 8:13995.  https://doi.org/10.1038/ncomms13995 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Dehaene S, Cohen L (2011) The unique role of the visual word form area in reading. Trends Cogn Sci 15:254–262CrossRefPubMedGoogle Scholar
  15. Dehaene S et al (2010) How learning to read changes the cortical networks for vision and language. Science 330:1359–1364CrossRefPubMedGoogle Scholar
  16. Di Virgilio G, Clarke S (1997) Direct interhemispheric visual input to human speech areas. Human Brain Mapp 5:347–354CrossRefGoogle Scholar
  17. Doria V, Beckmann CF, Arichi T, Merchant N, Groppo M, Turkheimer FE, Edwards AD et al (2010) Emergence of resting state networks in the preterm human brain. Proc Natl Acad Sci USA 107(46):20015–20020.  https://doi.org/10.1073/pnas.1007921107 CrossRefPubMedGoogle Scholar
  18. Dubois J et al (2014) The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276:48–71CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dubois J, Adibpour P, Poupon C, Hertz-Pannier L, Dehaene-Lambertz G (2016) MRI and M/EEG studies of the white matter development in human fetuses and infants: review and opinion. Brain Plast 2:49–69CrossRefPubMedPubMedCentralGoogle Scholar
  20. Elman JL, Bates E, Johnson MH, Karmiloff-Smith A, Parisi D, Plunkett K (1996) Rethinking innateness: a connectionist perspective on development. MIT Press, CambridgeGoogle Scholar
  21. Embree L, James W (1983) The principles of psychology. Philos Phenomenol Res 44:124CrossRefGoogle Scholar
  22. Fischl B, Rajendran N, Busa E, Augustinack J, Hinds O, Yeo BT, Zilles K (2008) Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex 18(8):1973–1980.  https://doi.org/10.1093/cercor/bhm225 CrossRefPubMedGoogle Scholar
  23. Fransson P, Skiold B, Horsch S, Nordell A, Blennow M, Lagercrantz H, Aden U (2007) Resting-state networks in the infant brain. Proc Natl Acad Sci USA 104(39):15531–15536CrossRefPubMedGoogle Scholar
  24. Fransson P, Skiold B, Engstrom M, Hallberg B, Mosskin M, Aden U, Blennow M (2009) Spontaneous brain activity in the newborn brain during natural sleep—an fMRI study in infants born at full term. Pediatr Res 66(3):301–305.  https://doi.org/10.1203/PDR.0b013e3181b1bd84 CrossRefPubMedGoogle Scholar
  25. Fransson P, Aden U, Blennow M, Lagercrantz H (2011) The functional architecture of the infant brain as revealed by resting-state fMRI. Cereb Cortex 21(1):145–154.  https://doi.org/10.1093/cercor/bhq071 CrossRefPubMedGoogle Scholar
  26. Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, Van Essen DC (2016) A multi-modal parcellation of human cerebral cortex. Nature 536(7615):171–178.  https://doi.org/10.1038/nature18933 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gomez J, Barnett MA, Natu V, Mezer A, Palomero-Gallagher N, Weiner KS, Grill-Spector K (2017) Microstructural proliferation in human cortex is coupled with the development of face processing. Science 355(6320):68–71.  https://doi.org/10.1126/science.aag0311 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hannagan T, Amedi A, Cohen L, Dehaene-Lambertz G, Dehaene S (2015) Origins of the specialization for letters and numbers in ventral occipitotemporal cortex. Trends Cogn Sci 19(7):374–382.  https://doi.org/10.1016/j.tics.2015.05.006 CrossRefPubMedGoogle Scholar
  29. Huth AG, de Heer WA, Griffiths TL, Theunissen FE, Gallant JL (2016) Natural speech reveals the semantic maps that tile human cerebral cortex. Nature 532:453–458CrossRefPubMedPubMedCentralGoogle Scholar
  30. Innocenti GM, Berbel P, Clarke S (1988) Development of projections from auditory to visual areas in the cat. J Comp Neurol 272:242–259CrossRefPubMedGoogle Scholar
  31. Johnson MH (2011) Interactive specialization: a domain-general framework for human functional brain development? Dev Cogn Neurosci 1(1):7–21.  https://doi.org/10.1016/j.dcn.2010.07.003 CrossRefPubMedGoogle Scholar
  32. Kabdebon C, Leroy F, Simmonet H, Perrot M, Dubois J, Dehaene-Lambertz G (2014) Anatomical correlations of the international 10–20 sensor placement system in infants. Neuroimage 99:342–356.  https://doi.org/10.1016/j.neuroimage.2014.05.046 CrossRefPubMedGoogle Scholar
  33. Kennedy DN et al (1999) Structural and functional brain asymmetries in human situs inversus totalis. Neurology 53:1260–1265CrossRefPubMedGoogle Scholar
  34. Kostović I, Judaš M (2010) The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatr 99:1119–1127CrossRefPubMedGoogle Scholar
  35. Leroy F et al. (2011) Atlas-free surface reconstruction of the cortical grey-white interface in infants. PLoS ONE 6.  https://doi.org/10.1371/journal.pone.0027128 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Mahmoudzadeh M, Dehaene-Lambertz G, Fournier M, Kongolo G, Goudjil S, Dubois J, Wallois F (2013) Syllabic discrimination in premature human infants prior to complete formation of cortical layers. Proc Natl Acad Sci USA 110(12):4846–4851.  https://doi.org/10.1073/pnas.1212220110 CrossRefPubMedGoogle Scholar
  37. Mahmoudzadeh M, Wallois F, Kongolo G, Goudjil S, Dehaene-Lambertz G (2016) Functional maps at the onset of auditory inputs in very early preterm human neonates. Cerebral CortexGoogle Scholar
  38. Marín-Padilla M (2011) Human motor cortex: development and cytoarchitecture. In: The human brain. Springer, Berlin, Heidelberg, pp 11–34.  https://doi.org/10.1007/978-3-642-14724-1_3
  39. Pinel P, Dehaene S (2009) Beyond hemispheric dominance: brain regions underlying the joint lateralization of language and arithmetic to the left hemisphere. J Cogn Neurosci 22(1):48–66CrossRefGoogle Scholar
  40. Pinel P, Lalanne C, Bourgeron T, Fauchereau F, Poupon C, Artiges E, Dehaene S (2014) Genetic and environmental influences on the visual word form and fusiform face areas. Cereb Cortex.  https://doi.org/10.1093/cercor/bhu048 PubMedCrossRefGoogle Scholar
  41. Power JD, Schlaggar BL, Petersen SE (2015) Recent progress and outstanding issues in motion correction in resting state fMRI. Neuroimage 105:536–551.  https://doi.org/10.1016/j.neuroimage.2014.10.044 CrossRefPubMedGoogle Scholar
  42. Quartz SR, Sejnowski TJ (1997) The neural basis of cognitive development: a constructivist manifesto. Behav Brain Sci 20(4):537–556; discussion 556–596PubMedGoogle Scholar
  43. Raichle ME (2015) The restless brain: how intrinsic activity organizes brain function. Philos Trans R Soc Lond B Biol Sci, 370(1668).  https://doi.org/10.1098/rstb.2014.0172
  44. Rakic P (1988) Specification of cerebral cortical areas. Science 241(4862):170–176CrossRefPubMedGoogle Scholar
  45. Rockland KS, Ojima H (2003) Multisensory convergence in calcarine visual areas in macaque monkey. Int J Psychophysiol 50:19–26CrossRefPubMedGoogle Scholar
  46. Sai FZ (2005) The role of the mother’s voice in developing mother’s face preference: Evidence for intermodal perception at birth. Infant Child Dev 14:29–50CrossRefGoogle Scholar
  47. Saygin ZM, Osher DE, Koldewyn K, Reynolds G, Gabrieli JD, Saxe RR (2012) Anatomical connectivity patterns predict face selectivity in the fusiform gyrus. Nat Neurosci 15(2):321–327.  https://doi.org/10.1038/nn.3001 CrossRefGoogle Scholar
  48. Saygin ZM, Osher DE, Norton ES, Youssoufian DA, Beach SD, Feather J, Kanwisher N (2016) Connectivity precedes function in the development of the visual word form area. Nat Neurosci 19(9):1250–1255.  https://doi.org/10.1038/nn.4354 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Shum J, Hermes D, Foster BL, Dastjerdi M, Rangarajan V, Winawer J, Parvizi J (2013) A brain area for visual numerals. J Neurosci 33(16):6709–6715.  https://doi.org/10.1523/JNEUROSCI.4558-12.2013 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Smith SM, Vidaurre D, Beckmann CF, Glasser MF, Jenkinson M, Miller KL, Van Essen DC (2013) Functional connectomics from resting-state fMRI. Trends Cogn Sci 17(12):666–682.  https://doi.org/10.1016/j.tics.2013.09.016 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Smyser CD, Inder TE, Shimony JS, Hill JE, Degnan AJ, Snyder AZ, Neil JJ (2010) Longitudinal analysis of neural network development in preterm infants. Cereb Cortex 20(12):2852–2862.  https://doi.org/10.1093/cercor/bhq035 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Smyser CD, Snyder AZ, Neil JJ (2011) Functional connectivity MRI in infants: exploration of the functional organization of the developing brain. Neuroimage.  https://doi.org/10.1016/j.neuroimage.2011.02.073 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Sours C, Raghavan P, Foxworthy WA, Meredith MA, El Metwally D, Zhuo J, Gullapalli RP et al (2017) Cortical multisensory connectivity is present near birth in humans. Brain Imaging Behav 11(4):1207–1213.  https://doi.org/10.1007/s11682-016-9586-6 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Striem-Amit E, Cohen L, Dehaene S, Amedi A (2012) Reading with sounds: sensory substitution selectively activates the visual word form area in the blind. Neuron 76:640–652CrossRefPubMedGoogle Scholar
  55. Takahashi N, Sakurai T, Davis KL, Buxbaum JD (2011) Linking oligodendrocyte and myelin dysfunction to neurocircuitry abnormalities in schizophrenia. Prog Neurobiol 93:13–24CrossRefPubMedGoogle Scholar
  56. Tanaka K (1996) Inferotemporal cortex and object vision. Annu Rev Neurosci 19:109–139CrossRefPubMedGoogle Scholar
  57. Toulmin H, Beckmann CF, O’Muircheartaigh J, Ball G, Nongena P, Makropoulos A, Edwards AD et al (2015) Specialization and integration of functional thalamocortical connectivity in the human infant. Proc Natl Acad Sci USA 112(20):6485–6490.  https://doi.org/10.1073/pnas.1422638112 CrossRefPubMedGoogle Scholar
  58. Tovar-Moll F et al (2006) Neuroplasticity in human callosal dysgenesis: a diffusion tensor imaging study. Cereb Cortex 17:531–541CrossRefPubMedGoogle Scholar
  59. van den Heuvel MP, Kersbergen KJ, de Reus MA, Keunen K, Kahn RS, Groenendaal F, Benders MJ et al (2015) The neonatal connectome during preterm brain development. Cereb Cortex 25(9):3000–3013.  https://doi.org/10.1093/cercor/bhu095 CrossRefPubMedGoogle Scholar
  60. Vinckier F, Dehaene S, Jobert A, Dubus JP, Sigman M, Cohen L (2007) Hierarchical coding of letter strings in the ventral stream: dissecting the inner organization of the visual word-form system. Neuron 55(1):143–156.  https://doi.org/10.1016/j.neuron.2007.05.031 CrossRefPubMedGoogle Scholar
  61. Weiner KS, Golarai G, Caspers J, Chuapoco MR, Mohlberg H, Zilles K, Grill-Spector K et al (2014) The mid-fusiform sulcus: a landmark identifying both cytoarchitectonic and functional divisions of human ventral temporal cortex. Neuroimage 84:453–465.  https://doi.org/10.1016/j.neuroimage.2013.08.068 CrossRefPubMedGoogle Scholar
  62. Weiner KS, Barnett MA, Lorenz S, Caspers J, Stigliani A, Amunts K, Grill-Spector K (2016) The cytoarchitecture of domain-specific regions in human high-level visual cortex. Cereb Cortex.  https://doi.org/10.1093/cercor/bhw361 PubMedCentralCrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • P. Barttfeld
    • 1
    • 2
  • S. Abboud
    • 4
    • 5
  • H. Lagercrantz
    • 6
  • U. Adén
    • 6
  • N. Padilla
    • 6
  • A. D. Edwards
    • 7
  • L. Cohen
    • 4
    • 5
  • M. Sigman
    • 3
  • S. Dehaene
    • 1
    • 8
  • G. Dehaene-Lambertz
    • 1
  1. 1.Cognitive Neuroimaging Unit, CEA DSV/I2BM, INSERMUniversité Paris-Sud, Université Paris-Saclay, NeuroSpin CenterGif-sur-YvetteFrance
  2. 2.Instituto de Investigaciones Psicológicas (IIPsi), CONICETUniversidad Nacional de CórdobaCórdobaArgentina
  3. 3.Universidad Torcuato Di TellaBuenos AiresArgentina
  4. 4.INSERM, U 1127ParisFrance
  5. 5.Institut Du Cerveau Et De La Moelle Epinière, ICM, PICNIC LabParisFrance
  6. 6.Department of Women’s and Children’s HealthKarolinska InstitutetStockholmSweden
  7. 7.Centre for the Developing Brain, Division of Imaging Sciences and Biomedical EngineeringKing’s College LondonLondonUK
  8. 8.Collège de FranceParisFrance

Personalised recommendations