Neurons regulating the duration of forward locomotion in Caenorhabditis elegans

Wakabayashi, Tokumitsu; Kitagawa, Izumi; Shingai, Ryuzo

doi:10.1016/j.neures.2004.06.005

Cited by 171 publications

(221 citation statements)

References 36 publications

Supporting

Mentioning

203

Contrasting

Order By: Relevance

“…Dauer formation and L1 arrest were also similar to wild type in the npr-9 mutant (data not shown). When the animals are not on food, the npr-9 mutant animals display shortened forward movement and high angle turns equivalent to (N2) wild-type animals (23,24) (Fig. 2C).…”

Section: Npr-9 Ismentioning

confidence: 94%

A Caenorhabditis elegans allatostatin/galanin-like receptor NPR-9 inhibits local search behavior in response to feeding cues

Bendena

Boudreau

Papanicolaou

et al. 2008

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

View full text Add to dashboard Cite

Movement inCaenorhabditis elegans is the result of sensory cues creating stimulatory and inhibitory output from sensory neurons. Four interneurons (AIA, AIB, AIY, and AIZ) are the primary recipients of this information that is further processed en route to motor neurons and muscle contraction. C. elegans has >1,000 G proteincoupled receptors (GPCRs), and their contribution to sensory-based movement is largely undefined. We show that an allatostatin/ galanin-like GPCR (NPR-9) is found exclusively in the paired AIB interneuron. AIB interneurons are associated with local search/ pivoting behavior. npr-9 mutants display an increased local search/ pivoting that impairs their ability to roam and travel long distances on food. With impaired roaming behavior on food npr-9 mutants accumulate more intestinal fat as compared with wild type. Overexpression of NPR-9 resulted in a gain-of-function phenotype that exhibits enhanced forward movement with lost pivoting behavior off food. As such the animal travels a great distance off food, creating arcs to return to food. These findings indicate that NPR-9 has inhibitory effects on the AIB interneuron to regulate foraging behavior, which, in turn, may affect metabolic rate and lipid storage.neuropeptide receptor ͉ nerve transmission ͉ foraging ͉ glutamate receptor ͉ interneuron A major challenge in neurobiology is to understand the control of behavior at the molecular level. Neuropeptides and their receptors offer promising candidates for the regulation of various behaviors and changes in physiology. The Caenorhabditis elegans genome sequence has allowed the identification of 109 putative neuropeptide genes encoding precursors that may be processed to Ϸ250 neuropeptides (1-3). These neuropeptides are grouped into three families: FMRFamide-related peptides (f lp), insulin-like peptides (ins), and neuropeptide-like-peptides (nlps). C. elegans expresses Ͼ1,000 orphan G protein-coupled receptors (GPCRs). More than 50 GPCRs resemble known receptors for known neuropeptide families based on phylogenetic comparisons with known vertebrate GPCRs (4). Of these GPCRs, based on sequence identity, C. elegans gene ZK455.3 expresses an nlp receptor, NPR-9, that is most similar to insect allatostatin/ mammalian galanin receptors (5-8). Allatostatins are a family of neuropeptides that share a conserved C-terminal sequence -Tyr/PheXaaPheGlyLeu-NH 2 and are widespread throughout the invertebrate lineage (9, 10). In insects, allatostatins regulate numerous physiological functions, including inhibition of juvenile hormone biosynthesis (11, 12), inhibition of muscle contraction (13), myoendocrine regulation (14, 15), neuromodulation (16), and regulation of enzymatic activities (17) and ecdysis (18). Similarly, mammalian galanin modulates a wide variety of processes that range from neurotransmission, nociception, feeding and metabolism, energy and osmotic homeostasis and learning and memory (19). We report that NPR-9 is uniquely localized in interneuron AIB to negatively regulate a variety of inputs th...

show abstract

Section: Npr-9 Ismentioning

confidence: 94%

A Caenorhabditis elegans allatostatin/galanin-like receptor NPR-9 inhibits local search behavior in response to feeding cues

Bendena

Boudreau

Papanicolaou

et al. 2008

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

View full text Add to dashboard Cite

show abstract

“…Shortly upon removal of food, animals exhibit an "arearestricted search behavior" characterized by high frequency of reversals, whereas on prolonged removal of food the frequency of reversals is decreased with coordinated increase in the duration of forward movement [42][43][44][45]. These behaviors are regulated by inputs from distinct sets of chemosensory neurons [42,43].…”

Section: The Importance Of Chemosensationmentioning

confidence: 99%

“…It is not yet known whether the synaptic connections between these sensory neurons and interneurons are excitatory or inhibitory. Indeed, the AWC chemosensory neurons are predicted to inhibit the AIY, and activate the AIB interneurons under specific environmental conditions and in response to prior experience, although this remains to be shown physiologically [42][43][44]. Primary interneurons synapse onto a layer of secondary interneurons or motor neurons, which in turn are presynaptic to the command interneurons directing backward or forward locomotory movement [53,66] (Fig.…”

Section: Wiring the Chemosensory Circuitmentioning

confidence: 99%

“…As in other chemosensory systems, interaction of an odorant with its cognate ligand is predicted to either activate or inhibit synaptic output of a chemosensory neuron [42,43] (C. Bargmann, personal communication). Although the physiological mechanisms by which activation or inhibition is mediated have not yet been described, many of the molecules required for chemosensory signal transduction have been identified using forward or reverse Fig.…”

Section: The Molecules For Taste and Smellmentioning

confidence: 99%

See 1 more Smart Citation

Generation and modulation of chemosensory behaviors in C. elegans

Sengupta

2007

Pflugers Arch - Eur J Physiol

View full text Add to dashboard Cite

C. elegans recognizes and discriminates among hundreds of chemical cues using a relatively compact chemosensory nervous system. Chemosensory behaviors are also modulated by prior experience and contextual cues. Because of the facile genetics and genomics possible in this organism, C. elegans provides an excellent system in which to explore the generation of chemosensory behaviors from the level of a single gene to the motor output. This review summarizes the current knowledge on the molecular and neuronal substrates of chemosensory behaviors and chemosensory behavioral plasticity in C. elegans.

show abstract

“…Immediately following removal from food wild type C. elegans alter their locomotory pattern by increasing high angle turning and restricting movement to their local environment (local or area-restricted search). [10][11][12][13] With more prolonged food deprivation (20-30 minutes), animals transition to a dispersal-like behavior, characterized by long forward runs of movement that carry the animal into previously unexplored territory. We found that nlp-12 was required for wild type performance of local searching.…”

Section: Introductionmentioning

confidence: 99%