GCY-20 signaling controls suppression of Caenorhabditis elegans egg laying by moderate cold.

Organisms sensing environmental cues and internal states and integrating the sensory information to control fecundity are essential for survival and proliferation. The present study finds that a moderate cold temperature of 11°C reduces egg laying in Caenorhabditis elegans. ASEL and AWC neurons sense the cold via GCY-20 signaling and act antagonistically on egg laying through the ASEL and AWC/AIA/HSN circuits. Upon cold stimulation, ASEL and AWC release glutamate to activate and inhibit AIA interneurons by acting on highly and lowly sensitive ionotropic GLR-2 and GLC-3 receptors, respectively. AIA inhibits HSN motor neuron activity via acetylcholinergic ACR-14 receptor signaling and suppresses egg laying. Thus, ASEL and AWC initiate and reduce the cold suppression of egg laying. ASEL's action on AIA and egg laying dominates AWC's action. The biased opposite actions of these neurons on egg laying provide animals with a precise adaptation of reproductive behavior to environmental temperatures.

Disexcitation in the ASH/RIM/ADL negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in Caenorhabditis elegans.

Sensations, especially nociception, are tightly controlled and regulated by the central and peripheral nervous systems. Osmotic sensation and related physiological and behavioral reactions are essential for animal well-being and survival. In this study, we find that interaction between secondary nociceptive ADL and primary nociceptive ASH neurons upregulates Caenorhabditis elegans avoidance of the mild and medium hyperosmolality of 0.41 and 0.88 Osm but does not affect avoidance of high osmolality of 1.37 and 2.29 Osm. The interaction between ASH and ADL is actualized through a negative feedback circuit consisting of ASH, ADL, and RIM interneurons. In this circuit, hyperosmolality-sensitive ADL augments the ASH hyperosmotic response and animal hyperosmotic avoidance; RIM inhibits ADL and is excited by ASH; thus, ASH exciting RIM reduces ADL augmenting ASH. The neuronal signal integration modality in the circuit is disexcitation. In addition, ASH promotes hyperosmotic avoidance through ASH/RIC/AIY feedforward circuit. Finally, we find that in addition to ASH and ADL, multiple sensory neurons are involved in hyperosmotic sensation and avoidance behavior.

Positive interaction between ASH and ASK sensory neurons accelerates nociception and inhibits behavioral adaptation.

Central and peripheral sensory neurons tightly regulate nociception and avoidance behavior. The peripheral modulation of nociception provides more veridical and instantaneous information for animals to achieve rapid, more fine-tuned and concentrated behavioral responses. In this study, we find that positive interaction between ASH and ASK sensory neurons is essential for the fast-rising phase of ASH Ca2+ responses to noxious copper ions and inhibits the adaption of avoiding Cu2+. We reveal the underlying neuronal circuit mechanism. ASK accelerates the ASH Ca2+ responses by transferring cGMP through gap junctions. ASH excites ASK via a disinhibitory neuronal circuit composed of ASH, AIA, and ASK. Avoidance adaptation depends on the slope rate of the rising phase of ASH Ca2+ responses. Thus, in addition to amplitude, sensory kinetics is significant for sensations and behaviors, especially for sensory and behavioral adaptations.