A Glutamate-Neuropeptide Circuit Converts Transient Mate Contact into a Persistent Local Search State in Caenorhabditis elegans Males
Transient sensory encounters can trigger behavioral states that persist long after the initiating stimulus has disappeared, yet how neural circuits initiate and sustain these states remains poorly understood. Here, we show that brief contact with a suitable mate induces a persistent local search state in male Caenorhabditis elegans, characterized by increased reversals and spatially restricted exploration that continues after mate removal. Transient optogenetic activation of male-specific ray type B (RnB) sensory neurons recapitulates this state, with its magnitude and persistence increasing with stimulation strength. Glutamatergic signaling promotes neuronal responses within the interconnected RnB sensory network and contributes to prolonged activity in downstream LUA interneurons. In contrast, loss of the LUA-derived neuropeptide NLP-13 or its receptor DMSR-2 preserves initial stimulus-evoked neuronal responses but reduces prolonged LUA calcium activity and behavioral persistence. LUA-specific restoration of NLP-13 rescues persistent local search, identifying these interneurons as a functionally important source of the neuropeptide. Together, our findings reveal complementary contributions of glutamatergic and neuropeptidergic signaling to the generation and persistence of behavioral states, illustrating how distinct signaling mechanisms cooperate to transform transient social encounters into prolonged circuit activity and persistent behavior.