Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans

Abstract

Following prolonged exposure to an odorant, C. elegans exhibits a diminished response to the odorant for several hours. This olfactory adaptation is odorant selective; animals can adapt independently to different odorants sensed by a single pair of olfactory neurons, the AWC neurons. The mechanism of olfactory adaptation is genetically complex, with different genes required for adaptation to different odorants. Animals mutant for the gene adp-1 fail to adapt to a subset of AWC-sensed odorants; adp-1 affects a calcium-dependent process required for adaptation. Mutations in another gene, osm-9, affect adaptation to a different but overlapping subset of AWC-sensed odorants. Mutations in adp-1 and osm-9 do not diminish the ability of unadapted animals to respond to odorants, indicating that odorant sensation and odorant adaptation are distinct processes.

Generation and modulation of chemosensory behaviors in C. elegans

“…In the background of a high constant concentration of one chemical, animals fail to respond to a point source of that chemical, but continue to respond to other chemicals sensed by that neuron type [71]. Similarly, prolonged exposure to one odorant decreases the response to that odorant while sparing responses to other chemicals sensed by that neuron [142,[145][146][147]. These observations indicate that the chemosensory system is able to discriminate among chemicals sensed by one neuron type.…”

“…As mentioned above, prolonged exposure to high concentrations of a chemical results in worms failing to respond to a point source of the chemical. Adaptation appears to be biphasic with an early, rapid stage, and a later prolonged stage [145,146]. Chemosensory responses are restored upon removal from the adapting chemical, with the time period of exposure correlating with the time required for recovery [146].…”

“…Adaptation appears to be biphasic with an early, rapid stage, and a later prolonged stage [145,146]. Chemosensory responses are restored upon removal from the adapting chemical, with the time period of exposure correlating with the time required for recovery [146]. Early steps in adaptation may be mediated via modulation of activity of signaling components such as receptors, channels, and other signaling molecules via posttranslational mechanisms, resulting in cue-specific changes in sensory neuron responses [115,145,153,154] (Fig.…”

“…a Molecules acting in the AWC neurons to modulate AWC neuron plasticity are shown in red. ARR-1 encodes an arrestin possibly playing a role in receptor desensitization [154]; overexpression of the ODR-1 receptor guanylyl cyclase alters adaptation to a subset of AWC-sensed odorants [142]; the TBX-2 transcription factor acts cytoplasmically to regulate olfactory adaptation via as yet unknown mechanisms [156]; the EGL-4 cGMP-dependent protein kinase phosphorylates the TAX-2 channel, and also translocates to the nucleus to regulate early and late steps in olfactory adaptation, respectively [145]; Ca 2+ entry through the OSM-9 TRPV channel is required for olfactory adaptation to a subset of AWC-sensed chemicals [146]; the TAX-6 Ca 2+ -dependent calcineurin phosphatase negatively regulates adaptation [155]. b Simplified summary of intercellular mechanisms proposed to mediate chemosensory behavioral plasticity.…”

Insulin-like signaling pathway functions in integrative response to an olfactory and a gustatory stimuli in Caenorhabditis elegans

“…Components of the insulin-like signaling pathway are required for sensory integration learning in C. elegans Several learning paradigms in C. elegans, such as salt chemotaxis learning (Saeki et al, 2001;Tomioka et al, 2006), olfactory adaptation (Colbert and Bargmann, 1995), and temperature learning (Mohri et al, 2005) have been utilized to investigate associative learning and memory. The components of the insulin-like signaling pathway in C. elegans are highly conserved with those in mammals, the mammalian orthologs in C. elegans including DAF-2, a homolog of the insulin receptor; AGE-1, a PI 3-kinase homolog; DAF-18, a PTEN (phosphatase and tensin homolog deleted on chromosome 10) lipid phosphatase homolog; PDK-1, AKT-1/2 and SGK-1, homologs of phosphoinositide-dependent protein kinases; and DAF-16, a FOXO family transcription factor (Fig.…”