Top

Published in:

Open Access 01-12-2018 | Original Article

Interactive histogenesis of axonal strata and proliferative zones in the human fetal cerebral wall

Authors: Iris Žunić Išasegi, Milan Radoš, Željka Krsnik, Marko Radoš, Vesna Benjak, Ivica Kostović

Published in: Brain Structure and Function | Issue 9/2018

Abstract

Development of the cerebral wall is characterized by partially overlapping histogenetic events. However, little is known with regards to when, where, and how growing axonal pathways interact with progenitor cell lineages in the proliferative zones of the human fetal cerebrum. We analyzed the developmental continuity and spatial distribution of the axonal sagittal strata (SS) and their relationship with proliferative zones in a series of human brains (8–40 post-conceptional weeks; PCW) by comparing histological, histochemical, and immunocytochemical data with magnetic resonance imaging (MRI). Between 8.5 and 11 PCW, thalamocortical fibers from the intermediate zone (IZ) were initially dispersed throughout the subventricular zone (SVZ), while sizeable axonal “invasion” occurred between 12.5 and 15 PCW followed by callosal fibers which “delaminated” the ventricular zone-inner SVZ from the outer SVZ (OSVZ). During midgestation, the SS extensively invaded the OSVZ, separating cell bands, and a new multilaminar axonal-cellular compartment (MACC) was formed. Preterm period reveals increased complexity of the MACC in terms of glial architecture and the thinning of proliferative bands. The addition of associative fibers and the formation of the centrum semiovale separated the SS from the subplate. In vivo MRI of the occipital SS indicates a “triplet” structure of alternating hypointense and hyperintense bands. Our results highlighted the developmental continuity of sagittally oriented “corridors” of projection, commissural and associative fibers, and histogenetic interaction with progenitors, neurons, and glia. Histogenetical changes in the MACC, and consequently, delineation of the SS on MRI, may serve as a relevant indicator of white matter microstructural integrity in the developing brain.

Angevine JB, Bodian D, Coulombre AJ et al (1970) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166:257–261

Arai Y, Taverna E (2017) Neural progenitor cell polarity and cortical development. Front Cell Neurosci 11:384PubMedPubMedCentral

Axer M, Grässel D, Kleiner M et al (2011) High-resolution fiber tract reconstruction in the human brain by means of three-dimensional polarized light imaging. Front Neuroinform 5:34PubMedPubMedCentral

Back SA, Luo NL, Borenstein NS et al (2001) Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 21:1302–1312PubMedPubMedCentral

Baldwin MKL, Balaram P, Kaas JH (2017) The evolution and functions of nuclei of the visual pulvinar in primates. J Comp Neurol 525:3207–3226PubMed

Barkovich AJ, Kjos BO, Jackson DE Jr et al (1988) Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. Radiology 166:173–180PubMed

Bassi L, Ricci D, Volzone A et al (2008) Probabilistic diffusion tractography of the optic radiations and visual function in preterm infants at term equivalent age. Brain 131:573–582PubMed

Battin MR, Maalouf EF, Counsell SJ et al (1998) Magnetic resonance imaging of the brain in very preterm infants: visualization of the germinal matrix, early myelination, and cortical folding. Pediatrics 101:957–962PubMed

Bayatti N, Moss JA, Sun L et al (2008) A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cereb Cortex 18:1536–1548PubMed

Bayer S, Altman J (1991) Neocortical development. Raven Press, New York

Bicknese AR, Sheppard AM, O’Leary DD, Pearlman AL (1994) Thalamocortical axons extend along a chondroitin sulfate proteoglycan-enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J Neurosci 14:3500–3510PubMedPubMedCentral

Borrell V, Reillo I (2012) Emerging roles of neural stem cells in cerebral cortex development and evolution. Dev Neurobiol 72:955–971PubMed

Brodmann K (1914) Physiologie des Gehirns. Die anatomische Feldertopographie der Grosshirnoberflache. In: Krause F (ed) Die Allgemeine Chirurgie der Gehirnkrankheiten. Ferdinand Enke, Stuttgart, pp 99–112

Brody BA, Kinney HC, Kloman AS et al (1987) Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J Neuropathol Exp Neurol 46:283–301PubMed

Bystron I, Blakemore C, Rakic P (2008) Development of the human cerebral cortex: boulder committee revisited. Nat Rev Neurosci 9:110–122PubMed

Cao M, Huang H, He Y (2017) Developmental connectomics from infancy through early childhood. Trends Neurosci 40:494–506PubMedPubMedCentral

Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132PubMed

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

Charron F (2005) Novel brain wiring functions for classical morphogens: a role as graded positional cues in axon guidance. Development 132:2251–2262PubMed

Clowry G, Molnár Z, Rakic P (2010) Renewed focus on the developing human neocortex. J Anat 217:276–288PubMedPubMedCentral

Collin G, Van Den Heuvel MP (2013) The ontogeny of the human connectome: development and dynamic changes of brain connectivity across the life span. Neuroscientist 19:616–628PubMed

Corbett-Detig J, Habas PA, Scott JA et al (2011) 3D global and regional patterns of human fetal subplate growth determined in utero. Brain Struct Funct 215:255–263PubMed

De Juan Romero C, Borrell V (2015) Coevolution of radial glial cells and the cerebral cortex. Glia 63:1303–1319PubMedPubMedCentral

Dehay C, Savatier P, Cortay V, Kennedy H (2001) Cell-cycle kinetics of neocortical precursors are influenced by embryonic thalamic axons. J Neurosci 21:201–214PubMedPubMedCentral

Dehay C, Kennedy H, Kosik KS (2015) The outer subventricular zone and primate-specific cortical complexification. Neuron 85:683–694PubMed

Déjerine J (1895) Anatomie des centres nerveux. Rueff, Paris

Del Río JA, Martínez A, Auladell C, Soriano E (2000) Developmental history of the subplate and developing white matter in the murine neocortex. Neuronal organization and relationship with the main afferent systems at embryonic and perinatal stages. Cereb cortex 10:784–801PubMed

Dubois J, Dehaene-Lambertz G, Kulikova S et al (2014) The early development of brain white matter: A review of imaging studies in fetuses, newborns and infants. Neuroscience 276:48–71PubMed

Dubois J, Kostović I, Judaš M (2015) Development of structural and functional connectivity. In: Toga AW (ed) Brain mapping: an encyclopedic reference. Academic Press, pp 423–437

Duque A, Krsnik Z, Kostović I, Rakic P (2016) Secondary expansion of the transient subplate zone in the developing cerebrum of human and nonhuman primates. Proc Natl Acad Sci 113:9892–9897PubMedPubMedCentral

Eyre JA (2003) Development and plasticity of the corticospinal system in man. Neural Plast 10:93–106PubMedPubMedCentral

Eyre JA, Miller S, Clowry GJ et al (2000) Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres. Brain 123:51–64PubMed

Fischl B, Salat DH, Busa E et al (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355PubMed

Flechsig P (1920) Anatomie des menschlichen Gehirns und Ruchen-marks auf myelogenetischer Grundlage. Thieme, Leipzig

González Gómez M, Meyer G (2014) Dynamic expression of calretinin in embryonic and early fetal human cortex. Front Neuroanat 8:41PubMedPubMedCentral

Guzzetta A, D’acunto G, Rose S et al (2010) Plasticity of the visual system after early brain damage. Dev Med Child Neurol 52:891–900PubMed

Hagmann P, Cammoun L, Gigandet X et al (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:1479–1493

Hansen DV, Lui JH, Parker PRL, Kriegstein AR (2010) Nerurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554–561PubMed

Haydar TF, Wang F, Schwartz ML, Rakic P (2000) Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 20:5764–5774PubMedPubMedCentral

Hevner RF (2000) Development of connections in the human visual system during fetal mid-gestation: a DiI-tracing study. J Neuropathol Exp Neurol 59:385–392PubMed

Hevner RF (2006) From radial glia to pyramidal-projection neuron: transcription factor cascades in cerebral cortex development. Mol Neurobiol 33:33–50PubMed

Hoerder-Suabedissen A, Molnár Z (2015) Development, evolution and pathology of neocortical subplate neurons. Nat Rev Neurosci 16:133–146PubMed

Hosoya T, Adachi M, Yamaguchi K, Haku T (1998) MRI anatomy of white matter layers around the trigone of the lateral ventricle. Neuroradiology 40:477–482PubMed

Howard BM, Mo Z, Filipovic R et al (2008) Radial glia cells in the developing human brain. Neuroscientist 14:459–473PubMedPubMedCentral

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

Huang H, Zhang J, Wakana S et al (2006) White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage 33:27–38PubMed

Huang H, Jeon T, Sedmak G et al (2013) Coupling diffusion imaging with histological and gene expression analysis to examine the dynamics of cortical areas across the fetal period of human brain development. Cereb Cortex 23:2620–2631PubMed

Jakovcevski I, Zecevic N (2005) Sequence of oligodendrocyte development in the human fetal telencephalon. Glia 49:480–491PubMed

Jones E (1987) Cerebral cortex. In: Adelman G (ed) Encyclopedia of neuroscience, vol 1. Birkhäuser, Boston, pp 209–211

Jovanov-Milosevic N, Culjat M, Kostovic I (2009) Growth of the human corpus callosum: modular and laminar morphogenetic zones. Front Neuroanat 3:6PubMedPubMedCentral

Judaš M, Jovanov Milošević N, Rašin MR et al (2003) Complex patterns and simple architects: molecular guidance cues for developing axonal pathways in the telencephalon. Prog Mol Subcell Biol 32:1–32PubMed

Judaš M, Radoš M, Jovanov-Miloševic N et al (2005) Structural, immunocytochemical, and MR imaging properties of periventricular crossroads of growing cortical pathways in preterm infants. Am J Neuroradiol 26:2671–2684PubMedPubMedCentral

Judaš M, Šimić G, Petanjek Z et al (2011) The Zagreb Collection of human brains: a unique, versatile, but underexploited resource for the neuroscience community. Ann N Y Acad Sci

Kasprian G, Brugger PC, Weber M et al (2008) In utero tractography of fetal white matter development. Neuroimage 43:213–224PubMed

Kidokoro H, Anderson PJ, Doyle LW et al (2011) High signal intensity on T2-weighted MR imaging at term-equivalent age in preterm infants does not predict 2-year neurodevelopmental outcomes. Am J Neuroradiol 32:2005–2010PubMedPubMedCentral

Kinney HC, Brody BA, Kloman AS, Gilles FH (1988) Sequence of central nervous system myelination in human infancy. II. Patterns of myelination in autopsied infants. J Neuropathol Exp Neurol 47:217–234PubMed

Kirischuk S, Sinning A, Blanquie O et al (2017) Modulation of neocortical development by early neuronal activity: physiology and pathophysiology. Front Cell Neurosci 11:379PubMedPubMedCentral

Kostović I (1986) Prenatal development of nucleus basalis complex and related fiber systems in man: a histochemical study. Neuroscience 17:1047–1077PubMed

Kostović I, Goldman-Rakić PS (1983) Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. J Comp Neurol 219:431–447PubMed

Kostović I, Rakic P (1984) Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining. J Neurosci 4:25–42PubMedPubMedCentral

Kostović I, Jovanov-Milošević N (2006) The development of cerebral connections during the first 20–45 weeks’ gestation. Semin Fetal Neonatal Med 11:415–422PubMed

Kostović I, Judaš M (2007) Transient patterns of cortical lamination during prenatal life: Do they have implications for treatment? Neurosci Biobehav Rev 31:1157–1168PubMed

Kostović I, Judaš M (2010) The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatr 99:1119–1127PubMed

Kostović I, Judaš M (2015) Embryonic and fetal development of the human cerebral cortex. In: Toga AW (ed) Brain mapping: an encyclopedic reference. Academic Press, pp 167–175

Kostović I, Rakić P (1990) Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297:441–470PubMed

Kostović I, Štefulj-Fučić A, Mrzljak L et al (1991) Prenatal and perinatal development of the somatostatin-immunoreactive neurons in the human prefrontal cortex. Neurosci Lett 124:153–156PubMed

Kostović I, Judaš M, Radoš M, Hrabač P (2002a) Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 12:536–544PubMed

Kostović I, Rašin MR, Petanjek Z, Judaš M (2002b) Morphological characteristics of the cells in the subcallosal zone (nucleus septohippocampalis) of the human fetus. Neuroembryology 1:97–104

Kostović I, Jovanov-Milošević N, Radoš M et al (2014a) Perinatal and early postnatal reorganization of the subplate and related cellular compartments in the human cerebral wall as revealed by histological and MRI approaches. Brain Struct Funct 219:231–253PubMed

Kostović I, Kostović-Srzentić M, Benjak V et al (2014b) Developmental dynamics of radial vulnerability in the cerebral compartments in preterm infants and neonates. Front Neurol 5:139PubMedPubMedCentral

Krägeloh-Mann I, Horber V (2007) The role of magnetic resonance imaging in furthering understanding of the pathogenesis of cerebral palsy. Dev Med Child Neurol 49:948PubMed

Krsnik Ž, Majić V, Vasung L et al (2017) Growth of thalamocortical fibers to the somatosensory cortex in the human fetal brain. Front Neurosci 11:233PubMedPubMedCentral

LaMantia AS (1995) The usual suspects: GABA and glutamate may regulate proliferation in the neocortex. Neuron 15:1223–1225PubMed

Lennartsson F, Nilsson M, Flodmark O, Jacobson L (2014) Damage to the immature optic radiation causes severe reduction of the retinal nerve fiber layer, resulting in predictable visual field defects. Invest Ophthalmol Vis Sci 55(12):8278–8288PubMed

Levitt P, Cooper ML, Rakic P (1981) Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J Neurosci 1:27–39PubMedPubMedCentral

Lewitus E, Kelava I, Huttner WB (2013) Conical expansion of the outer subventricular zone and the role of neocortical folding in evolution and development. Front Hum Neurosci 7:424PubMedPubMedCentral

LoTurco JJ, Owens DF, Heath MJS et al (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287–1298PubMed

Lukaszewicz A, Savatier P, Cortay V et al (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47:353–364PubMedPubMedCentral

Maas LC, Mukherjee P, Carballido-Gamio J et al (2004) Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. Neuroimage 22:1134–1140PubMed

Makris N, Meyer JW, Bates JF et al (1999) MRI-based topographic parcellation of human cerebral white matter and nuclei: II. Rationale and applications with systematics of cerebral connectivity. Neuroimage 9:18–45PubMed

Makris N, Papadimitriou G, Sorg S, Kennedy D (2007) The occipitofrontal fascicle in humans: A quantitative, in vivo, DT-MRI study. Neuroimage 37:1100–1111PubMed

Marin-Padilla M (1970) Prenatal and early postnatal ontogenesis of the human motor cortex: a Golgi study. I. The sequential development of the cortical layers. Brain Res 23:167–183PubMed

Meyer G, Schaaps JP, Moreau L, Goffinet AM (2000) Embryonic and early fetal development of the human neocortex. J Neurosci 20:1858–1868PubMedPubMedCentral

Mitter C, Prayer D, Brugger PC et al (2015) In vivo tractography of fetal association fibers. PLoS One 10(3):e0119536. https://doi.org/10.1371/journal.pone.0119536 CrossRefPubMedPubMedCentral

Molliver ME, Kostović I, Van Der Loos H (1973) The development of synapses in cerebral cortex of the human fetus. Brain Res 50:403–407PubMed

Molnár Z, Clowry G (2012) Cerebral cortical development in rodents and primates. Prog Brain Res 195:45–70PubMed

Molnár Z, Adams R, Blakemore C (1998) Mechanisms underlying the early establishment of thalamocortical connections in the rat. J Neurosci 18:5723–5745PubMedPubMedCentral

Mori S, van Zijl PCM (2002) Fiber tracking: principles and strategies—a technical review. NMR Biomed 15:468–480PubMed

Mrzljak L, Uylings HB, Kostović I, Van Eden CG (1988) Prenatal development of neurons in the human prefrontal cortex: I. A qualitative golgi study. J Comp Neurol 271:355–386PubMed

Naidich T, Krayenbuhl N, Kollias S et al (2013) White matter. In: Naidich T, Castillo M, Cha S, Smirniotopoulos J (eds) Imaging of the brain. Elsevier Saunders, Philadelphia, pp 205–244

Nobin A, Björklund A (1973) Topography of the monoamine neuron systems in the human brain as revealed in fetuses. Acta Physiol Scand Suppl 388:1–40PubMed

Nowakowski TJ, Pollen AA, Sandoval-Espinosa C, Kriegstein AR (2016) Transformation of the radial glia scaffold demarcates two stages of human cerebral cortex development. Neuron 91:1219–1227PubMedPubMedCentral

Olson L, Boréus LO, Seiger Å (1973) Histochemical demonstration and mapping of 5-hydroxytryptamine- and catecholamine-containing neuron systems in the human fetal brain. Z Anat Entwicklungsgesch 139:259–282PubMed

Polleux F, Dehay C, Goffinet A, Kennedy H (2001) Pre- and post-mitotic events contribute to the progressive acquisition of area-specific connectional fate in the neocortex. Cereb Cortex 11:1027–1039PubMed

Polyak S (1932) The main afferent fiber systems of the cerebral cortex in primates, vol 2. University of California Press, Berkeley

Polyak S (1957) The vertebrate visual system. University press, Chicago

Popovitchenko T, Rasin M-R (2017) Transcriptional and post-transcriptional mechanisms of the development of neocortical lamination. Front Neuroanat 11:102PubMedPubMedCentral

Radoš M, Judaš M, Kostović I (2006) In vitro MRI of brain development. Eur J Radiol 57:187–198PubMed

Rakić P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183(4123):425–427PubMed

Rakić P (1988) Specification of cerebral cortical areas. Science 241(4862):170–176PubMed

Rakic P, Yakovlev PI (1968) Development of the corpus callosum and cavum septi in man. J Comp Neurol 132:45–72PubMed

Rakić P (1981) Developmental events leading to laminar and areal organization of the neocortex. In: Scmhmitt F, Worden F, Adelman G, Dennis S (eds) The organization of the cerebral cortex: proceedings of a neuroscience research program colloquium. The MIT Press, Cambridge, pp 7–28

Reillo I, Borrell V (2012) Germinal zones in the developing cerebral cortex of ferret: ontogeny, cell cycle kinetics, and diversity of progenitors. Cereb Cortex 22:2039–2054PubMed

Reillo I, De Juan Romero C, García-Cabezas M, Borrell V (2011) A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex 21:1674–1694PubMed

Ren T, Anderson A, Shen WB et al (2006) Imaging, anatomical, and molecular analysis of callosal formation in the developing human fetal brain. Anat Rec Part A Discov Mol Cell Evol Biol 288:191–204

Rutherford MA, Pennock JM, Counsell SJ et al (1998) Abnormal magnetic resonance signal in the internal capsule predicts poor neurodevelopmental outcome in infants with hypoxic-ischemic encephalopathy. Pediatrics 102:323–328PubMed

Sachs H (1892) Das Hemisphaerenmark des menschlichen Grosshirns. I. Der Hinterhauptlappen. Georg Thieme Verlag, Leipzig

Sarnat HB (2013) Clinical neuropathology practice guide 5-2013: markers of neuronal maturation. Clin Neuropathol 32:340–369PubMedPubMedCentral

Schmahmann JD, Pandya DN (2006) Fibre pathways of the brain. Oxford University Press, Oxford

Schmahmann JD, Pandya DN (2007) Cerebral white matter—historical evolution of facts and notions concerning the organization of the fiber pathways of the brain. J Hist Neurosci 16:237–267PubMed

Selden N (1998) Trajectories of cholinergic pathways within the cerebral hemispheres of the human brain. Brain 121:2249–2257PubMed

Smart IH, Dehay C, Giroud P et al (2002) Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12:37–53PubMed

Spitzer NC (2006) Electrical activity in early neuronal development. Nature 444:707–712PubMed

Sporns O, Tononi G, Kötter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1:0245–0251

Staudt M (2007) (Re-)organization of the developing human brain following periventricular white matter lesions. Neurosci Biobehav Rev 31:1150–1156PubMed

Takahashi E, Folkerth RD, Galaburda AM, Grant PE (2012) Emerging cerebral connectivity in the human fetal Brain: an MR tractography study. Cereb Cortex 22:455–464PubMed

Tamura H, Takahashi S, Kurihara N et al (2003) Practical visualization of internal structure of white matter for image interpretation: staining a spin-echo T2-weighted image with three echo-planar diffusion-weighted images. Am J Neuroradiol 24:401–409PubMedPubMedCentral

Tessier-Lavigne M (1992) Axon guidance by molecular gradients. Curr Opin Neurobiol 2:60–65PubMed

Tymofiyeva O, Hess CP, Xu D, Barkovich AJ (2014) Structural MRI connectome in development: challenges of the changing brain. Br J Radiol 87:20140086PubMedPubMedCentral

Vasung L, Huang H, Jovanov-Milošević N et al (2010) Development of axonal pathways in the human fetal fronto-limbic brain: histochemical characterization and diffusion tensor imaging. J Anat 217:400–417PubMedPubMedCentral

Vasung L, Jovanov-Milošević N, Pletikos M et al (2011) Prominent periventricular fiber system related to ganglionic eminence and striatum in the human fetal cerebrum. Brain Struct Funct 215:237–253PubMed

Vasung L, Lepage C, Radoš M et al (2016) Quantitative and qualitative analysis of transient fetal compartments during prenatal human brain development. Front Neuroanat 10:11PubMedPubMedCentral

Vasung L, Raguz M, Kostovic I, Takahashi E (2017) Spatiotemporal relationship of brain pathways during human fetal development using high-angular resolution diffusion MR imaging and histology. Front Neurosci 11:348PubMedPubMedCentral

Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8:110–124PubMedPubMedCentral

Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA (2011) The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci 29:423–440PubMedPubMedCentral

Von Monakow C (1905) Gehirnpathologie. Alfred Hölder, Wienn

Wang X, Pettersson DR, Studholme C, Kroenke CD (2015) Characterization of laminar zones in the mid-gestation primate brain with magnetic resonance imaging and histological methods. Front Neuroanat 9:147PubMedPubMedCentral

Wedeen VJ, Rosene DL, Wang R et al (2012) The geometric structure of the brain fiber pathways. Science 335:1628–1634PubMedPubMedCentral

Wichmann W, Müller-Forell W (2006) Anatomy. In: Müller-Forell W (ed) Imaging of orbital and visual pathway pathology. Springer, Germany, pp 25–60

Widjaja E, Geibprasert S, Mahmoodabadi SZ et al (2010) Alteration of human fetal subplate layer and intermediate zone during normal development on MR and diffusion tensor imaging. Am J Neuroradiol 31:1091–1099PubMedPubMedCentral

Xu G, Takahashi E, Folkerth RD et al (2014) Radial coherence of diffusion tractography in the cerebral white matter of the human fetus: neuroanatomic insights. Cereb Cortex 24:579–592PubMed

Yakovlev PI, Lecours AR (1967) The myelogenetic cycles of regional maturation of the brain. In: Minkowski A (ed) Regional development of brain in early life. Blackwell, Oxford, pp 3–70

Zecevic N, Verney C (1995) Development of the catecholamine neurons in human embryos and fetuses, with special emphasis on the innervation of the cerebral cortex. J Comp Neurol 351:509–535PubMed

Zecevic N, Chen Y, Filipovic R (2005) Contributions of cortical subventricular zone to the development of the human cerebral cortex. J Comp Neurol 491:109–122PubMedPubMedCentral

Zilles K, Palomero-Gallagher N, Gräßel D et al (2016) High-resolution fiber and fiber tract imaging using polarized light microscopy in the human, monkey, rat, and mouse brain. In: Rockland K (ed) Axons and brain architecture. Elsevier, Amsterdam, pp 369–389

Title: Interactive histogenesis of axonal strata and proliferative zones in the human fetal cerebral wall
Authors: Iris Žunić Išasegi
Milan Radoš
Željka Krsnik
Marko Radoš
Vesna Benjak
Ivica Kostović
Publication date: 01-12-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 9/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1721-2

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Interactive histogenesis of axonal strata and proliferative zones in the human fetal cerebral wall

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 9/2018

Hippocampal proBDNF facilitates place learning strategy associated with neural activity in rats

Whole mouse brain structural connectomics using magnetic resonance histology

Proliferative cells in the rat developing neocortical grey matter: new insights into gliogenesis

Modifications of the axon initial segment during the hibernation of the Syrian hamster

Foxp2 loss of function increases striatal direct pathway inhibition via increased GABA release

Claustrum circuit components for top–down input processing and cortical broadcast