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...

Descripción completa

Detalles Bibliográficos
Autores principales: König, Christian, Khalili, Afshin, Ganesan, Mathangi, Nishu, Amrita P., Garza, Alejandra P., Niewalda, Thomas, Gerber, Bertram, Aso, Yoshinori, Yarali, Ayse
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