Residual stress in the adult mouse brain

This work provides direct evidence that sustained tensile stress exists in white matter of the mature mouse brain. This finding has important implications for the mechanisms of brain development, as tension in neural axons has been hypothesized to drive cortical folding in the human brain. In addition, knowledge of residual stress is required to fully understand the mechanisms behind traumatic brain injury and changes in mechanical properties due to aging and disease. To estimate residual stress in the brain, we performed serial dissection experiments on 500-mum thick coronal slices from fresh adult mouse brains and developed finite element models for these experiments. Radial cuts were made either into cortical gray matter, or through the cortex and the underlying white matter tract composed of parallel neural axons. Cuts into cortical gray matter did not open, but cuts through both layers consistently opened at the point where the cut crossed the white matter. We infer that the cerebral white matter is under considerable tension in the circumferential direction in the coronal cerebral plane, parallel to most of the neural fibers, while the cerebral cortical gray matter is in compression. The models show that the observed deformation after cutting can be caused by more growth in the gray matter than in the white matter, with the estimated tensile stress in the white matter being on the order of 100–1,000 Pa.

[1]  Amy Brooks-Kayal,et al.  Disorders of cortical development and epilepsy. , 2002, Archives of neurology.

[2]  Barclay Morrison,et al.  Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation. , 2007, Journal of neurotrauma.

[3]  David F Meaney,et al.  Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. , 2006, Biophysical journal.

[4]  C. Löhr,et al.  Co-expression of myosin II regulatory light chain and the NMDAR1 subunit in neonatal and adult mouse brain , 2007, Brain Research Bulletin.

[5]  K. Chinzei,et al.  Constitutive modelling of brain tissue: experiment and theory. , 1997, Journal of biomechanics.

[6]  J. van Dommelen,et al.  The mechanical behaviour of brain tissue: large strain response and constitutive modelling. , 2006, Biorheology.

[7]  Matthew L. Baker,et al.  Ab Initio Modeling of the Herpesvirus VP26 Core Domain Assessed by CryoEM Density , 2006, PLoS Comput. Biol..

[8]  Larry A Taber,et al.  On the effects of residual stress in microindentation tests of soft tissue structures. , 2004, Journal of biomechanical engineering.

[9]  King H. Yang,et al.  Biomechanics of neurotrauma , 2001, Neurological research.

[10]  Facundo Valverde,et al.  Golgi Atlas of the Postnatal Mouse Brain , 2004 .

[11]  Corina Stefania Drapaca,et al.  A Quasi-linear Viscoelastic Constitutive Equation for the Brain: Application to Hydrocephalus , 2006 .

[12]  H. Barbas,et al.  Developmental mechanics of the primate cerebral cortex , 2005, Anatomy and Embryology.

[13]  S. Margulies,et al.  Age-dependent material properties of the porcine cerebrum: effect on pediatric inertial head injury criteria. , 1998, Journal of biomechanics.

[14]  W. Welker,et al.  Why Does Cerebral Cortex Fissure and Fold ? A Review of Determinants of Gyri and Sulci , 2022 .

[15]  A. Gefen,et al.  Are in vivo and in situ brain tissues mechanically similar? , 2004, Journal of biomechanics.

[16]  G. Busatto,et al.  Reduced cortical folding in schizophrenia: an MRI morphometric study. , 2003, The American journal of psychiatry.

[17]  M. Prange,et al.  Regional, directional, and age-dependent properties of the brain undergoing large deformation. , 2002, Journal of biomechanical engineering.

[18]  Francisco Aboitiz,et al.  Species Differences and Similarities in the Fine Structure of the Mammalian Corpus callosum , 2001, Brain, Behavior and Evolution.

[19]  D. V. van Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system. , 1997, Nature.

[20]  Claus C. Hilgetag,et al.  Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex , 2006, PLoS Comput. Biol..

[21]  R. Buxbaum,et al.  The cytomechanics of axonal elongation and retraction , 1989, The Journal of cell biology.

[22]  C. Gans,et al.  Biomechanics: Motion, Flow, Stress, and Growth , 1990 .

[23]  T. Heiman-Patterson,et al.  Elevated Cortical Extracellular Fluid Glutamate in Transgenic Mice Expressing Human Mutant (G93A) Cu/Zn Superoxide Dismutase , 2000, Journal of neurochemistry.

[24]  P. Hüppi,et al.  Diffusion tensor imaging of normal and injured developing human brain ‐ a technical review , 2002, NMR in biomedicine.

[25]  Robert E. Buxbaum,et al.  Direct evidence that growth cones pull , 1989, Nature.

[26]  A. Gefen,et al.  Age-dependent changes in material properties of the brain and braincase of the rat. , 2003, Journal of neurotrauma.

[27]  Y. Fung,et al.  Biomechanics: Mechanical Properties of Living Tissues , 1981 .

[28]  S Chada,et al.  Cytomechanics of neurite outgrowth from chick brain neurons. , 1997, Journal of cell science.

[29]  L A Taber,et al.  Biomechanics of cardiovascular development. , 2001, Annual review of biomedical engineering.

[30]  D. V. van Essen,et al.  Cortical Folding Abnormalities in Autism Revealed by Surface-Based Morphometry , 2007, The Journal of Neuroscience.

[31]  Renato Perucchio,et al.  Modeling Heart Development , 2000 .

[32]  Jean-Marie Bonny,et al.  In vivo analysis of the post‐natal development of normal mouse brain by DTI , 2007, NMR in biomedicine.

[33]  P. Todd A geometric model for the cortical folding pattern of simple folded brains. , 1982, Journal of theoretical biology.

[34]  Karol Miller,et al.  Brain mechanics For neurosurgery: modeling issues , 2002, Biomechanics and modeling in mechanobiology.

[35]  K. Miller,et al.  Reassessment of brain elasticity for analysis of biomechanisms of hydrocephalus. , 2004, Journal of biomechanics.

[36]  J. Chun,et al.  Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding , 2003, Nature Neuroscience.

[37]  A. McCulloch,et al.  Stress-dependent finite growth in soft elastic tissues. , 1994, Journal of biomechanics.

[38]  Y. Burnod,et al.  A morphogenetic model for the development of cortical convolutions. , 2005, Cerebral cortex.

[39]  S. Laughlin,et al.  Ion-Channel Noise Places Limits on the Miniaturization of the Brain’s Wiring , 2005, Current Biology.

[40]  W. Welker Why Does Cerebral Cortex Fissure and Fold , 1990 .

[41]  D. V. Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system , 1997, Nature.

[42]  K. Chinzei,et al.  Mechanical properties of brain tissue in tension. , 2002, Journal of biomechanics.

[43]  Larry A. Taber,et al.  Theoretical study of Beloussov’s hyper-restoration hypothesis for mechanical regulation of morphogenesis , 2008, Biomechanics and modeling in mechanobiology.

[44]  K Miller,et al.  Mechanical properties of brain tissue in-vivo: experiment and computer simulation. , 2000, Journal of biomechanics.

[45]  Brittany Coats,et al.  Material properties of porcine parietal cortex. , 2006, Journal of biomechanics.

[46]  M. Goldberg,et al.  AMPA/Kainate Receptor Activation Mediates Hypoxic Oligodendrocyte Death and Axonal Injury in Cerebral White Matter , 2001, The Journal of Neuroscience.

[47]  V. Caviness,et al.  Mechanical model of brain convolutional development. , 1975, Science.

[48]  L. Bilston,et al.  Unconfined compression of white matter. , 2007, Journal of biomechanics.

[49]  K. Miller,et al.  Constitutive model of brain tissue suitable for finite element analysis of surgical procedures. , 1999, Journal of biomechanics.

[50]  Robert E. Buxbaum,et al.  Mechanical tension can specify axonal fate in hippocampal neurons , 2002, The Journal of cell biology.

[51]  P. Levitt,et al.  Myosin II distribution in neurons is consistent with a role in growth cone motility but not synaptic vesicle mobilization , 1992, Neuron.