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Mechanics of the brain: perspectives, challenges, and opportunities.

Goriely A, Geers MG, Holzapfel GA, Jayamohan J, Jérusalem A, Sivaloganathan S, Squier W, van Dommelen JA, Waters S, Kuhl E - Biomech Model Mechanobiol (2015)

Bottom Line: Despite a clear evidence that mechanical factors play an important role in regulating brain activity, current research efforts focus mainly on the biochemical or electrophysiological activity of the brain.This opinion piece synthesizes expertise in applied mathematics, solid and fluid mechanics, biomechanics, experimentation, material sciences, neuropathology, and neurosurgery to address today's open questions at the forefront of neuromechanics.The multi-disciplinary analysis of these various phenomena and pathologies presents new opportunities and suggests that mechanical modeling is a central tool to bridge the scales by synthesizing information from the molecular via the cellular and tissue all the way to the organ level.

View Article: PubMed Central - PubMed

Affiliation: Mathematical Institute, University of Oxford, Oxford, OX2 6GG, UK, Alain.Goriely@maths.ox.ac.uk.

ABSTRACT
The human brain is the continuous subject of extensive investigation aimed at understanding its behavior and function. Despite a clear evidence that mechanical factors play an important role in regulating brain activity, current research efforts focus mainly on the biochemical or electrophysiological activity of the brain. Here, we show that classical mechanical concepts including deformations, stretch, strain, strain rate, pressure, and stress play a crucial role in modulating both brain form and brain function. This opinion piece synthesizes expertise in applied mathematics, solid and fluid mechanics, biomechanics, experimentation, material sciences, neuropathology, and neurosurgery to address today's open questions at the forefront of neuromechanics. We critically review the current literature and discuss challenges related to neurodevelopment, cerebral edema, lissencephaly, polymicrogyria, hydrocephaly, craniectomy, spinal cord injury, tumor growth, traumatic brain injury, and shaken baby syndrome. The multi-disciplinary analysis of these various phenomena and pathologies presents new opportunities and suggests that mechanical modeling is a central tool to bridge the scales by synthesizing information from the molecular via the cellular and tissue all the way to the organ level.

No MeSH data available.


Related in: MedlinePlus

The multiple coupled mechanisms resulting in cytotoxic and vasogenic cerebral edemas. BBB stands for blood brain barrier. The inset shows the possible motion of charges in the capillaries, cells, and tissues, adapted with permission from Lang (2014)
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Fig6: The multiple coupled mechanisms resulting in cytotoxic and vasogenic cerebral edemas. BBB stands for blood brain barrier. The inset shows the possible motion of charges in the capillaries, cells, and tissues, adapted with permission from Lang (2014)

Mentions: During swelling, the fluid enters the tissue from the cerebral capillaries. As shown in Fig. 6, there are several possible mechanisms creating this influx of water. During impact injury, the integrity of the blood vessels can be compromised and blood can directly enter the tissue. After an ischemic stroke, however, it is the ionic imbalance that creates swelling. In a healthy brain tissue, both the composition of the intracellular fluid and the cell volume are actively controlled by ion pumps in the cell membrane. During ischemia, due to a lack of oxygen, the cells cannot properly control the active pumping across the cell membrane, and the osmotic equilibrium is perturbed. As a result, there is a net flux of ions into the cell following electrochemical potential gradients and, accordingly, an uptake of water from the extracellular space into the cell. This cell swelling does not, however, produce tissue swelling as it only trades fluid with the interstitium (Liang et al. 2007). Nevertheless, cytotoxic swelling can have a profound effect on the tissue as it changes ion and protein concentrations of the interstitial fluid. This imbalance can provide a driving force for vasogenic edema and lead to bulk swelling (Kawamata et al. 2007). Further, highly swollen cells may burst, causing their contents to become merged with the interstitium. In particular, cells can release negatively charged macromolecules such as glycosaminoglycans and proteoglycans (Syková and Nicholson 2008). Due to their large size, these molecules contribute to the overall fixed charge density, that is, the overall negative immobile charges attached to the tissue. The presence of these immobile charges induces an ionic concentration difference between the tissue and the capillary bed, and drives water movement into the tissue through the Donnan effect (Donnan 1924). Under these conditions, the tight endothelial junctions of the blood brain barrier are disrupted and the water influx causes vasogenic edema, an overall penetration of fluid in the tissue due to the disruption of the blood brain barrier.Fig. 6


Mechanics of the brain: perspectives, challenges, and opportunities.

Goriely A, Geers MG, Holzapfel GA, Jayamohan J, Jérusalem A, Sivaloganathan S, Squier W, van Dommelen JA, Waters S, Kuhl E - Biomech Model Mechanobiol (2015)

The multiple coupled mechanisms resulting in cytotoxic and vasogenic cerebral edemas. BBB stands for blood brain barrier. The inset shows the possible motion of charges in the capillaries, cells, and tissues, adapted with permission from Lang (2014)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4562999&req=5

Fig6: The multiple coupled mechanisms resulting in cytotoxic and vasogenic cerebral edemas. BBB stands for blood brain barrier. The inset shows the possible motion of charges in the capillaries, cells, and tissues, adapted with permission from Lang (2014)
Mentions: During swelling, the fluid enters the tissue from the cerebral capillaries. As shown in Fig. 6, there are several possible mechanisms creating this influx of water. During impact injury, the integrity of the blood vessels can be compromised and blood can directly enter the tissue. After an ischemic stroke, however, it is the ionic imbalance that creates swelling. In a healthy brain tissue, both the composition of the intracellular fluid and the cell volume are actively controlled by ion pumps in the cell membrane. During ischemia, due to a lack of oxygen, the cells cannot properly control the active pumping across the cell membrane, and the osmotic equilibrium is perturbed. As a result, there is a net flux of ions into the cell following electrochemical potential gradients and, accordingly, an uptake of water from the extracellular space into the cell. This cell swelling does not, however, produce tissue swelling as it only trades fluid with the interstitium (Liang et al. 2007). Nevertheless, cytotoxic swelling can have a profound effect on the tissue as it changes ion and protein concentrations of the interstitial fluid. This imbalance can provide a driving force for vasogenic edema and lead to bulk swelling (Kawamata et al. 2007). Further, highly swollen cells may burst, causing their contents to become merged with the interstitium. In particular, cells can release negatively charged macromolecules such as glycosaminoglycans and proteoglycans (Syková and Nicholson 2008). Due to their large size, these molecules contribute to the overall fixed charge density, that is, the overall negative immobile charges attached to the tissue. The presence of these immobile charges induces an ionic concentration difference between the tissue and the capillary bed, and drives water movement into the tissue through the Donnan effect (Donnan 1924). Under these conditions, the tight endothelial junctions of the blood brain barrier are disrupted and the water influx causes vasogenic edema, an overall penetration of fluid in the tissue due to the disruption of the blood brain barrier.Fig. 6

Bottom Line: Despite a clear evidence that mechanical factors play an important role in regulating brain activity, current research efforts focus mainly on the biochemical or electrophysiological activity of the brain.This opinion piece synthesizes expertise in applied mathematics, solid and fluid mechanics, biomechanics, experimentation, material sciences, neuropathology, and neurosurgery to address today's open questions at the forefront of neuromechanics.The multi-disciplinary analysis of these various phenomena and pathologies presents new opportunities and suggests that mechanical modeling is a central tool to bridge the scales by synthesizing information from the molecular via the cellular and tissue all the way to the organ level.

View Article: PubMed Central - PubMed

Affiliation: Mathematical Institute, University of Oxford, Oxford, OX2 6GG, UK, Alain.Goriely@maths.ox.ac.uk.

ABSTRACT
The human brain is the continuous subject of extensive investigation aimed at understanding its behavior and function. Despite a clear evidence that mechanical factors play an important role in regulating brain activity, current research efforts focus mainly on the biochemical or electrophysiological activity of the brain. Here, we show that classical mechanical concepts including deformations, stretch, strain, strain rate, pressure, and stress play a crucial role in modulating both brain form and brain function. This opinion piece synthesizes expertise in applied mathematics, solid and fluid mechanics, biomechanics, experimentation, material sciences, neuropathology, and neurosurgery to address today's open questions at the forefront of neuromechanics. We critically review the current literature and discuss challenges related to neurodevelopment, cerebral edema, lissencephaly, polymicrogyria, hydrocephaly, craniectomy, spinal cord injury, tumor growth, traumatic brain injury, and shaken baby syndrome. The multi-disciplinary analysis of these various phenomena and pathologies presents new opportunities and suggests that mechanical modeling is a central tool to bridge the scales by synthesizing information from the molecular via the cellular and tissue all the way to the organ level.

No MeSH data available.


Related in: MedlinePlus