Cargando…
Reinforcement signaling of punishment versus relief in fruit flies
Painful events establish opponent memories: cues that precede pain are remembered negatively, whereas cues that follow pain, thus coinciding with relief are recalled positively. How do individual reinforcement-signaling neurons contribute to this “timing-dependent valence-reversal?” We addressed thi...
Autores principales: | , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cold Spring Harbor Laboratory Press
2018
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5959229/ https://www.ncbi.nlm.nih.gov/pubmed/29764970 http://dx.doi.org/10.1101/lm.047308.118 |
_version_ | 1783324357140938752 |
---|---|
author | König, Christian Khalili, Afshin Ganesan, Mathangi Nishu, Amrita P. Garza, Alejandra P. Niewalda, Thomas Gerber, Bertram Aso, Yoshinori Yarali, Ayse |
author_facet | König, Christian Khalili, Afshin Ganesan, Mathangi Nishu, Amrita P. Garza, Alejandra P. Niewalda, Thomas Gerber, Bertram Aso, Yoshinori Yarali, Ayse |
author_sort | König, Christian |
collection | PubMed |
description | Painful events establish opponent memories: cues that precede pain are remembered negatively, whereas cues that follow pain, thus coinciding with relief are recalled positively. How do individual reinforcement-signaling neurons contribute to this “timing-dependent valence-reversal?” We addressed this question using an optogenetic approach in the fruit fly. Two types of fly dopaminergic neuron, each comprising just one paired cell, indeed established learned avoidance of odors that preceded their photostimulation during training, and learned approach to odors that followed the photostimulation. This is in striking parallel to punishment versus relief memories reinforced by a real noxious event. For only one of these neuron types, both effects were strong enough for further analyses. Notably, interfering with dopamine biosynthesis in these neurons partially impaired the punishing effect, but not the relieving after-effect of their photostimulation. We discuss how this finding constraints existing computational models of punishment versus relief memories and introduce a new model, which also incorporates findings from mammals. Furthermore, whether using dopaminergic neuron photostimulation or a real noxious event, more prolonged punishment led to stronger relief. This parametric feature of relief may also apply to other animals and may explain particular aspects of related behavioral dysfunction in humans. |
format | Online Article Text |
id | pubmed-5959229 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | Cold Spring Harbor Laboratory Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-59592292018-06-01 Reinforcement signaling of punishment versus relief in fruit flies König, Christian Khalili, Afshin Ganesan, Mathangi Nishu, Amrita P. Garza, Alejandra P. Niewalda, Thomas Gerber, Bertram Aso, Yoshinori Yarali, Ayse Learn Mem Research Painful events establish opponent memories: cues that precede pain are remembered negatively, whereas cues that follow pain, thus coinciding with relief are recalled positively. How do individual reinforcement-signaling neurons contribute to this “timing-dependent valence-reversal?” We addressed this question using an optogenetic approach in the fruit fly. Two types of fly dopaminergic neuron, each comprising just one paired cell, indeed established learned avoidance of odors that preceded their photostimulation during training, and learned approach to odors that followed the photostimulation. This is in striking parallel to punishment versus relief memories reinforced by a real noxious event. For only one of these neuron types, both effects were strong enough for further analyses. Notably, interfering with dopamine biosynthesis in these neurons partially impaired the punishing effect, but not the relieving after-effect of their photostimulation. We discuss how this finding constraints existing computational models of punishment versus relief memories and introduce a new model, which also incorporates findings from mammals. Furthermore, whether using dopaminergic neuron photostimulation or a real noxious event, more prolonged punishment led to stronger relief. This parametric feature of relief may also apply to other animals and may explain particular aspects of related behavioral dysfunction in humans. Cold Spring Harbor Laboratory Press 2018-06 /pmc/articles/PMC5959229/ /pubmed/29764970 http://dx.doi.org/10.1101/lm.047308.118 Text en © 2018 König et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article, published in Learning & Memory, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/. |
spellingShingle | Research König, Christian Khalili, Afshin Ganesan, Mathangi Nishu, Amrita P. Garza, Alejandra P. Niewalda, Thomas Gerber, Bertram Aso, Yoshinori Yarali, Ayse Reinforcement signaling of punishment versus relief in fruit flies |
title | Reinforcement signaling of punishment versus relief in fruit flies |
title_full | Reinforcement signaling of punishment versus relief in fruit flies |
title_fullStr | Reinforcement signaling of punishment versus relief in fruit flies |
title_full_unstemmed | Reinforcement signaling of punishment versus relief in fruit flies |
title_short | Reinforcement signaling of punishment versus relief in fruit flies |
title_sort | reinforcement signaling of punishment versus relief in fruit flies |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5959229/ https://www.ncbi.nlm.nih.gov/pubmed/29764970 http://dx.doi.org/10.1101/lm.047308.118 |
work_keys_str_mv | AT konigchristian reinforcementsignalingofpunishmentversusreliefinfruitflies AT khaliliafshin reinforcementsignalingofpunishmentversusreliefinfruitflies AT ganesanmathangi reinforcementsignalingofpunishmentversusreliefinfruitflies AT nishuamritap reinforcementsignalingofpunishmentversusreliefinfruitflies AT garzaalejandrap reinforcementsignalingofpunishmentversusreliefinfruitflies AT niewaldathomas reinforcementsignalingofpunishmentversusreliefinfruitflies AT gerberbertram reinforcementsignalingofpunishmentversusreliefinfruitflies AT asoyoshinori reinforcementsignalingofpunishmentversusreliefinfruitflies AT yaraliayse reinforcementsignalingofpunishmentversusreliefinfruitflies |