An Afferent Neuropeptide System Transmits Mechanosensory Signals Triggering Sensitization and Arousal in C. elegans

Sensitization is a simple form of behavioral plasticity by which an initial stimulus, often signaling danger, leads to increased responsiveness to subsequent stimuli. Cross-modal sensitization is an important feature of arousal in many organisms, yet its molecular and neural mechanisms are incomplet...

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Published in:Neuron (Cambridge, Mass.) Mass.), 2018-09, Vol.99 (6), p.1233-1246.e6
Main Authors: Chew, Yee Lian, Tanizawa, Yoshinori, Cho, Yongmin, Zhao, Buyun, Yu, Alex J., Ardiel, Evan L., Rabinowitch, Ithai, Bai, Jihong, Rankin, Catharine H., Lu, Hang, Beets, Isabel, Schafer, William R.
Format: Article
Language:English
Subjects:
Animals
Arousal
Arousal - physiology
Behavior
Behavior, Animal - physiology
Behavioral plasticity
behavioral states
C. elegans
Caenorhabditis elegans - metabolism
Caenorhabditis elegans Proteins - metabolism
Central Nervous System - metabolism
Chemoreception
Cross-modal
Experiments
Locomotion - physiology
Locomotor activity
Mechanical stimuli
Neurons
Neurons - physiology
Neuropeptides
Neuropeptides - metabolism
Peptides - metabolism
sensitization
Sensory neurons
Sleep
Statistical analysis
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Summary:Sensitization is a simple form of behavioral plasticity by which an initial stimulus, often signaling danger, leads to increased responsiveness to subsequent stimuli. Cross-modal sensitization is an important feature of arousal in many organisms, yet its molecular and neural mechanisms are incompletely understood. Here we show that in C. elegans, aversive mechanical stimuli lead to both enhanced locomotor activity and sensitization of aversive chemosensory pathways. Both locomotor arousal and cross-modal sensitization depend on the release of FLP-20 neuropeptides from primary mechanosensory neurons and on their receptor FRPR-3. Surprisingly, the critical site of action of FRPR-3 for both sensory and locomotor arousal is RID, a single neuroendocrine cell specialized for the release of neuropeptides that responds to mechanical stimuli in a FLP-20-dependent manner. Thus, FLP-20 peptides function as an afferent arousal signal that conveys mechanosensory information to central neurons that modulate arousal and other behavioral states. [Display omitted] •A novel arousal paradigm in C. elegans requires a cascade of neuropeptide signaling•Mechanosensory stimulation leads to long-lasting motor and sensory sensitization•Arousal requires FLP-20 peptides released by touch neurons and receptor FRPR-3•FRPR-3 activity then confers behavioral state information via the interneuron RID Arousal is an important conserved behavioral state where animals show increased sensory responsiveness and locomotor hyperactivity. Chew et al. identify a neuromodulatory pathway that enables mechanosensory neurons to promote both sensory and locomotor arousal via activation of a neuroendocrine center.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2018.08.003