Abstract
Dendritic spines are specialized postsynaptic structures that transduce presynaptic signals, 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 reported in C. elegans (Philbrook et al., 2018), suggesting that the experimental advantages of smaller model organisms could be exploited to study the biology of dendritic spines. Here, we used super-resolution microscopy, electron microscopy, live-cell imaging and genetics to show that C. elegans motor neurons have functional dendritic spines that: (1) are structurally defined by a dynamic actin cytoskeleton; (2) appose presynaptic dense projections; (3) localize ER and ribosomes; (4) display calcium transients triggered by presynaptic activity and propagated by internal Ca++ stores; (5) respond to activity-dependent signals that regulate spine density. 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.
Highlights
The majority of excitatory synapses in the mammalian brain feature short, local protrusions from postsynaptic dendrites that respond to presynaptic neurotransmitter release (Rochefort and Konnerth, 2012)
Spine morphology and density are regulated by neural activity in plastic responses that are strongly correlated with learning and memory (Kozorovitskiy et al, 2005; Moser et al, 1997)
We used Airyscan imaging, a type of super-resolution microscopy (Korobchevskaya et al, 2017), to detect spine-like projections on the ventral processes of adult Dorsal D (DD) neurons labeled with a cytosolic mCherry marker (Figure 1B)
Summary
The majority of excitatory synapses in the mammalian brain feature short, local protrusions from postsynaptic dendrites that respond to presynaptic neurotransmitter release (Rochefort and Konnerth, 2012). These dendritic ‘spines’ were originally described by Ramon y Cajal (Yuste, 2015) and are recognized as key functional components of neural circuits. The anatomy of the C. elegans nervous system was originally defined by reconstruction of electron micrographs (EM) of serial sections This approach revealed that a small subset of neurons displays short, spine-like protrusions. Neuroscience like structures in GABAergic motor neurons (DD and VD) exhibit the salient hallmarks of dendritic spines
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