Ultrastructure of a Somatic Spine Mat for Nicotinic Signaling in Neurons

Abstract

Chick ciliary neurons have somatic spines grouped in discrete clumps or mats tightly folded against the soma and enriched in nicotinic receptors containing ␣7 subunits. An embryonic ciliary neuron has one to two dozen such spine mats, all overlaid by a large presynaptic calyx engulfing the cell. Three-dimensional tomographic reconstruction from serial thick sections revealed 13 somatic spines in one complete spine mat on a ciliary neuron late in embryogenesis. The spines varied in morphology and usually were branched but had numerous similarities to dendritic spines, including mean length, volume, surface area, presence of endoplasmic reticulum, and occasional multivesicular bodies. The spines invariably were connected to the soma via a narrow neck of ϳ0.2 m in diameter as found for dendritic spines, suggesting restricted access from spine lumen to soma. A prominent difference between dendritic and somatic spines is the absence of postsynaptic densities from most somatic spines both on embryonic and adult ciliary neurons. Transmitter access to receptors on the spines may occur either by lateral diffusion from release sites over nearby postsynaptic densities or by release directly onto spines from the overlying calyx lined with vesicles. The latter is less likely in the adult, where some spines are adjacent to but not overlaid by vesicle-enriched presynaptic structures. The anatomical configuration of spine mats suggests coordinate spine activation by transmitter release into a confined volume while spine morphology is used to control the chemical consequences of synaptic signaling.

The diversity of subunit composition in nAChRs: Evolutionary origins, physiologic and pharmacologic consequences

“…As described previously, the motor autonomic synapse is made up of clusters of ␣3␤4␣5(␤2) receptors located in postsynaptic densities, surrounded by scattered ␣7 receptors (Shoop et al, 1999(Shoop et al, , 2002. The constructions of chimeric ␣7 subunits, carrying the cytoplasmic portion of ␣3, triggered a retargeting of the receptors formed by the chimera to the postsynaptic densities (Williams et al, 1998).…”

Nicotinic α7 receptors: Synaptic options and downstream signaling in neurons

“…This is most clear in the case of chick ciliary neurons where ␣7-nAChRs are largely confined to somatic spines emanating from the neurons and are absent from PSDs (Fig. 1) either on the soma or on the spines (Jacob and Berg, 1983;Loring et al, 1985;Wison Horch and Sargent, 1995;Shoop et al, 1999Shoop et al, , 2002. PSDs on the neurons contain either heteromeric nicotinic receptors composed of ␣3, ␤4, ␣5, and sometimes ␤2 subunits (Jacob et al, 1984;Loring and Zigmond, 1987;Vernallis et al, 1993) or, alternatively, glycine receptors (Tsen et al, 2000).…”

“…Unexpectedly, the presynaptic receptors displayed little desensitization, although ␣7-nAChRs are usually found to have very rapid desensitization (Zorumski et al, 1992;Alkondon and Albuquerque, 1993;Zhang et al, 1994). Possibly the low concentrations of agonist reaching the presynap- (Shoop et al, 2002). The sections were obtained from a neuron in an embryonic day 15 (E15) chick ciliary ganglion.…”

“…The fact that both the spines and PSDs are overlaid by a large vesicle-filled presynaptic calyx engulfing the ciliary neuron suggests that even "perisynaptic" ␣7-nAChRs, i.e. those not in PSDs, are readily exposed to transmitter in this case (Shoop et al, 1999(Shoop et al, , 2002. This expectation is consistent with the large size of the evoked synaptic currents generated by ␣7-nAChRs on the neurons and by the contribution of ␣7-nAChRs to spontaneous miniature synaptic currents as well (Zhang et al, 1996;Ullian et al, 1997;P.…”

“…An attractive hypothesis is that receptor function is regulated by components tethered in the immediate vicinity. The receptors are positioned on somatic spines containing endoplasmic reticulum, which could serve as the calcium source for internal release (Shoop et al, 2001(Shoop et al, , 2002.…”