Abstract
Here we examine the structure of the various types of spine synapses throughout the animal kingdom. Based on available evidence, we suggest that there are two major categories of spine synapses: invaginating and non-invaginating, with distributions that vary among different groups of animals. In the simplest living animals with definitive nerve cells and synapses, the cnidarians and ctenophores, most chemical synapses do not form spine synapses. But some cnidarians have invaginating spine synapses, especially in photoreceptor terminals of motile cnidarians with highly complex visual organs, and also in some mainly sessile cnidarians with rapid prey capture reflexes. This association of invaginating spine synapses with complex sensory inputs is retained in the evolution of higher animals in photoreceptor terminals and some mechanoreceptor synapses. In contrast to invaginating spine synapse, non-invaginating spine synapses have been described only in animals with bilateral symmetry, heads and brains, associated with greater complexity in neural connections. This is apparent already in the simplest bilaterians, the flatworms, which can have well-developed non-invaginating spine synapses in some cases. Non-invaginating spine synapses diversify in higher animal groups. We also discuss the functional advantages of having synapses on spines and more specifically, on invaginating spines. And finally we discuss pathologies associated with spine synapses, concentrating on those systems and diseases where invaginating spine synapses are involved.
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The micrograph in a2 is figure 3B from Gray et al. (2009; Biol. Bull. 217:35–49), reprinted with permission from the Marine Biological Laboratory, Woods Hole, MA (and from Dr. R.A. Satterlie); that in d2 is a reprint of Figure 11 from Holmberg (1970), with permission from Springer Publishing Company (Color figure online)
The micrograph in a2 is a reprint of Figure 2D from Budelmann and Thies (1977) with permission from Springer Publishing Company (Color figure online)
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Acknowledgments
This work was supported by the Intramural Research Programs of NIDCD/NIH and NIA/NIH. The code for the Advanced Imaging Core of NIDCD is ZIC DC000081-03. We thank Megan Wyeth for helpful discussion about hippocampal CA3 mossy terminal synapse function and inhibitory interneurons.
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Petralia, R.S., Wang, YX., Mattson, M.P. et al. The Diversity of Spine Synapses in Animals. Neuromol Med 18, 497–539 (2016). https://doi.org/10.1007/s12017-016-8405-y
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DOI: https://doi.org/10.1007/s12017-016-8405-y