In vivo, homozygous staggerer (Rorasg/sg) Purkinje cells (PCs) remain in an early stage of development with rudimentary spineless dendrites, associated with a lack of parallel fiber (PF) input and the persistence of multiple climbing fibers (CFs). In this immunocytochemical study we used cerebellar organotypic cultures to monitor the development of Rorasg/sg PF‐PC synapses in the absence of CF innervation. Ex vivo the vesicular glutamate transporters VGluT1 and VGluT2 reactivity was preferentially localized around the Rorasg/sg PC soma and proximal dendrites, which are typically CF domains. The shift from VGluT2 to VGluT1 in PF terminals during development was delayed in Rorasg/sg slices. The postsynaptic receptors mGluR1 and GluRδ2 were differently distributed on Rorasg/sg PCs. mGluR1 reactivity was evenly distributed in PC soma and dendrites, whereas GluRδ2 reactivity, normally restricted at PF synapses, was dense in Rorasg/sg PC somata. The presynaptic distribution of VGluT1 and VGluT2 on Rorasg/sg PCs matched the postsynaptic distribution of the glutamate receptor GluRδ2, but not mGluR1. J. Comp. Neurol. 512:467–477, 2009. © 2008 Wiley‐Liss, Inc.