Abstract
Sensing changes in the environment is crucial for survival. Animals from invertebrates to vertebrates use both visual and olfactory stimuli to direct survival behaviors including identification of food sources, finding mates, and predator avoidance. In primary sensory neurons there are signal transduction mechanisms that convert chemical or light signals into an electrical response through ligand binding or photoactivation of a receptor, that can be propagated to the olfactory and visual centers of the brain to create a perception of the odor and visual landscapes surrounding us. The fundamental principles of olfactory and phototransduction pathways within vertebrates are somewhat analogous. Signal transduction in both systems takes place in the ciliary sub-compartments of the sensory cells and relies upon the activation of G protein-coupled receptors (GPCRs) to close cyclic nucleotide-gated (CNG) cation channels in photoreceptors to produce a hyperpolarization of the cell, or in olfactory sensory neurons open CNG channels to produce a depolarization. However, while invertebrate phototransduction also involves GPCRs, invertebrate photoreceptors can be either ciliary and/or microvillar with hyperpolarizing and depolarizing responses to light, respectively. Moreover, olfactory transduction in invertebrates may be a mixture of metabotropic G protein and ionotropic signaling pathways. This review will highlight differences of the visual and olfactory transduction mechanisms between vertebrates and invertebrates, focusing on the implications to the gain of the transduction processes, and how they are modulated to allow detection of small changes in odor concentration and light intensity over a wide range of background stimulus levels.
Highlights
Phototransduction and Olfactory Transduction Adaptation vertebrate olfactory sensory neurons (OSNs) and photoreceptors (PRs) both rely upon G protein signaling cascades, while using distinct classes of G and effector proteins: A G-protein-coupled receptor (GPCR) detects a stimulus and modulates the open probability of cyclic nucleotide-gated (CNG) ion channels via classical G protein-coupled receptors (GPCRs) signaling cascades involving the activation of an effector enzyme (E), adenylyl cyclase (AC) in the OSN and phosphodiesterase (PDE) in photoreceptors
Olfactory signal transduction in invertebrates is not understood in detail, it is often mediated by ligand-gated odor receptor (OR)/co-receptor (Orco) heteromer that may be regulated by metabotropic pathway(s) (Wicher et al, 2008; Nakagawa and Vosshall, 2009; Hansson et al, 2010)
There is some evidence that phosphorylation of the OR in vertebrates by GRK3 may be important for the fast inactivation of the activated receptor, it is not known if any Ca2+ feedback mechanisms exist to regulate the lifetime of the active ORs
Summary
Phototransduction and olfaction have been widely investigated in both invertebrate (Hardie and Raghu, 2001; Touhara and Vosshall, 2009; Yau and Hardie, 2009; Hardie and Juusola, 2015; Honkanen et al, 2017; Fleischer et al, 2018; Schmidt and Benton, 2020) and vertebrate (Schild and Restrepo, 1998; Burns and Baylor, 2001; Fain et al, 2001; Arshavsky et al, 2002; Luo et al, 2008; Kaupp, 2010; Pifferi et al, 2010; Vinberg et al, 2018) species. Mechanisms that accelerate response recovery and/or regulate the sensitivity of the receptor cells to odors/light by modulating the homeostasis of second messengers and the affinity of cyclic nucleotides to CNG channels will be discussed below in the context of adaptation.
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