Defects of neuronal migration and the pathogenesis of cortical malformations

doi:10.1016/S0079-6123(08)60494-X

Progress in Brain Research

Volume 73, 1988, Pages 15-37

https://doi.org/10.1016/S0079-6123(08)60494-X Get rights and content

Publisher Summary

This chapter focuses on cell movements during corticogenesis. In terms of orientation and directionality of cell movement, migration can be classified into (1) radial—proceeding from the ventricular to the pial surface and (2) tangential—running parallel to the surface of developing brain. With regard to pathway selection, migrating neurons fall into three major categories: (1) gliophilic cells that follow elongated glial fibers and bypass other neurons that are encountered within the sphere of their trajectory, (2) neurophilic cells that follow neuronal, particularly axonal surfaces, and bypass nearby glial shafts, and (3) biphilic cells that display temporal or regional affinities towards either glial or neuronal surfaces. Conceptual and factual advances in understanding neuronal migration in the past two decades have provided new insight into the pathogenesis of human brain malformations at the cellular, molecular, and functional levels. Nevertheless, methodological and conceptual advances made in recent years open new possibilities for understanding the effect of the environment on synaptic connectivity in the human brain at the molecular, cellular and functional levels.

References (91)

P.S. Goldman-Rakic
Morphological consequences of prenatal injury to the primate brain
Prog. Brain Res.
(1980)
M.E. Hatten et al.
Neuron-astroglia interactions in vitro and in vivo
Trends Neurosci.
(1986)
R. Johnston et al.
Regulation of the elongating nerve fiber
Curr. Top. Dev. Biol.
(1980)
P.C. Letourneau
Cell-to-substratum adhesion and guidance of axonal elongation
Dev. Biol.
(1975)
P. Levitt et al.
Early divergence and changing proportions of neuronal and glial precursor cells in the primate cerebral ventricular zone
Dev. Biol.
(1983)
H.G.W. Lidov et al.
The structure of cerebral cortex in the rat following prenatal administration of 6-hydroxydopamine
Dev. Brain Res.
(1982)
J. Lindner et al.
Experimental modification of postnatal cerebellar granule cell migration in vitro
Brain Res.
(1986)
T. Maeda et al.
Modification of postnatal development of neocortex in rat brain with deprivation of locus coeruleus
Brain Res.
(1974)
P. Rakic
Timing of major ontogenetic events in the visual cortex of the rhesus monkey
P. Rakic
Neuronal-glial interactions during brain development
Trends Neurosci.
(1981)

P. Rakic

Mechanisms of ocular dominance segregation in this lateral geniculate nucleus: Competitive elimination hypothesis

Trends Neurosci.

(1986)

R.L. Sidman et al.

Neuronal migration, with special reference to developing human brain: a review

Brain Res.

(1973)

S. Wendlandt et al.

The involvement of the noradrenergic system arising from the locus coeruleus in the postnatal development of the neocortex in rat brain

Brain Res.

(1977)

J.B. Angevine et al.

Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse

Nature

(1961)

H. Antomicek et al.

Biochemical and functional characterization of a novel neuron-glia adhesion molecule that is involved in neuronal migration

Cell Biol.

(1987)

C.U. Ariëns Kappers

The Evolution of the Nervous System

(1929)

C.U. Ariëns Kappers et al.

The Comparative Anatomy of the Nervous System of Vertebrates Including Man

(1936)

J.S. Bolton

The exact histological localization of the visual area of the human cerebral cortex

Phil. Trans. R. Soc. Lond. B.

(1900)

J.-P. Bourgeois et al.

Distribution, density and ultrastructure of synapses in the visual cortex in monkeys devoid of retinal input from early embryonic stages

Soc. Neurosci. Abstr.

(1987)

D. Bray

Model for membrane movements in the neural growth cone

Nature

(1973)

M.S. Bretscher

Endocytosis: relation to capping and cell locomotion

Science

(1984)

K. Brodmann

Vergleichende Lokalisationslehre der Grosshirninde

(1909)

V.S. Caviness

Development of neocortical afferent systems: studies in the reeler mouse

Neurosci. Res. Program Bull.

(1982)

V.S. Caviness et al.

Mechanisms of cortical development: a view from mutations in mice

Ann. Rev. Neurosci.

(1978)

V.S. Caviness et al.

Cellular patterns in developmental malformations of neocortex: Neuronal-glial interactions

The Developing Brain and Its Disorders

(1985)

O.D. Creutzfeldt

Generality of the functional structure of the neocortex

Naturwissenschaften

(1977)

A.S. Dekaban

Differential vulnerability to irradiation of various cerebral structures during prenatal development

Radiation Biology of the Fetal and Juvenile Mammal

(1969)

P. Ebersole et al.

Development of visual cortex of rats treated with 6-hydroxydopamine in early life

Anat. Embryol.

(1981)

J.C. Eccles

The cerebral neocortex. A theory of its operation

M.F. Eckenhoff et al.

Radial organization of the hippocampal dentate gyrus: A Golgi, ultrastructural and immunohistochemical analysis in the developing rhesus monkey

J. Comp. Neurol.

(1984)

G.M. Edelman

Cell adhesion molecules

Science

(1983)

D. Eidelberg et al.

Symmetry and asymmetry in the human posterior thalamus

Arch. Neurol.

(1982)

D.L. Felton et al.

Evidence for a neurotrophic role of noradrenalin neurons in the postnatal development of rat cerebral cortex

J. Neurocytol.

(1982)

E. Freytag et al.

Neuropathologic findings in patients of a hospital for the mentally deficient: A survey of 359 cases

Johns Hopkins Med. J.

(1967)

R.L. Friede

Developmental Neuropathology

(1975)

D.J. Goldberg

Actin and myosin in nerve cells

P.S. Goldman et al.

Columnar organization of association and motor cortex: Autoradiographic evidence for cortico-cortical and commissural columns in the frontal lobe of the newborn rhesus monkey

Brain Res.

(1977)

P.S. Goldman-Rakic

Development and plasticity of primate frontal association cortex

P.S. Goldman-Rakic et al.

Experimental modification of gyral patterns

L. Goldstein et al.

Etiology of the illhealth in children born after maternal pelvic irradiation. Part II. Defective children born after postconception pelvic irradiation

Am. J. Roentgenol.

(1929)

M.E. Hatten et al.

Astroglia provide a template for the positioning of cerebellar neurons in vitro

J. Cell Biol.

(1981)

M.E. Hatten et al.

Defects in specific associations between astroglia and neurons occur in microcultures of weaver mouse cerebellar cells

J. Neurosci.

(1984)

L.M. Hemendinger et al.

Cellular migration in developing cerebral wall explants in vitro

Dev. Brain Res.

(1988)

S.P. Hicks et al.

The development of the mammalian nervous system. I. Malformations of the brain, especially the cerebral cortex, induced in rats by radiation. II. Some mechanisms of the malformations of the cortex

J. Comp. Neurol.

(1959)

D.H. Hubel et al.

Ferrier lecture. Functional architecture of macaque monkey visual cortex

Proc. R. Soc. Lond. B.

(1977)

Cited by (284)

FEZ1 participates in human embryonic brain development by modulating neuronal progenitor subpopulation specification and migrations
2023, iScience
Mutations in the human fasciculation and elongation protein zeta 1 (FEZ1) gene are found in schizophrenia and Jacobsen syndrome patients. Here, using human cerebral organoids (hCOs), we show that FEZ1 expression is turned on early during brain development and is detectable in both neuroprogenitor subtypes and immature neurons. FEZ1 deletion disrupts expression of neuronal and synaptic development genes. Using single-cell RNA sequencing, we detected abnormal expansion of homeodomain-only protein homeobox (HOPX)^- outer radial glia (oRG), concurrent with a reduction of HOPX⁺ oRG, in FEZ1-null hCOs. HOPX⁻ oRGs show higher cell mobility as compared to HOPX⁺ oRGs. Ectopic localization of neuroprogenitors to the outer layer is seen in FEZ1-null hCOs. Anomalous encroachment of TBR2⁺ intermediate progenitors into CTIP2⁺ deep layer neurons further indicated abnormalities in cortical layer formation these hCOs. Collectively, our findings highlight the involvement of FEZ1 in early cortical brain development and how it contributes to neurodevelopmental disorders.
Consistency and variation in the placement of cortical folds: A perspective
2023, Brain Multiphysics
Cortical folds, known as gyri and sulci, are prominent features of the human brain that play a crucial role in its function. These folds exhibit both consistency and variation within and across individuals and species, presenting a scientific challenge to our understanding of the underlying mechanisms. In this perspective paper, we summarize current knowledge about fold development and placement. We discuss the temporal and anatomical differences between primary, secondary, and tertiary folds, highlighting the consistency of primary folds and the increasing variation in later-developing folds. We explore the biological and mechanical factors that influence fold placement, including gene expression, tissue growth, axonal tension, curvature, thickness, and stiffness, which likely work together in a complex, coupled manner. We also highlight the need for advanced computational modeling approaches to unravel the mechanisms of precise placement of primary folds and further our understanding of brain complexity.
Statement of significance: Understanding the factors driving both the consistency and variation in fold patterns is essential for unraveling the functional implications and potential links to neurological and psychiatric disorders. Ultimately, gaining deeper insights into fold development and placement could have significant implications for our fundamental understanding of the brain, as well as mental health research and clinical applications.
Systematic cortical thickness and curvature patterns in primates
2023, NeuroImage
Humans are known to have significant and consistent differences in thickness throughout the cortex, with thick outer gyral folds and thin inner sulcal folds. Our previous work has suggested a mechanical basis for this thickness pattern, with the forces generated during cortical folding leading to thick gyri and thin sulci, and shown that cortical thickness varies along a gyral–sulcal spectrum in humans. While other primate species are expected to exhibit similar patterns of cortical thickness, it is currently unknown how these patterns scale across different sizes, forms, and foldedness. Among primates, brains vary enormously from roughly the size of a grape to the size of a grapefruit, and from nearly smooth to dramatically folded; of these, human brains are the largest and most folded. These variations in size and form make comparative neuroanatomy a rich resource for investigating common trends that transcend differences between species. In this study, we examine 12 primate species in order to cover a wide range of sizes and forms, and investigate the scaling of their cortical thickness relative to the surface geometry. The 12 species were selected due to the public availability of either reconstructed surfaces and/or population templates. After obtaining or reconstructing 3D surfaces from publicly available neuroimaging data, we used our surface-based computational pipeline (https://github.com/mholla/curveball) to analyze patterns of cortical thickness and folding with respect to size (total surface area), geometry (i.e. curvature, shape, and sulcal depth), and foldedness (gyrification). In all 12 species, we found consistent cortical thickness variations along a gyral–sulcal spectrum, with convex shapes thicker than concave shapes and saddle shapes in between. Furthermore, we saw an increasing thickness difference between gyri and sulci as brain size increases. Our results suggest a systematic folding mechanism relating local cortical thickness to geometry. Finally, all of our reconstructed surfaces and morphometry data are available for future research in comparative neuroanatomy.
Feature level-based group lasso method for amnestic mild cognitive impairment diagnosis
2021, Computer Methods and Programs in Biomedicine
Previous studies have indicated that brain morphological measures change in patients with amnestic mild cognitive impairment (aMCI). However, most existing classification methods cannot take full advantage of these measures. In this study, we improve traditional multitask learning framework by fully considering the relevance among related tasks and supplementary information from other unrelated tasks at the same time.
We propose a feature level-based group lasso (FL-GL) method in which a feature represents the average value of each ROI for each measure. First, we design a correlation matrix in which each row represents the relationship among different measures for each ROI. And this matrix is used to guide the feature selection based on a group lasso framework. Then, we train specific support vector machine (SVM) classifiers with the selected features for each measure. Finally, a weighted voting strategy is applied to combine these classifiers for a final prediction of aMCI from normal control (NC).
We use the leave-one-out cross-validation strategy to verify our method on two datasets, the Xuan Wu Hospital dataset and the ADNI dataset. Compared with the traditional method, the results show that the classification accuracies can be improved by 6.12 and 4.92% with the FL-GL method on the two datasets.
The results of an ablation study indicated that feature level-based group sparsity term was the core of our method. So, considering correlation at the feature level could improve the traditional multitask learning framework and our FL-GL method obtained better classification performance of patients with MCI and NCs.
Mapping Connectome in Mammalian Brain: A Novel Approach by Bioengineering Neuro-Glia specific Vectors
2020, Journal of Theoretical Biology
The connectome is the comprehensive map of the brain represented by wiring diagram of the full set of neuro-glia and synapses within entire brain of an organism. Some recent scientific efforts have successfully been made to visualize such map at neuro-glial networking level, however, capturing it as one unit of the entire brain have never been elucidated. Moreover, in order to derive structure-function relationship of different brain regions in response to a defined stimulus, there is a need to elucidate the connectome at single neuro-glial ensemble level after brain is challenged with the known memory function. This needs developing molecular approaches to tag neuro-glial activities in response to a conditioned brain function. Such approaches of using specific molecular tags have been tried to visualize independently neuron and glial specific events in response to a memory function, however, they could not tag the connectome together at single neuro-glia ensemble level.
Therefore, there is a need to develop new methods for mapping entire connectome up to a single neuro-glial precision and resolution, with a purpose of tagging specific brain region accountable to execute a special memory formation process. The present hypothetical paper aims to propose a novel molecular method to generate the structural connectome at neuro-glial level in mice brain. Herein, we propose to tag the entire connectome at neuro-glia precision by generating a transgenic mice via transposing and recombining engineered novel “Neuro-Glia specific Vectors” (NGVs: specific to excitatory neurons, inhibitory neurons and glial cells) vis a vis “Transcriptional/ Translational Messenger (TMs: specific to metalloproteinases, MMP-9) coupled with different color protein tags, followed by the Clarity. Herein, the NGVs will be translated via Neuro-glia specific promoters, while TMs will be translated via endogenous MMP-9 promoter in all neuro-glial cells. The viability of all constructs will be verified in cortical/ hippocampal culture by inducing them to undergo chemically induced long term potentionation (cLTP) following visualization of different colored pattern. This will be further confirmed by Immunostaning, Western Blot and RT-PCR analysis. Additionally, in this approach, one can decipher the dynamics of molecular and cellular events associated with MMP-9 seretome by monitoring the trafficking of tagged endogenous MMP-9 protein after neuronal stimulation by cLTP in vitro. However, for visualizing complete connectome, the adult transgenic mice will be challenged with fear consolidation (Fear context and contextual cue) tests followed by Clarity coupled Light Sheet Microscopy to analyze neuro-glia ensemble following whole brain imaging.
Robust multitask feature learning for amnestic mild cognitive impairment diagnosis based on multidimensional surface measures
2020, Medicine in Novel Technology and Devices
Citation Excerpt :
Cortical thickness is a measure of the shortest distance from the surface towards the white matter [10]. Surface area for each vertex on the pial surface is defined as the mean area of all triangles linked to this vertex [8]. GM volume is calculated by multiplying the thickness and surface area at each vertex.
Previous studies have shown that amnestic mild cognitive impairment (aMCI) involves in the morphological abnormalities of multiple regions, including cortical thickness, sulcus depth, surface area, gray matter volume, jacobian metric and average curvature. All the measures have unique neuropathological and genetic meanings. However, most existing methods simply average or concatenate these measures when constructing the classifiers, which may include redundant information and ignore the relationships among them. In this study, we treat each measure as a task in our multitask learning framework. Considering the actual situation that we do not know the correlation between tasks in advance, we use a robust multitask feature learning (rMTFL) method to select a group of features among correlated measures and provide additional information by identifying outlier tasks at the same time. Then, we train several SVM classifiers and for each measure, we input the selected features into the corresponding SVM classifier. Finally, we use an ensemble classification strategy to combine the results of these classifiers based on the accuracy to make the final prediction. We use the leave-one-out cross-validation to evaluate our proposed method with 46 amnestic mild cognitive impairment (aMCI) and 52 normal controls (NC). The results show that rMTFL algorithm is superior to the group lasso method and average curvature is the outlier task based on multidimensional surface measures.

View all citing articles on Scopus

: Source: B. Brouwer (1946) In Memoriam Prof. Dr. Cornelius Ubbo Ariëns Kappers, Psychiatrische en Neurologische Bladen, pp. 1-16.

View full text

Defects of neuronal migration and the pathogenesis of cortical malformations

Publisher Summary

Prog. Brain Res.

Trends Neurosci.

Curr. Top. Dev. Biol.

Dev. Biol.

Dev. Biol.

Dev. Brain Res.

Brain Res.

Brain Res.

Trends Neurosci.

Trends Neurosci.

Brain Res.

Brain Res.

Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse

Nature

Biochemical and functional characterization of a novel neuron-glia adhesion molecule that is involved in neuronal migration

Cell Biol.

The Evolution of the Nervous System

The Comparative Anatomy of the Nervous System of Vertebrates Including Man

The exact histological localization of the visual area of the human cerebral cortex

Phil. Trans. R. Soc. Lond. B.

Distribution, density and ultrastructure of synapses in the visual cortex in monkeys devoid of retinal input from early embryonic stages

Soc. Neurosci. Abstr.

Model for membrane movements in the neural growth cone

Nature

Endocytosis: relation to capping and cell locomotion

Science

Vergleichende Lokalisationslehre der Grosshirninde

Development of neocortical afferent systems: studies in the reeler mouse

Neurosci. Res. Program Bull.

Mechanisms of cortical development: a view from mutations in mice

Ann. Rev. Neurosci.

Cellular patterns in developmental malformations of neocortex: Neuronal-glial interactions

The Developing Brain and Its Disorders

Generality of the functional structure of the neocortex

Naturwissenschaften

Differential vulnerability to irradiation of various cerebral structures during prenatal development

Radiation Biology of the Fetal and Juvenile Mammal

Development of visual cortex of rats treated with 6-hydroxydopamine in early life

Anat. Embryol.

The cerebral neocortex. A theory of its operation

Radial organization of the hippocampal dentate gyrus: A Golgi, ultrastructural and immunohistochemical analysis in the developing rhesus monkey

J. Comp. Neurol.

Cell adhesion molecules

Science

Symmetry and asymmetry in the human posterior thalamus

Arch. Neurol.

Evidence for a neurotrophic role of noradrenalin neurons in the postnatal development of rat cerebral cortex

J. Neurocytol.

Neuropathologic findings in patients of a hospital for the mentally deficient: A survey of 359 cases

Johns Hopkins Med. J.

Developmental Neuropathology

Actin and myosin in nerve cells

Columnar organization of association and motor cortex: Autoradiographic evidence for cortico-cortical and commissural columns in the frontal lobe of the newborn rhesus monkey

Brain Res.

Development and plasticity of primate frontal association cortex

Experimental modification of gyral patterns

Etiology of the illhealth in children born after maternal pelvic irradiation. Part II. Defective children born after postconception pelvic irradiation

Am. J. Roentgenol.

Astroglia provide a template for the positioning of cerebellar neurons in vitro

J. Cell Biol.

Defects in specific associations between astroglia and neurons occur in microcultures of weaver mouse cerebellar cells

J. Neurosci.

Cellular migration in developing cerebral wall explants in vitro

Dev. Brain Res.

The development of the mammalian nervous system. I. Malformations of the brain, especially the cerebral cortex, induced in rats by radiation. II. Some mechanisms of the malformations of the cortex

J. Comp. Neurol.

Ferrier lecture. Functional architecture of macaque monkey visual cortex

Proc. R. Soc. Lond. B.