Human Cortical Development: Insights from Imaging
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1 Human Cortical Development: Insights from Imaging David C. Van Essen Anatomy & Neurobiology Department Washington University School of Medicine OHBM Educational Course Anatomy June 7, 2015 Honolulu, Hawaii NICHD, NIMH, NIH Neuroscience Blueprint
2 Cortical Development Insights from Imaging Prenatal cortical development Morphogenesis of the cortical sheet Cortical arealization Cortical convolutions Postnatal maturation: Regional expansion & differentiation Abnormal maturation in preterm infants
3 General features of adult cerebral cortex Macaque Human Surface area (per hemisphere) 110 cm 2 1,000 cm 2 Thickness 1-3 mm 2-4 mm Convolutions Stereotyped Highly variable # of cortical areas ~ ? ~ ? Size range ~100x ~100x Inter-areal pathways ~5,000? >5,000? Van Essen et al. (2012a) Van Essen et al. (2012b) Markov et al. (2012)
4 Variability and heritability of cortical folding W, X = twins Y, Z = twins These are two pairs of identical twins Which are the twin pairs?! Some regions are consistently folded (e.g., central sulcus) Other regions are highly variable (e.g., posterior ITS) Folding patterns are heritable, but only modestly so (Van Essen et al., OHBM 2014) Botteron, Dierker, Todd et al., 2008
5 Key issues in Cortical Morphogenesis Why is the cortex a sheet, with variable thickness? What determines cortical surface area? Why and how does the cortex fold? Why is human cortical folding so variable? How does the cortex become parcellated? How are specific connections established? Morphogenesis is driven by: Cell proliferation, migration, differentiation Physical forces: tension & pressure (D Arcy Thompson, 1917)
6 Why is the cortex a sheet, whereas nuclei are blobs? Observation: Neuronal processes generate mechanical tension [1] Hypothesis: radial anisotropies (dendrites, axons, glia) lead to sheets Isotropic cellular architecture leads to blob-like nuclei [2] [1] Bray (1984); Dennerll et al., (1988) [2] Van Essen (Nature, 1997)
7 Cortical areal differentiation I. Early stages in mouse: A protomap in cortical progenitors (VZ) (O Leary et al., Neuron, 2007) Gradients of morphogens in cortical plate and ventricular zone (TGF8, Emx2, Nr2f1, Pax6, Eomes, TBR1 ) Human Mouse
8 Cortical areal differentiation I. Early stages in mouse: A protomap in cortical progenitors (VZ) (O Leary et al., Neuron, 2007) Gradients of morphogens in cortical plate and ventricular zone (TGF8, Emx2, Nr2f1, Pax6, Eomes, TBR1 ) Many similarities between human and mouse (Miller et al., Nature, 2014) Human Mouse Brainspan project: Human 15 week, 21 week - near peak of cortical neurogenesis Broad fronto-temporal gradients No sharp boundaries or areaspecific patches
9 Cortical areal differentiation II. How does this. lead to this?!! Later stages: differentiation of the full areal mosaic Additional morphogens and gradients?? Area-specific markers?? (mystery molecules - micro-rna s?) Activity dependence?? Emergence of new areas in humans? Areal duplication and divergence? (e.g., Grove et al. 2012) How is specificity of long-distance connections established?
10 Human cortical folding mainly in third trimester Hill et al. (J. Neuroscience, 2010) Overlaps with formation of connections
11 What causes convolutions? Coogan & Van Essen (1996) Lunate sulcus Earliest V1-V2 connections ~E108 (Coogan & Van Essen, 1996) Folding brings V1 and V2 retinotopic maps closer together, roughly in register How - by tension along axons??!!
12 Tension-based cortical folding: Strongly interconnected regions win (gyrus in between) Weakly interconnected regions lose (sulcus in between) Variable folding may reflect variabililty in areal sizes and/or connectivity Van Essen (Nature, 1997)
13 Alternative mechanisms proposed (cf. Welker, 1990) Richman, 1975 Buckling (differential laminar growth) (Richman, 1975; Toro & Burnod, 2005; Ronan et al., Cerebral Cortex, 2013) Constraints imposed by skull (LeGros Clark, 1945; but see Barron, 1950) Toro & Burnod, 2005 Differential proliferation in SVZ (Kriegstein et al., 2006; Reillo et al., 2011)
14 Differential proliferation in Outer SubVentricular Zone Mouse Ferret Thick OSVZ in gyrencephalic species Intermediate Radial Glial (IRG) cells produce neurons + glia More IRG cells, thicker OSVZ below gyri Reillo et al. (Cerebral Cortex, 2011)
15 Plausibility of cortical folding mechanisms Differential proliferation: Plausible for primary folds (before proliferation ceases) Implausible for tertiary (irregular) human folds Tension-based folding: Neurites generate tension (Bray, 1984; Dennerll et al.,1988; but see Xu et al, 2010) Broad explanatory power (sheets and folds) Wiring length minimization comes for free! Multiple mechanisms? (as often in biology)
16 Cortical Development Insights from Imaging Prenatal cortical development Morphogenesis of the cortical sheet Cortical arealization Cortical convolutions Postnatal maturation: Regional expansion & differentiation Abnormal maturation in preterm infants
17 MR contrast changes during early development T2w Gestational weeks Serag et al. (Neuroimage, 2012) Leroy et al. (PLoS, 2011) Prenatal & early postnatal: low tissue contrast, nonuniform White matter myelination: mainly postnatal Regional differences in myelination onset
18 Postnatal cortical expansion: adults vs healthy term infants Hill et al. (J. Neurosci, 2010) Hemispheric asymmetries evident at birth
19 Postnatal cortical expansion: large regional differences 3-fold overall postnatal expansion Adult/neonatal surface area ratio High-expansion: frontal, parietal, lateral temporal Low-expansion: occipital, medial temporal, parietal Postnatal differences are discernible in individuals Hill et al. (PNAS, 2010)
20 Postnatal cortical expansion occurs mainly in the first 2 years Li et al. (Cerebral Cortex, 2012) Hill et al. (PNAS, 2010) Adult vs neonate Similarities exceed differences Differences might be methodological or neurobiological
21 Postnatal dendritic arbor maturation Human prefrontal cortex Layer 3C Petanjek et al. (Cerebral Cortex, 2008) Layer 5 Dendritic arbors expand in early postnatal development Major regional differences, pruning in some regions (Elston et al., 2009)
22 Myelin maps in cerebral cortex Sensory-motor strip T1-weighted Divide and conquer: T2-weighted image T1w/T2w ratio brighter darker Auditory MT+ darker brighter Myelin content Low Glasser & Van Essen (2011); Van Essen & Glasser (2013) High Early myelination: Heavy adult myelination
23 Many features correlate with postnatal expansion pattern Postnatal Myelin map Human/Macaque Cortical thickness Onset of myelination Regions of high postnatal expansion: expanded recently in human evolution tend to have:! lighter myelination! delayed myelination! thicker cortex! larger, late-developing dendritic arbors! lower neuronal density
24 Abnormal cortical maturation in premature infants Immature folding in some term-equivalent infants Selective vulnerability of lateral temporal cortex?
25 Cortical morphometry in very preterm (VPT) children studied at age 7 years (Zhang et al., 2015) Cortical surface area: 9% smaller in VPT vs TC Shallower Superior Temporal Sulcus in VPT Regional differences in relative surface area VPT reduced in parietal operculum VPT expanded, more convoluted in cingulate cortex
26 Anatomy of Cortical Development & Maturation Rapid prenatal development (3 rd trimester) Postnatal maturation over many years Regional sensitivity to perturbation and injury Insights into individual variability, role of experience Brain connectivity and function during development: Human Connectome Project (HCP, Major advances in data acquisition and analysis A baseline for studies of development, aging, and disease Lifespan pilot project (children, older adults) Three NIH Lifespan RFAs: Baby; Development; Aging Developing Human Connectome Project (dhcp) Prenatal brain development (D. Edwards et al., Kings/Imperial/Oxford)
27 ACKNOWLEDGMENTS Donna Dierker Matt Glasser John Harwell Erin Reid Terrie Inder Jeff Neil Jim Alexopoulos Jason Hill Erin Engelhardt Yuning Zhang Washington University University of Minnesota Oxford University Kamil Ugurbil (co-pi); 101 HCP consortium members HCP funding from the NIH Blueprint! Saint Louis University University d Annunzio Indiana University Warwick University Ernst Strungmann Institute Radboud University Duke University
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