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.
Highlights
The vast majority of molecular machinery to generate neurons from progenitors are commonly conserved in amniotes (Englund et al, 2005; Martínez-Cerdeño et al, 2016; Nomura et al, 2016; Turrero García et al, 2016; Yamashita et al, 2018), the alignment of neurons in matured brains exhibits remarkable diversity
Most glutamatergic projection neurons are born in the dorsal proliferative region and migrate into the cortical plate (CP) radially (Nadarajah and Parnavelas, 2002; Noctor et al, 2004; Tabata et al, 2009), whereas GABAergic interneurons are born in the ventral proliferative region and migrate into the CP tangentially, resulting in a highly organized six-layered structure (Anderson et al, 1997; Batista-Brito and Fishell, 2009)
The measurements were carried out using atomic force microscopy (AFM) (Bioscope Resolve, NanoScope 9.4, Bruker), which was mounted on an inverted microscope (Nikon, ECLIPSE Ti2)
Summary
The vast majority of molecular machinery to generate neurons from progenitors are commonly conserved in amniotes (Englund et al, 2005; Martínez-Cerdeño et al, 2016; Nomura et al, 2016; Turrero García et al, 2016; Yamashita et al, 2018), the alignment of neurons in matured brains exhibits remarkable diversity (Medina and Abellán, 2009; Jarvis et al, 2013; Comparative Analysis of Brain StiffnessPuelles et al, 2017; Cárdenas and Borrell, 2019; Pessoa et al, 2019). Intensive research using atomic force microscopy (AFM) has revealed the spatiotemporal diversity and crucial roles of the mechanical properties of the extracellular environment, especially stiffness, in the developing central nervous system (Elkin et al, 2007, 2010; Christ et al, 2010; Iwashita et al, 2014; Nagasaka et al, 2016; Thompson et al, 2019; Kjell et al, 2020). It remains unclear how stiffness controls cellular behavior to form species-specific brain structures
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