Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons

Chalasani, Sreekanth H.; Kato, Saul; Albrecht, Dirk; Nakagawa, Takao; Abbott, L. F.; Bargmann, Cornelia I.

doi:10.1038/nn.2526

Cited by 232 publications

(286 citation statements)

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“…Indeed, all the genes discussed in our model are known to be expressed in and required within or act on, in the case of ins-1, the AWC to mediate olfactory adaptation (Colbert et al, 1997;L'Etoile et al, 2002;Palmitessa et al, 2005;Chalasani et al, 2010;Lin et al, 2010), lending support to the remarkable notion that the majority of processing occurs within the primary olfactory neuron. Indeed, this appears to be a common theme in a number of paradigms in C. elegans.…”

Section: Discussionsupporting

confidence: 61%

“…starvation associative learning leads to a modulation of the temperature at which the temperature-sensing AFD primary sensory neurons (Kimura et al, 2004) and AWC neurons fire calcium transients (Biron et al, 2008;Kuhara et al, 2008). Similarly, Chalasani et al (2010) have argued that in ins-1 mutants, AWC firing behavior after training is distinct from that seen in wild-type animals. Together, these findings suggests that information processing that is highly distributed over various substrates in more complex organisms is, in C. elegans, condensed to the level of the sensory neuron, which itself performs large amounts of processing, and a few interneurons (de Bono and Maricq, 2005).…”

Section: Discussionmentioning

confidence: 99%

“…A number of genes have been implicated in AWC adaptation, including members of the insulin signaling pathway (Chalasani et al, 2010;Lin et al, 2010), the transient receptor potential type V (TRPV) channel osm-9 (Colbert et al, 1997), the cGMPdependent kinase egl-4 (L' Etoile et al, 2002), the arrestin arr-1 (Palmitessa et al, 2005), and the guanalyl cyclase gcy-28 (Tsuno-zaki et al, 2008). We therefore mimicked the approach of Atkinson-Leadbeater et al (2004), instead analyzing candidate genes to assign them to specific components (acquisition or retrieval) or types (habituation or associative learning) of memory.…”

Section: With Its Feeding State (Us)mentioning

confidence: 99%

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Two Forms of Learning following Training to a Single Odorant in Caenorhabditis elegans AWC Neurons

Pereira

Kooy²

2012

Journal of Neuroscience

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The nematode Caenorhabditis elegans can adapt to both the AWC-sensed odorants benzaldehyde (Bnz) and isoamyl alcohol (IsoA) and can reciprocally cross-adapt. Yet we reveal that these four adaptation scenarios actually represent two distinct forms of learning: nonassociative habituation and associative learning by pairing with a starvation unconditioned stimulus. Training to the single odorant IsoA leads to both associative and nonassociative memory traces, which can be preferentially accessed by either a Bnz or IsoA retrieval stimulus, respectively. This represents the first demonstration in which the form of learning displayed after training to a single stimulus is a function of the retrieval stimulus used. Furthermore, these two forms of learning can be genetically double dissociated despite both forms occurring within the AWC primary sensory neuron. We find that associative learning requires the cGMP-dependent kinase egl-4 and insulin signaling, which acts downstream of egl-4. In contrast, nonassociative learning requires neither of these genes, but does require the TRPV channel osm-9, which is dispensable for associative learning. In addition, we find that the arrestin arr-1 is promiscuous between associative and nonassociative learning in mediating the adaptive response to the IsoA retrieval stimulus, suggesting that distinct forms of memory may nonetheless use common downstream effectors.

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Section: Discussionsupporting

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Section: With Its Feeding State (Us)mentioning

confidence: 99%

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Two Forms of Learning following Training to a Single Odorant in Caenorhabditis elegans AWC Neurons

Pereira

Kooy²

2012

Journal of Neuroscience

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“…Although the enhancement of 2-nonanone avoidance in C. elegans does not require an external unconditioned stimulus, it could be a primitive form of dopamine-regulated behavioral plasticity caused by an unpleasant experience similar to the examples in flies and rodents. Thus, taking advantage of available tools in C. elegans such as cell-specific RNAi (Esposito et al, 2007) and calcium imaging of the defined small neuronal network (for example, see Kuhara et al, 2008;Chalasani et al, 2010), further analysis of the enhancement of 2-nonanone avoidance may reveal the fundamental mechanism of dopamine signaling in regulating experience-dependent behavioral plasticity in animals.…”

Section: The Enhancement Of 2-nonanone Avoidance Is Regulated By Dopamentioning

confidence: 99%

Enhancement of Odor Avoidance Regulated by Dopamine Signaling inCaenorhabditis elegans

Kimura¹,

Fujita²,

Izui³

2010

J. Neurosci.

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The enhancement of sensory responses after prior exposure to a stimulus is a fundamental mechanism of neural function in animals. Its molecular basis, however, has not been studied in as much depth as the reduction of sensory responses, such as adaptation or habituation. We report here that the avoidance behavior of the nematode Caenorhabditis elegans in response to repellent odors (2-nonanone or 1-octanol) is enhanced rather than reduced after preexposure to the odors. This enhancement effect of preexposure was maintained for at least 1 h after the conditioning. The enhancement of 2-nonanone avoidance was not dependent on the presence or absence of food during conditioning, which generally functions as a strong positive or negative unconditioned stimulus in the animals. These results suggest that the enhancement is acquired as a type of nonassociative learning. In addition, genetic and pharmacological analyses revealed that the enhancement of 2-nonanone avoidance requires dopamine signaling via D 2 -like dopamine receptor DOP-3, which functions in a pair of RIC interneurons to regulate the enhancement. Because dopamine signaling has been tightly linked with food-related information to modulate various behaviors of C. elegans, it may play different role in the regulation of the enhancement of 2-nonanone avoidance. Thus, our data suggest a new genetic and pharmacological paradigm for nonassociative enhancement of neural responses that is regulated by dopamine signaling.

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“…Prolonged exposure to many sensory stimuli results in behavioral adaptation, which can occur either in the primary sensory neuron or in circuitry downstream of the sensory neuron (24)(25)(26)(27)(28). We tested whether CO 2 avoidance behavior adapts to prolonged CO 2 exposure by exposing animals to 1%, 5%, or 10% CO 2 for either 1 or 5 min and then testing their ability to respond to 5% or 10% CO 2 in an acute avoidance assay.…”

mentioning

confidence: 99%

Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans

Hallem

Spencer

McWhirter

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

124

173

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CO 2 is both a critical regulator of animal physiology and an important sensory cue for many animals for host detection, food location, and mate finding. The free-living soil nematode Caenorhabditis elegans shows CO 2 avoidance behavior, which requires a pair of ciliated sensory neurons, the BAG neurons. Using in vivo calcium imaging, we show that CO 2 specifically activates the BAG neurons and that the CO 2 -sensing function of BAG neurons requires TAX-2/ TAX-4 cyclic nucleotide-gated ion channels and the receptor-type guanylate cyclase GCY-9. Our results delineate a molecular pathway for CO 2 sensing and suggest that activation of a receptor-type guanylate cyclase is an evolutionarily conserved mechanism by which animals detect environmental CO 2 .guanylyl cyclase | olfaction | transcriptional profiling | regulator of G protein signaling | chemosensation T he ability to detect and respond to changing concentrations of environmental CO 2 is widespread among animals and plays a critical role in locating food, finding hosts and mates, and avoiding danger (1-4). CO 2 exposure can also have profound physiological effects, including altered respiration, motility, fecundity, and emotional state (5-7). CO 2 is sensed as an aversive cue by many free-living animals, including humans (3,6,8,9). By contrast, many parasites and disease vectors are attracted to CO 2 , which serves as a sensory cue for host location (1, 10).Nematodes constitute a large and highly diverse phylum that includes both free-living and parasitic species. Many parasitic nematodes, including some of the most devastating human-and plant-parasitic nematodes, are attracted to CO 2 . By contrast, adults of the free-living species Caenorhabditis elegans are repelled by CO 2 (11-14). CO 2 avoidance by C. elegans requires a pair of head neurons called the BAG neurons (13), which also mediate responses to decreases in ambient oxygen levels (15). Whether the BAG neurons directly sense CO 2 is not known, and the signaling pathways that mediate CO 2 detection are poorly understood.We show here that environmental CO 2 specifically activates the BAG neurons and not other neurons that drive avoidance behavior, suggesting that the BAG neurons are primary sensory neurons that detect CO 2 . Prolonged CO 2 exposure causes desensitization of avoidance behavior and the BAG neurons themselves, indicating that behavioral adaptation to CO 2 occurs at the level of the BAG neurons. In addition, we show that the CO 2 -evoked activity of the BAG neurons requires a cGMP signaling pathway consisting of the receptor guanylate cyclase GCY-9 and the cGMP-gated cation channel TAX-2/TAX-4. Insects detect CO 2 using a pair of gustatory receptors (16, 17), whereas some mammals detect CO 2 using the receptor-type guanylate cyclase, guanylate cyclase D (GC-D), and soluble adenylate cyclase (18)(19)(20). Our results show that the mechanism of CO 2 detection in C. elegans more closely resembles that of mammals than insects and suggest an evolutionarily ancient role for receptor-type guanyl...

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Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons

Cited by 232 publications

References 49 publications

Two Forms of Learning following Training to a Single Odorant in Caenorhabditis elegans AWC Neurons

Two Forms of Learning following Training to a Single Odorant in Caenorhabditis elegans AWC Neurons

Enhancement of Odor Avoidance Regulated by Dopamine Signaling inCaenorhabditis elegans

Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans

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