Structure, Distribution, and Function of Neuronal/Synaptic Spinules and Related Invaginating Projections

Abstract

Neurons and especially their synapses often project long thin processes that can invaginate neighboring neuronal or glial cells. These “invaginating projections” can occur in almost any combination of postsynaptic, presynaptic, and glial processes. Invaginating projections provide a precise mechanism for one neuron to communicate or exchange material exclusively at a highly localized site on another neuron, e.g., to regulate synaptic plasticity. The best-known types are postsynaptic projections called “spinules” that invaginate into presynaptic terminals. Spinules seem to be most prevalent at large very active synapses. Here, we present a comprehensive review of all kinds of invaginating projections associated with both neurons in general and more specifically with synapses; we describe them in all animals including simple, basal metazoans. These structures may have evolved into more elaborate structures in some higher animal groups exhibiting greater synaptic plasticity. In addition to classic spinules and filopodial invaginations, we describe a variety of lesser-known structures such as amphid microvilli, spinules in giant mossy terminals and en marron/brush synapses, the highly specialized fish retinal spinules, the trophospongium, capitate projections, and fly gnarls, as well as examples in which the entire presynaptic or postsynaptic process is invaginated. These various invaginating projections have evolved to modify the function of a particular synapse, or to channel an effect to one specific synapse or neuron, without affecting those nearby. We discuss how they function in membrane recycling, nourishment, and cell signaling and explore how they might change in aging and disease.

Fine Structure of the Neuroganglia in the Central Nervous System of the Harvestman Leiobunum japonicum (Arachnida: Opiliones)

“…These results strengthen the premise that euchromatin is lightly packed in the form of DNA, RNA, and protein, and is usually under active transcription of DNA to mRNA products (Fortuny & Polo, 2017;Taneja et al, 2017). Because euchromatin is rich in gene concentration, and substantial part of the genome is continually being transcribed in keeping with the active synthetic state of cell (Petralia et al, 2015), the nuclear chromatin is generally dispersed when seen with the electron microscope and the nucleus usually has a vesicular appearance when viewed with the light microscope. As seen in EM, the ribosomal material is mainly in the form of multiple stacks of rER, free ribosomes and attached ribosomes.…”

The Diversity of Spine Synapses in Animals

“…In the micrograph shown in the paper (Fig. 28 in Pavans de Ceccatty 1966; see also illustrations in Petralia et al 2015), a few of these filaments appear to extend up into the spine-like structure, which also contains some irregular vesiculate organelles. The cytoplasm of the opposing cell (a scleroblast) contains a variety of vesicles and vesiculate organelles near the invaginating spine-like structure, with at least one small vesicle appearing to contact the opposing membrane (i.e., that is across the “cleft”), and a mitochondrion also is adjacent to this contact point.…”

“…Both the bouton-like and spine-like structures invaginate into the sides of other cells (Pavans de Ceccatty 1966). Invaginating projections are common in the nervous system of most kinds of animals, including many kinds that are directly associated with synapses, but in most cases, they are not definitive synaptic spines, simply because they do not form a direct chemical synapse with a presynaptic process; and except for this one example in sponges, they will not be described in this review (we have reviewed these structures in detail previously; Petralia et al 2015). While many of these invaginating projections are rather small structures, in some cases, the entire synaptic spine can be an invaginating projection into the presynaptic terminal.…”

“…We cannot rule out that such spine-like structures have only a mechanical function in sponges, but if they do represent some kind of early evolved synaptic spine precursor, it is curious that the first ones would be invaginating structures. Invaginating projections may have a number of different functions, not directly related to definitive chemical neurotransmission (Petralia et al 2015). Notably they form an efficient means to isolate the transfer of a chemical signal from one cell to another, i.e., there is less chance of spillover of the chemical messenger if it is confined to an invagination.…”

“…Takasaka and Smith (1971) note that afferent processes “occasionally make small invaginations” into the hair cells of the adult pigeon, although they do not illustrate this phenomenon; however, they do show partial invagination of a presynaptic efferent terminal into a hair cell. Images in Hamilton (1968) show invaginating postsynaptic processes in some vestibular hair cells of the adult rat, but it is not clear whether these are really involved directly in a synaptic connection (Petralia et al 2015). The formation of invaginating spines in the hair cell synapses of the mouse ear in early postnatal development, as described above (Sobkowicz et al 2003) is paralleled by a similar formation of invaginating spine synapses in the next synapse in the hearing neural pathway.…”