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Review
. 2020 Nov 5:14:595523.
doi: 10.3389/fncel.2020.595523. eCollection 2020.

A Comparison of the Primary Sensory Neurons Used in Olfaction and Vision

Colten K Lankford  1 , Joseph G Laird  1 , Shivangi M Inamdar  1 , Sheila A Baker  1   2
Affiliations
Review

A Comparison of the Primary Sensory Neurons Used in Olfaction and Vision

Colten K Lankford et al. Front Cell Neurosci. .

Abstract

Vision, hearing, smell, taste, and touch are the tools used to perceive and navigate the world. They enable us to obtain essential resources such as food and highly desired resources such as mates. Thanks to the investments in biomedical research the molecular unpinning's of human sensation are rivaled only by our knowledge of sensation in the laboratory mouse. Humans rely heavily on vision whereas mice use smell as their dominant sense. Both modalities have many features in common, starting with signal detection by highly specialized primary sensory neurons-rod and cone photoreceptors (PR) for vision, and olfactory sensory neurons (OSN) for the smell. In this chapter, we provide an overview of how these two types of primary sensory neurons operate while highlighting the similarities and distinctions.

Keywords: GPCR; olfaction; olfactory sensory neuron; photoreceptor; ribbon synapse; sensory receptors; vision; voltage-gated ion channel.

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Figures

Figure 1
Figure 1
Anatomy of olfactory sensory neurons (OSN) and photoreceptors (PR). (A) OSN are defined by the expression of a unique odorant receptor, OSN expressing the same receptor (red, green, blue, or orange) are dispersed throughout the olfactory epithelium (OE) but the axons of these OSN converge to synapse in the same glomeruli of the olfactory bulb (OB). The major compartments of OSN are the cilia for signal detection which extends from an apical dendritic knob, a bipolar cell body for housekeeping functions and housing the genome, and an axon that traverses the cribriform plate (CP) to synapse in the OB. The cell bodies and dendrites of OSN are surrounded by support cells (brown). Basal cells (gray) are stem cells that generate the immature OSN (pale red, green, blue, or orange). (B) PR consist of rods for dim light vision (gray) and cones for bright light and color vision (red, green and blue). The major compartments of PRs are organized into four layers—outer segments (OS) for signal detection, inner segments (IS) for housekeeping functions, the nucleus in the outer nuclear layer (ONL) for housing the genome, and the synaptic terminal in the outer plexiform layer (OPL). PR are supported by retinal pigment epithelial (RPE) cells (black) and by Muller Glia (brown).
Figure 2
Figure 2
Odorant transduction. (Top) In the absence of odorant, odorant receptors (OR; pink), are associated with the GDP bound heterotrimeric Gαolf (orange, mauve). Adenylate cyclase 3 (AC3; blue) is inactive. cyclic nucleotide gated (CNG; green) and transmembrane protein 16B (TMEM16B; dark green) channels are closed. (Middle) Activation of the cascade begins when odorant binding to an OR activates Gαolf and the GTP bound alpha subunit dissociates to activate AC3. The increase in cyclic adenosine monophosphate (cAMP) concentration opens CNG channels and the resulting influx of calcium opens TMEM16B channels. The cascade is inactivated when Ca2+-calmodulin (CaM; brown) directly inhibits CNG channels and indirectly inhibits AC3 via calmodulin-dependent kinase II (CamKII; light brown) phosphorylation. AC3 is further inhibited by regulator of G-protein signaling 2 (RGS2; reddish-brown). The OR is phosphorylated by protein kinase A (PKA) and GPCR kinase (GRK; light gray) allowing arrestin (gray) binding which inactivates the receptor.
Figure 3
Figure 3
Phototransduction. (Top) In the absence of light, inactive, 11-cis retinal bound, rhodopsin (pink) is associated with the GDP bound heterotrimeric GαT (orange, mauve). Phosphodiesterase 6 (PDE6; blue) is basally autoinhibited. Guanylate cyclase (not shown) generates cyclic guanosine monophosphate (cGMP) that keeps CNG channels (green) open. (Middle) Activation of the cascade begins when photon absorption isomerizes 11-cis-retinal to the all-trans conformation. The activated rhodopsin activates GαT; the GTP bound alpha subunit dissociates to bind PDEγ thus removing the autoinhibition of PDE6. The decrease in cGMP concentration closes CNG channels. (Bottom) The cascade is inactivated when the GTPase Activating Complex consisting of R9AP (brown), Gβ5 (light brown), and RGS9 (reddish-brown) activates GTP hydrolysis on GαT. Rhodopsin is phosphorylated by GRK (light gray) allowing arrestin (gray) binding which inactivates the receptor.
Figure 4
Figure 4
Conventional vs. Ribbon synapses. (Top) OSN make conventional flat synapses with the dendrites of mitral and tufted cells in the OB. The arrival of an action potential depolarizes the membrane. This triggers the opening of Cav2.1 channels and the resulting calcium influx triggers the fusion of synaptic vesicles. (Bottom) PR terminals are invaginated with bipolar dendrites and horizontal cell processes forming a triad synapse. In the dark, Cav1.4 channels are open and synaptic vesicles are fusing to release neurotransmitters. Activation of the phototransduction cascade causes graded hyperpolarization of the membrane which causes Cav1.4 channels to close and synaptic vesicle fusion to slow.
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