Chapter Two - Neuromechanics: From Neurons to Brain

https://doi.org/10.1016/bs.aams.2015.10.002Get rights and content

Abstract

Arguably, the brain is the most complex organ in the human body, and, at the same time, the least well understood. Today, more than ever before, the human brain has become a subject of narcissistic study and fascination. The fields of neuroscience, neurology, neurosurgery, and neuroradiology have seen tremendous progress over the past two decades; yet, the field of neuromechanics remains underappreciated and poorly understood. Here, we show that mechanical stretch, strain, stress, and force play a critical role in modulating the structure and function of the brain. We discuss the role of neuromechanics across the scales, from individual neurons via neuronal tissue to the whole brain. We review current research highlights and discuss challenges and potential future directions. Using the nonlinear field theories of mechanics, we illustrate three phenomena which are tightly regulated by mechanical factors: neuroelasticity, the extremely soft behavior of the brain independent of time; neurodevelopment, the evolution of the brain at extremely long time scales; and neurodamage, the degradation of the brain at extremely short time scales. We hope that this review will become a starting point for a multidisciplinary approach to the mechanics of the brain with potential impact in preventing, diagnosing, and treating neurological disorders.

Section snippets

Motivation

Embedded in the skull, surrounded by the cerebrospinal fluid, and enveloped by the meninges, our brain is remarkably well protected and mechanically isolated from its environment (Nolte, 2009). It is no surprise that many scientists believe that its mechanical behavior is entirely irrelevant to its structure and function. Over the past two decades, however, we have come to realize that virtually all of the 210 different cell types in our body respond to mechanical factors, and that

Neuroelasticity

Under small deformations, our brain is essentially elastic and its deformations are almost entirely reversible. In this section, we focus on the neuroelasticity of the brain. Specifically, we restrict our attention to phenomena that take place on relatively slow time scales, where viscous effects play a less significant role. We highlight the elasticity of single neurons in Section 2.1, the elasticity of gray and white matter tissue in Section 2.2, and the elasticity of the brain in Section 2.3

Neurodevelopment

Under large deformations, over long time scales, our brain becomes inelastic and capable of adapting to environmental cues. In this section, we focus on the inelasticity associated with neurodevelopment. We restrict our attention to phenomena on relatively slow time scales, at which the brain is able to sense, respond to, and adapt to changes in its environment. We collectively refer to these phenomena as growth. While many environmental conditions may impact the brain during neurodevelopment,

Neurodamage

Under large deformations, over short time scales, our brain becomes inelastic and vulnerable to damage. In this section, we focus on the inelasticity associated with neurodamage. We consider phenomena on relatively fast time scales, on which the brain is unable to respond to environmental changes. While rate effects may play a more significant role during damage than during elasticity and development, for the sake of clarity, here we focus primarily on rate-independent effects, but include

Open Questions and Challenges

While many scientists believe that understanding the human brain is primarily a question of biochemical and electrical events, increasing evidence suggests that mechanical regulators play an equally important role in neuronal development, degeneration, regeneration, and aging (Franze et al., 2013). In this review, we have highlighted selected pathologies which undoubtably show a mechanical trace, including the prominent examples of axon elongation (Suter & Miller, 2011), cortical folding (Xu et

Acknowledgments

This study was supported by the Wolfson/Royal Society Merit Award and the EC Reintegration Grant under Framework VII to A.G., the German National Science Foundation grant STE 544/50-1 to S.B.; and the National Science Foundation INSPIRE grant 1233054 and the National Institutes of Health Grant U54GM072970 to E.K.

Glossary

Axon
Long, slender projection from the cell body of a nerve cell, or neuron, that transmits electrical signals from the cell body to other neurons.
Cerebral Cortex
Outer 2–4 mm-thick gray matter layer around the brain that consists primarily of cell bodies and plays an important role in attention, awareness, mconsciousness, language, memory, and thought.
Cerebrospinal Fluid
Clear and colorless body fluid that acts as a cushion for the cerebral cortex and provides a basic mechanical protection for

References (122)

  • Y. Feng et al.

    Viscoelastic properties of the ferret brain measured in vivo at multiple frequencies by magnetic resonance elastography

    Journal of Biomechanics

    (2013)
  • G. Franceschini et al.

    Brain tissue deforms similarly to filled elastomers and follows consolidation theory

    Journal of the Mechanics and Physics of Solids

    (2006)
  • K. Garikipati et al.

    A continuum treatment of growth in biological tissue: The coupling of mass transport and mechanics

    Journal of the Mechanics and Physics of Solids

    (2004)
  • S. Göktepe et al.

    A generic approach towards finite growth with examples of athlete's heart, cardiac dilation, and cardiac wall thickening

    Journal of the Mechanics and Physics of Solids

    (2010)
  • A.Y. Hardan et al.

    Increased frontal cortical folding in autism: A preliminary MRI study

    Psychiatry Research

    (2004)
  • T. Kaster et al.

    Measurement of the hyperelastic properties of ex vivo brain tissue slices

    Journal of Biomechanics

    (2011)
  • S. Kleiven et al.

    Consequences of head size following trauma to the human head

    Journal of Biomechanics

    (2002)
  • D.E. Koser et al.

    CNS cell distribution and axon orientation determine local spinal cord mechanical properties

    Biophysical Journal

    (2015)
  • N. Memarian et al.

    Multimodal data and machine learning for surgery outcome prediction in complicated cases of mesial temporal lobe epilepsy

    Computers in Biology and Medicine

    (2015)
  • K. Miller et al.

    Constitutive modelling of brain tissue: Experiment and theory

    Journal of Biomechanics

    (1997)
  • K. Miller et al.

    Mechanical properties of brain tissue in tension

    Journal of Biomechanics

    (2002)
  • M. O’Toole et al.

    A physical model of axonal elongation: Force, viscosity, and adhesions govern the mode of outgrowth

    Biophysical Journal

    (2008)
  • F. Pervin et al.

    Dynamic mechanical response of bovine gray matter and white matter brain tissues under compression

    Journal of Biomechanics

    (2009)
  • T.P. Prevost et al.

    Biomechanics of brain tissue

    Acta Biomater

    (2011)
  • B. Rashid et al.

    Mechanical characterization of brain tissue in simple shear at dynamic strain rates

    Journal of the Mechanical Behavior of Biomedical Materials

    (2013)
  • C. Raybaud et al.

    Development and dysgenesis of the cerebral cortex: Malformations of cortical development

    Neuroimaging Clinics of North America

    (2011)
  • E.K. Rodriguez et al.

    Stress-dependent finite growth in soft elastic tissues

    Journal of Biomechanics

    (1994)
  • N.J. Abbot

    Evidence for bulk flow of brain interstitial fluid: Significance for physiology and pathology

    Neurochemistry International

    (2004)
  • B. Alberts et al.

    Molecular biology of the cell

    (2014)
  • H.G. Allen

    Analysis and design of structural sandwich panels

    (1969)
  • A.C. Bain et al.

    Tissue-level thresholds for axonal damage in an experimental model of central nervous system white matter injury

    Journal of Biomechanical Engineering

    (2000)
  • A.C. Bain et al.

    Dynamic stretch correlates to both morphological abnormalities and electrophysiological impairment in a model of traumatical axonal injury

    Journal of Neurotrauma

    (2001)
  • J. Bardin

    Neuroscience: Making connections

    Nature

    (2012)
  • A.J. Barkovich et al.

    A developmental and genetic classification for malformations of cortical development: Update 2012

    Brain

    (2012)
  • P.V. Bayly et al.

    A cortical folding model incorporating stress-dependent growth explains gyral wavelengths and stress patterns in the developing brain

    Physical Biology

    (2013)
  • R. Bernal et al.

    Mechanical properties of axons

    Physical Review Letters

    (2007)
  • L.E. Bilston

    Neural tissue biomechanics

    (2011)
  • L.E. Bilston et al.

    Large strain behavior of brain tissue in shear: Some experimental data and differential constitutive model

    Biorheology

    (2001)
  • M.A. Biot

    Folding instability of a layered viscoelastic medium under compression

    Proceedings of the Royal Society of London A

    (1957)
  • S. Budday et al.

    Period-doubling and period-tripling in growing bilayered systems

    Philosophical Magazine

    (2015)
  • S. Budday et al.

    Mechanical properties of gray and white matter brain tissue by indentation

    Journal of the Mechanical Behavior of Biomedical Materials

    (2014)
  • S. Budday et al.

    A mechanical model predicts morphological abnormalities in the developing human brain

    Scientific Reports

    (2014)
  • S. Budday et al.

    Physical biology of human brain development

    Frontiers in Cellular Neuroscience

    (2015)
  • S. Budday et al.

    Secondary instabilities modulate cortical complexity in the mammalian brain

    Philosophical Magazine

    (2015)
  • A. Buganza et al.

    Review: Systems-based approaches towards wound healing

    Pediatric Research

    (2013)
  • D.B. Camarillo et al.

    An instrumented mouthguard for measuring linear and angular head impact kinematics in American football

    Annals of Biomedical Engineering

    (2013)
  • S. Chatelin et al.

    Fifty years of brain tissue mechanical testing: From in vitro to in vivo investigations

    Biorheology

    (2010)
  • P. Ciarletta et al.

    Pattern selection in growing tubular tissues

    Physical Review Letters

    (2014)
  • R.J.H. Cloots et al.

    Micromechanics of diffuse axonal injury: Influence of axonal orientation and anisotropy

    Biomechanics and Modeling in Mechanobiology

    (2011)
  • R.J.H. Cloots et al.

    Multi-scale mechanics of traumatic brain injury: Predicting axonal strains from head loads

    Biomechanics and Modeling in Mechanobiology

    (2013)
  • Cited by (0)

    View full text