Abstract
The cerebellum represents one of the most morphologically variable structures in the vertebrate brain. To shed light on its evolutionary history, we have examined the molecular anatomy and proliferation of the developing cerebellum of the North American paddlefish, Polyodon spathula. Absence of an external proliferative cerebellar layer and the restriction of Atonal1 expression to the rhombic lip and valvular primordium demonstrate that transit amplification in a cerebellar external germinal layer, a prominent feature of amniote cerebellum development, is absent in paddlefish. Furthermore, expression of Sonic hedgehog, which drives secondary proliferation in the mouse cerebellum, is absent from the paddlefish cerebellum. These data are consistent with what has been observed in zebrafish and suggest that the transit amplification seen in the amniote cerebellum was either lost very early in the ray-finned fish lineage or evolved in the lobe-finned fish lineage. We also suggest that the Atoh1-positive proliferative valvular primordium may represent a synapomorphy (shared derived character) of ray-finned fishes. The topology of valvular primordium development in paddlefish differs significantly from that of zebrafish and correlates with the adult cerebellar form. The distribution of proliferative granule cell precursors in different vertebrate taxa is thus the likely determining factor in cerebellar morphological diversity.
Highlights
The vertebrate cerebellum is a remarkable neural structure whose synaptic architecture is highly conserved but which varies widely in its size and gross anatomy (Voogd and Glickstein 1998)
To shed light on its evolutionary history, we have examined the molecular anatomy and proliferation of the developing cerebellum of the North American paddlefish, Polyodon spathula
Expression of Sonic hedgehog, which drives secondary proliferation in the mouse cerebellum, is absent from the paddlefish cerebellum. These data are consistent with what has been observed in zebrafish and suggest that the transit amplification seen in the amniote cerebellum was either lost very early in the ray‐finned fish lineage or evolved in the lobe‐finned fish lineage
Summary
The vertebrate cerebellum is a remarkable neural structure whose synaptic architecture is highly conserved but which varies widely in its size and gross anatomy (Voogd and Glickstein 1998). Despite the similarities in cerebellar circuit organization across vertebrates, it plays a variety of functional roles, acting principally as a coordinating centre for proprioception in anamniotes (Sherrington 1906; Wingate 2005) and having a well described function in mammalian motor learning and coordination (Manto 2008). The cerebellum plays a significant role in primate cognition (Schmahmann 2010; Basson and Wingate 2013), and it is possible that not all cerebellar functions have as yet been described. Increasing evidence that cerebellar granule cell development, in particular, involves different migratory and proliferative strategies in different taxa (Butts et al 2011) points to a correlation between mode of granule cell development and cerebellar morphology
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