School of Life Science and Technology, ShanghaiTech University, Shanghai, China; University of Chinese Academy of Sciences, Beijing, China; Institute of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
Wan-Xin Zeng
School of Life Science and Technology, ShanghaiTech University, Shanghai, China; University of Chinese Academy of Sciences, Beijing, China; Institute of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
Yue Hao
School of Life Science and Technology, ShanghaiTech University, Shanghai, China; University of Chinese Academy of Sciences, Beijing, China; Institute of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
Xian-Ting Zeng
School of Life Science and Technology, ShanghaiTech University, Shanghai, China
Haowen Liu
Queensland Brain Institute, Clem Jones Centre for Ageing Dementia Research (CJCADR), The University of Queensland, Brisbane, Australia
Lei Li
Queensland Brain Institute, Clem Jones Centre for Ageing Dementia Research (CJCADR), The University of Queensland, Brisbane, Australia
Lili Chen
College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, China
Fu-min Tian
School of Life Science and Technology, ShanghaiTech University, Shanghai, China; University of Chinese Academy of Sciences, Beijing, China
Cindy Chang
Department of Molecular Biology, Massachusetts General Hospital, Boston, United States; Department of Neurobiology, Harvard Medical School, Boston, United States
Qi Hall
Department of Molecular Biology, Massachusetts General Hospital, Boston, United States; Department of Neurobiology, Harvard Medical School, Boston, United States
Chun-Xue Song
Center for Brain Science, Shanghai Children's Medical Center, Shanghai, China; Department of Anatomy and Physiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Department of Molecular Biology, Massachusetts General Hospital, Boston, United States; Department of Neurobiology, Harvard Medical School, Boston, United States
Center for Brain Science, Shanghai Children's Medical Center, Shanghai, China; Department of Anatomy and Physiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Shanghai Research Center for Brain Science and Brain-Inspired Intelligence, Shanghai, China
The development of functional synapses in the nervous system is important for animal physiology and behaviors, and its disturbance has been linked with many neurodevelopmental disorders. The synaptic transmission efficacy can be modulated by the environment to accommodate external changes, which is crucial for animal reproduction and survival. However, the underlying plasticity of synaptic transmission remains poorly understood. Here we show that in Caenorhabditis elegans, the male environment increases the hermaphrodite cholinergic transmission at the neuromuscular junction (NMJ), which alters hermaphrodites’ locomotion velocity and mating efficiency. We identify that the male-specific pheromones mediate this synaptic transmission modulation effect in a developmental stage-dependent manner. Dissection of the sensory circuits reveals that the AWB chemosensory neurons sense those male pheromones and further transduce the information to NMJ using cGMP signaling. Exposure of hermaphrodites to the male pheromones specifically increases the accumulation of presynaptic CaV2 calcium channels and clustering of postsynaptic acetylcholine receptors at cholinergic synapses of NMJ, which potentiates cholinergic synaptic transmission. Thus, our study demonstrates a circuit mechanism for synaptic modulation and behavioral flexibility by sexual dimorphic pheromones.