A subset of cholinergic mushroom body neurons blocks long-term memory formation in Drosophila
Chun-Chao Chen,
Hsuan-Wen Lin,
Kuan-Lin Feng,
Der-Wan Tseng,
J. Steven de Belle,
Ann-Shyn Chiang
Affiliations
Chun-Chao Chen
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan; Corresponding author
Hsuan-Wen Lin
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan
Kuan-Lin Feng
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan
Der-Wan Tseng
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan
J. Steven de Belle
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan; School of Life Sciences, Arizona State University, Tempe, AZ 85281, USA; 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
Ann-Shyn Chiang
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; Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung 80780, Taiwan; Institute of Molecular and Genomic Medicine, National Health Research Institutes, Miaoli 35053, Taiwan; Graduate Institute of Clinical Medical Science, 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) requires learning-induced synthesis of new proteins allocated to specific neurons and synapses in a neural circuit. Not all learned information, however, becomes permanent memory. How the brain gates relevant information into LTM remains unclear. In Drosophila adults, weak learning after a single training session in an olfactory aversive task typically does not induce protein-synthesis-dependent LTM. Instead, strong learning after multiple spaced training sessions is required. Here, we report that pre-synaptic active-zone protein synthesis and cholinergic signaling from the early α/β subset of mushroom body (MB) neurons produce a downstream inhibitory effect on LTM formation. When we eliminated inhibitory signaling from these neurons, weak learning was then sufficient to form LTM. This bidirectional circuit mechanism modulates the transition between distinct memory phase functions in different subpopulations of MB neurons in the olfactory memory circuit.
