Adaptation-dependent plasticity of rod bipolar cell axon terminal morphology in the rat retina

Abstract

We chose synaptic terminals of rat rod bipolar cells as a model system to study activity-related changes in the overall morphology and the fine structure of synaptic sites. Using confocal laser scanning microscopy in conjunction with three-dimensional reconstruction and electron microscopy, we examined the effect of light and dark adaptation on axon terminals identified by protein kinase C (PKC) immunoreactivity. Rod bipolar cell axon terminals consisted of 2-3 polymorphic boutons situated close to the ganglion cell layer and a single ovoid swelling located more distally. Both components of the terminal complex showed adaptation-dependent differences in the distribution of PKC immunoreactivity and in their morphology. In light-adapted rod bipolar cell axon terminals, PKC immunoreactivity was homogeneously distributed throughout the cytoplasm, whereas terminals from dark-adapted animals showed PKC immunoreactivity preferentially localised in the submembrane compartment and a reduced staining of the more central cytoplasm. In three-dimensional reconstructions of optical sections and at the ultrastructural level, the shape of light-adapted axon terminals was round and smooth and exhibited more convexly curved synaptic membranes. In contrast, dark-adapted terminals had irregular contours, numerous dimples and a concave synaptic curvature. No spinules of bipolar cell terminals were observed in dark-adapted material. These observations are discussed in the context of activity-related morphological plasticity of central nervous system synapses and of the functions of PKC in the cycle of vesicle fusion and retrieval at the tonically active ribbon synapses of the rod bipolar axon terminal.