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[
Genome Biol,
2007]
: A report on the 16th International Caenorhabditis elegans Meeting, Los Angeles, USA, 27 June-1 July 2007.
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[
Nature,
2007]
Although many properties of the nervous system are shared among animals and systems, it is not known whether different neuronal circuits use common strategies to guide behaviour. Here we characterize information processing by Caenorhabditis elegans olfactory neurons (AWC) and interneurons (AIB and AIY) that control food- and odour-evoked behaviours. Using calcium imaging and mutations that affect specific neuronal connections, we show that AWC neurons are activated by odour removal and activate the AIB interneurons through AMPA-type glutamate receptors. The level of calcium in AIB interneurons is elevated for several minutes after odour removal, a neuronal correlate to the prolonged behavioural response to odour withdrawal. The AWC neuron inhibits AIY interneurons through glutamate-gated chloride channels; odour presentation relieves this inhibition and results in activation of AIY interneurons. The opposite regulation of AIY and AIB interneurons generates a coordinated behavioural response. Information processing by this circuit resembles information flow from vertebrate photoreceptors to ''OFF'' bipolar and ''ON'' bipolar neurons, indicating a conserved or convergent strategy for sensory information processing.
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[
Nat Neurosci,
2010]
Many neurons release classical transmitters together with neuropeptide co-transmitters whose functions are incompletely understood. Here we define the relationship between two transmitters in the olfactory system of C. elegans, showing that a neuropeptide-to-neuropeptide feedback loop alters sensory dynamics in primary olfactory neurons. The AWC olfactory neuron is glutamatergic and also expresses the peptide NLP-1. Worms with
nlp-1 mutations show increased AWC-dependent behaviors, suggesting that NLP-1 limits the normal response. The receptor for NLP-1 is the G protein-coupled receptor NPR-11, which acts in postsynaptic AIA interneurons. Feedback from AIA interneurons modulates odor-evoked calcium dynamics in AWC olfactory neurons and requires INS-1, a neuropeptide released from AIA. The neuropeptide feedback loop dampens behavioral responses to odors on short and long timescales. Our results point to neuronal dynamics as a site of behavioral regulation and reveal the ability of neuropeptide feedback to remodel sensory networks on multiple timescales.
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[
International Worm Meeting,
2019]
Patterned neural activity has been shown to underlie the perception of olfactory stimuli. However, most work to date has focused on early stages of sensory processing, and thus it is unclear how the rest of the nervous system interprets information transduced at the sensory periphery. Here, we used whole-brain calcium imaging of thirty immobilized Caenorhabditis elegans to study how different chemical stimuli induce unique patterns of neural activity. We exposed groups of three worms to one of ten conditions: benzaldehyde (BZ), diacetyl (DA), isoamyl alcohol (IAA), 2-nonanone (NN), or NaCl, at either high or low concentrations. We generated networks that describe the functional interactions between neurons using mutual information, and extracted 22 graph-theoretic properties that characterize the network's functional integration, segregation, and resilience. We identified a few properties that can distinguish between low and high stimulus concentrations, one between attractants (BZ, DA, IAA, and a low concentration of NaCl) and repellents (NN and a high concentration of NaCl), and a third set of properties that can accurately classify the attractants. High concentrations of chemical stimuli tend to induce a network that is more functionally segregated, while repellents induce a network with a shorter path between any two neurons. Furthermore, attractants can be grouped by three different properties - the centrality of an average neuron, how often a strongly connected neuron is connected to weakly connected neurons, and the distance between the furthest apart pair of neurons. Importantly, all of these properties have values that are different from those obtained by analyzing the structural connectivity between neurons in the head of the worm. Thus, we conclude that the structural connectome provides a rich substrate that is employed in very distinct ways to support perception and, ultimately, behavior. Many of these graph-theoretic features deal with how efficiently information is transmitted throughout the C. elegans nervous system, and may reflect the saliency of the stimulus in question.
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[
International Worm Meeting,
2009]
Animals increase their pirouette frequency in response to removal from food stimulus for a period of 15 min. The AWC and ASK sensory neurons and the AIB interneurons stimulate pirouettes immediately after removal from food, while the AIY and AIA interneurons inhibit pirouettes (Wakabayashi et al 2004, Gray et al 2005). We have found that AWC sensory neurons become active in response to removal of stimulus, releasing two neurotransmitters (glutamate and a neuropeptide NLP-1). The released glutamate acts to activate AIB and inhibit AIY interneurons, promoting reversals (Chalasani et al 2007). In contrast to glutamate, AWC-released NLP-1 acts on AIA interneurons to suppress reversals, suggesting that reversal frequencies are regulated by at least two opposing signaling systems. AWC calcium responses are modulated in these neurotransmitter mutants, suggesting that feedback pathways affect AWC neuronal activity. References: Chalasani, S. H., Chronis, N., Tsunozaki, M., Gray, J. M., Ramot, D., Goodman, M. B., and Bargmann, C. I. (2007). Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450, 63-70. Gray, J.M., Hill, J.J., and Bargmann, C.I. (2005). A circuit for navigation in Caenorhabditis elegans. Proc. Natl. Acad. Sci. 102, 3184-3191. Wakabayashi, T., Kitagawa, I., and Shingai, R. (2004). Neurons regulating the duration of forward locomotion in Caenorhabditis elegans. Neurosci. Res. 50, 103-111.
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[
MicroPubl Biol,
2020]
Sensation of environmental cues and decisions made as a result of processing of specific sensory cues underlies a myriad of behavioral responses that control every-day life decisions and ultimately survival in many organisms. Despite the appreciation that organisms can sense, process, and translate sensory cues into a behavioral response, the neural mechanisms and molecules that mediate these behaviors are still unclear. Neurotransmitters, such as glutamate, have been implicated in a variety of sensory-dependent behavioral responses, including olfaction, nociception, mechanosensation, and gustation (Mugnaini et al., 1984, Wendy et al., 2013, Daghfous et al., 2018). Despite understanding the importance of glutamate signaling in sensation and translation of contextual cues on behavior, the molecular mechanisms underlying how glutamatergic transmission influences sensory behavior is not fully understood. The nematode, C. elegans, is able to sense a variety of sensory cues. These types of sensory-dependent behavioral responses are mediated through olfactory, gustatory, mechanosensory and aerotactic circuits of the worm (Lans and Jansen, 2004, Milward et al., 2011, Bretscher et al., 2011, Kodama-Namba et al., 2013, Ghosh et al., 2017). Odor guided behavior toward attractants, such as, food cues requires neurotransmitters, that include, glutamate (Chalasani et al., 2007, Chalasani et al., 2010). More specifically, once on a food source, wild type N2 hermaphrodites will generally be retained on a food source (Shtonda and Avery, 2006, Milward et al., 2011, Harris et al., 2019). The types, quality, pathogenicity, and perception of food can modulate food recognition, food leaving rates, and overall navigational strategies towards food (Zhang et al., 2005, Shtonda and Avery, 2006; Ollofsson et al., 2014). These types of behaviors are based on detection of environmental cues, including oxygen, metabolites, pheromones, and odors. Food leaving behaviors have been shown to be influenced by a number of neuronal signals (Shtonda and Avery, 2006, Bendesky et al., 2011, Ollofsson et al., 2014, Meisel et al., 2014, Hao et al., 2018).
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[
International Worm Meeting,
2015]
The balance between proliferation and differentiation of stem cell populations must be responsive to changing molecular and physiological conditions. However, the mechanism behind this plasticity is not well understood. The C. elegans nematode is a tractable organism to study the influence of food sensation on physiology. Recent studies suggest that the number of proliferating germ cells (PGCs), the only stem cell population in the adult C. elegans body, respond to the environment by communicating with sensory neurons. Sensory neurons are able to relay information about food abundance to the PGCs. Specifically, TGF-b signaling from the ASI gustatory neuron promotes increased PGCs when food is abundant and reduced PGCs when food is scarce [Dalfo et al. 2012]. The olfactory sensory neurons (OSNs), AWA and AWC, are also food-sensing neurons [Chalasani et al. 2007] and thus, may also regulate the PGCs. Indirect evidence suggests that the OSNs along with ASI reduce lifespan, perhaps via the germline [Alcedo et al. 2004 and Hsin et al. 1999]. Studies also suggest that the neurons secrete signals to affect behavioral responses to odor [Chalasani et al. 2010]. We propose that the OSNs may affect the physiology of the C. elegans nematode, as assessed by the PGCs and brood size, via secreted molecules. PGC counts and brood sizes from animals with genetically dysfunctional AWA or AWC neurons are discussed in this poster.A mobile RNA intermediate is an attractive candidate to mediate the communication between the OSNs and the germline. Published data from the L'Etoile lab shows that 22G RNAs synthesized in the AWC show increased levels worm-wide upon odor exposure [Juang et al. 2013] and unpublished data indicate that this increase is dependent on the presence of SID-1 dsRNA channels. We discuss the effect of dysfunctional SID-1 channels on the PGC pool and brood size.Finally, the nuclear RNAi pathway, involving NRDE-1, 2 and 4, is able to regulate gene expression in the germline nuclei [Burton et al. 2011]. Preliminary studies have shown that siRNA knockdown of the human homolog of NRDE-2 decreases the viability of mammalian cells transformed with the oncogene Aurora B kinase, which functions in chromosomal segregation during both mitosis and meiosis. We therefore examined the effect of mutant
nrde-2 on the C. elegans PGC pool and brood size. Our results lead us to believe that
nrde-2 has a conserved function in maintaining proper cellular proliferation.
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[
Neuronal Development, Synaptic Function and Behavior, Madison, WI,
2010]
Neural circuits transform sensory signals to generate behaviors on timescales from seconds to hours. In some C.elegans behaviors, sensory inputs lead to long lasting and complex behavioral outputs. Animals that have been removed from food spend about 15 minutes exploring a local area by interrupting long forward movements with reversals and turns (Wakabayashi et al., 2004, Gray et al 2005). AWC sensory neurons regulate this behavior by releasing two neurotransmitters, glutamate (promoting turns) and NLP-1 (inhibiting turns). AWC sensory neuron released glutamate activates AIB and inhibits AIY and AIA interneurons (Chalasani et al 2007). In contrast to glutamate, AWC neuron released NLP-1 acts on AIA interneurons to suppress reversals, indicating that turn frequencies are regulated by at least two opposing systems. AWC calcium responses are modulated in these neurotransmitter mutants suggesting that multiple pathways can influence AWC dependent behavior and neuronal activity. ReferencesChalasani, S. H., et. al. Dissecting a neural circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450, 63-70 (2007).Gray, J.M., et. al. A circuit for navigation in Caenorhabditis elegans. Proc. Natl. Acad. Sci. 102, 3184-3191 (2005).Wakabayashi, T., et. al. Neurons regulating the duration of forward locomotion in Caenorhabditis elegans. Neurosci. Res. 50, 103-111 (2004).