Skip to main content

Advertisement

SpringerLink
Log in

Development of white matter tracts between and within the dorsal and ventral streams

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The degree of interaction between the ventral and dorsal visual streams has been discussed in multiple scientific domains for decades. Recently, several white matter tracts that directly connect cortical regions associated with the dorsal and ventral streams have become possible to study due to advancements in automated and reproducible methods. The developmental trajectory of this set of tracts, here referred to as the posterior vertical pathway (PVP), has yet to be described. We propose an input-driven model of white matter development and provide evidence for the model by focusing on the development of the PVP. We used reproducible, cloud-computing methods and diffusion imaging from adults and children (ages 5–8 years) to compare PVP development to that of tracts within the ventral and dorsal pathways. PVP microstructure was more adult-like than dorsal stream microstructure, but less adult-like than ventral stream microstructure. Additionally, PVP microstructure was more similar to the microstructure of the ventral than the dorsal stream and was predicted by performance on a perceptual task in children. Overall, results suggest a potential role for the PVP in the development of the dorsal visual stream that may be related to its ability to facilitate interactions between ventral and dorsal streams during learning. Our results are consistent with the proposed model, suggesting that the microstructural development of major white matter pathways is related, at least in part, to the propagation of sensory information within the visual system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Data, description of analyses, and web-links to the open-source code and open cloud services used in the creation of this dataset can be viewed in their entirety here: https://doi.org/10.25663/brainlife.pub.23. Additional code used for the statistical analyses can be found here: https://github.com/svincibo/PVP-development.

References

  • Ades-Aron B, Veraart J, Kochunov P, McGuire S, Sherman P, Kellner E, Novikov DS, Fieremans E (2018) Evaluation of the accuracy and precision of the diffusion parameter EStImation with Gibbs and NoisE removal pipeline. Neuroimage 183:532–543

    Article  PubMed  Google Scholar 

  • Amigó E, Gonzalo J, Artiles J, Verdejo F (2009) A comparison of extrinsic clustering evaluation metrics based on formal constraints. Inf Retrieval 12(4):461–486

    Article  Google Scholar 

  • Arthur D, Vassilvitskii S (2006) k-means++: the advantages of careful seeding. http://ilpubs.stanford.edu:8090/778

  • Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34(1):51–61

    Article  CAS  PubMed  Google Scholar 

  • Avesani P, McPherson B, Hayashi S, Caiafa CF, Henschel R, Garyfallidis E, Kitchell L, Bullock D, Patterson A, Olivetti E, Sporns O, Saykin AJ, Wang L, Dinov I, Hancock D, Caron B, Qian Y, Pestilli F (2019) The open diffusion data derivatives, brain data upcycling via integrated publishing of derivatives and reproducible open cloud services. Scientific Data 6(1):69

    Article  PubMed  PubMed Central  Google Scholar 

  • Baizer JS, Ungerleider LG, Desimone R (1991) Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. J Neurosci 11(1):168–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66(1):259–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beery KE (2004) Beery VMI: the Beery-Buktenica developmental test of visual-motor integration. Minneapolis, MN: Pearson. https://www.uv.uio.no/isp/english/about/oslo-spesialpedagogikk-og-laeringslab/tests/visual-and-motor-skills/vmi-6.pdf

  • Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H, Ullén F (2005) Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 8(9):1148–1150

    Article  CAS  PubMed  Google Scholar 

  • Binkofski F, Buxbaum LJ (2013) Two action systems in the human brain. Brain Lang 127(2):222–229

    Article  PubMed  Google Scholar 

  • Bonekamp D, Nagae LM, Degaonkar M, Matson M, Abdalla WMA, Barker PB, Mori S, Horská A (2007) Diffusion tensor imaging in children and adolescents: reproducibility, hemispheric, and age-related differences. Neuroimage 34(2):733–742

    Article  PubMed  Google Scholar 

  • Broce IJ, Bernal B, Altman N, Bradley C, Baez N, Cabrera L, Hernandez G, De Feria A, Dick AS (2019) Fiber pathways supporting early literacy development in 5–8-year-old children. Brain Cogn 134:80–89

    Article  PubMed  Google Scholar 

  • Bullock D (2019a) Remove Tract Outliers (new wmc input/output). brainlife.io. https://doi.org/10.25663/BRAINLIFE.APP.195

  • Bullock D (2019b) White Matter Anatomy Segmentation. brainlife.io. https://doi.org/10.25663/BRAINLIFE.APP.188

  • Bullock D, Takemura H, Caiafa CF, Kitchell L, McPherson B, Caron B, Pestilli F (2019) Associative white matter connecting the dorsal and ventral posterior human cortex. Brain Struct Funct. https://doi.org/10.1007/s00429-019-01907-8

    Article  PubMed  Google Scholar 

  • Bullock DN, Hayday EA, Grier MD, Tang W, Pestilli F, Heilbronner S (2021) A taxonomy of the brain’s white matter: twenty-one major tracts for the twenty-first century. https://doi.org/10.31234/osf.io/fvk5r

  • Cameron CE, Brock LL, Murrah WM, Bell LH, Worzalla SL, Grissmer D, Morrison FJ (2012) Fine motor skills and executive function both contribute to kindergarten achievement. Child Dev 83(4):1229–1244

    Article  PubMed  PubMed Central  Google Scholar 

  • Cantlon JF, Pinel P, Dehaene S, Pelphrey KA (2011) Cortical representations of symbols, objects, and faces are pruned back during early childhood. Cereb Cortex 21(1):191–199

    Article  PubMed  Google Scholar 

  • Carlson AG, Rowe E, Curby TW (2013) Disentangling fine motor skills’ relations to academic achievement: the relative contributions of visual-spatial integration and visual-motor coordination. J Genet Psychol 174(5–6):514–533

    Article  PubMed  Google Scholar 

  • Caron B (n.d.) FSL Top-up & Eddy—CUDA. https://doi.org/10.25663/brainlife.app.287

  • Caron B (2019) Tract analysis profiles. brainlife.io. https://doi.org/10.25663/BRAINLIFE.APP.185

  • Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17(1):77–94

    Article  PubMed  Google Scholar 

  • Catani M, Jones DK, Donato R, Ffytche DH (2003) Occipito-temporal connections in the human brain. Brain 126(9):2093–2107

    Article  PubMed  Google Scholar 

  • Catani M, Jones DK, Ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57(1):8–16

    Article  PubMed  Google Scholar 

  • Cattell RB (1966) The scree test for the number of factors. Multivar Behav Res 1(2):245–276

    Article  CAS  Google Scholar 

  • Choi S-H, Jeong G, Kim Y-B, Cho Z-H (2020) Proposal for human visual pathway in the extrastriate cortex by fiber tracking method using diffusion-weighted MRI. Neuroimage 220:117145

    Article  PubMed  Google Scholar 

  • Ciric R, Wolf DH, Power JD, Roalf DR, Baum GL, Ruparel K, Shinohara RT, Elliott MA, Eickhoff SB, Davatzikos C, Gur RC, Gur RE, Bassett DS, Satterthwaite TD (2017) Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity. Neuroimage 154:174–187

    Article  PubMed  Google Scholar 

  • Clark GJ (2010) The relationship between handwriting, reading, fine motor and visual-motor skills in kindergarteners. https://lib.dr.iastate.edu/cgi/viewcontent.cgi?article=2432&context=etd

  • Cohen MA, Dilks DD, Koldewyn K, Weigelt S, Feather J, Kell AJ, Keil B, Fischl B, Zöllei L, Wald L, Saxe R, Kanwisher N (2019) Representational similarity precedes category selectivity in the developing ventral visual pathway. Neuroimage 197:565–574

    Article  PubMed  Google Scholar 

  • Cox MAA, Cox TF (2008) Multidimensional scaling. In: Chen C-H, Härdle W, Unwin A (eds) Handbook of data visualization. Springer, Berlin, pp 315–347

    Chapter  Google Scholar 

  • Culham JC, Danckert SL, DeSouza JFX, Gati JS, Menon RS, Goodale MA (2003) Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp Brain Res 153(2):180–189

    Article  PubMed  Google Scholar 

  • de Schotten MT, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DGM, Catani M (2011) A lateralized brain network for visuospatial attention. Nat Neurosci 14:1245

    Article  CAS  Google Scholar 

  • Dekker T, Mareschal D, Sereno MI, Johnson MH (2011) Dorsal and ventral stream activation and object recognition performance in school-age children. Neuroimage 57(3):659–670

    Article  PubMed  Google Scholar 

  • Destrieux C, Fischl B, Dale A, Halgren E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53(1):1–15

    Article  PubMed  Google Scholar 

  • Deutsch GK, Dougherty RF, Bammer R, Siok WT, Gabrieli JDE, Wandell B (2005) Children’s reading performance is correlated with white matter structure measured by diffusion tensor imaging. Cortex 41(3):354–363

    Article  PubMed  Google Scholar 

  • Dick AS, Garic D, Graziano P, Tremblay P (2019) The frontal aslant tract (FAT) and its role in speech, language and executive function. Cortex 111:148–163

    Article  PubMed  Google Scholar 

  • Dinehart LH (2015) Handwriting in early childhood education: current research and future implications. J Early Child Lit 15(1):97–118

    Article  Google Scholar 

  • Drakesmith M, Harms R, Rudrapatna SU, Parker GD, Evans CJ, Jones DK (2019) Estimating axon conduction velocity in vivo from microstructural MRI. Neuroimage 203:116186

    Article  PubMed  Google Scholar 

  • Dubois J, Dehaene-Lambertz G, Kulikova S, Poupon C, Hüppi PS, Hertz-Pannier L (2014) The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276:48–71

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg IW, Bissett PG, Zeynep Enkavi A, Li J, MacKinnon DP, Marsch LA, Poldrack RA (2019) Uncovering the structure of self-regulation through data-driven ontology discovery. Nat Commun 10(1):2319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fears NE, Lockman JJ (2018) How beginning handwriting is influenced by letter knowledge: visual–motor coordination during children’s form copying. J Exp Child Psychol 171:55–70

    Article  PubMed  Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47

    Article  CAS  PubMed  Google Scholar 

  • Fischl B (2012) FreeSurfer. Neuroimage 62(2):774–781

    Article  PubMed  Google Scholar 

  • 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(1):313–327

    Article  PubMed  Google Scholar 

  • Freud E, Culham JC, Namdar G, Behrmann M (2019) Object complexity modulates the association between action and perception in childhood. J Exp Child Psychol 179:56–72

    Article  PubMed  Google Scholar 

  • Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, Xu J, Jbabdi S, Webster M, Polimeni JR, Van Essen DC, Jenkinson M, WU-Minn HCP Consortium (2013) The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage 80:105–124

    Article  PubMed  Google Scholar 

  • Golarai G, Ghahremani DG, Whitfield-Gabrieli S, Reiss A, Eberhardt JL, Gabrieli JDE, Grill-Spector K (2007) Differential development of high-level visual cortex correlates with category-specific recognition memory. Nat Neurosci 10(4):512–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodale M, Milner D (2013) Sight unseen: an exploration of conscious and unconscious vision. OUP Oxford

  • Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25

    Article  CAS  PubMed  Google Scholar 

  • Greve DN, Fischl B (2009) Accurate and robust brain image alignment using boundary-based registration. Neuroimage 48(1):63–72

    Article  PubMed  Google Scholar 

  • Grill-Spector K, Golarai G, Gabrieli J (2008) Developmental neuroimaging of the human ventral visual cortex. Trends Cogn Sci 12(4):152–162

    Article  PubMed  Google Scholar 

  • Grissmer D, Grimm KJ, Aiyer SM, Murrah WM, Steele JS (2010) Fine motor skills and early comprehension of the world: two new school readiness indicators. Dev Psychol 46(5):1008–1017

    Article  PubMed  Google Scholar 

  • Hanisch C, Konczak J, Dohle C (2001) The effect of the Ebbinghaus illusion on grasping behaviour of children. Exp Brain Res 137(2):237–245

    Article  CAS  PubMed  Google Scholar 

  • Hayashi S, Kitchell L, Pestilli F (2017) Freesurfer. brainlife.io. https://doi.org/10.25663/BL.APP.0

  • Hayashi S, McPherson B, Caron B (2018) HCP ACPC alignment (T1). brainlife.io. https://doi.org/10.25663/BL.APP.99

  • Hegdé J, Felleman DJ (2007) Reappraising the functional implications of the primate visual anatomical hierarchy. Neurosci 13(5):416–421

    Google Scholar 

  • Huang H, Vasung L (2014) Gaining insight of fetal brain development with diffusion MRI and histology. Int J Dev Neurosci 32:11–22

    Article  PubMed  Google Scholar 

  • Huber E, Donnelly PM, Rokem A, Yeatman JD (2018) Rapid and widespread white matter plasticity during an intensive reading intervention. Nat Commun 9(1):2260

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • James KH (2010) Sensori-motor experience leads to changes in visual processing in the developing brain. Dev Sci 13(2):279–288

    Article  PubMed  PubMed Central  Google Scholar 

  • James KH (2017) The importance of handwriting experience on the development of the literate brain. Curr Dir Psychol Sci 26(6):502–508

    Article  Google Scholar 

  • James KH, Engelhardt L (2012) The effects of handwriting experience on functional brain development in pre-literate children. Trends Neurosci Educ 1(1):32–42

    Article  PubMed  PubMed Central  Google Scholar 

  • James KH, Gauthier I (2006) Letter processing automatically recruits a sensory–motor brain network. Neuropsychologia 44(14):2937–2949

    Article  PubMed  Google Scholar 

  • James KH, Kersey AJ (2018) Dorsal stream function in the young child: an fMRI investigation of visually guided action. Dev Sci. https://doi.org/10.1111/desc.12546

    Article  PubMed  Google Scholar 

  • James KH, Humphrey GK, Goodale MA (2001) Manipulating and recognizing virtual objects: where the action is. Can J Exp Psychol 55(2):111–120

    Article  CAS  PubMed  Google Scholar 

  • James TW, Culham J, Humphrey GK, Milner AD, Goodale MA (2003) Ventral occipital lesions impair object recognition but not object-directed grasping: an fMRI study. Brain 126(11):2463–2475

    Article  PubMed  Google Scholar 

  • Janssen P, Verhoef BE, Premereur E (2018) Functional interactions between the macaque dorsal and ventral visual pathways during three-dimensional object vision. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior. https://www.sciencedirect.com/science/article/pii/S0010945217300357?casa_token=Vl7Vwf2J4G0AAAAA:-RpRzBiru5vV_6_ZBD2e6p9kVgo6I6wYNkqZ5kmc1Vs7M733G3mneUBmogfLvBrdjozhjcpsA5x1

  • Jeremy D, Schmahmann DNP (2006) Fiber pathways of the brain. Oxford University Press, Oxford

    Google Scholar 

  • Johansen-Berg H, Baptista CS, Thomas AG (2012) Human structural plasticity at record speed [review of Human structural plasticity at record speed]. Neuron 73(6):1058–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalyvas A, Koutsarnakis C, Komaitis S, Karavasilis E, Christidi F, Skandalakis GP, Liouta E, Papakonstantinou O, Kelekis N, Duffau H, Stranjalis G (2020) Mapping the human middle longitudinal fasciculus through a focused anatomo-imaging study: shifting the paradigm of its segmentation and connectivity pattern. Brain Struct Funct 225(1):85–119

    Article  PubMed  Google Scholar 

  • Kamali A, Flanders AE, Brody J, Hunter JV, Hasan KM (2014a) Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Struct Funct 219(1):269–281

    Article  PubMed  Google Scholar 

  • Kamali A, Sair HI, Radmanesh A, Hasan KM (2014b) Decoding the superior parietal lobule connections of the superior longitudinal fasciculus/arcuate fasciculus in the human brain. Neuroscience 277:577–583

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T, Takemura H, Pestilli F, Silva AC, Ye FQ, Leopold DA (2020) Spatial organization of occipital white matter tracts in the common marmoset. Brain Struct Funct 225(4):1313–1326

    Article  PubMed  PubMed Central  Google Scholar 

  • Klaver P, Marcar V, Martin E (2011) Chapter 7—neurodevelopment of the visual system in typically developing children. In: Braddick O, Atkinson J, Innocenti GM (Eds.) Progress in Brain Research,Vol. 189. Elsevier: 113–136

  • Klingberg T, Hedehus M, Temple E, Salz T, Gabrieli JD, Moseley ME, Poldrack RA (2000) Microstructure of temporo-parietal white matter as a basis for reading ability: evidence from diffusion tensor magnetic resonance imaging [Review of Microstructure of temporo-parietal white matter as a basis for reading ability: evidence from diffusion tensor magnetic resonance imaging]. Neuron 25(2):493–500

    Article  CAS  PubMed  Google Scholar 

  • Kruskal JB (1964) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29(2):115–129

    Article  Google Scholar 

  • Latini F, Mårtensson J, Larsson E-M, Fredrikson M, Åhs F, Hjortberg M, Aldskogius H, Ryttlefors M (2017) Segmentation of the inferior longitudinal fasciculus in the human brain: a white matter dissection and diffusion tensor tractography study. Brain Res 1675:102–115

    Article  CAS  PubMed  Google Scholar 

  • Lawes INC, Barrick TR, Murugam V, Spierings N, Evans DR, Song M, Clark CA (2008) Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage 39(1):62–79

    Article  PubMed  Google Scholar 

  • Lebel C, Deoni S (2018) The development of brain white matter microstructure. Neuroimage 182:207–218

    Article  PubMed  Google Scholar 

  • Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C (2008) Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40(3):1044–1055

    Article  CAS  PubMed  Google Scholar 

  • Lebel C, Treit S, Beaulieu C (2019) A review of diffusion MRI of typical white matter development from early childhood to young adulthood. NMR Biomed 32(4):e3778

    Article  PubMed  Google Scholar 

  • Leipsic PFO (1901) Developmental (Myelogenetic) localisation of the cerebral cortex in the human subject. The Lancet 158(4077):1027–1030

    Article  Google Scholar 

  • Lerner Y, Hendler T, Ben-Bashat D, Harel M, Malach R (2001) A hierarchical axis of object processing stages in the human visual cortex. Cereb Cortex 11(4):287–297

    Article  CAS  PubMed  Google Scholar 

  • Li J, Osher DE, Hansen HA, Saygin ZM (2020) Innate connectivity patterns drive the development of the visual word form area. Sci Rep 10(1):18039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Ye FQ, Newman JD, Szczupak D, Tian X, Yen CC-C, Majka P, Glen D, Rosa MGP, Leopold DA, Silva AC (2020) A resource for the detailed 3D mapping of white matter pathways in the marmoset brain. Nat Neurosci 23(2):271–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loenneker T, Klaver P, Bucher K, Lichtensteiger J, Imfeld A, Martin E (2011) Microstructural development: organizational differences of the fiber architecture between children and adults in dorsal and ventral visual streams. Hum Brain Mapp 32(6):935–946

    Article  PubMed  Google Scholar 

  • Longcamp M, Boucard C, Gilhodes J-C, Anton J-L, Roth M, Nazarian B, Velay J-L (2008) Learning through hand- or typewriting influences visual recognition of new graphic shapes: behavioral and functional imaging evidence. J Cogn Neurosci 20(5):802–815

    Article  PubMed  Google Scholar 

  • Mahon BZ, Kumar N, Almeida J (2013) Spatial frequency tuning reveals interactions between the dorsal and ventral visual systems. J Cogn Neurosci 25(6):862–871

    Article  PubMed  PubMed Central  Google Scholar 

  • Majka P, Bai S, Bakola S, Bednarek S, Chan JM, Jermakow N, Passarelli L, Reser DH, Theodoni P, Worthy KH, Wang X-J, Wójcik DK, Mitra PP, Rosa MGP (2020) Open access resource for cellular-resolution analyses of corticocortical connectivity in the marmoset monkey. Nat Commun 11(1):1133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makris N, Papadimitriou GM, Kaiser JR, Sorg S, Kennedy DN, Pandya DN (2009) Delineation of the middle longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI Study. Cereb Cortex 19(4):777–785

    Article  PubMed  Google Scholar 

  • Makris N, Preti MG, Wassermann D, Rathi Y, Papadimitriou GM, Yergatian C, Dickerson BC, Shenton ME, Kubicki M (2013) Human middle longitudinal fascicle: segregation and behavioral-clinical implications of two distinct fiber connections linking temporal pole and superior temporal gyrus with the angular gyrus or superior parietal lobule using multi-tensor tractography. Brain Imaging Behav 7(3):335–352

    Article  CAS  PubMed  Google Scholar 

  • Makris N, Zhu A, Papadimitriou GM, Mouradian P, Ng I, Scaccianoce E, Baselli G, Baglio F, Shenton ME, Rathi Y, Dickerson B, Yeterian E, Kubicki M (2017) Mapping temporo-parietal and temporo-occipital cortico-cortical connections of the human middle longitudinal fascicle in subject-specific, probabilistic, and stereotaxic Talairach spaces. Brain Imaging Behav 11(5):1258–1277

    Article  PubMed  PubMed Central  Google Scholar 

  • Maldarelli JE, Kahrs BA, Hunt SC, Lockman JJ (2015) Development of early handwriting: visual-motor control during letter copying. Dev Psychol 51(7):879–888

    Article  PubMed  PubMed Central  Google Scholar 

  • Maldonado IL, de Champfleur NM, Velut S, Destrieux C, Zemmoura I, Duffau H (2013) Evidence of am iddle l ongitudinal f asciculus in the human brain from fiber dissection. J Anat 223(1):38–45

    Article  PubMed  PubMed Central  Google Scholar 

  • Matthews CG, Klove H (1964) Instruction manual for the adult neuropsychology test battery. University of Wisconsin Medical School, Madison, p 36

    Google Scholar 

  • Maurer D, Lewis TL (2018) Visual systems. The Neurobiology of Brain and Behavioral. https://www.sciencedirect.com/science/article/pii/B978012804036200008X

  • McPherson B (2018a) mrtrix3 act. brainlife.io. https://doi.org/10.25663/BL.APP.101

  • McPherson B (2018b) mrtrix3 preprocess. brainlife.io. https://doi.org/10.25663/BL.APP.68

  • Menjot de Champfleur N, Lima Maldonado I, Moritz-Gasser S, Machi P, Le Bars E, Bonafé A, Duffau H (2013) Middle longitudinal fasciculus delineation within language pathways: a diffusion tensor imaging study in human. Eur J Radiol 82(1):151–157

    Article  PubMed  Google Scholar 

  • Merker B, Podell K (2011) Grooved pegboard test. In: Kreutzer JS, DeLuca J, Caplan B (eds) Encyclopedia of clinical neuropsychology. Springer, New York, pp 1176–1178

    Chapter  Google Scholar 

  • Meyer A (1981a) Paul Flechsig’s System of Myelogenetic cortical localization in the light of recent research in neuroanatomy and neurophysiology part I. Can J Neurol Sci 8(1):1–6

    Article  CAS  PubMed  Google Scholar 

  • Meyer A (1981b) Paul Flechsig’s System of Myelogenetic cortical localization in the light of recent research in neuroanatomy and neurophysiology part II. Can J Neurol Sci 8(2):95–104

    Article  CAS  PubMed  Google Scholar 

  • Milner AD (2017) How do the two visual streams interact with each other? Exp Brain Res 235(5):1297–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milner AD, Goodale MA (2008) Two visual systems re-viewed. Neuropsychologia 46(3):774–785

    Article  CAS  PubMed  Google Scholar 

  • Mishkin M, Ungerleider LG (1982) Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys. Behav Brain Res 6(1):57–77

    Article  CAS  PubMed  Google Scholar 

  • Mishkin M, Ungerleider LG, Macko KA (1983) Object vision and spatial vision: two cortical pathways. Trends Neurosci 6:414–417

    Article  Google Scholar 

  • Mori S, Kaufmann WE, Davatzikos C, Stieltjes B, Amodei L, Fredericksen K, Pearlson GD, Melhem ER, Solaiyappan M, Raymond GV et al (2002) Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn Reson Med 47(2):215–223

    Article  PubMed  Google Scholar 

  • Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, Toga AW, Pike GB, Neto PR, Evans A, Zhang J, Huang H, Miller MI, van Zijl P, Mazziotta J (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40(2):570–582

    Article  PubMed  Google Scholar 

  • Moseley M (2002) Diffusion tensor imaging and aging—a review. NMR Biomed 15(7–8):553–560

    Article  PubMed  Google Scholar 

  • Moulton E, Bouhali F, Monzalvo K, Poupon C, Zhang H, Dehaene S, Dehaene-Lambertz G, Dubois J (2019) Connectivity between the visual word form area and the parietal lobe improves after the first year of reading instruction: a longitudinal MRI study in children. Brain Struct Funct 224(4):1519–1536

    PubMed  Google Scholar 

  • Ortibus E, Verhoeven J, Sunaert S, Casteels I, de Cock P, Lagae L (2012) Integrity of the inferior longitudinal fasciculus and impaired object recognition in children: a diffusion tensor imaging study. Dev Med Child Neurol 54(1):38–43

    Article  PubMed  Google Scholar 

  • Osher DE, Saxe RR, Koldewyn K, Gabrieli JDE, Kanwisher N, Saygin ZM (2016) Structural connectivity fingerprints predict cortical selectivity for multiple visual categories across cortex. Cereb Cortex 26(4):1668–1683

    Article  PubMed  Google Scholar 

  • Panesar SS, Yeh F-C, Jacquesson T, Hula W, Fernandez-Miranda JC (2018) A quantitative tractography study into the connectivity, segmentation and laterality of the human inferior longitudinal fasciculus. Front Neuroanat 12:47

    Article  PubMed  PubMed Central  Google Scholar 

  • Pestilli F, Yeatman JD, Rokem A, Kay KN, Wandell BA (2014) Evaluation and statistical inference for human connectomes. Nat Methods 11(10):1058–1063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters BD, Ikuta T, DeRosse P, John M, Burdick KE, Gruner P, Prendergast DM, Szeszko PR, Malhotra AK (2014) Age-related differences in white matter tract microstructure are associated with cognitive performance from childhood to adulthood. Biol Psychiat 75(3):248–256

    Article  PubMed  Google Scholar 

  • Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36(6):893–906

    Article  CAS  PubMed  Google Scholar 

  • Poggio T, Ullman S (2013) Vision: are models of object recognition catching up with the brain? Ann N Y Acad Sci 1305:72–82

    Article  PubMed  Google Scholar 

  • Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59(3):2142–2154

    Article  PubMed  Google Scholar 

  • Qiu A, Mori S, Miller MI (2015) Diffusion tensor imaging for understanding brain development in early life. Annu Rev Psychol 66:853–876

    Article  PubMed  PubMed Central  Google Scholar 

  • Reveley C, Seth AK, Pierpaoli C, Silva AC, Yu D, Saunders RC, Leopold DA, Ye FQ (2015) Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography. Proc Natl Acad Sci USA 112(21):E2820–E2828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds JE, Grohs MN, Dewey D, Lebel C (2019) Global and regional white matter development in early childhood. Neuroimage 196:49–58

    Article  PubMed  Google Scholar 

  • Riesenhuber M, Poggio T (1999) Hierarchical models of object recognition in cortex. Nat Neurosci 2(11):1019–1025

    Article  CAS  PubMed  Google Scholar 

  • Rizzolatti G, Matelli M (2003) Two different streams form the dorsal visual system: anatomy and functions. Exp Brain Res 153(2):146–157

    Article  PubMed  Google Scholar 

  • Rokem A, Takemura H, Bock AS, Scherf KS, Behrmann M, Wandell BA, Fine I, Bridge H, Pestilli F (2017) The visual white matter: the application of diffusion MRI and fiber tractography to vision science. J vis 17(2):4

    Article  PubMed  PubMed Central  Google Scholar 

  • Saber GT, Pestilli F, Curtis CE (2015) Saccade planning evokes topographically specific activity in the dorsal and ventral streams. J Neurosci 35(1):245–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampaio-Baptista C, Khrapitchev AA, Foxley S, Schlagheck T, Scholz J, Jbabdi S, DeLuca GC, Miller KL, Taylor A, Thomas N, Kleim J, Sibson NR, Bannerman D, Johansen-Berg H (2013) Motor skill learning induces changes in white matter microstructure and myelination. J Neurosci 33(50):19499–19503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampaio-Baptista C, Sanders Z-B, Johansen-Berg H (2018) Structural plasticity in adulthood with motor learning and stroke rehabilitation. Annu Rev Neurosci 41:25–40

    Article  CAS  PubMed  Google Scholar 

  • Sani I, McPherson BC, Stemmann H, Pestilli F, Freiwald WA (2019) Functionally defined white matter of the macaque monkey brain reveals a dorso-ventral attention network. Elife. https://doi.org/10.7554/eLife.40520

    Article  PubMed  PubMed Central  Google Scholar 

  • Saygin ZM, Osher DE, Koldewyn K, Reynolds G, Gabrieli JDE, Saxe RR (2011) Anatomical connectivity patterns predict face selectivity in the fusiform gyrus. Nat Neurosci 15(2):321–327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saygin ZM, Osher DE, Norton ES, Youssoufian DA, Beach SD, Feather J, Gaab N, Gabrieli JDE, Kanwisher N (2016) Connectivity precedes function in the development of the visual word form area. Nat Neurosci 19(9):1250–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scherf KS, Behrmann M, Humphreys K, Luna B (2007) Visual category-selectivity for faces, places and objects emerges along different developmental trajectories. Dev Sci 10(4):F15–F30

    Article  PubMed  Google Scholar 

  • Schrank FA, Wendling BJ (2018) The Woodcock--Johnson IV. Contemporary Intellectual Assessment: Theories, Tests, and Issues, 383

  • Seber GAF (2009) Multivariate observations. Wiley, Hoboken

    Google Scholar 

  • Seger CA, Miller EK (2010) Category learning in the brain. Annu Rev Neurosci 33:203–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Serre T, Oliva A, Poggio T (2007) A feedforward architecture accounts for rapid categorization. Proc Natl Acad Sci USA 104(15):6424–6429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith RE, Tournier J-D, Calamante F, Connelly A (2012) Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage 62(3):1924–1938

    Article  PubMed  Google Scholar 

  • Stiles J, Akshoomoff N, Haist F (2013) The development of visuospatial processing. In: Neural circuit development and function in the brain. Elsevier: 271–296

  • Striem-Amit E, Vannuscorps G, Caramazza A (2017) Sensorimotor-independent development of hands and tools selectivity in the visual cortex. Proc Natl Acad Sci USA 114(18):4787–4792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takemura H, Rokem A, Winawer J, Yeatman JD, Wandell BA, Pestilli F (2015) A major human white matter pathway between dorsal and ventral visual cortex. Cereb Cortex 26(5):2205–2214

    Article  PubMed  PubMed Central  Google Scholar 

  • Takemura H, Caiafa CF, Wandell BA, Pestilli F (2016) Ensemble tractography. PLoS Comp Biol 12(2):e1004692

    Article  CAS  Google Scholar 

  • Takemura H, Pestilli F, Weiner KS, Keliris GA, Landi SM, Sliwa J, Ye FQ, Barnett MA, Leopold DA, Freiwald WA, Logothetis NK, Wandell BA (2017) Occipital white matter tracts in human and macaque. Cereb Cortex 27(6):3346–3359

    Article  PubMed  PubMed Central  Google Scholar 

  • Takemura H, Pestilli F, Weiner KS (2019) Comparative neuroanatomy: Integrating classic and modern methods to understand association fibers connecting dorsal and ventral visual cortex. Neurosci Res 146:1–12

    Article  PubMed  Google Scholar 

  • Thomas C, Ye FQ, Irfanoglu MO, Modi P, Saleem KS, Leopold DA, Pierpaoli C (2014) Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci USA 111(46):16574–16579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torgerson WS (1952) Multidimensional scaling: I. Theory and method. Psychometrika 17(4):401–419

    Article  Google Scholar 

  • Tournier J-D, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35(4):1459–1472

    Article  PubMed  Google Scholar 

  • Tournier J-D, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22(1):53–66

    Article  Google Scholar 

  • Tusa RJ, Ungerleider LG (1985) The inferior longitudinal fasciculus: a reexamination in humans and monkeys. Ann Neurol 18(5):583–591

    Article  CAS  PubMed  Google Scholar 

  • Uda S, Matsui M, Tanaka C, Uematsu A, Miura K, Kawana I, Noguchi K (2015) Normal development of human brain white matter from infancy to early adulthood: a diffusion tensor imaging study. Dev Neurosci 37(2):182–194

    Article  CAS  PubMed  Google Scholar 

  • Ungerleider LG, Haxby JV (1994) “What”and “where”in the human brain. Curr Opin Neurobiol 4(2):157–165

    Article  CAS  PubMed  Google Scholar 

  • Vinci-Booher S, James TW, James KH (2016) Visual-motor functional connectivity in preschool children emerges after handwriting experience. Trends Neurosci Educ 5(3):107–120

    Article  Google Scholar 

  • Wakefield EM, James KH (2011) Effects of Sensori-motor learning on melody processing across development. Cognition Brain Behav 15(4):505–534

    Google Scholar 

  • Wandell BA, Yeatman JD (2013) Biological development of reading circuits. Curr Opin Neurobiol 23(2):261–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Young KM (2014) White matter plasticity in adulthood. Neuroscience 276:148–160

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Yushkevich P (2013) Multi-atlas segmentation with joint label fusion and corrective learning—an open source implementation. Front Neuroinform 7:27

    PubMed  PubMed Central  Google Scholar 

  • Wang Y, Mauer MV, Raney T, Peysakhovich B, Becker BLC, Sliva DD, Gaab N (2017) Development of tract-specific white matter pathways during early reading development in at-risk children and typical controls. Cereb Cortex 27(4):2469–2485

    PubMed  Google Scholar 

  • Wassermann D, Makris N, Rathi Y, Shenton M, Kikinis R, Kubicki M, Westin CF (2013) On describing human white matter anatomy: the white matter query language. Medical Image Computing and Computer-Assisted Intervention: MICCAI International Conference on Medical Image Computing and Computer-Assisted Intervention 16 (Pt.1): 647–654

  • Wassermann D, Makris N, Rathi Y, Shenton M, Kikinis R, Kubicki M, Westin C-F (2016) The white matter query language: a novel approach for describing human white matter anatomy. Brain Struct Funct 221(9):4705–4721

    Article  PubMed  PubMed Central  Google Scholar 

  • Weiner KS, Yeatman JD, Wandell BA (2017) The posterior arcuate fasciculus and the vertical occipital fasciculus. Cortex 97:274–276

    Article  PubMed  Google Scholar 

  • Wu Y, Sun D, Wang Y, Wang Y, Wang Y (2016) Tracing short connections of the temporo-parieto-occipital region in the human brain using diffusion spectrum imaging and fiber dissection. Brain Res 1646:152–159

    Article  CAS  PubMed  Google Scholar 

  • Yeatman JD, White AL (2021) Reading: the confluence of vision and language. Ann Rev Vision Sci. https://doi.org/10.1146/annurev-vision-093019-113509

    Article  Google Scholar 

  • Yeatman JD, Dougherty RF, Rykhlevskaia E, Sherbondy AJ, Deutsch GK, Wandell BA, Ben-Shachar M (2011) Anatomical properties of the arcuate fasciculus predict phonological and reading skills in children. J Cogn Neurosci 23(11):3304–3317

    Article  PubMed  PubMed Central  Google Scholar 

  • Yeatman JD, Dougherty RF, Ben-Shachar M, Wandell BA (2012a) Development of white matter and reading skills. Proc Natl Acad Sci USA 109(44):E3045–E3053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeatman JD, Dougherty RF, Myall NJ, Wandell BA, Feldman HM (2012b) Tract profiles of white matter properties: automating fiber-tract quantification. PLoS ONE 7(11):e49790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeatman JD, Weiner KS, Pestilli F, Rokem A, Mezer A, Wandell BA (2014) The vertical occipital fasciculus: a century of controversy resolved by in vivo measurements. Proc Natl Acad Sci USA 111(48):E5214–E5223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was funded by NSF OAC-1916518, NSF IIS-1912270, NSF IIS-1636893, NSF BCS-1734853, Microsoft Investigator Fellowship to F.P. Data collections as supported by The Emergent Areas or Research Indiana University to F. Pestilli, K. James and L. Smith, the Indiana University Bloomington Imaging Research Facility Brain Scan Credit Program, the Indiana Clinical and Translational Sciences Institute, and the Johnson Center for Innovation and Translational Research provided additional imaging funds. SVB was partially supported by the NIH and institute T32-HD007475-21, the EAR Initiative Linda Smith (Indiana University), and NSF SBE Postdoctoral Research Award #2004877. DNB was supported by NIH NIMH T32-MH103213 to William Hetrick (Indiana University). The authors would like to acknowledge the help of Dr. Hu Cheng for help with the imaging sequences, Soichi Hayashi and Brent McPherson for contributing to the development of brainlife.io.

Author information

Authors and Affiliations

  1. Indiana University, 1101 E. 10th Street, Bloomington, IN, 47405, USA

    S. Vinci-Booher, B. Caron, D. Bullock, K. James & F. Pestilli

  2. The University of Texas, 108 E Dean Keeton St, Austin, TX, 78712, USA

    F. Pestilli

Authors
  1. S. Vinci-Booher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Caron
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Bullock
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. James
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. F. Pestilli
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Sophia Vinci-Booher contributed to all aspects of the manuscript, including the original conception of the study, ongoing conceptual development, the design, data collection, analyses and software, writing the original draft of the paper, and revisions. Brad Caron and Dan Bullock contributed software and supported software development, participated in data quality checks, and commented on the manuscript. Karin James contributed to data collection, and commented on the manuscript. Franco Pestilli contributed to the original conception of the study, the conceptual development of the work, the design, the analyses, software, training of Sophia Vinci-Booher, and in the writing of the manuscript and revisions.

Corresponding authors

Correspondence to S. Vinci-Booher or F. Pestilli.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Research involving human participants and/or animals

Data collection was approved by the respective Institutional Review Boards (IRBs) at Indiana University.

Informed consent

Adult participants provided written informed consent to participate in the project. Parents/guardians provided written informed consent for child participants. Child participants who were 7 years or older provided written informed assent.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 4289 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vinci-Booher, S., Caron, B., Bullock, D. et al. Development of white matter tracts between and within the dorsal and ventral streams. Brain Struct Funct 227, 1457–1477 (2022). https://doi.org/10.1007/s00429-021-02414-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-021-02414-5

Keywords

Search

Navigation