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Comparative Analysis of Brain Stiffness Among Amniotes Using Glyoxal Fixation and Atomic Force Microscopy.

ABSTRACT: Brain structures are diverse among species despite the essential molecular machinery of neurogenesis being common. Recent studies have indicated that differences in the mechanical properties of tissue may result in the dynamic deformation of brain structure, such as folding. However, little is known about the correlation between mechanical properties and species-specific brain structures. To address this point, a comparative analysis of mechanical properties using several animals is required. For a systematic measurement of the brain stiffness of remotely maintained animals, we developed a novel strategy of tissue-stiffness measurement using glyoxal as a fixative combined with atomic force microscopy. A comparison of embryonic and juvenile mouse and songbird brain tissue revealed that glyoxal fixation can maintain brain structure as well as paraformaldehyde (PFA) fixation. Notably, brain tissue fixed by glyoxal remained much softer than PFA-fixed brains, and it can maintain the relative stiffness profiles of various brain regions. Based on this method, we found that the homologous brain regions between mice and songbirds exhibited different stiffness patterns. We also measured brain stiffness in other amniotes (chick, turtle, and ferret) following glyoxal fixation. We found stage-dependent and species-specific stiffness in pallia among amniotes. The embryonic chick and matured turtle pallia showed gradually increasing stiffness along the apico-basal tissue axis, the lowest region at the most apical region, while the ferret pallium exhibited a catenary pattern, that is, higher in the ventricular zone, the inner subventricular zone, and the cortical plate and the lowest in the outer subventricular zone. These results indicate that species-specific microenvironments with distinct mechanical properties emerging during development might contribute to the formation of brain structures with unique morphology.

SUBMITTER: Iwashita M

PROVIDER: S-EPMC7517470 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Comparative Analysis of Brain Stiffness Among Amniotes Using Glyoxal Fixation and Atomic Force Microscopy.

Iwashita Misato M Nomura Tadashi T Suetsugu Taeko T Matsuzaki Fumio F Kojima Satoshi S Kosodo Yoichi Y

Frontiers in cell and developmental biology 20200911

Brain structures are diverse among species despite the essential molecular machinery of neurogenesis being common. Recent studies have indicated that differences in the mechanical properties of tissue may result in the dynamic deformation of brain structure, such as folding. However, little is known about the correlation between mechanical properties and species-specific brain structures. To address this point, a comparative analysis of mechanical properties using several animals is required. Fo ...[more]

PMID: 33043008

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Project description:We present a magnetic force-based direct drive modulation method to measure local nano-rheological properties of soft materials across a broad frequency range (10 Hz to 2 kHz) using colloid-attached atomic force microscope (AFM) probes in liquid. The direct drive method enables artefact-free measurements over several decades of excitation frequency, and avoids the need to evaluate medium-induced hydrodynamic drag effects. The method was applied to measure the local mechanical properties of polyacrylamide hydrogels. The frequency-dependent storage stiffness, loss stiffness, and loss tangent (tan??) were quantified for hydrogels having high and low crosslinking densities by measuring the amplitude and the phase response of the cantilever while the colloid was in contact with the hydrogel. The frequency bandwidth was further expanded to lower effective frequencies (0.1 Hz to 10 Hz) by obtaining force-displacement (FD) curves. Slow FD measurements showed a recoverable but highly hysteretic response, with the contact mechanical behaviour dependent on the loading direction: approach curves showed Hertzian behaviour while retraction curves fit the JKR contact mechanics model well into the adhesive regime, after which multiple detachment instabilities occurred. Using small amplitude dynamic modulation to explore faster rates, the load dependence of the storage stiffness transitioned from Hertzian to a dynamic punch-type (constant contact area) model, indicating significant influence of material dissipation coupled with adhesion. Using the appropriate contact model across the full frequency range measured, the storage moduli were found to remain nearly constant until an increase began near ?100 Hz. The softer gels' storage modulus increased from 7.9 ± 0.4 to 14.5 ± 2.1 kPa (?85%), and the stiffer gels' storage modulus increased from 16.3 ± 1.1 to 31.7 ± 5.0 kPa (?95%). This increase at high frequencies may be attributed to a contribution from solvent confinement in the hydrogel (poroelasticity). The storage moduli measured by both macro-rheometry and AFM FD curves were comparable to those measured using the modulation method at their overlapping frequencies (10-25 Hz). In all cases, care was taken to ensure the contact mechanics models were applied within the important limit of small relative deformations. This study thus highlights possible transitions in the probe-material contact mechanical behaviour for soft matter, especially when the applied strain rates and the material relaxation rates become comparable. In particular, at low frequencies, the modulus follows Hertzian contact mechanics, while at high frequencies adhesive contact is well represented by punch-like behaviour. More generally, use of the Hertz model on hydrogels at high loading rates, at high strains, or during the retraction portion of FD curves, leads to significant errors in the calculated moduli.

Dataset Information

Comparative Analysis of Brain Stiffness Among Amniotes Using Glyoxal Fixation and Atomic Force Microscopy.

Publications

Comparative Analysis of Brain Stiffness Among Amniotes Using Glyoxal Fixation and Atomic Force Microscopy.

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