Neuropeptide F inhibits dopamine neuron interference of long-term memory consolidation in Drosophila
Kuan-Lin Feng,
Ju-Yun Weng,
Chun-Chao Chen,
Mohammed Bin Abubaker,
Hsuan-Wen Lin,
Ching-Che Charng,
Chung-Chuan Lo,
J. Steven de Belle,
Tim Tully,
Cheng-Chang Lien,
Ann-Shyn Chiang
Affiliations
Kuan-Lin Feng
Institute of Biotechnology, National Tsing Hua University, Hsinchu 30013, Taiwan
Ju-Yun Weng
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan
Chun-Chao Chen
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan
Mohammed Bin Abubaker
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan
Hsuan-Wen Lin
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan
Ching-Che Charng
Institute of Systems Neuroscience and Department of Life Science, National Tsing Hua University, Hsinchu 30013, Taiwan
Chung-Chuan Lo
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan; Institute of Systems Neuroscience and Department of Life Science, National Tsing Hua University, Hsinchu 30013, Taiwan
J. Steven de Belle
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan; Department of Psychological Sciences, University of San Diego, San Diego, CA 92110, USA; School of Life Sciences, University of Nevada, Las Vegas, NV 89154, USA; MnemOdyssey LLC, Escondido, CA 92027, USA
Tim Tully
Institute of Biotechnology, National Tsing Hua University, Hsinchu 30013, Taiwan; Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan
Cheng-Chang Lien
Institute of Neuroscience and Brain Research Center, National Yang Ming Chiao Tung University, Taipei 11221, Taiwan; Corresponding author
Ann-Shyn Chiang
Institute of Biotechnology, National Tsing Hua University, Hsinchu 30013, Taiwan; Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan; Institute of Systems Neuroscience and Department of Life Science, National Tsing Hua University, Hsinchu 30013, Taiwan; Kaohsiung Medical University, Kaohsiung 80708, Taiwan; National Health Research Institutes, Zhunan 35053, Taiwan; China Medical University, Taichung 40402, Taiwan; Kavli Institute for Brain and Mind, University of California at San Diego, La Jolla, CA 92093-0526, USA; Corresponding author
Summary: Long-term memory (LTM) formation requires consolidation processes to overcome interfering signals that erode memory formation. Olfactory memory in Drosophila involves convergent projection neuron (PN; odor) and dopaminergic neuron (DAN; reinforcement) input to the mushroom body (MB). How post-training DAN activity in the posterior lateral protocerebrum (PPL1) continues to regulate memory consolidation remains unknown. Here we address this question using targeted transgenes in behavior and electrophysiology experiments to show that (1) persistent post-training activity of PPL1-α2α′2 and PPL1-α3 DANs interferes with aversive LTM formation; (2) neuropeptide F (NPF) signaling blocks this interference in PPL1-α2α′2 and PPL1-α3 DANs after spaced training to enable LTM formation; and (3) training-induced NPF release and neurotransmission from two upstream dorsal-anterior-lateral (DAL2) neurons are required to form LTM. Thus, NPF signals from DAL2 neurons to specific PPL1 DANs disinhibit the memory circuit, ensuring that periodic events are remembered as consolidated LTM.
