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Physical biology of human brain development.

Budday S, Steinmann P, Kuhl E - Front Cell Neurosci (2015)

Bottom Line: Neurodevelopment is a complex, dynamic process that involves a precisely orchestrated sequence of genetic, environmental, biochemical, and physical events.However, the precise impact of neuronal differentiation, migration, and connection on the physical forces during cortical folding remains unknown.We revisit cortical folding as the instability problem of constrained differential growth in a multi-layered system.

View Article: PubMed Central - PubMed

Affiliation: Chair of Applied Mechanics, Department of Mechanical Engineering, University of Erlangen/Nuremberg Erlangen, Germany.

ABSTRACT
Neurodevelopment is a complex, dynamic process that involves a precisely orchestrated sequence of genetic, environmental, biochemical, and physical events. Developmental biology and genetics have shaped our understanding of the molecular and cellular mechanisms during neurodevelopment. Recent studies suggest that physical forces play a central role in translating these cellular mechanisms into the complex surface morphology of the human brain. However, the precise impact of neuronal differentiation, migration, and connection on the physical forces during cortical folding remains unknown. Here we review the cellular mechanisms of neurodevelopment with a view toward surface morphogenesis, pattern selection, and evolution of shape. We revisit cortical folding as the instability problem of constrained differential growth in a multi-layered system. To identify the contributing factors of differential growth, we map out the timeline of neurodevelopment in humans and highlight the cellular events associated with extreme radial and tangential expansion. We demonstrate how computational modeling of differential growth can bridge the scales-from phenomena on the cellular level toward form and function on the organ level-to make quantitative, personalized predictions. Physics-based models can quantify cortical stresses, identify critical folding conditions, rationalize pattern selection, and predict gyral wavelengths and gyrification indices. We illustrate that physical forces can explain cortical malformations as emergent properties of developmental disorders. Combining biology and physics holds promise to advance our understanding of human brain development and enable early diagnostics of cortical malformations with the ultimate goal to improve treatment of neurodevelopmental disorders including epilepsy, autism spectrum disorders, and schizophrenia.

No MeSH data available.


Related in: MedlinePlus

Early development and neurogenesis. Early development is characterized by interkinetic nuclear migration, an oscillatory process during which neuroepithelial cells divide symmetrically at the margin of the ventricle and undergo four phases. Early born neurons are referred to as interneurons and travel tangentially within the marginal and intermediate zones. Neurogenesis begins when progenitor cells switch from symmetric to asymmetric cell division. Apical progenitor cells in the ventricular zone and basal progenitor cells in the subventricular zone accumulate to become the major source of pyramidal neurons.
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Figure 1: Early development and neurogenesis. Early development is characterized by interkinetic nuclear migration, an oscillatory process during which neuroepithelial cells divide symmetrically at the margin of the ventricle and undergo four phases. Early born neurons are referred to as interneurons and travel tangentially within the marginal and intermediate zones. Neurogenesis begins when progenitor cells switch from symmetric to asymmetric cell division. Apical progenitor cells in the ventricular zone and basal progenitor cells in the subventricular zone accumulate to become the major source of pyramidal neurons.

Mentions: Intracranial pressure is now recognized as an important regulator of normal brain development (Desmond, 1985). In the absence pressure, the brain cavity volume enlarges less rapidly, brain tissue grows at a reduced rate, remains grossly disorganized, and tends to fold inward into the ventricular cavity (Desmond and Jacobson, 1977). In addition to the mechanical regulation through pressure, the cerebrospinal fluid provides biochemical regulation through diffusible extracellular signals, which modulate symmetric and asymmetric progenitor cell division during development and disease (Lehtinen et al., 2011). Figure 1 illustrates the timeline of early development and neurogenesis including cell division and cell migration.


Physical biology of human brain development.

Budday S, Steinmann P, Kuhl E - Front Cell Neurosci (2015)

Early development and neurogenesis. Early development is characterized by interkinetic nuclear migration, an oscillatory process during which neuroepithelial cells divide symmetrically at the margin of the ventricle and undergo four phases. Early born neurons are referred to as interneurons and travel tangentially within the marginal and intermediate zones. Neurogenesis begins when progenitor cells switch from symmetric to asymmetric cell division. Apical progenitor cells in the ventricular zone and basal progenitor cells in the subventricular zone accumulate to become the major source of pyramidal neurons.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4495345&req=5

Figure 1: Early development and neurogenesis. Early development is characterized by interkinetic nuclear migration, an oscillatory process during which neuroepithelial cells divide symmetrically at the margin of the ventricle and undergo four phases. Early born neurons are referred to as interneurons and travel tangentially within the marginal and intermediate zones. Neurogenesis begins when progenitor cells switch from symmetric to asymmetric cell division. Apical progenitor cells in the ventricular zone and basal progenitor cells in the subventricular zone accumulate to become the major source of pyramidal neurons.
Mentions: Intracranial pressure is now recognized as an important regulator of normal brain development (Desmond, 1985). In the absence pressure, the brain cavity volume enlarges less rapidly, brain tissue grows at a reduced rate, remains grossly disorganized, and tends to fold inward into the ventricular cavity (Desmond and Jacobson, 1977). In addition to the mechanical regulation through pressure, the cerebrospinal fluid provides biochemical regulation through diffusible extracellular signals, which modulate symmetric and asymmetric progenitor cell division during development and disease (Lehtinen et al., 2011). Figure 1 illustrates the timeline of early development and neurogenesis including cell division and cell migration.

Bottom Line: Neurodevelopment is a complex, dynamic process that involves a precisely orchestrated sequence of genetic, environmental, biochemical, and physical events.However, the precise impact of neuronal differentiation, migration, and connection on the physical forces during cortical folding remains unknown.We revisit cortical folding as the instability problem of constrained differential growth in a multi-layered system.

View Article: PubMed Central - PubMed

Affiliation: Chair of Applied Mechanics, Department of Mechanical Engineering, University of Erlangen/Nuremberg Erlangen, Germany.

ABSTRACT
Neurodevelopment is a complex, dynamic process that involves a precisely orchestrated sequence of genetic, environmental, biochemical, and physical events. Developmental biology and genetics have shaped our understanding of the molecular and cellular mechanisms during neurodevelopment. Recent studies suggest that physical forces play a central role in translating these cellular mechanisms into the complex surface morphology of the human brain. However, the precise impact of neuronal differentiation, migration, and connection on the physical forces during cortical folding remains unknown. Here we review the cellular mechanisms of neurodevelopment with a view toward surface morphogenesis, pattern selection, and evolution of shape. We revisit cortical folding as the instability problem of constrained differential growth in a multi-layered system. To identify the contributing factors of differential growth, we map out the timeline of neurodevelopment in humans and highlight the cellular events associated with extreme radial and tangential expansion. We demonstrate how computational modeling of differential growth can bridge the scales-from phenomena on the cellular level toward form and function on the organ level-to make quantitative, personalized predictions. Physics-based models can quantify cortical stresses, identify critical folding conditions, rationalize pattern selection, and predict gyral wavelengths and gyrification indices. We illustrate that physical forces can explain cortical malformations as emergent properties of developmental disorders. Combining biology and physics holds promise to advance our understanding of human brain development and enable early diagnostics of cortical malformations with the ultimate goal to improve treatment of neurodevelopmental disorders including epilepsy, autism spectrum disorders, and schizophrenia.

No MeSH data available.


Related in: MedlinePlus