Quantitative classification of cerebellar foliation in cartilaginous fishes (Class: Chondrichthyes) using 3D shape analysis and its implications for evolutionary biology

摘要

A true cerebellum appeared at the onset of the chondrichthyan radiation and is known to be essential for executing fast, accurate, and efficient movement. In addition to a high degree of variation in size, the corpus cerebellum in this group has a high degree of variation in convolution (or foliation) and symmetry, which ranges from a smooth cerebellar surface to deep, branched convexities and folds, although the functional significance of this trait is unclear. As variation in the degree of foliation similarly exists throughout vertebrate evolution, it becomes critical to understand this evolutionary process in a wide variety of species. However, current methods are either qualitative and lack numerical rigor or are restricted to two dimensions. In this paper, a recently developed method for the characterization of shapes embedded within noisy, three-dimensional (3D) data called the spherical wave decomposition (SWD) is applied to the problem of characterizing cerebellar foliation in cartilaginous fishes. The SWD method provides a quantitative characterization of shapes in terms of well-defined mathematical functions. An additional feature of the SWD method is the construction of a statistical criterion for the optimal fit, which represents the most parsimonious choice of parameters that fits to the data, without overfitting to background noise. We propose that this optimal fit can replace a previously described qualitative visual foliation index (VFI) in cartilaginous fishes with a quantitative analogue, the cerebellar foliation index (CFI). The capability of the SWD method is demonstrated on a series of volumetric images of brains from different chondrichthyan species that span the range of foliation gradings currently described for this group. The CFI is consistent with the qualitative grading provided by the VFI, delivers a robust measure of cerebellar foliation, and can provide a quantitative basis for brain shape characterization across taxa.