A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans
Physiological stress profoundly alters the internal states of the animals and could drive aversive learning, but signaling and circuit mechanisms underlying such behavioral plasticity remain incompletely understood. Here, we show that mitochondrial disruption in nonneural tissues of Caenorhabditis e...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 119; no. 11; pp. 1 - 9 |
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| Main Authors | , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
15.03.2022
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 1091-6490 |
| DOI | 10.1073/pnas.2115533119 |
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| Abstract | Physiological stress profoundly alters the internal states of the animals and could drive aversive learning, but signaling and circuit mechanisms underlying such behavioral plasticity remain incompletely understood. Here, we show that mitochondrial disruption in nonneural tissues of Caenorhabditis elegans induces learned aversion for nutritious bacterial food that displays features of long-term associative memory. Serotonin secreted from the modulatory NSM neuron acts through the SER-4 receptor in the RIB interneuron to drive bacterial avoidance, with NSM and RIB required for the establishment and retrieval for learned aversion, respectively. NSM serotonin synthesis increases early in the induction of systemic mitochondrial stress. Calcium imaging reveals altered RIB responses to bacterial cues in a fraction of stress-primed but not naïve animals. These findings uncover cellular circuits and neuromodulation that enable aversive learning under stress, and lay the foundation for future exploration of behavioral plasticity governed by internal state changes. |
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| AbstractList | Physiological stress triggers avoidance behavior, allowing the animals to stay away from potential threats and optimize their chance of survival. Mitochondrial disruption, a common physiological stress in diverse species, induces the nematode
Caenorhabditis elegans
to avoid non-pathogenic bacteria through a serotonergic neuronal circuit. We find that distinct neurons, communicated through serotonin and a specific serotonin receptor, are required for the formation and retrieval of this learned aversive behavior. This learned avoidance behavior is associated with increased serotonin synthesis, altered neuronal response property, and reprogramming of locomotion patterns. The circuit and neuromodulatory mechanisms described here offer important insights for stress-induced avoidance behavior.
Physiological stress profoundly alters the internal states of the animals and could drive aversive learning, but signaling and circuit mechanisms underlying such behavioral plasticity remain incompletely understood. Here, we show that mitochondrial disruption in nonneural tissues of
Caenorhabditis elegans
induces learned aversion for nutritious bacterial food that displays features of long-term associative memory. Serotonin secreted from the modulatory NSM neuron acts through the SER-4 receptor in the RIB interneuron to drive bacterial avoidance, with NSM and RIB required for the establishment and retrieval for learned aversion, respectively. NSM serotonin synthesis increases early in the induction of systemic mitochondrial stress. Calcium imaging reveals altered RIB responses to bacterial cues in a fraction of stress-primed but not naïve animals. These findings uncover cellular circuits and neuromodulation that enable aversive learning under stress, and lay the foundation for future exploration of behavioral plasticity governed by internal state changes. SignificancePhysiological stress triggers avoidance behavior, allowing the animals to stay away from potential threats and optimize their chance of survival. Mitochondrial disruption, a common physiological stress in diverse species, induces the nematode Caenorhabditis elegans to avoid non-pathogenic bacteria through a serotonergic neuronal circuit. We find that distinct neurons, communicated through serotonin and a specific serotonin receptor, are required for the formation and retrieval of this learned aversive behavior. This learned avoidance behavior is associated with increased serotonin synthesis, altered neuronal response property, and reprogramming of locomotion patterns. The circuit and neuromodulatory mechanisms described here offer important insights for stress-induced avoidance behavior.SignificancePhysiological stress triggers avoidance behavior, allowing the animals to stay away from potential threats and optimize their chance of survival. Mitochondrial disruption, a common physiological stress in diverse species, induces the nematode Caenorhabditis elegans to avoid non-pathogenic bacteria through a serotonergic neuronal circuit. We find that distinct neurons, communicated through serotonin and a specific serotonin receptor, are required for the formation and retrieval of this learned aversive behavior. This learned avoidance behavior is associated with increased serotonin synthesis, altered neuronal response property, and reprogramming of locomotion patterns. The circuit and neuromodulatory mechanisms described here offer important insights for stress-induced avoidance behavior. Physiological stress profoundly alters the internal states of the animals and could drive aversive learning, but signaling and circuit mechanisms underlying such behavioral plasticity remain incompletely understood. Here, we show that mitochondrial disruption in nonneural tissues of Caenorhabditis elegans induces learned aversion for nutritious bacterial food that displays features of long-term associative memory. Serotonin secreted from the modulatory NSM neuron acts through the SER-4 receptor in the RIB interneuron to drive bacterial avoidance, with NSM and RIB required for the establishment and retrieval for learned aversion, respectively. NSM serotonin synthesis increases early in the induction of systemic mitochondrial stress. Calcium imaging reveals altered RIB responses to bacterial cues in a fraction of stress-primed but not naïve animals. These findings uncover cellular circuits and neuromodulation that enable aversive learning under stress, and lay the foundation for future exploration of behavioral plasticity governed by internal state changes. SignificancePhysiological stress triggers avoidance behavior, allowing the animals to stay away from potential threats and optimize their chance of survival. Mitochondrial disruption, a common physiological stress in diverse species, induces the nematode to avoid non-pathogenic bacteria through a serotonergic neuronal circuit. We find that distinct neurons, communicated through serotonin and a specific serotonin receptor, are required for the formation and retrieval of this learned aversive behavior. This learned avoidance behavior is associated with increased serotonin synthesis, altered neuronal response property, and reprogramming of locomotion patterns. The circuit and neuromodulatory mechanisms described here offer important insights for stress-induced avoidance behavior. |
| Author | Chiang, Yueh-Chen Pan, Chun-Liang Liao, Chien-Po |
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| Cites_doi | 10.1016/j.neuron.2014.02.010 10.1523/JNEUROSCI.2674-19.2020 10.1126/science.6805073 10.1016/S0896-6273(00)81199-X 10.1038/nmeth1075 10.1016/j.neuron.2016.10.030 10.1016/j.cell.2016.01.007 10.1038/nature04216 10.1534/genetics.112.142125 10.1016/j.cub.2020.09.022 10.1038/nature12354 10.1016/j.cell.2012.02.050 10.1016/j.devcel.2021.04.021 10.1002/neu.10245 10.1016/S0021-9258(19)36543-3 10.1002/j.1460-2075.1991.tb04966.x 10.1371/journal.pbio.1000372 10.1016/j.neuron.2008.07.038 10.1002/iub.1021 10.1016/0166-4328(90)90074-O 10.1016/j.neuron.2014.10.035 10.1093/genetics/77.1.71 10.1016/j.cell.2013.08.001 10.1523/JNEUROSCI.19-01-00072.1999 10.1126/science.7886454 10.1038/nature13204 10.1038/nature13818 10.1016/j.cell.2018.11.023 10.1016/j.neuron.2019.05.036 10.1038/35000609 10.1016/S0896-6273(00)80527-9 10.1098/rstb.1986.0056 10.1038/nature09545 10.1016/0092-8674(93)80053-H 10.1016/j.neuron.2013.02.018 10.1038/s41583-019-0151-3 10.1038/336638a0 10.1073/pnas.1424954112 10.1016/j.neuron.2010.11.025 10.1073/pnas.1400615111 10.1038/nature06292 10.1016/S0092-8674(00)80399-2 10.1016/j.neuron.2019.05.029 10.1523/JNEUROSCI.19-21-09557.1999 10.1016/j.conb.2020.08.009 |
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| Keywords | stress C. elegans serotonin aversive learning mitochondria |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Edited by Piali Sengupta, Brandeis University, Waltham, MA; received August 23, 2021; accepted February 1, 2022 by Editorial Board Member Michael Rosbash Author contributions: Y.-C.C., C.-P.L., and C.-L.P. designed research; Y.-C.C. and C.-P.L. performed research; Y.-C.C., C.-P.L., and C.-L.P. analyzed data; and Y.-C.C. and C.-L.P. wrote the paper. 1Present address: Howard Hughes Medical Institute and Department of Biological Sciences, Columbia University, NY 10027. |
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| Snippet | Physiological stress profoundly alters the internal states of the animals and could drive aversive learning, but signaling and circuit mechanisms underlying... Physiological stress triggers avoidance behavior, allowing the animals to stay away from potential threats and optimize their chance of survival. Mitochondrial... SignificancePhysiological stress triggers avoidance behavior, allowing the animals to stay away from potential threats and optimize their chance of survival.... |
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| SubjectTerms | Animals Associative learning Associative memory Aversion Avoidance Learning Bacteria Behavioral plasticity Biological Sciences Caenorhabditis elegans - physiology Calcium (mitochondrial) Calcium imaging Circuits Food aversion Host-Pathogen Interactions Interneurons - metabolism Learning Mitochondria Mitochondria - metabolism Neuromodulation Plasticity Receptors, Serotonin - metabolism Serotonergic Neurons - physiology Serotonin Serotonin - metabolism Stress (physiology) Stress, Physiological |
| Title | A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans |
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