Dendritic spines on GABAergic neurons respond to cholinergic signaling in the Caenorhabditis elegans motor circuit.

Abstract

Dendritic spines are specialized postsynaptic structures that detect and integrate presynaptic signals. The shape and number of dendritic spines are regulated by neural activity and correlated with learning and memory. Most studies of spine function have focused on the mammalian nervous system. However, spine-like protrusions have been previously reported in invertebrates, suggesting that the experimental advantages of smaller model organisms could be exploited to study the biology of dendritic spines. Here, we document the presence of dendritic spines in Caenorhabditis elegans motor neurons. We used super-resolution microscopy, electron microscopy, live-cell imaging and genetic manipulation to show that GABAergic motor neurons display functional dendritic spines. Our analysis revealed salient features of dendritic spines: (1) A key role for the actin cytoskeleton in spine morphogenesis; (2) Postsynaptic receptor complexes at the tips of spines in close proximity to presynaptic active zones; (3) Localized postsynaptic calcium transients evoked by presynaptic activity; (4) The presence of endoplasmic reticulum and ribosomes; (5) The regulation of spine density by presynaptic activity. These studies provide a solid foundation for a new experimental paradigm that exploits the power of C. elegans genetics and live-cell imaging for fundamental studies of dendritic spine morphogenesis and function.\n\nHIGHLIGHTS- Spines in C. elegans GABAergic motor neurons are enriched in actin cytoskeleton.\n- Spines are dynamic structures.\n- Spines display Ca++ transients coupled with presynaptic activation.\n- Spine density is regulated during development and is modulated by actin dynamics and cholinergic signaling.