The Diversity of Spine Synapses in Animals

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.

Invaginating Presynaptic Terminals in Neuromuscular Junctions, Photoreceptor Terminals, and Other Synapses of Animals

“…In sections, the groove appears to be a deep invagination with its outside boundary covered by the basal lamina of the hair cell (Burighel et al 2003; Manni et al 2006). Many of these neurites are definitive postsynaptic afferents, with presynaptic vesicles on the hair cell side of the cleft; we already have illustrated this in Petralia et al 2016, as an example of multiple, postsynaptic processes in an invagination. But the former authors also describe presynaptic efferent terminals within these invaginations, forming synapses with the base of the hair cell, as well as with the neurites that form the afferent synapses.…”

“…The first hint of what could be invaginating synaptic processes in animal evolution is found in a sponge, and we already have discussed this in detail in Petralia et al (2015, 2016). Briefly sponges (Porifera) do not have definitive neurons or chemical synapses, but the sponge, Tethya lyncurium, has some cells with elongate processes that roughly resemble neurons (Pavans de Ceccatty 1966).…”

“…While we have described previously the invaginating postsynaptic processes at vertebrate photoreceptor synapses (Petralia et al 2016), here we will examine these same synapses, but now from the point of view of invaginating presynaptic or efferent processes, i.e., processes within the same invagination, but that mediate neurotransmission retrograde, to the photoreceptor cell terminal. The presynaptic active zone in the base of photoreceptor cells of jawless fish varies in structure, from clusters of presynaptic vesicles lacking any presynaptic dense body, seen in the Atlantic hagfish, Myxine glutinosa, to various round to irregular dense bodies surrounded by clusters of vesicles, seen in the Pacific hagfish, Polistotrema stouti and Eptatretus burgeri , finally to distinctive presynaptic ribbons lined with vesicles in the lamprey, Lampetra fluviatilis; the latter structure remains the standard for most other vertebrates (Holmberg 1970, 1971; Holmberg and Öhman 1976).…”

“…Most of these synapses involve connections between a presynaptic axonal terminal containing synaptic vesicles, some of which concentrate at an active zone where the presynaptic membrane is separated by a synaptic cleft from a specialized patch of postsynaptic membrane. This postsynaptic membrane occurs along the surface of a dendrite (or soma), or the head of a synaptic spine (Shepherd 2004; Petralia et al 2016). Interestingly, many synapses include invaginating structures that extend into corresponding invaginations in the synaptic partner cell; invaginations are unique synaptic modifications that can isolate or subdivide regions of the synapse to facilitate specialized modulation or signaling functions of the synapse (Petralia et al 2015, 2016).…”

“…Another type of invaginating structure is the postsynaptic spine, which invaginates into the presynaptic terminal (Fig. 1a3; reviewed by Petralia et al 2016). A distinctive feature of these invaginating spines is that they contact one or more synaptic active zones where presynaptic vesicles can release neurotransmitter that binds to receptors on the postsynaptic membrane of the invaginating spine.…”