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. 2018 Apr 5;10:4. doi: 10.3389/fnsyn.2018.00004

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Copyright © 2018 Petralia, Wang, Mattson and Yao.

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

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Examples of specialized invaginating structures. (A) A drawing of an unusual example of a category 1 invaginating structure: a presynaptic terminal invaginates into the postsynaptic soma. The synapse has characteristics of inhibitory terminals with a less prominent PSD (arrowheads) and oval-shaped synaptic vesicles. The GABA receptors are on the postsynaptic membrane, lining the PSD (arrowheads) and ringing the invagination, and there are endocannabinoid synthetic enzymes on the postsynaptic side of the invagination (shown in yellow). Endocannabinoid release activates cannabinoid receptors in the presynaptic membrane, and these then mediate retrograde suppression of neurotransmitter release from the terminal. (B) A drawing of a specialized example of a category 3 invaginating structure: a generalized mammalian neuromuscular junction (NMJ). In this example, the presynaptic terminal is only partly invaginated (indented) into the muscle fiber. The indention is lined with deep subjunctional folds in the postsynaptic membrane. A thin basal lamina (gray) extends within the synaptic cleft and into the folds. (C) EM micrographs show examples of invaginating structures combining categories 1 and 2. These are from the CA3 MFT region, as described in Figure 1C. Thorny excrescences (category 2) also commonly invaginate spinules (s; category 1) into the MFTs, especially apparent in the upper three micrographs. Note in the left, lower micrograph how thin portions of the MFT shown between the two green arrows surround part of the invaginated thorny excrescence. A tiny spinule is barely visible near the top green arrow. Note also how this MFT isolates the thorny excrescence surface from possible spillover from an adjacent inhibitory terminal (i); the latter is identified by the elongate symmetrical density as well as by some obscure pleomorphic synaptic vesicles (compare to the more distinctive and rounder excitatory synaptic vesicles in the MFTs). Common organelles in the thorny excrescences include the spine apparatus (sa) and multivesicular body (mv). (D) A drawing of a specialized invaginating structure combining categories 2 and 3. A photoreceptor terminal-synaptic ribbon (r) contacts a deep invagination containing postsynaptic processes (category 2) from horizontal (h) and bipolar (b) neurons, as well as projections from the terminal. Rod terminals in mammals usually have a single invaginated ribbon/active zone with two horizontal and two bipolar cell processes, as well as “fingers” of rod cytoplasm, while cone terminals have multiple invaginated ribbon/active zones, each with two horizontal and 1–2 bipolar cell processes (Rao-Mirotznik et al., 1995; Sterling and Demb, 2004; Petralia et al., 2017). The horizontal cell processes also may act as invaginating presynaptic terminals (category 3) since they send a retrograde signal to the photoreceptor terminal, mediating a feedback mechanism.