Distinct Dopamine Receptor Pathways Underlie the Temporal Sensitivity of Associative Learning
Animals rely on the relative timing of events in their environment to form and update predictive associations, but the molecular and circuit mechanisms for this temporal sensitivity remain incompletely understood. Here, we show that olfactory associations in Drosophila can be written and reversed on...
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| Vydáno v: | Cell Ročník 178; číslo 1; s. 60 |
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| Hlavní autoři: | , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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27.06.2019
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| ISSN: | 1097-4172, 1097-4172 |
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| Abstract | Animals rely on the relative timing of events in their environment to form and update predictive associations, but the molecular and circuit mechanisms for this temporal sensitivity remain incompletely understood. Here, we show that olfactory associations in Drosophila can be written and reversed on a trial-by-trial basis depending on the temporal relationship between an odor cue and dopaminergic reinforcement. Through the synchronous recording of neural activity and behavior, we show that reversals in learned odor attraction correlate with bidirectional neural plasticity in the mushroom body, the associative olfactory center of the fly. Two dopamine receptors, DopR1 and DopR2, contribute to this temporal sensitivity by coupling to distinct second messengers and directing either synaptic depression or potentiation. Our results reveal how dopamine-receptor signaling pathways can detect the order of events to instruct opposing forms of synaptic and behavioral plasticity, allowing animals to flexibly update their associations in a dynamic environment. |
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| AbstractList | Animals rely on the relative timing of events in their environment to form and update predictive associations, but the molecular and circuit mechanisms for this temporal sensitivity remain incompletely understood. Here, we show that olfactory associations in Drosophila can be written and reversed on a trial-by-trial basis depending on the temporal relationship between an odor cue and dopaminergic reinforcement. Through the synchronous recording of neural activity and behavior, we show that reversals in learned odor attraction correlate with bidirectional neural plasticity in the mushroom body, the associative olfactory center of the fly. Two dopamine receptors, DopR1 and DopR2, contribute to this temporal sensitivity by coupling to distinct second messengers and directing either synaptic depression or potentiation. Our results reveal how dopamine-receptor signaling pathways can detect the order of events to instruct opposing forms of synaptic and behavioral plasticity, allowing animals to flexibly update their associations in a dynamic environment.Animals rely on the relative timing of events in their environment to form and update predictive associations, but the molecular and circuit mechanisms for this temporal sensitivity remain incompletely understood. Here, we show that olfactory associations in Drosophila can be written and reversed on a trial-by-trial basis depending on the temporal relationship between an odor cue and dopaminergic reinforcement. Through the synchronous recording of neural activity and behavior, we show that reversals in learned odor attraction correlate with bidirectional neural plasticity in the mushroom body, the associative olfactory center of the fly. Two dopamine receptors, DopR1 and DopR2, contribute to this temporal sensitivity by coupling to distinct second messengers and directing either synaptic depression or potentiation. Our results reveal how dopamine-receptor signaling pathways can detect the order of events to instruct opposing forms of synaptic and behavioral plasticity, allowing animals to flexibly update their associations in a dynamic environment. Animals rely on the relative timing of events in their environment to form and update predictive associations, but the molecular and circuit mechanisms for this temporal sensitivity remain incompletely understood. Here, we show that olfactory associations in Drosophila can be written and reversed on a trial-by-trial basis depending on the temporal relationship between an odor cue and dopaminergic reinforcement. Through the synchronous recording of neural activity and behavior, we show that reversals in learned odor attraction correlate with bidirectional neural plasticity in the mushroom body, the associative olfactory center of the fly. Two dopamine receptors, DopR1 and DopR2, contribute to this temporal sensitivity by coupling to distinct second messengers and directing either synaptic depression or potentiation. Our results reveal how dopamine-receptor signaling pathways can detect the order of events to instruct opposing forms of synaptic and behavioral plasticity, allowing animals to flexibly update their associations in a dynamic environment. |
| Author | Zeng, Jianzhi Li, Yulong Handler, Annie Siliciano, Andrew F Morantte, Ianessa Graham, Thomas G W Cohn, Raphael Ruta, Vanessa |
| Author_xml | – sequence: 1 givenname: Annie surname: Handler fullname: Handler, Annie organization: Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, NY 10065, USA – sequence: 2 givenname: Thomas G W surname: Graham fullname: Graham, Thomas G W organization: Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, NY 10065, USA – sequence: 3 givenname: Raphael surname: Cohn fullname: Cohn, Raphael organization: Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, NY 10065, USA – sequence: 4 givenname: Ianessa surname: Morantte fullname: Morantte, Ianessa organization: Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, NY 10065, USA – sequence: 5 givenname: Andrew F surname: Siliciano fullname: Siliciano, Andrew F organization: Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, NY 10065, USA – sequence: 6 givenname: Jianzhi surname: Zeng fullname: Zeng, Jianzhi organization: State Key Laboratory of Membrane Biology, Peking University School of Life Sciences, PKU-IDG/McGovern Institute for Brain Research, Peking-Tsinghua Center for Life Sciences, 100871 Beijing, China – sequence: 7 givenname: Yulong surname: Li fullname: Li, Yulong organization: State Key Laboratory of Membrane Biology, Peking University School of Life Sciences, PKU-IDG/McGovern Institute for Brain Research, Peking-Tsinghua Center for Life Sciences, 100871 Beijing, China – sequence: 8 givenname: Vanessa surname: Ruta fullname: Ruta, Vanessa email: ruta@rockefeller.edu organization: Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, NY 10065, USA. Electronic address: ruta@rockefeller.edu |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31230716$$D View this record in MEDLINE/PubMed |
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| Keywords | associative learning memory Drosophila mushroom body G-protein second messengers olfaction synaptic plasticity dopamine |
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| SubjectTerms | Animals Association Learning - physiology Behavior, Animal - physiology Conditioning, Classical - physiology Dopamine - metabolism Dopaminergic Neurons - metabolism Drosophila - physiology Drosophila Proteins - metabolism Mushroom Bodies - physiology Neuronal Plasticity Odorants Receptors, Dopamine - metabolism Receptors, Dopamine D1 - metabolism Reward Smell - physiology Synaptic Potentials - physiology Time Factors |
| Title | Distinct Dopamine Receptor Pathways Underlie the Temporal Sensitivity of Associative Learning |
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