In this study, we examined the stiffness of pallia among amniotes: mice, turtles, songbirds, chicks, and ferrets. To understand the role of stiffness in organizing diverse brain structures, a comparative analysis of stiffness in several animal brains is required. However, it remains unclear how stiffness controls cellular behavior to form species-specific brain structures. Indeed, 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). Migrating neurons respond not only to biochemical signals but also to mechanical cues from distinct extracellular environments on the way to their destinations ( Park et al., 2002 Huang, 2009 Honda et al., 2011 Long and Huttner, 2019). In the mammalian telencephalon, 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 mammalian neocortex (NCx) is originated in the most dorsal part of embryonic telencephalon ( Puelles, 2013 Nieuwenhuys, 2017). During brain formation, newly generated neurons in the proliferative region migrate to their final destinations. For instance, the mammalian brain has a six-layered structure, while the avian brains consist of compartmentalized nuclear slabs. 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.Īlthough 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 Puelles et al., 2017 Cárdenas and Borrell, 2019 Pessoa et al., 2019). 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. We found stage-dependent and species-specific stiffness in pallia among amniotes. We also measured brain stiffness in other amniotes (chick, turtle, and ferret) following glyoxal fixation. Based on this method, we found that the homologous brain regions between mice and songbirds exhibited different stiffness patterns. 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. 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. 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. To address this point, a comparative analysis of mechanical properties using several animals is required. However, little is known about the correlation between mechanical properties and species-specific brain structures. Recent studies have indicated that differences in the mechanical properties of tissue may result in the dynamic deformation of brain structure, such as folding. 3RIKEN Center for Biosystems Dynamics Research, Kobe, Japanīrain structures are diverse among species despite the essential molecular machinery of neurogenesis being common.2Developmental Neurobiology, Kyoto Prefectural University of Medicine, Kyoto, Japan.1Korea Brain Research Institute, Daegu, South Korea.Misato Iwashita 1*, Tadashi Nomura 2, Taeko Suetsugu 3, Fumio Matsuzaki 3, Satoshi Kojima 1 and Yoichi Kosodo 1*
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