The relationship between hodological and cytoarchitectonic organization in the vestibular complex of the 11-day chicken embryo

Abstract

To understand the relationship between structure and function in specific brain regions, it is necessary to ascertain which anatomical features are physiologically relevant. Physiological studies of brain function traditionally have been set in the context of anatomical features based on cytoarchitectonics and myeloarchitectonics, but the relationship between structure and function in this context can be complex. Alternative schemes of anatomical organization, such as that based on hodology (the mapping of projections) may provide greater insight. Here, we make a direct comparison of the hodological and the cytoarchitectonic organization of the vestibular complex in the mid-term chicken embryo, using retrograde tracing and three-dimensional reconstruction. In one set of experiments, vestibulospinal and vestibulo-ocular neuron groups were selectively labeled with biotin dextran-amines and aligned with the cytoarchitectonically defined vestibular nuclei in alternating sections that were then combined into intercalated three-dimensional models. This allowed a semiquantitative analysis of the apportionment of individual hodological groups among cytoarchitectonic nuclei. In another set of experiments, vestibulospinal and vestibulo-ocular neuron groups were labeled differentially with fluorescent dextran-amines, three-dimensionally reconstructed, and subjected to a quantitative analysis of spatial overlap. Our results provide the first three-dimensional representation and quantitative analysis of the hodological compartmentalization of the vestibular complex (the "hodological mosaic"). They also show directly how each hodologically defined neuron group relates to the conventional vestibular nuclei, underscoring the fact that the units of the hodological mosaic do not bear a one-to-one correspondence to the cytoarchitectonic nuclear divisions. Some hodologically defined groups are localized to restricted portions of a nucleus, whereas others overlap multiple nuclei. Thus, hodology and cytoarchitectonic features appear to be separately regulated in the vestibular complex of the chicken embryo, possibly through different sets of positional specification mechanisms. The three-dimensional representations we present here provide a foundation for integrating anatomical, physiological, developmental, and evolutionary studies of the vestibular system.